Biodiversity Impacts of Some Agricultural Commodity Production Systems

Issues in International Conservation Biodiversity Impacts of Some Agricultural Commodity Production Systems Introduction Despite centuries of urbanization and industrialization, around half of the world s people still live as subsistence or small-scale farmers. The production of agricultural export commodities represents a major source of foreign income for many developing countries, and commodities such as coffee and cocoa rank second in importance only to oil in legal international trade. Such crops are inevitably produced on land formerly covered with natural habitats, and their production usually involves the loss of some or most of the biodiversity formerly present. Around 15 million ha of the Earth s primary forest are lost each year, most of it in the tropics. Of this, approximately 60% is lost to slash-and-burn agriculture, the rest to logging, other forms of agriculture, and fire (ICRAF 1995). Because tropical forests may support as much as 70% of the planet s plant and animal species, deforestation in the tropics represents the greatest single threat to global biodiversity. Deforestation is proceeding most rapidly in those countries holding the planet s richest biodiversity (Balmford & Long 1994). An estimated 10 9 ha of land (an area approximately equal to all the planet s remaining tropical forests; Mayaux et al. 1998) may be cleared for cultivation in the developing world by 2050, mostly in Latin America and sub- Saharan Africa (Tilman et al. 2001). The external impacts of agriculture, such as water and air pollution, could affect even larger areas. Forest clearance by burning accounts for 25% of total CO 2 emissions, making it a major contributor to global climate change (Newmark 1998). Agriculture is an anthropogenic threat to biodiversity that can adversely affect vast areas (e.g., Donald et al. 2001). There are significant conservation implications of agricultural production systems that go beyond their replacement of natural habitats. In many systems, management spans a gradient from low to high intensity. A growing number of consumers in the developed world are prepared to pay a premium to encourage less intensive forms of production in the belief that these have environmental benefits. Quantifying these benefits and identifying the important ecosystem properties of such systems, however, is not easy. The extent to which particular commodity production systems are deemed beneficial or deleterious to the conservation of biodiversity is at least partly subjective. The conversion of natural habitats to commodity production, however sympathetically managed, is likely to result in a loss of biodiversity. On the other hand, environmentally sustainable forms of commodity production are often regarded as valuable habitats in their own right and greatly preferable to other forms of habitat exploitation. Whether habitat conversion to agricultural commodity systems or the subsequent intensification of those systems has the greater environmental impact is unclear, but is likely to differ between crops. Consumers in the developed world are becoming increasingly aware of the environmental advantages of lowintensity production and are prepared to pay a premium on produce from such systems. The next few years are likely to be influential in developing the planet s long-term agricultural and environmental policies (Crompton & Hardstaff 2001) and in determining the buying patterns of consumers in the developed world of products grown in the developing world for export (Donald et al. 2004), so a review of current knowledge is timely. I reviewed published and unpublished scientific evidence to assess and quantify the environmental implications of several important agricultural commodity production systems. These were chosen to encompass a range of product types (oils, grain, and fruits) grown mainly for export in areas of rich biodiversity where systems of production have changed radically during recent decades. All are regarded as potential threats to biodiversity in at least some parts of their range. A number of other crops, such as tea (Camillia sinensis L.) and rubber (Hevea brasiliensis [Willd.] Muell.- Arg.), would have fulfilled these criteria, but too little quantitative information on biodiversity in these crops was available to permit any general conclusions (though see Wu et al. 2001; Schroth et al. 2003). A specific aim of my review is to identify research priorities. Sources of Data Agricultural statistics on area, yield, and total production were taken from the FAOSTAT database of the United, Pages 17 37 17

18 Issues in International Conservation Donald Nations Food and Agriculture Organization (FAO) (correct as of 31 July 2003). I used a combination of electronic literature searches, Internet searches, requests for information to and discussion with key organizations and individuals, and requests for information over a number of relevant email specialist interest groups to identify sources of data. Despite my attempts to locate all relevant data, it is likely that many studies remain unpublished, so the data I reviewed cannot be regarded as comprehensive. Cacao (Cocoa) Theobroma cacao L. Methods of Production Cocoa is the world s third most important agricultural export commodity, after coffee and sugar, and a major earner of foreign income for the small number of countries that dominate production. Despite being an Amazonian plant, around 60% of the world s cocoa is produced in West Africa (Appendix). Over 70% of the world s cocoa production comes from 5 to 6 million low-intensity small holdings, usually <10 ha in size. Planting can take place under thinned primary-forest canopy, under naturally regenerating forest after clear felling, or under the canopy of artificially planted trees (Greenberg 1998; N goran 1998). Shade trees provide farmers with a variety of products, including firewood, construction materials, pharmaceutical products, and food ( Herzog 1994). Being an understory tree, it has been assumed that cacao thrives best under heavy forest shade. This viewhasgivenway,however,toa prescription of mild shade for both yield levels and precocity. The ability of Upper Amazon hybrid varieties to produce high yields in the absence of shade has been recognized since the 1970s, and the area of cocoa grown without shade in West Africa has expanded, largely at the expense of primary forest. The transition from shade to full-sun growth has been the major contributor to Côte d Ivoire s massive increase in production since the 1970s. In Latin America, there has also been a shift to full-sun cultivation, leading to higher yields. Research in the main Brazilian growing area of Bahia from the 1960s showed that full-sun production produced significantly higher yields than shaded growth, whether fertilizer was used or not (Cabala-Rosand et al. 1976). Nonshade crops, however, are more prone to insect attack than shade crops and require insecticide applications to maintain yield. The collapse of the Malaysian cocoa industry from 1980 onwards stimulated desperate attempts to increase yield. Growers converted shade cocoa to full-sun production with pesticide applications. On good soils, this significantly increased yields, and gross profit per hectare in full-sun systems is nearly three times that in traditional shade systems (Chok 1998). This placed significant ecological stress on the cocoa trees, however, which became susceptible to a number of diseases. These diseases have contributed to the collapse of the industry in Malaysia, where cocoa is produced on large intensive farms, whereas in Indonesia, where traditional small-scale practices persist, the industry has fared better. Only recently have technological improvements so raised yields that plantations have become more profitable than low-intensity production systems when prices are high. The majority of producers lack the resources to expand or improve their farms, and much traditional shade survives because of this laissez faire approach rather than because of deliberate management. Production is limited by pests and diseases, which reduce income and therefore the farmers ability to purchase inputs. Generally, smallholders have coped better with the slump in world prices than larger commercial producers. Although world demand for cocoa is likely to remain high in the coming years, due partly to the stability of sugar prices, overproduction is likely to keep prices low. Overproduction arises from the tendency of smallholders, lacking strategic organization, to plant new trees when prices are high. A history of cacao production and a description of the many production methods commonly in use are given by Laird et al. (1996). Impacts on Biodiversity Cocoa production areas occur almost wholly within areas identified as biodiversity hotspots (Myers et al. 2000), suggesting that cocoa production may have an environmental impact disproportional to its area. In many of these regions, cocoa cultivation is a major cause of deforestation because new planting along the edges of primary forest is cheaper than felling and replanting existing plantations when they become exhausted. Although the original canopy trees are often maintained in reduced numbers, they are generally replaced by non-native trees as they die. Although cocoa cultivation may represent a serious threat to biodiversity, there are a number of reasons for regarding shaded cocoa cultivation as environmentally preferable to many other forms of agriculture in tropical forest regions (e.g., Greenberg 1998; Power & Flecker 1998). Initial land clearance and preparation causes minimal damage to soil and because cacao trees are semipermanent, soil structure is maintained, and there is no need to annually clearcut new forest. Carbon sequestration is higher than in slash-and-burn agriculture, which in many areas is the main alternative. However, constant cropping results in a loss of soil nutrients, which often have to be replaced with fertilizers. When exhausted, cocoa trees can be cleared and replanted without damaging the canopy trees, although abandonment and replanting elsewhere is more common (Rice & Greenberg 2000). The use of shade trees ensures the survival of at least some structural and biotic diversity, aiding pollination and the biological control of pests and diseases. Some

Donald Issues in International Conservation 19 shade trees are planted fruit trees, such as citrus and mango, but others are native hardwoods, which as well as providing timber, medicine, food, and fruit also retain elements of the native flora and fauna. Although there are a number of good reasons for assuming that shade cocoa has environmental benefits over other forms of forest exploitation, there is little scientific evidence available to quantify such benefits. The majority of research suggests that shade cacao is generally environmentally preferable to full sun cacao and other crops, but not as good as pristine forest (Table 1). Reitsma et al. (2001) and Estrada et al. (1997) both suggest shade cacao could have positive environmental effects in landscapes already much impoverished by human activities. Cocoa agroforests make up a small proportion of the total forested and wooded areas of virtually all producing countries, so environmentally sustainable shade cocoa cultivation alone is unlikely to act as a major stop to global deforestation. However, in certain countries, such as Côte d Ivoire, Ghana, and the Dominican Republic, cocoa agroforests make up a significant proportion of all woodland. In such countries, environmentally sympathetic management of cocoa stands is likely to contribute positively to national biodiversity. The Brazilian cocoa-growing region of Bahia, which produces almost all the country s cocoa, comprises a large proportion of the little that remains of the country s Atlantic rainforest. Much of what survives (2 7%) is now heavily shaded cabrucagem cocoa plantations, and the habitat is now threatened by low market prices for cocoa and the arrival of the witches broom fungus (Crinipellis perniciosa), which has devastated cocoa production elsewhere (Alger & Caldas 1994). Forest loss has been caused mainly by large landowners, either to increase cocoa tree density in times of high cocoa prices or, more recently, to sell trees to earn income during periods of low prices. However, large landowners, who have gained most from government-funded aid programs, are more interested than smallholders in preserving some of the remaining forests, and maintain a higher proportion of their land in traditional cabrucagem plantations and forest (Alger & Caldas 1994). Ironically, the government body (Comissãu Executiva do Plano da Lavoura Cacaueira [CEPLAC]) that unsuccessfully tried in the 1960s to intensify cocoa production by removing shade trees, now actively supports the traditional cabrucagem agroecosystem. The future of the cabrucagem, and hence much of the remainder of the Atlantic forests of Brazil, depends to a large extent on fluctuation in the world cocoa supply and demand and the provision of specific aid to cabrucagem farmers to maintain forest cover (Johns 1999). This is an area where cocoa production has actually slowed deforestation because the forest cover remains high and cocoa farmers have prevented the settling and subsequent felling of forested land by squatters. However, 30,000 ha of cocoa were felled in Bahia between 1992 and 1996, and recent estimates by Conservation International suggest that 15 20% of the cocoa forests in Bahia will be logged and converted to pasture in the next 10 years. The CEPLAC estimates that up to half the cabrucagem will be lost to other forms of agriculture, as cocoa and shade trees are felled for pasture, coffee, or plantation agroforestry. The Bahia region of Brazil is perhaps the most environmentally important area of cocoa production in the world. Despite the frequent assumption that cacao plantations are biodiverse and sustainable, there is little scientific evidence to support this idea (Greenberg 1998). Greenberg et al. (2000) questioned the conservation value of cacao plantations with planted shade trees, even when such shade was relatively diverse, and suggested that rustic systems with natural shade trees were far better for birds. Parrish et al. (1998) and Reitsma et al. (2001), in the most detailed examination of bird populations in cocoa, compared only the least intensive cocoa production systems with pristine forest fragments. No one has statistically compared biodiversity (or any element of it) across the whole spectrum of pristine forest, from different shade systems to full-sun production. This makes it difficult to assess quantitatively the implications of cacao production for biodiversity and to identify the specific elements of shade production that are important. The effects of isolation and fragment size are poorly known. Cocoa production is likely to remain a major contributor to deforestation at the forest-agriculture interface, particularly in Indonesia and Cameroon, where much pristine forest remains. Greenberg (1998) argues that the conservation of shade-grown cacao plantations needs to entail financial incentives for the grower and ecosystem services for the consumer. These incentives could be derived in four ways: (1) an appeal to the market to purchase more environmentally friendly products; (2) an appreciation of the financial benefits of the ecological services arising from shade production; (3) an appreciation of the income derived from noncrop plants; and (4) national or international programs to subsidize lowintensity management. Alger (1998), however, assessing the conservation potential of surviving cocoa farms in southern coastal Brazil, concluded that premium prices for organic, shade, and fair trade cocoa would not necessarily require farmers to maintain forest reserves, retain the interconnectivity of forest fragments, or reduce hunting or burning. Economic, political, and social changes coincident with low world cocoa prices and the arrival of the witches broom fungus mean that the conservation of the cabrucagem is unlikely to occur naturally and requires fundamental political change.

20 Issues in International Conservation Donald Table 1. Summary of results of quantitative studies comparing low- and high-intensity production systems and comparing commodity production systems with natural habitats. Low-intensity shade Low-intensity shade No difference between Low-intensity shade Low-intensity systems systems preferable to systems preferable to shade and full-sun systems comparable to less desirable than the intensive full-sun other agricultural systems, or full-sun or better than natural habitats plantations land use systems better pristine habitats they replace Cacao Soil quality and erosion West Africa (CIBLE 1994, cited in Laird et al. 1996) Indonesia (Siebert 2002) Pollution West Africa (CIBLE 1994, cited in Laird et al. 1996) Human health and welfare West Africa (CIBLE 1994, cited in Laird et al. 1996) South America (Hay 1991) Carbon stock West Africa (IRAD 1997, cited in Duguma et al. 2001) Plant biodiversity Indonesia (Siebert 2002) West Africa (Duguma et al. 2001) Soil microfauna West Africa (Duguma et al. 2001) Mammals Mexico (Estrada et al. 1994) Mexico (Estrada & Coates-Estrada 1996) West Africa (CIBLE 1994, cited in Laird et al. 1996) West Africa (CIBLE 1994, cited in Laird et al. 1996) West Africa (Ekande 1987) West Africa (IRAD 1997, cited in Duguma et al. 2001) West Africa (Kotto-Same et al. 1997) West Africa (Duguma et al. 2001) Cameroon (Zapfack et al. 2002) West Africa (Duguma et al. 2001) South America (Alves 1990) Mexico (Estrada et al. 1993) Birds (forest specialists) South America (Alves 1990) Birds (habitat generalists) Indonesia (Siebert 2002) Mexico (Estrada et al. 1994) Mexico (Estrada et al. 1997) Central America (Power & Flecker 1998) Central America (Reitsma et al. 2001) Mexico (Estrada et al. 1994) Mexico (Estrada et al. 1997) Central America (Power & Flecker 1998) Mexico (Greenberg et al. 2000) Herptiles Central America (Power & Flecker 1998) Central America (Reitsma et al. 2001) Mexico (Estrada et al. 1994) Mexico (Estrada et al. 1997) Central America (Power & Flecker 1998) Mexico (Greenberg et al. 2000) Central America (Heinen 1992) Central America (Glor et al. 2001)

Donald Issues in International Conservation 21 Table 1. (continued) Low-intensity shade Low-intensity shade No difference between Low-intensity shade Low-intensity systems systems preferable to systems preferable to shade and full-sun systems comparable to less desirable than the intensive full-sun other agricultural systems, or full-sun or better than natural habitats plantations land use systems better pristine habitats they replace Arthropods Mexico (Estrada et al. 1998) Central America (Roth et al. 1994) Indonesia (Klein et al. 2002b) Central America (Power & Flecker 1998) Costa Rica (Klein et al. 2002a) Mexico (Estrada et al. 1998) Mexico (Estrada et al. 1998) Coffee Birds (all species) Central America (Wunderle & Latta 1996, 1998) Central America (Calvo & Blake 1998) Central America (Greenberg et al. 1997a) Mexico (Cesar Tejeda-Cruz, unpubl. data) Central America (Greenberg et al. 1997b) Mexico (Cesar Tejeda-Cruz, unpubl. data) Mexico (Aguilar-Ortiz 1982) Central America (Greenberg et al. 1997a) Central America (Greenberg et al. 1997b) Mexico (Aguilar-Ortiz 1982) Mexico (Estrada et al. 1997) Indonesia (Siebert 2002) South America (Canaday 1997) Central America (Petit et al. 1999) Mexico (Moguel & Toledo 1998) Birds (Nearctic migrants) Central America (Greenburg et al. 1996) Central America (Parrish & Petit 1995) Birds (forest specialists) Central America (Roberts et al. 2000b) Central America (Greenburg et al. 1997a) Central America (Greenberg et al. 1997a) Central America (Greenberg et al. 1997b) Central America (Robbins et al. 1992) Central America (Petit et al. 1999) Caribbean (Johnson & Sherry 2001) Central America (Parrish & Petit 1995) Central America (Roth et al. 1994) Central America (Wunderle & Latta 1996) Central America (Calvo & Blake 1998) Mexico (Perfecto et al. 2003) Mexico (Aguilar-Ortiz 1982) Mexico (Estrada et al. 1997) South America (Canaday 1997) Central America (Petit et al. 1999) Costa Rica (Lindell & Smith 2003) Central America (Parrish & Petit 1995)

22 Issues in International Conservation Donald Table 1. (continued) Low-intensity shade Low-intensity shade No difference between Low-intensity shade Low-intensity systems systems preferable to systems preferable to shade and full-sun systems comparable to less desirable than the intensive full-sun other agricultural systems, or full-sun or better than natural habitats plantations land use systems better pristine habitats they replace Invertebrates Mexico (Perfecto et al. 1997) Mexico (Perfecto & Snelling 1995) Mexico (Perfecto & Vandermeer 2002) Central America (Wunderle & Latta 1996) Central America (Roberts et al. 2000a) Mexico (Perfecto & Vandermeer 2002) Mexico (Ibarra-Nuñes 1990) Mexico (Perfecto et al. 2003) Mexico (Estrada et al. 1998) Mexico (Nestel et al. 1993) Mexico (Armbrecht & Perfecto 2003) Costa Rica (Benitez & Perfecto 1990) Costa Rica (Perfecto & Vandermeer 1994) Central America (Rojas et al. 2001) Central America (Roberts et al. 2000a) Mammals Mexico (Gallina et al. 1996) Plants Indonesia (Siebert 2002) Pollution Central America (Rice & Ward 1996) Central America (Babbar & Zak 1995) Central America (Torres 1984) Mexico (Perfecto et al. 1996) Mexico (Perfecto et al. 1997) SE Asia (Stork & Brendell 1990) Traditional systems Traditional systems No difference between Traditional systems Traditional systems less better than better than other traditional and comparable to or better desirable than the natural Rice modern systems forms of agriculture modern systems than natural wetlands habitats they replace General biodiversity Global (Roger et al. 1991) Global (Power & Flecker 1998) Global (Lawler 2001) Waterbirds USA (Miller et al. 1989) USA (Elphick 2000) France (Tourenq et al. 2001) France (Hafner et al. 1986) Japan (Narusue & Uchida 1993) S Europe (Fasola et al. 1996) SEurope(Fasola&Ruíz 1996) France (Tamisier & Grillas 1994) Australia (Richardson et al. 2001) Japan (Lane & Fujioka 1998) S Europe (Fasola & Ruíz USA (Day & Colwell 1998) 1997) Spain (Riera et al. 1998) Amphibia Japan (Fujioka & Lane 1997) Madagascar (Vallan 2002) Fish Japan (Katano et al. 2003) Plant biomass France (Tamisier & Grillas 1994) Total cell entries 42 11 3 37 31

Donald Issues in International Conservation 23 One possibility for conservation of cabrucagem suggested by Alger (1998) and Newmark (1998) is the global trading of carbon offsets, though such a system needs to ensure that biodiverse habitats, rather than commercial plantations, receive protection. Alger and Caldas (1994) suggest that farmers maintaining forests should be regarded as performing a global public good, which should attract financial incentives such as tax waivers or subsidies to protect forests. Elsewhere, projects to protect low-intensity, high-biodiversity cacao systems in Costa Rica, Panama, and Belize are already underway through organic certification schemes, help for farmers to plant shade trees, and development of ecotourism. Future conservation of low-intensity cacao production systems might be achieved through carbon-sequestration payments, payments for ecosystems benefits of shade production (e.g., water capture, medicinal products), and international loans and aid projects (Greenberg 1998; Parrish et al. 1998). All such methods require that complex financial and social considerations be taken into account, the most important of which is the world price of cocoa (Donald et al. 2004). Research Requirements Parrish et al. (1998) identified a number of research and management recommendations arising from their work. These include determining the long-term stability of bird and other faunal populations within cacao of different management intensities to ensure that cacao habitats are not population sinks for tropical diversity; comparing the biological value of similarly managed plantations that differ greatly in size; and comparing biodiversity in organic and pesticidetreated cacao farms of similar landscape and vegetation configurations to determine the impact of agrochemical use. Greenberg (1998) suggests that much research is necessary to develop an integrated conservation plan for cacao-producing areas. This research should compare cacao farms with other agricultural habitats and different management schemes among cacao farms and should emphasize the ability of cacao to harbor forest-dependent flora and fauna. The long-term stability of populations of forest trees and other organisms (birds, epiphytes, fungi) in traditional cacao plantations also needs to be assessed. Particularly important in the development of an integrated agroecosystem is an evaluation of the selection of species of shade tree and the mode of shade management necessary to optimize farm productivity and biological diversity. Research should include a detailed regional assessment of the use of shade trees by forest organisms of selected major taxa overlaid on information garnered on the silvicultural and agronomic properties of the same tree species. The ability of low-intensity systems to dampen outbreaks of pest and disease organisms and improve pollination levels requires further investigation. Considerable socioeconomic research is necessary to develop a full range of incentives for farmers to grow cacao in a biodiversity-friendly manner, including fair-trade practices, access to preharvest credit, carbonsequestration credits, development of ecotourism, and environmental funds based on taxing agrochemical inputs. Coffee Coffea arabica L. (also C. canephora P., C. liberica Bull ex Hiern. and others) Methods of Production The original C. arabica is native to southwestern Ethiopia and C. canephora var. robusta (also known as C. robusta) to equatorial Africa. C. liberica and a small number of other forms make up a tiny proportion of total production. Arabica is typically grown in cool but frost-free areas at elevations of 500 2000 m, robusta typically from sea level to 1000 m. Production is most successful at elevations of 600 1200 m on steep slopes at the boundary of the tropical and temperate ecotones (Moguel & Toledo 1998). Arabica produces better-quality beans than robusta, although the latter is resistant to the water-borne coffee leaf rust Hemileia vastatrix and so replaces arabica in wetter regions, such as west and central Africa and Asia. The presence of pollinating insects can greatly increase yields, and recent analyses show that the introduction of African bees to Central and South America has increased yields, in some cases by over 50% (Roubik 2002). Detailed descriptions of the structure, development, and ecology of the coffee plant are given by Clowes and Allison (1982) and Cannell (1983). Coffee is the world s second most important commodity in legal international trade after oil (O Brien & Kinnaird 2003), and, with an annual value of $100 billion, the developing world s most important earner of foreign capital. A third of the world s coffee is exported to the United States, where coffee comprises the third largest import after oil and steel. World production is approximately 7 million tons, produced from approximately 11.5 million ha. Coffee represents a crucial source of income for up to 25 million people, largely smallholders. Forty-one countries produced in excess of 10,000 tons of coffee in 2001, and 25 countries produced more than 50,000 tons (Appendix). Latin America produces most of the world s arabica, whereas Asia dominates robusta production. However, plans are in place in Vietnam to rapidly increase arabica production, largely in forested uplands of rich biodiversity. There has been a massive increase in coffee production in Vietnam, which now produces 160 times more than it did in 1961, and a fall in production in Brazil, brought about partly by the destruction of crops by frosts and by the introduction of minimum wage laws

24 Issues in International Conservation Donald that increased the costs of hired labor (Kaimowitz & Smith 2001). Coffee production is dominated by smallholders. In Central America and Mexico, 90% and 98% of coffee enterprises, respectively, are smaller than 10 ha (Rice & Ward 1996). However, larger enterprises hold disproportionate amounts of better-quality land. Despite their small size, coffee enterprises are labor-intensive, requiring around 73 person-days/ha/ year and the efforts of whole families. They are therefore efficient at absorbing human populations. In Colombia nearly 23% of the agricultural labor force is involved in coffee production. A feature of smallholder coffee production is the use of shade trees to provide resources such as building materials and alternative sources of income. In parts of Nicaragua, traditional coffee systems incorporate over 25 species of fruit and timber trees, many of them native, and one study in El Salvador recorded 18 exotic and 119 native tree species in shaded coffee plantations (O. Komar, personal communication). The yield of world coffee plantations depends largely on world coffee prices, fluctuations in which can lead to increases or decreases in the area under and methods of production. The relationship between prices, production, and environment in Mexico was examined by Fuentes Flores (1982) and Nestel (1995), who showed that rising coffee prices during the 1970s and 1980s led to increases in both the area under cultivation and the yield per unit area. There is a strong positive correlation between world coffee prices and rates of deforestation in producing countries (O Brien & Kinnaird 2003). Heavy dependence on a single commodity has led to a history of overproduction by coffee farmers, leading to low prices. Despite a doubling in the cost of living in the United States during the 1970s, the price of coffee remained unchanged. For a while, overproduction was moderated by the International Coffee Agreement, which encouraged participating countries to stockpile surpluses to keep prices high. The collapse of this agreement in 1989 and the removal of quotas led to liberalization of the market, a collapse in prices, and a crisis in the coffee production industry. Coffee can be grown in a wide variety of ways, ranging from nearwild conditions to modern monocultural plantations with high levels of chemical inputs and mechanization. The system employed in any location is the result, not the cause, of sociocultural and economic conditions set within the ecological constraints of limited natural resources (Fuentes Flores 1982). Traditional methods of coffee production involved the planting of coffee bushes under a selectively thinned canopy of existing rainforest trees. These were integrated agroforestry systems, with planters deriving income not only from the coffee but also from the shade trees. Shade cover up to 50% actually increases yields (Soto-Pinto et al. 2000). The presence of shade trees can control pest problems, the optimal levels of shade for doing so varying with climate, elevation, and soils (Staver et al. 2001). Furthermore, the quality and size of coffee beans, and the taste of the finished product, are better under shade systems than under systems with no shade trees (Muschler 2001). Despite the benefits of shade production, there has been a recent trend to full-sun production ( technified production) because on good soils and in favorable climates this method produces higher yields per unit area (although not necessarily per plant). This trend was prompted in part by the arrival in the Americas of coffee leaf rust, which was thought to be controllable with chemicals in the lower humidity of full-sun systems. However, intensive production has led to increased pest problems and secondary pesticide problems (Staver et al. 2001). Control of pests through sustainable, integrated methods has been adopted by only a minority of growers with reserves of capital and access to technological training (Chaves & Riley 2001) Most growers rely on increased pesticide use. Intensification of production has, in most Latin American countries, been supported and encouraged by government, trade, and international aid organizations in a bid to raise production. Such support has been mediated largely through the provision of subsidies, many originating in the United States (the U.S. Agency for International Development has been a major supporter of the modernization of coffee production in Latin America). Shading is now largely employed only where it is necessary to reduce yields to keep production sustainable on poor-nutrient soils, where shadeloving varieties are grown, and where shade trees form part of economic agroforestry systems. Particularly in marginal growing areas, some coffee is grown under modified natural forest cover ( rustic plantations) or under a tall and diverse planted canopy, which greatly reduces weed growth (Nestel & Altieri 1992). In many high-production areas, however, where coffee covers large and continuous blocks, shade plantations are heavily managed, with the canopy being made up of planted, shortstature, usually leguminous nitrogenfixing trees (e.g., Inga, Gliricidia, and Erythrina), which are heavily pruned to maintain a parasol architecture (Greenberg et al. 1997a). Some of these planted shade trees lose their leaves during the dry season, rendering their structure similar to fullsun systems. Replacement of natural forest cover with planted monocultures of shade trees was thought to increase yields, though this may not be the case (Romero-Alvarado et al. 2002). Calvo and Blake (1998) point out that all shade coffee plantations are not equivalent, nor are they likely to be equally beneficial as habitats for birds. Moguel and Toledo (1998) recognized at least five different types of coffee production systems in Mexico, ranging from traditional smallholdings shaded by native trees to larger full-sun systems relying on chemical

Donald Issues in International Conservation 25 Table 2. A summary of some typical characteristics of traditional and modern coffee systems. Traditional Modern Shade cover 60 90% 0 50% Shade trees mixed monoculture Shade tree size tall (25 m), natural short (5 8 m), planted Coffee plant size tall (3 5 m) short (2 3 m) Coffee plant density 1 2,000/ha 3 10,000/ha Yield per hectare low high Yield per tree high low Bean quality higher lower Time to first harvest 4 6 years 3 4 years Productive life >30 years 12 15 years Production scale smallholders larger producers Chemical use none/low high, essential Fertilizer use low high Pruning none/light heavy Labor seasonal year round Irrigation low high Soil erosion low high Soil acidification low high Soil quality high low Air temperature low high Soil temperature low high Leaf litter production high low Incidence of disease low high Insect pollination high low Structural complexity high low Weed cover low high From Rice and Ward (1996), Perfecto et al. (1996), Araroff and Monasterio (1997), Babbar and Zak (1995), Aranguren et al. (1982), Muschler (2001), Roubik (2002), Siebert (2002), Soto-Pinto et al. (2002) and others. inputs and year-round labor. Nestel (1995) maintained that there are too many forms of production to derive a single typology of coffee agroecosystems (Table 2). In parts of Central and South America, much coffee remains in the form of traditional shade-grown systems (Perfecto et al. 1996), although there is a trend toward full-sun production. Of the 2.8 million ha of coffee in Mexico, Colombia, the Caribbean, and Central America, 1.1 million were converted to full-sun production during the early 1990s (Rice & Ward 1996). In Columbia nearly 70% of coffee is now in full-sun systems (Rice & Ward 1996). In Vietnam all coffee is grown in intensive full-sun systems because there is no history of shade production in the country. Technified coffee represents a major cause of deforestation in Vietnam. The ratio of sun to shade coffee depends to some extent on world prices. When prices are high, it pays producers to intensify production because increased yields more than compensate for increased production costs. When prices fall, many producers cannot afford the high inputs of intensive systems and revert to less-intensive systems, often planting shade trees (Greenberg et al. 1997a). In Colombia, rising world prices during the 1970s led to the conversion of 220,000 ha of traditional coffee agroecosystems into low-shade or full-sun production (Nestel 1995), whereas in Mexico, recent falls in coffee price have encouraged coffee growers to convert to other crops such as sugar cane (Nestel 1995; Gallina et al. 1996). Coffee production is associated with some loss of habitat, either of forest or shade coffee plantations, however high or low world prices are. Stabilization of world prices appears to be an effective way of preventing further habitat loss (Nestel 1995; Donald et al. 2004). Low-intensity production systems are generally the most economically efficient at producing coffee and the most profitable (Boyce et al. 1994; Simán, cited in Perfecto et al. 1996). Lyngbaek et al. (2001) examined the yield and profitability of paired organic and conventional coffee farms in Costa Rica. Although average yields were approximately 22% lower on organic farms, the premium prices for organic produce meant that net income was the same when organic certification costs were excluded. The very high costs of certification meant, however, that the premiums paid to organic producers would have to increase by 38% if net income were to reach that of conventional farmers. The conversion of even the most intensive coffee production systems to achieve biodiversity-friendly certification criteria is likely to be financially viable (Gobbi 2000). Impacts on Biodiversity As early as the 1930s, conservationists were aware of the potential

26 Issues in International Conservation Donald biodiversity benefits of shade coffee. Griscom (1932) described the collection of birds in Guatemala in the 1920s and 1930s in shaded systems:...the avifauna was little, if any, different from its original condition. Threats to wildlife posed by the conversion of shade coffee to fullsun production systems were first discussed in detail by Borrero (1986). As with cocoa, coffee-growing areas fall largely within areas identified as biodiversity hotspots (Myers et al. 2000). This means that, despite its relatively small global area (approximately the same as that of Cuba), coffee has an impact on biodiversity disproportional to its area. Most coffee is grown on land formerly under forest, so coffee production has historically been a cause of deforestation. In Central and South America, coffee plantations make up some 54% of the permanent croplands that have replaced cloud and premontane rainforests (Roberts et al. 2000b). However, in many areas that have suffered severe deforestation, shade coffee systems may now represent an important refuge for forest biota (Brash 1987; Perfecto et al. 1996; Komar 1998). I found few quantitative studies outside the Americas comparing biodiversity between shaded and intensive coffee systems and between shaded coffee and pristine forest (Table 1). As with cacao, this metaanalysis showed that shaded systems are generally preferable to unshaded systems, that shaded systems are comparable to pristine forest for nonspecialist taxa, and that forest specialists ( particularly forest raptors, terrestrial insectivores, and large frugivores) tend to suffer from any conversion of primary forest. The results are consistent with the general ecological principle that species richness and diversity increase with increasing structural and floristic diversity of the habitat but also suggest that the structure of communities changes with increased habitat disturbance. Even the most structurally complex shade systems support bird communities that differ in guild and species composition from pristine forest (e.g., Greenberg et al. 1997a,b). Shade systems vary greatly in their suitability as wildlife habitats, depending on the species of shade trees, size of the fragment, and the fragment s distance from remaining forest. A number of researchers (Greenberg et al. 1997a; Wunderle & Latta 1998; Johnson 2000; Johnson & Sherry 2001; Soto-Pinto et al. 2001) have shown that structurally complex and flower-rich shade trees, such as Inga, support higher biodiversity than structurally simple trees such as Gliricidia. Canopy management of shade trees and the species richness of shade trees are also important determinants of the biodiversity value of shaded coffee systems (e.g., Calvo & Blake 1998). Choice of shade trees in coffee plantations is based on a number of criteria (Beer et al. 1998). Wunderle (1999) modeled variation in the abundance of migrant and resident bird species in shade-coffee plantations in the Dominican Republic in terms of habitat structure, elevation, patch size, and isolation. Migrant species responded only to elevation, whereas resident birds responded positively to larger and older plantations at lower elevations and plantations with numerous larger stems, little or no pruning of upper branches, and high maximum canopy cover. In Panama as the distance from remaining forest increases, the bird communities of shaded coffee plantations become increasingly different from those in forests or forest-edge plantations (Parrish & Petit 1995). This change was the result of an increasingly migrantdominated bird community in more distant plantations. Discussion about the relative conservation merits of coffee plantations vary according to initial stance. In landscapes with little natural cover left, shade-coffee plantations represent a vestige of more complex habitats, support high biodiversity relative to surrounding landscape types (e.g., Brash 1987; Perfecto et al. 1996, 2003; Greenberg et al. 1997a,b; Moguel & Toledo 1998; Sherry 2000), and can support large numbers of threatened species (Dietsch 2000). However, coffee is a net contributor to deforestation, and isolated coffee plantations cannot be considered a sufficient ecological replacement for large tracts of pristine forest. The trend toward intensification of coffee production has led to a loss of structural vegetation diversity due to clearance of shade trees and to increases in environmental pollution. Heavy and generally under-regulated pesticide use is an integral part of fullsun systems and includes chemicals such as chlordane, endosulfan, and DDT, which are banned in the countries that consume the most coffee (Rice & Ward 1996). Poisoning from pesticide contamination is common among plantation workers, stemming largely from lack of training and lack of awareness of their dangers (Popper et al. 1996). Furthermore, intensification and loss of shade trees necessitates high inputs of nitrogenous fertilizers (around 300 kg N/ha/year in Costa Rica). Full-sun plantations leach nearly three times the amount of nitrates into surrounding environments than shade coffee systems (Babbar & Zak 1995). The processing of coffee also has environmental consequences. The process of separating the coffee beans from the fruits generates huge volumes of pulp, usually disposed of directly into waterways, which leads to pollution of fresh water bodies and coastal regions near river mouths. The loss of biodiversity in increasingly intensive systems is likely to have negative feedback on production. Formerly considered selfpollinating, coffee has recently been shown to have greatly increased yields where there are abundant pollinating insects. The arrival in Central America of introduced African bees has led to a significant increase in yield, in some places by over 50% (Roubik 2002). In Indonesia, fruit set of highland coffee increases with the species diversity of pollinating bees,

Donald Issues in International Conservation 27 rising from 60% in the presence of three bee species to 90% where 20 bee species are present (Klein et al. 2003). In this example, diversity and not abundance explained variation in fruit set. This has clear implications for the conservation of biodiversity because the loss of biodiversity will result in a loss of pollinators. Research elsewhere has shown that pollinating bees occur at highest densities in the presence of large trees (Liow et al. 2001). Retaining areas of natural forests and shade trees within or adjacent to coffee plantations will ensure the persistence of pollinating insects. Concern in North America about losses of habitat for wintering migrant birds (e.g., Robbins et al. 1989) has led to greatly increased marketing of organic, fair trade, bird friendly, and other more environmentally and socially aware coffees (Messer et al. 2000). This culminated in the drafting of a comprehensive set of guidelines Conservation Principles for Coffee Production by a number of U.S. conservation organizations in June 2001 (see http:// www.consumerscouncil.org/coffee/ principles index.htm). These principles include elements of nature conservation, soil and water conservation, and sustainable livelihoods for farmers. Markets for conscience coffees remain small compared with total consumption (Messer et al. 2000), but the massive increase in global demand for specialty or gourmet coffees represents a possible mechanism to deliver environmental and social benefits, not least because the slower ripening of shade coffee produces a higher content of flavor-bearing oils. Organic coffee represents the fastest-growing sector of the specialty coffee market, and the Specialty Coffee Association of America has established an Environmental Policy Task Force. Although making up only 5 7% of the current market, organic coffee is expected to reach 10% in the near future. In Europe, where the connection between coffee and conservation is less immediate (African coffee plantations are not considered an important habitat for European migrants), there is far less emphasis on environmentally friendly production or brands. The marketing of environmentally friendly coffee is not the only driving force in the protection and enhancement of traditional coffee production methods (Perfecto et al. 1996). Formerly geared at modernizing coffee production, projects funded by international aid, such as PROMECAFE, are increasingly seeking ways to support sustainable coffee production. Furthermore, there is a move to provide farmers with incentives that would enable smallholders to compete with larger production enterprises on the grounds that they are acting as stewards of the environment. Fair-trade movements support traditional coffee production in many parts of the world through the International Coffee Register (ICR), a democratic association of 300 cooperatives representing the interests of half a million smallholders. The register certifies fair-trade practices that include the provision of credit and advice on organic production to smallholders. A further driver of making traditional systems preferable to intensive production would be the internalization of environmental costs. Currently, producers do not meet the pollution costs of intensive production. Internalization of such costs would make ecologically sustainable systems more attractive. The recent massive increase in coffee production in Vietnam, Indonesia, and Papua New Guinea is of considerable environmental concern (Siebert 2002). It is highly unlikely that such growth rates and high yields could be achieved without considerable damage to existing habitats, and much current deforestation in Southeast Asia is due to coffee planting. Most of these new plantings are fullsun, robusta systems because there is no tradition of shade production in, for example, Vietnam. An increase in demand for cheap robusta coffee, which might originate in countries such as Russia, Eastern Europe, and China that are in transition from tea to coffee consumption, would spur further loss of lowland tropical forests for coffee growing in Southeast Asia. Increased demand for arabica might, on the other hand, take pressure off lowland forests, which are most threatened. Although traditionally a robusta growing area, Vietnam is rapidly increasing its area of arabica and hopes to become the world s largest producer. Research Requirements Rice and Ward (1996) list a number of priorities for future research on the relationship between coffee and the environment in Latin America: (1) determine the current spatial distribution of traditional, shaded-coffee areas; (2) research the relative benefits of different shade-tree species; (3) research appropriate levels of thinning or pruning of shade trees to maximize biodiversity; (4) investigate the characteristics of different shade-tree species, such as flowering or fruiting patterns, to determine the optimal mix; (5) further compare environmental protection measures between sun and shade stands; (6) conduct market analysis for environmentally friendly coffee; (7) estimate the external costs of coffee production; and (8) conduct economic comparisons of different production systems at the farm level. In the 8 years since Rice and Ward listed these priorities for research, few have been addressed. Many of these research needs apply equally to producing countries outside the New World, where the level of knowledge is generally far lower. My review suggests a number of other research priorities, including (1) assessment of which habitats are being lost to new coffee planting, particularly in regions of massive new planting; (2) evaluation of the breeding success and persistence of forest taxa in shade coffee stands and forest remnants; and (3) basic research into coffee production methods and their effects on biodiversity outside Latin America.

28 Issues in International Conservation Donald Rice Oryza sativa L. (also O. glaberrima Steud.) Methods of Production Native to the tropics and subtropics of Southeast Asia, rice is an erect annual grass that grows up to 1.2 m tall. It can survive in a wide range of rainfall and temperatures, allowing its spread to many parts of the world. However, in dryer areas it requires irrigation (in terraces in upland rice systems) or permanent inundation (lowland rice). Each ton of rice produced in this way requires 2000 tons of water. It is now grown from northern Japan (42 N) to Queensland (23 S). It is grown mostly in humid coastal lowlands and deltas, where the soil holds water well, and shows little frost tolerance. Two of the approximately 25 known species of rice are cultivated commercially, Oryza sativa and O. glaberrima. Because of intensive selection, many localized varieties have been replaced by a few commercially successful cultivars. Around 40% of the world s population depends on rice for their survival (Fasola & Ruíz 1997). A fundamental change in global rice farming began in the mid-1960s with dissemination of the first high-yield varieties. These variations on traditional cultivars (often called MV or modern varieties) could produce over twice the yield of older varieties. This green revolution, hailed then as a timely miracle to prevent famine, has benefited many rice producers and led to an intensification of production methods. Rice is grown primarily for the grain. It is the world s most widely cultivated crop, covering 1.55 million km 2, which is over 11% of the world s total arable land, over 3% of its total agricultural land, and over 1% of its total land surface. Global rice production in 2000 approached 600 million tons, an increase of nearly 180% since 1960 (Appendix). This increase has been brought about largely by increases in yield, although the total area of production has also risen by over 25% since 1960. Unlike coffee and cocoa, which are grown largely for export, much rice production is intended for home consumption. The main exporters of rice are Thailand (6.8 million tons, 30% of total production), Vietnam (4.6 million tons, or 14% of total production), China (2.8 million tons, or 1.5% of production), the United States (2.7 million tons), India (2.6 million tons), and Pakistan (1.8 million tons). Rice is produced in many ways, ranging from dry fields (50% of all rice production) through seasonally flooded fields to deep permanent inundation. In Japan fields are flooded to a depth of 10 15 cm in April, and seedlings are planted soon after. Fields are drained toward the end of June to allow the surface to harden sufficiently for harvesting machinery to enter the field. After this, fields are either reflooded and drained or left permanently undrained until harvest. In the Camargue of southern France, fields are also flooded to a depth of 20 30 cm in April or May, just before sowing. Fields are sown either with seed (e.g., United States) or with cultivated seedlings (Asia). As with other arable crops, continual cropping soon depletes soil fertility, so rice is grown in rotation with a wide variety of other crops, such as soybeans, bananas, sugar cane, and corn. Nitrogen applications up to 90 kg/ ha increase yields, but beyond this there is little benefit. Once seedlings are rooted, water levels are periodically reduced, and fields are dried completely some days before harvesting. Harvesting takes place in September or October with combines or by hand. Post-harvest stubble is usually burned or plowed in. Some fields are flooded over winter to provide a refuge for water birds for shooting, but most remain dry. Impacts on Biodiversity The effects of rice production on biodiversity vary with production methods, which include fields managed organically or with agrochemicals and varied irrigation and planting systems and winter management regimes. A recent change in rice production in Japan has been the replacement of old irrigation systems that diverted water from rivers into paddies with more modern systems in which water is pumped through underground pipes directly into paddies that drain off into concrete-sided canals (Hasegawa & Tabuchi 1995). These new irrigation methods now comprise 80% of total rice production in Japan and may restrict the movement of fish and other aquatic wildlife into paddies (Narusue & Uchida 1993; Fujioka & Lane 1997; Katano et al. 2003). Conversion to rice production has been one of the main causes of loss of natural wetlands. In many areas, natural wetlands have been completely replaced by rice production. For example, the internationally important waterfowl populations wintering in California s central valley are increasingly depend on rice agriculture for their survival (Reid & Heitmeyer 1995). As a result, a number of researchers have compared biodiversity on rice fields with those on natural wetlands, and others have examined the biodiversity implications of different forms of rice production. Results of these studies suggest that traditional systems are ecologically preferable to modern systems and that traditional systems can be as good as or less desirable than natural wetlands (Table 1). Variations in rice management systems can have profound effects on the ecological suitability of rice fields (Lawler 2001). Management techniques known to affect the ecological suitability of the resulting rice fields include water management, pesticide use, and fish population management. Intermittent flooding to control pests reduces biodiversity benefits compared with prolonged flooding methods. Although crop diversity is low, traditional paddies are ecologically diverse in two respects (Power & Flecker 1998). Systems that are managed more traditionally hold high genetic diversity in the form of many hundreds of traditional varieties of rice. This genetic diversity means that rice has been relatively resistant to pests and disease, reducing the need

Donald Issues in International Conservation 29 for pesticides (Roger et al. 1991). Furthermore, wetland rice systems support a high number of aquatic species. Traditional rice systems are sufficiently complex ecosystems that a wide range of organisms can be harvested from them. These include plants, fish, molluscs, and crustacea. Indeed, traditional systems often rely on a fish-rice polyculture to provide maximum returns. Although high fish populations can depress numbers of other taxa, their presence greatly reduces the need for pesticide applications (Lawler 2001). Changes in management have led to decreased genetic diversity, however, as traditional varieties have been replaced by a small number of high-yield varieties, which require the application of high doses of pesticides, and to a reduction in wetland diversity as irrigation systems have been simplified. This has led to a reduction in biodiversity in rice fields (Roger et al. 1991) and the consequent emergence of a number of new pest types (Wilby & Thomas 2002). Modern intensive rice production relies on the use of pesticides to compensate for the natural pest and disease resistance of genetically more variable traditional crops. Rice seed treated with insecticides posed a severe threat to foraging wildfowl during the 1960s, when chemicals such as aldrin were still in widespread use. Declines in waterfowl populations in Texas were ascribed to direct poisoning with aldrin (Flickinger & King 1972). More recently, treatment of sown rice with poisons designed to kill birds appears to have relatively little impact on nontarget species (e.g., Cummings et al. 2002), and nonlethal chemical repellents are now available (Avery et al. 2001). Rice fields are also major producers of methane, a greenhouse gas that traps around 20 times more energy than carbon dioxide. Rice fields may produce as much methane as all the world s natural wetlands combined, although exact quantification is problematic (Van Bodegom et al. 2002). A number of techniques to reduce methane emission from paddy rice have been developed, including water management, organic amendments, use of sulfate-rich fertilizers, and the selection of appropriate cultivars. Although each may have an effect individually, a combination of mitigation measures is likely to achieve the best results (Majumdar 2003; Singh et al. 2003). An unusual consequence of the intensification of rice production systems is a growing threat to the conservation of the crop itself. Rice occurs in many varieties, some of them probably subspecifically or even specifically distinct, and rice is therefore a crop with an unusually high genetic diversity (Gao 2003). This diversity allows farmers to grow the crop in heterogeneous environments and provides a valuable genetic repository for future varieties. Recommendations to intersperse traditional and hybrid varieties in China have led to a resurgence in the use of traditional varieties, including some that were previously locally extinct (Zhu et al. 2003). Little is known about the effects on biodiversity of the transformation of natural habitats to rice production systems. However, even populations of amphibia, a dominant group in rice systems, appear to suffer. Vallan (2002) found that conversion of tropical forest to rice fields led to an 88% decline in species richness. Research Requirements Most of the quantitative studies comparing rice production in traditional and intensive systems derived from work on lowland paddy rice. Little information is available with which to assess the biodiversity impacts of changes in rice production in hill rice systems. Oil Palm Elaeis guineensis Jacq. Methods of Production The oil palm, a native of West Africa, is generally grown at low elevations in wet tropical zones 10 on either side of the equator. Per unit area, oil palm is the highest-yielding vegetable oil crop in the world. The oil is used in the manufacture of cooking oil, margarine, soap, and cosmetics, and it has industrial uses. Commercial oil production is possible within 2 years of planting, and trees have a long productive life of up to 30 years. Oil palm has become one of the world s largest plantation crops, with individual plantations sometimes exceeding 20,000 ha. Palm oil now makes up about 21% of world production of edible oils and fats, second only to soybean oil. Current global production of oil palm fruit is 97.7 million tons, produced from 10.7 million ha (Appendix). The dominance of Asia in global palm oil production is relatively recent, Malaysia and Indonesia overtaking Nigeria as recently as the 1970s. Palm oil is Malaysia s second largest export earner, and oil palm plantations comprise 56% of the country s forest and woodland cover (Appendix). Oil palm requires high maintenance, and attempts to mechanize production have met with little success. The bulk of production is therefore undertaken in countries with low wages. Oil palm plantations consume large amounts of agrochemicals. Although active oil palm plantations themselves have relatively little environmental impact, the deforestation that precedes planting is likely to be a major environmental problem (World Wildlife Fund Malaysia 2000). In the main producing countries, oilpalm planting represents the major cause of loss of natural forests and traditional mixed agroforestry systems (e.g., McMorrow & Talip 2001). Population declines of endangered species such as the Sumatran orangutan (Pongo abelii) are being driven largely by loss of forests to oil-palm plantations (Robertson & van Schaik 2001). Threatened habitats include the Choco Forest in Ecuador, one of the most biodiverse regions in the world, and forests in Papua New Guinea, Indonesia, and Malaysia. Oilpalm plantations are replacing natural forests and sustainable sources

30 Issues in International Conservation Donald of commodity production, such as sago (Metroxylon sagu) (Chew et al. 1999). The burning of forests to plant oil palms has caused significant atmospheric pollution. In Sarawak, for example, the air pollution index (API) regularly exceeds 500, a level at which residents are supposed to be evacuated. Fires started deliberately in Indonesia in 1997 to clear primary forest for new plantations burned out of control, destroying more than 5 million ha of forest and existing plantations and caused significant smoke and air pollution, many deaths, and several billion dollars worth of damage (see http://www.mongabay.com/ 08indo fires.htm). Malaysian government officials are attempting to get oil-palm plantations recognized as forest in official statistics, claiming that plantations offer environmental benefits such as carbon sequestration, biodiversity conservation, and timber production. The fibrous trunk of oil palms has little use in timber production, however, and old trees are generally poisoned and either left to rot or burned, releasing carbon back into the environment. The waste products of oil-palm-plantations take up large amounts of biologically active oxygen, which causes a drop in the oxygen content of any water these waste products enter (effluent from palm-oil mills has an oxygen-depleting power over 100 times greater than that of domestic sewage). This can lead to the extinction of fish, plants, and other aquatic organisms. In Malaysia, steps have been taken to ensure that mill waste is treated and not put directly into natural water bodies, but pollution from oil-palm processing is equivalent to that generated by 1.5 million people. Impacts on Biodiversity There are few published quantitative comparisons of biodiversity in oilpalm plantations with that in other land-use types. Power and Flecker (1998); Chung et al. (2000), and Glor et al. (2001) examined vertebrate ( bird and lizard) and invertebrate ( beetle and ant) faunas in a number of agricultural land-use types. These studies showed that oil-palm plantations supported extremely low numbers and diversity of birds compared with shaded cacao, pasture, and natural forest. Lizard abundance in oil-palm plantations was higher than in active pastures, the same as in shade cacao stands, and only marginally lower than in pristine forest. However, species diversity was low (Glor et al. 2001). Beetle assemblages in oil-palm plantations were considerably more impoverished and more dominated by a few common species than those in acacia plantations or logged forest. Furthermore, there were fewer predators and more herbivores in the beetle communities of oil-palm plantations, with implications for natural pest control (Chung et al. 2000). Low predatory beetle populations might explain the high populations of Chrysomelid pests in oil-palm plantations (Mariau 1999). Ant species richness was lower in oil-palm plantations than in pastures, shade cacao, or pristine forest, but overall ant abundance, though low compared with that of open pastures, was similar to that of natural forest. Ant species overlap was high between oil palms, shade cacao, and natural forest (Glor et al. 2001). In a comparison of ant populations in a number of different habitats in Papua New Guinea, monocultural oil-palm plantations held the lowest species richness of any (Room 1975). Replacement of natural forest by shaded cacao systems had a significantly less adverse impact on wildlife than the replacement of forests by oilpalm plantations (Power & Flecker 1998). In Sumatra, conversion to oil palm resulted in communities of vertebrate taxa that were simple and speciespoor, with low diversity, few specialized species, and few species of conservation importance (Danielsen & Heegaard 1995). Less than 10% of the original primary-forest bird species remained in oil-palm plantations. Tree shrews, squirrels, and all but one species of primate disappeared completely. Bat species richness declined by over 75%, and the species composition changed. Species composition changed by over 60% in all vertebrate taxa examined. The authors concluded that oil-palm plantations hold nothing of importance to biodiversity conservation, but oil palm might contribute to the abundance of a few taxa within plantations and in adjacent habitats. Numbers of some large-bodied snakes, such as pythons, increase with the numbers of their main prey, commensal rodents, in oil plantations in Sumatra (Shine et al. 1999). In Malaysia, Ickes (2001) found extremely high populations of wild pigs (Sus scrofula) in forest fragments surrounding oil-palm plantations. Their presence was attributed to the extinction of natural predators through fragmentation and the abundant food in the form of fallen oilpalm fruit in the adjacent plantations. Extremely high densities of foragers such as pigs may be detrimental to forest structure. Certain primates also appear able to use oil-palm plantations (Williams & Vaughan 2001), although whether this is to a greater or lesser extent than their use of other habitats is unclear. The area of land converted to oilpalm production seems set to rise. In Indonesia a 20-fold increase in oilpalm area between 1967 and 1997 slowed during the late 1990s for a number of economic, social, and climatic reasons (Casson 2000). A return to boom production is expected, however, because many of the economic brakes have been reversed. In Kalimantan, local governments are supporting the expansion of oil-palm plantations because they are seen as the best option to generate income and development (Potter & Lee 1998). Smallholder rubber producers are being bought out by oil-palm companies, who give in return a small allotment of oil palm that is planted according to company specifications and processed in the company s mill (Potter & Lee 1998). Although falling

Donald Issues in International Conservation 31 prices may dissuade oil-palm companies from much more planting in the near future, massive global markets and quick profits mean that oilpalm production is likely to increase. Indonesia in particular plans to become the world s largest producer of palm oil, and increases in area are likely to be largely at the expense of primary forests. Local administrations and oil-palm companies view environmental losses as a price worth paying for profits and jobs, and social pressure might provide the main impetus for reducing the spread of oil-palm plantations. In many of the main oil-palm-producing states, there is open, popular opposition to increasing the area of plantations. In Sarawak, for example, this has led to violence between the local Iban with hereditary land rights and workers of oil-palm companies encroaching on their land (http://www.wrm. org.uy/bulletin/27/malaysia.html). Similarly, there is increasing conflict between smallholders and estate owners in Côte d Ivoire. Recognition by largely western consumers of the problems of deforestation caused by oil-palm plantations has led to the recent development of environmental standards. The World Wide Fund for Nature has, in conjunction with major European importers, developed criteria for environmentally sustainable oilpalm plantations. These discourage the planting of new plantations on recently deforested land and the illegal acquisition or appropriation of land and encourage certification for good practices, the retention of wildlife areas and corridors, and targets to minimize impacts on soil and water. Research Requirements Given the importance of oil palm as a threat to biodiversity, surprisingly little research has been carried out to quantify biodiversity loss associated with conversion of different habitats to oil palm or the biodiversity impacts of different management systems. Soybean Glycine max L. Methods of Production The soybean is a legume originating from China. It is a bushy annual with a stem up to 1.8 m tall. It is an extremely variable plant with many varieties. Soybeans prefer well-drained, fertile soils but also grow better than most other crops on soil that is infertile, droughty, or poorly drained. The plant is propagated as seed, preceded by weed control. A number of insect pests of soybeans are routinely controlled by spraying. The soybean is now one of the world s most important sources of protein, the seeds containing up to 50% protein. Soybean seeds have many uses: products include highprotein flour and flour enrichers, tofu, meat substitutes, soy milk, animal feed, and oil (used, among other things, in the manufacture of paints, cosmetics, and soap). The vegetative portion of the plant is used for animal fodder, manure, and paper manufacture. Soybeans produce 15 20 times the amount of protein than can be produced from the same area in beef production. Global soybean production in 2001 was estimated at 172 million tons, nearly 90% of it coming from just four countries (Appendix). Production in all four countries has increased greatly since 1961, particularly in Argentina and Brazil, where production has increased more than 100- fold. This has been brought about by huge increases in the area cultivated and a more than doubling of yields per unit area. Part of the reason for the huge increases in production in Brazil and Argentina has been a gradual shift away from production in temperate zones to tropical areas where land is cheaper, the growing season longer, and labor requirements spread more evenly throughout the year (Fearnside 2001). These increases have been fueled by huge increases in producer prices, which have made soybean farming more profitable. Increased prices have resulted partly from the collapse of the Peruvian anchovy fisheries in the 1970s and droughts in the United States, both leading to a world shortage of animal fodder. China is the world s largest importer of soybeans and soybean products, a market that has encouraged the rapid proliferation of soybean growing in Brazil. The international soybean market consists of three products: whole soybeans, soy oil, and soy meal. Much of the oil is exported to Asia and much of the meal to Europe for animal fodder. Trends in soybean production reflect trends in global markets. In Brazil at least, this makes soybean production different from other forms of land-use conversion, such as ranching and logging (Fearnside 2001). Ranching has been largely motivated by ulterior motives such as land tenure and subsidies, and even logging has been determined mostly by local markets. Government subsidies for soybeans have speeded the spread of the crop even faster than would have happened through market forces alone. Being a legume, soybean plants have nitrogen-fixing nodules in their roots, although the correct bacteria need to be present in the soil for nitrogen fixation to take place. An important element in the rapid spread of soybean production in Brazil was the development of soybean-bacteria combinations with pseudosymbiotic relationships that allowed soybean plants to be planted without the need for nitrogenous fertilizers. Weed control is important early in the growing season and is carried out chemically, mechanically, or by hand. Impacts on Biodiversity The environmental consequences of soybean production in Brazil have been discussed and reviewed in detail by Fearnside (2001), who regarded soybeans as a recent and severe threat to tropical biodiversity. Fearnside identified two elements to the environmental threats posed by soybean production: the loss of

32 Issues in International Conservation Donald natural habitats to soybean production and the loss of habitats to other factors made possible by the infrastructure associated with soybeans. In Brazil much of the soybean planting has been on natural grasslands, such as cerrado, the world s most biodiverse savannah habitat. The remaining cerrado has a biodiversity importance similar to Amazonian rainforests, and the ecotone between cerrado and forest, which is particularly threatened, has a higher number of endemic plant species than either. More recently, production has spread into Amazonia, where soybeans are planted on land already felled by small-scale farmers who joined those displaced by soybean production to move on and clear forest elsewhere (Carvalho 1999, cited in Fearnside 2001). The profitability of soybeans in Brazil has led to the improvement or construction of eight industrial waterways, three railway lines and an extensive network of roads to bring in inputs and take away produce (Fearnside 2001). These have attracted private investment in logging, ranching, and other practices with severe impacts on biodiversity that are not accounted for in current environmental impact statements in Brazil. External costs of soybean production include displacement of former land occupiers, chemical pollution, soil erosion and exhaustion, extreme income concentration, social disparity, and the diversion of government subsidies that could otherwise be directed to education and health. Employment on soybean farms is minimal (as low as one worker per 200 ha of soybeans). Growth in the soybean industry has slowed development of the babassu palm (Attales spp.) industry. The babassu palm, a rainforest tree, sustainably produces oil and products for fodder and building. It represents a sustainable form of tropical forest use (Balick 1987). Another environmental implication of soybean production is soil erosion and depletion. Hoogmoed and Derpsch (1985) documented soil erosion on land recently converted from coffee to soybeans after the coffee plants were killed by frost. Soil erosion was estimated at over 400 tons/ha/year, and soybean production generates more soil erosion than most other crops. Fertilizers are leached from soybean production systems into local water supplies. Increases in nitrogen and phosphorous in the Mississippi River Basin are likely the result of an increase in soybean production in the river s watershed (Donner 2003). Conversion of uncultivated pasture to soybeans results in a fall in the diversity of economically important rhizobia (Coutinho et al. 1999). Future trends in soybean production will be determined by future demand. In particular, import demand from China will be of considerable importance. Because production in the United States is likely close to capacity, future demands from China will have to be met mostly from expanding areas in Latin America (Fearnside 2001). The soybean area in Latin America is likely to increase until supply exceeds demand, bringing prices down, or until South American governments place limits on soybean area for reasons of price control, social or environmental costs, or the burden of subsidies. Research Requirements There appear to be no quantitative studies of the biodiversity value of soybean growing areas or comparisons of biodiversity with the habitats they replace. However, their relatively intensive management, which is likely to become more intensive with the introduction of transgenic herbicide-resistant crops (Fearnside 2001), means that soybean crops are unlikely to harbor much important biodiversity. A comparative assessment of the biodiversity in soybean crops and an examination of factors explaining such variation are necessary if less intensive and more biodiverse soybean production systems are to be developed and promoted. Conclusions Massive increases in production of all five of the commodities I examined have been achieved by increases in both the area planted and in the yield achieved per unit area. The former has resulted in massive loss of natural habitats, the latter in the intensification of production methods. For each crop examined, each of these two separate elements of productivity increase results in environmental degradation and the loss of biodiversity. An approximately equal number of quantitative studies demonstrated no loss of biodiversity following conversion of natural habitat to low-intensity production as demonstrated an adverse effect (37 as opposed to 31 cells in Table 1). This simple comparison does not take into account the types of taxa involved, and habitat specialists are clearly more susceptible to disturbance of natural habitats than generalists. All 13 studies of bird populations demonstrated declines in forest-specialist species after conversion from forest to shade coffee or cocoa. The reasons for this are unclear, but they probably relate to a combination of reduced habitat complexity, increased disturbance, and the effects of fragmentation. It is clear, however, that the conversion of natural habitats to lowintensity production does not always result in a loss of biodiversity across all taxa, and some taxa might even benefit. In contrast, the majority of studies comparing biodiversity and other ecological attributes in lowand high-intensity systems demonstrate clear loss as systems intensify (42 cells in Table 1, as opposed to just 3 cells demonstrating no measurable effect). A general trend across most taxa is that the least-intensive systems support greater species richness, though not necessarily abundance. At their most extreme, intensive systems support simple communities, dominated by a few generalist species that may become serious pests of the crop.

Donald Issues in International Conservation 33 Two strategies exist to increase agricultural production: clearing natural habitats to plant new crops or intensifying output from existing crops. The clearance of pristine natural habitats for commodity production systems remains one of the greatest threats to global biodiversity. Within such commodity production systems, however, it is clear that the level of management can play an important part in determining the resulting loss of biodiversity. This review suggests that, for some crops, the loss of pristine habitats to lowintensity commodity production systems often has less of an impact on the environment than the intensification of those systems. In other words, biodiversity often differs less between natural habitats and lowintensity production systems than it does between low- intensity and highintensity systems. For crops such as coffee, cocoa, and rice, increased demand might be met with the lowest impact on biodiversity by increasing the area of low-intensity cropping. For other crops, such as oil palm and soybean, there are currently no production methods that come close to matching natural habitats in terms of biodiversity. For these crops, future demand might be achieved with least impact on biodiversity by seeking to raise yields in existing cropping systems. Acknowledgments I thank D. Cleary for tracking down and copying many of the references cited in this report and Ian Dawson and Lynn Giddings for getting hold of copies of the rest. Many people provided useful information and discussion, particularly R. Green, A. Balmford, P. Fearnside, R. Reitsma, various staff at Empressa Brasileira de Pesquisa Agropecuária (EMBRAPA), J. Parrish, D. Rice, S. Ratay, J. Lindsell, C. Tejeda-Cruz, C. McIntosh, C. Melo, D. O Keefe, D. Russell, R. MacLeod, F. Ortiz Crespo, H. Bartram, A. Luy, G. Wood, A. Pedersen, H. Bouwman, C. Sharpe, H. Rainey, D. Wege, K. Shurcliff, A. Napier, R. Grimmett, D. Melville, D. Pomeroy, R. Allan, P. Holt, T. Dodman, J. Pilgrim, P. Round, S. Marsden, F. Lambert, P. Wood, and T. Brooks. The paper was greatly improved by comments from O. Komar, J. Ginsberg, and an anonymous referee. Paul F. Donald Royal Society for the Protection of Birds, The Lodge, Sandy, Bedfordshire SG19 2DL, United Kingdom, email paul.donald@rspb.org.uk Literature Cited Aguilar-Ortiz, F. 1982. Estudio ecologico de las aves del cafetal. Pages 103 127 in E. Jiminez-Avilla and A. Gomez-Pompa editors, editors. Estudios ecologicos en el agroecosistema cafetalero. Instituto Nacional de Investigaciones sobre Recursos Bioticos, Veracruz, Mexico. Alger, K. 1998. The reproduction of the cocoa industry and biodiversity in southern Bahia, Brazil. Proceedings of the Smithsonian Migratory Bird Centre Cacao Conference. Smithsonian Institution, Washington, D.C. Available from http://nationalzoo.si. edu/conservationandscience/migratory birds/research/cacao/papers.cfm (accessed November 2003). Alger, K., and M. Caldas. 1994. The declining cocoa economy and the Atlantic Forests of southern Bahia, Brazil: conservation attitudes of cocoa planters. The Environmentalist 14:107 119. Alves, M. C. 1990. The role of cocoa plantations in the conservation of the Atlantic forests of southern Bahia, Brazil. M.S. thesis. University of Florida, Gainesville. Aranguren, J., G. Escalante, and R. Herrera. 1982. Nitrogen cycle of tropical perennial crops under shade trees. Plant and Soil 67:247 258. Araroff, M., and M. Monasterio. 1997. Soil erosion under different management of coffee plantations in the Venezuelan Andes. Soil Technology 11:95 108. Armbrecht, I., and I. Perfecto. 2003. Littertwig dwelling ant species richness and predation potential within a forest fragment and neighbouring coffee plantations of contrasting habitat quality in Mexico. Agriculture, Ecosystems and Environment 97:107 115. Avery, M. L., E. A. Tillman, and C. C. Laukert. 2001. Evaluation of chemical repellants for reducing crop damage by Dickcissels in Venezuela. International Journal of Pest Management 47:31 314. Babbar, L., and D. Zak. 1995. Nitrogen loss from coffee agroecosystems in Costa Rica: leaching and denitrification in the presence and absence of shade trees. Journal of Environmental Quality 24:227 233. Balick, M. J. 1987. The economic utilization of the babassu palm: a conservation strategy for sustaining tropical forest resources. Journal of the Washington Academy of Sciences 77:215 223. Balmford, A., and A. Long. 1994. Avian endemism and forest loss. Nature 372:623 624. Beer, J., R. Muschler, D. Kass, and E. Somarriba. 1998. Shade management in coffee and cacao plantations. Agroforestry Systems 38:139 164. Benitez, J., and I. Perfecto. 1990. Efecto de diferentes tipos de manejo de cafe sobre las comunidades de hormigas. Agroecologia Neotropical 5:11 15. Borrero, J. I. 1986. La substitucion de cafetales de sombrio por caturrales y su efecto negativo sobre la fauna de vertebrados. Caldasia 15:725 732. Boyce, J. K., A. Fernandez Gonzales, E. Furst, and O. Segura Bonilla. 1994. Café y desarrollo sostenible: del cultivo agroquimico a la produccion organica en Costa Rica. Editorial Fundacion Universidad Nacional, Heredia. Brash, A. R. 1987. The history of avian extinction and forest conversion on Puerto Rica. Biological Conservation 39:97 111. Cabala-Rosand, P., C. J. L. de Santana, and E. R. de Miranda. 1976. Respuesta del cacaotero al abonamiento en el sure de Bahia, Brasil. Technical bulletin no. 43, Centro de Pesquisas do Cacau, Comissão Executiva do Plano da Lavoura Cacaueira, Itabuna, Brazil. Calvo, L., and J. Blake. 1998. Bird diversity and abundance on two different shade coffee plantations in Guatemala. Bird Conservation International 8:297 308. Canaday, C. 1997. Loss of insectivorous birds along a gradient of human impact in Amazonia. Biological Conservation 77:63 77. Cannell, M. G. R. 1983. Coffee. Biologist 30:257 263. Casson, A. 2000. The hesitant boom: Indonesia s oil palm sub-sector in an era of economic crisis and political change. Occasional paper no. 29. Center for International Forestry Research, Bogor, Indonesia. Chaves, B., and J. Riley. 2001. Determination of factors influencing integrated pest management adoption in coffee berry borer in Colombian farms. Agriculture, Ecosystems and Environment 87:159 177. Chew, T. A., A. B. Isa, and M. G. bin Mohayidin. 1999. Sago (Metroxylin sagu Rottboll), the forgotten palm. Journal of Sustainable Agriculture 14:5 17. Chok, D. 1998. Cocoa development and its environmental dilemma. Proceedings of the Smithsonian Migratory Bird Center cacao conference. Available from http:// nationalzoo.si.edu/conservationandscience/

34 Issues in International Conservation Donald migratorybirds/research/cacao/papers.cfm (accessed November 2003). Chung, A. Y. C., P. Eggleton, M. R. Speight, P. M. Hammond, and V. K. Chey. 2000. The diversity of beetle assemblages in different habitat types in Sabah, Malaysia. Bulletin of Entomological Research 90:475 496. Clowes, M., St J., and J. C. S. Allison. 1982. A review of the coffee plant (Coffea arabica L.), its environment and management in relation to coffee-growing in Zimbabwe. Zimbabwe Journal of Agricultural Research 20:1 19. Coutinho, H. L. C., V. M. Oliveira, A. Lovato, A. H. N. Maia, and G. P. Manfio. 1999. Evaluation of the diversity of rhizobia in Brazilian agricultural soils cultivated with soybeans. Applied Soil Ecology 13:159 167. Crompton, T., and P. Hardstaff. 2001. Eat this: fresh ideas on the WTO Agreement on Agriculture. Royal Society for the Protection of Birds, Sandy, United Kingdom. Cummings, J. L., J. F. Glahn, E. A. Wilson, and J. E. Davis. 2002. Potential hazards of DRC- 1339 treated rice to non-target birds when used at roost staging areas in Louisiana to reduce local populations of depredating blackbirds. International Biodeterioration and Biodegradation 2 3:185 188. Danielsen, F., and H. Heegaard. 1995. Impact of logging and plantation development on species diversity: a case study from Sumatra. Pages 73 92 in Ø. Sandbukt, editor. Management of tropical forests: towards an integrated perspective. Centre for Development and the Environment, University of Oslo, Oslo. Day, J. H., and M. A. Colwell. 1998. Waterbird communities in rice fields subjected to different post-harvest treatments. Colonial Waterbirds 21:185 198. Dietsch, T. V. 2000. Assessing the conservation value of shade-grown coffee: a biological perspective using Neotropical birds. Endangered Species Update 17:122 124. Donald, P. F., R. E. Green, and M. F. Heath. 2001. Agricultural intensification and the collapse of Europe s farmland bird populations. Proceedings of the Royal Society of London Series B 263:25 29. Donald, P. F., A. Shiel, M. Crawford, and P. Hardstaff. 2004. Wake up and smell the coffee: the need for international action to address the environmental and social impacts of commodity production. Royal Society for the Protection of Birds, Sandy, United Kingdom. Donner, S. 2003. The impact on cropland cover on river nutrient levels in the Mississippi River Basin. Global Ecology and Biogeography 12:341 355. Duguma, B., J. Gockowski, and J. Bakala. 2001. Smallholder cacao (Theobroma cacao L.) cultivation in agroforestry systems of West and Central Africa: challenges and opportunities. Agroforestry Systems 51: 177 188. Ekanade, O. 1987. Small-scale cocoa farmers and environmental change in the tropical rain forest regions of south-west Nigeria. Journal of Environmental Management 25:61 70. Elphick, C. S. 2000. Functional equivalency between rice fields and seminatural wetland habitats. 14:181 191. Estrada, A., and R. Coates-Estrada. 1996. Tropical rain forest fragmentation and wild populations of primates at Los Tuxtlas, Mexico. International Journal of Primatology 17:759 783. Estrada, A., R. Coates-Estrada, and D. A. Meritt. 1993. Bat species richness and abundance in tropical rain forest fragments and in agricultural habitats at Los Tuxtlas, Mexico. Ecography 16:309 318. Estrada, A., R. Coates-Estrada, and D. A. Meritt. 1994. Non flying mammals and landscape changes in the tropical rain forest region of Los Tuxtlas, Mexico. Ecography 17:229 241. Estrada, A., R. Coates-Estrada, and D. A. Meritt. 1997. Anthropogenic landscape changes and avian diversity at Los Tuxtlas, Mexico. Biodiversity and Conservation 6:19 43. Estrada A., Coates-Estrada R., A. Anzures Dadda, and P. Cammarano. 1998. Dung and carrion beetles in tropical rain forest fragments and agricultural habitats at Los Tuxtlas, Mexico. Journal of Tropical Ecology 14:577 593. Fasola, M., L. Canova, and N. Saino. 1996. Rice fields support a large portion of herons breeding in the Mediterranean region. Colonial Waterbirds 19(special publication 1): 129 134. Fasola, M., and X. Ruíz. 1996. The value of rice fields as substitutes for natural wetlands for waterbirds in the Mediterranean region. Colonial Waterbirds 19(special publication 1): 122 128. Fasola, M., and X. Ruíz. 1997. Rice farming and waterbirds: integrated management in an artificial landscape. Pages 210 235 in D. J. Pain, and M. W. Pienkowski, editors. Farming and birds in Europe: the Common Agricultural Policy and its implications for bird conservation. Academic Press, London. Fearnside, P. M. 2001. Soybean cultivation as a threat to the environment in Brazil. Environmental Conservation 28:23 38. Flickinger, E. L., and K. A. King. 1972. Some effects of aldrin-treated rice on Gulf Coast wildlife. Journal of Wildlife Management 36:706 727. Fuentes-Flores, R. 1982. Coffee production systems in Mexico. Pages 60 72 in G. de las Salas, editor. Pages 60 72 in Agro-forestry systems in Latin America, Workshop proceedings. Centro Agronómico Tropical de Investigación y Enseñanza, Turrialba, Costa Rica. Fujioka, M., and S. J. Lane. 1997. The impact of changing irrigation practices in rice fields on frog populations of the Kanto Plain, central Japan. Ecological Research 12:101 108. Gallina, S., S. Mandujano, and González- Romero A. 1996. Conservation of mammalian biodiversity in coffee plantations of central Veracruz, México. Agroforestry Systems 33:13 27. Gao, L. Z. 2003. The conservation of Chinese rice biodiversity: genetic erosion, ethnobotany and prospects. Genetic Resources and Crop Evolution 50:17 32. Glor, R. E., A. S. Flecker, M. F. Benard, and A. G. Power. 2001. Lizard diversity and agricultural disturbance in a Caribbean forest landscape. Biodiversity and Conservation 10:711 723. Gobbi, J. A. 2000. Is biodiversity-friendly coffee financially viable? An analysis of five different coffee production systems in western El Salvador. Ecological Economics 33:267 281. Greenberg, R. 1998. Biodiversity in the cacao agroecosystems: shade management and landscape considerations. Proceedings of the Smithsonian Migratory Bird Center cacao conference. Available from http:// nationalzoo.si.edu/conservationandscience/ migratorybirds/research/cacao/papers.cfm (accessed November 2003). Greenberg, R., P. Bichier, A. Cruz, and R. Reitsma. 1997a. Bird populations in shade and sun coffee plantations in central Guatemala. 11:448 459. Greenberg, R., P. Bichier, and J. Sterling. 1997b. Bird populations in rustic and planted shade coffee plantations of eastern Chiapas, Mexico. Biotropica 29:501 514. Greenberg, R., P. Bichier, and A. Cruz Angón. 2000. The conservation value for birds of cacao plantations with diverse planted shade in Tabasco, Mexico. Animal Conservation 3:105 112. Griscom, L. 1932. The distribution of bird-life in Guatemala: a contribution to a study of the origin of Central American bird-life. Bulletin 64. American Museum of Natural History, New York. Hafner, H., P. J. Dugan, and V. Boy. 1986. Use of artificial and natural wetlands as feeding sites by Little Egrets (Egretta garzetta L.) in the Camargue, southern France. Colonial Waterbirds 9:149 154. Hasegawa, S., and T. Tabuchi. 1995. Well facilitated paddy fields in Japan. Pages 103 124 in T. Tabuchi, and S. Hasegawa, editors. Paddy fields of the world. Japanese Society of Irrigation, Drainage and Reclamation Engineering, Tokyo. Hay, A. 1991. A recent assessment of cocoa and pesticides in Brazil: an unhealthy blend for plantation workers. The Science of the Total Environment 106:97 109. Heinen, J. T. 1992. Comparisons of the leaf herpetofauna in abandoned cacao plantations and primary rain forest in Costa Rica: some

Donald Issues in International Conservation 35 implications for faunal restoration. Biotropica 24:431 439. Herzog, F. 1994. Multipurpose shade trees in coffee and cocoa plantations in Côte d Ivoire. Agroforestry Systems 27:259 267. Hoogmoed, W. B., and R. Derpsch. 1985. Chisel ploughing as an alternative tillage system in Parana, Brazil. Soil and Tillage Research 6:53 67. Ibarra-Nuñes, G. 1990. Arthropods associated with coffee plants in mixed coffee plantations at Soconusco, Chiapas, Mexico. Folia Entomologica Mexicana 97:207 233. Ickes, K. 2001. Hyper-abundance of native wild pigs (Sus scrofula) in a lowland dipterocarp rain forest of peninsular Malaysia. Biotropica 33:682 690. International Center for Research in Agroforestry (ICRAF). 1995. Alternatives to slash-and-burn: a global initiative. ICRAF, Nairobi, Kenya. Johns, N. D. 1999. Conservation in Brazil s Chocolate Forest: the unlikely persistence of the traditional cocoa agroecosystems. Environmental Management 23:31 47. Johnson, M. D. 2000. Effects of shade-tree species and crop structure on the winter arthropod and bird communities in a Jamaican shade coffee plantations. Biotropica 32:133 145. Johnson, M. D., and T. W. Sherry. 2001. Effects of food availability on the distribution of migratory warblers among habitats in Jamaica. Journal of Animal Ecology 70:546 560. Kaimowitz, D., and J. Smith. 2001. Soybean technology and the loss of natural vegetation in Brazil and Bolivia. Pages 195 212 in A. Angelson, and D. Kaimowitz, editors. Agricultural technologies and tropical deforestation. CAB International, Wallingford, United Kingdom. Katano, O., K. Hosoya, K. Iguchi, M. Yamaguchi, Y. Aonuma, and S. Kitano. 2003. Species diversity and abundance of freshwater fishes in irrigation ditches around rice fields. Environmental Biology of Fishes 66:107 121. Klein, A. M., I. Steffan-Dewenter, and T. Tscharntke. 2002a. Predator-prey ratios on cocoa along a land-use gradient in Indonesia. Biodiversity and Conservation 11:683 693. Klein, A. M., I. Steffan-Dewenter, D. Buchori, and T. Tscharntke. 2002b. Effects of landuse intensity in tropical agroforestry systems on coffee flower visiting and trapnesting bees and wasps. 16:1003 1014. Klein, A. M., I. Steffan-Derwenter, and T. Tscharntke. 2003. Fruit set of highland coffee increases with the diversity of pollinating bees. Proceedings of the Royal Society of London Series B 270:955 961. Komar, O. 1998. Avian diversity in El Salvador. Wilson Bulletin 110:511 533. Kotto-Same, J., P. L. Woomer, M. Appolinaire, and Z. Louis. 1997. Carbon dynamics in slash-and-burn agriculture and land use alternatives in the humid forest zone of Cameroon. Agriculture, Ecosystems and Environment 65:245 256. Laird, S. A., C. Obialor, and E. A. Skinner. 1996. An introductory handbook to cocoa certification: a feasibility study and regional profile of West Africa. Rainforest Alliance, New York. Lane, S. J., and M. Fujioka. 1998. The impact of changes in irrigation practices on the distribution of foraging egrets and herons (Ardeidae) in the rice fields of central Japan. Biological Conservation 83:221 230. Lawler, S. P. 2001. Rice fields as temporary wetlands: a review. Israel Journal of Zoology 47:513 528. Lindell, C., and M. Smith. 2003. Nesting bird species in sun coffee, pasture and understory forest in southern Costa Rica. Biodiversity and Conservation 12:423 440. Liow, L. H., N. S. Sodhi, and T. Elmqvist. 2001. Bee diversity along a disturbance gradient in tropical lowland forests of south-east Asia. Journal of Applied Ecology 38:180 192. Lyngbaek, A. E., R. G. Muschler, and F. L. Sinclair. 2001. Productivity and profitability of multistrata organic versus conventional coffee farms in Costa Rica. Agroforestry Systems 53:205 213. Majumdar, D. 2003. Methane and nitrous oxide emission from irrigated rice fields: proposed mitigation strategies. Current Science 84:1317 1326. Mariau, D. 1999. Chrysomelidae (Coleoptera) living off oil palm and coconut, and their parasitoids. Annales de la Societe Entomologique de France 35:230 237. Mayaux, P., F. Achard, and J.-P. Malingreau 1998. Global tropical forest area measurements derived from coarse resolution satellite imagery: a comparison with other approaches. Environmental Conservation 25:37 52. McMorrow, J. and M. A. Talip. 2001. Decline of forest area in Sabah, Malaysia: relationship to state policies, land code and land capacity. Global Environmental Change Human and Policy Dimensions 11:217 230. Messer, K. D., M. J. Kotchen, and M. R. Moore. 2000. Can shade-grown coffee help conserve tropical biodiversity? A market perspective. Endangered Species Update 17:125 131. Miller, M. R., D. E. Sharp, D. S. Gilmer, and W. R. Mulvaney. 1989. Rice available to waterfowl in harvested fields in the Sacramento Valley, California. California Fish and Game 75:113 123. Moguel, P., and V. M. Toledo. 1998. Biodiversity conservation in traditional coffee systems in Mexico. 13:11 21. Muschler, R. G. 2001. Shade improves coffee quality in a sub-optimal coffee-zone of Costa Rica. Agroforestry Systems 85:131 139. Myers, N., R. A. Mittermeier, C. G. Mittermeier, G. A. B. da Fonseca, and J. Kent. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853 858. Narusue, M., and H. Uchida. 1993. The effect of structural changes of paddy fields on foraging egrets. Strix 12:121 130. Nestel, D. 1995. Coffee in Mexico: international market, agricultural landscape and ecology. Ecological Economics 15:165 178. Nestel, D., and M. A. Altieri. 1992. The weed community of Mexican coffee agroecosystems: effect of management upon plant biomass and species composition. Acta Oecologica 13:715 726. Nestel, D., F. Dickschen, and M. A. Altieri. 1993. Diversity patterns of soil macro-coleoptera in Mexican shaded and unshaded coffee agroecosystems: an indication of habitat perturbation. Biodiversity and Conservation 2:70 78. Newmark, T. E. 1998. Carbon sequestration and cocoa production: financing sustainable development by trading carbon emission credits. Proceedings of the Smithsonian Migratory Bird Center cacao conference. Available from http://nationalzoo.si. edu/conservationandscience/migratorybirds/ research/cacao/papers.cfm (accessed November 2003). N Goran, K. 1998. Reflections on a sustainable cacao production system: the situation in the Ivory Coast, Africa. Proceedings of the Smithsonian Migratory Bird Center cacao conference. Available from http:// nationalzoo.si.edu/conservationandscience/ migratorybirds/research/cacao/papers.cfm (accessed November 2003). O Brien, T. G., and M. F. Kinnaird. 2003. Caffeine and conservation. Science 300:587. Parrish, J. D., and L. J. Petit. 1995. Value of shade coffee plantations for tropical birds: landscape and vegetation effects. Pages 113 124 in W. Lockeretz, editor. Environmental enhancement through agriculture. Tufts University, Boston. Parrish, J. D., R. Reitsma, and R. Greenberg. 1998. Cacao as crop and conservation tool: lessons from the Talamanca region of Costa Rica. Proceedings of the Smithsonian Migratory Bird Center cacao conference. Available from http://nationalzoo.si.edu/ conservationandscience/migratorybirds/ research/cacao/papers.cfm (accessed November 2003). Perfecto, I., and J. Vandermeer. 1994. Understanding biodiversity loss in agroecosystems: reduction of ant diversity resulting from transformation of the coffee ecosystem in Costa Rica. Entomology (Trends in Agricultural Sciences) 2:7 13. Perfecto, I., and R. Snelling. 1995. Biodiversity and the transformation of a tropical agroecosystems: ants in coffee plantations.

36 Issues in International Conservation Donald Ecological Applications 5:1084 1097. Perfecto, I., and J. Vandermeer. 2002. Quality of the agroecological matrix in a tropical montane landscape: ants in coffee plantations in southern Mexico. 16:174 182. Perfecto, I., R. A. Rice, R. Greenberg, and M. E. Ven der Voort. 1996. Shade coffee: a disappearing refuge for biodiversity. BioScience 46:598 608. Perfecto, I., J. Vandermeer, P. Hanson, and V. Cartin. 1997. Arthropod biodiversity loss and the transformation of a tropical agroecosystem. Biodiversity and Conservation 6:935 945. Perfecto, I., A. Mas, T. Dietsch, and J. Vandermeer. 2003. Conservation of biodiversity in coffee agroecosystems: a tri-taxa comparison in southern Mexico. Biodiversity and Conservation 12:1239 1252. Petit, L. J., D. R. Petit, D. G. Christian, and H. D. W. Powell. 1999. Bird communities of natural and modified habitats in Panama. Ecography 22:292 304. Popper, R., K. Andino, M. Bustamante, B. Hernandez, and L. Rodas. 1996. Knowledge and beliefs regarding agricultural pesticides in rural Guatemala. Environmental Management 20:241 248. Potter, L., and J. Lee. 1998. Tree planting in Indonesia: trends, impacts and directions. Occasional paper no. 18. Center for International Forestry Research, Bogor, Indonesia. Power, A. G., and A. S. Flecker. 1998. Agroecosystems and biodiversity. Proceedings of the Smithsonian Migratory Bird Center cacao conference. Available from http:// nationalzoo.si.edu/conservationandscience/ migratorybirds/research/cacao/papers.cfm (accessed November 2003). Reid, F. A., and M. E. Heitmeyer. 1995. Waterfowl and rice in California s Central Valley. California Agriculture 49:62. Reitsma, R., J. D. Parrish, and W. McLarney 2001. The role of cacao plantations in maintaining forest avian diversity in southeastern Costa Rica. Agroforestry Systems 53:185 193. Rice, R. A., and J. R. Ward. 1996. Coffee, conservation and commerce in the Western Hemisphere. Smithsonian Migratory Bird Center, Washington, D.C. Rice, R. A., and R. Greenberg. 2000. Cacao cultivation and the conservation of biological diversity. Ambio 29:167 173. Richardson, A. J., I. R. Taylor, and J. E. Growns. 2001. The foraging ecology of egrets in rice fields in southern New South Wales, Australia. Waterbirds 24:255 264. Riera, X., A. Curcó, and C. Ibàñez. 1998. L efecte de tres mètodes de gestió agrícola sobre l estructura de la comunitat d ocells en arrossars del Delta de l Ebre. Bull. Parc Natural Delta de l Ebre 10:4 9. Robbins, C. S., J. R. Sauer, R. Greenberg, and S. Droege. 1989. Population declines in North American birds that migrate to the Neotropics. Proceedings of the National Academy of Sciences of the United States of America 86:7658 7662. Roberts, D. L., R. J. Cooper, and L. J. Petit. 2000a. Use of premontane moist forest and shade coffee agroecosystems by army ants in western Panama. 14:192 199. Roberts, D. L., R. J. Cooper, and L. J. Petit. 2000b. Flock characteristics of antfollowing birds in premontane moist forest and coffee agroecosystems. Ecological Applications 10:1414 1425. Robertson, J. Y. M., and C. P. van Schaik. 2001. Causal factors underlying the dramatic decline of the Sumatran orang-utan. Oryx 35:26 38. Roger, P. A., K. L. Heong, and P. S. Teng. 1991. Biodiversity and sustainability of wetland rice production: role and potential of microorganisms and invertebrates. Pages 117 136 in D. L. Hawksworth, editor. The biodiversity of microorganisms and invertebrates: its role in sustainable agriculture. CAB International, United Kingdom. Rojas, L., C. Godoy, P. Hanson, C. Kleinn, and L. Hilje. 2001. Hopper (Homoptera: Auchenorrhyncha) diversity in shaded coffee systems of Turrialba, Costa Rica. Agroforestry Systems 53:171 177. Romero-Alvarado, Y., L. Soto-Pinto, L. Garcia- Barrios, and J. F. Barrera-Gaytan. 2002. Coffee yields and soil nutrients under the shades of Inga sp vs. multiple species in Chiapas, Mexico. Agroforestry Systems 54:215 224. Room, P. M. 1975. Diversity and organisation of the ground feeding ant faunas of forest, grassland and tree crops in Papua, New Guinea. Australian Journal of Zoology 23:71 89. Roth, D. S., I. Perfecto, and B. Rathcke. 1994. The effects of management systems on ground-foraging ant diveristy in Costa Rica. Ecological Applications 4:423 436. Roubik, D. W. 2002. The value of bees to the coffee harvest. Nature 417:708. Schroth, G., P. Coutinho, H. F. Moraes, and A. L. Albernaz. 2003. Rubber agroforests at the Tapajós river, Brazilian Amazon: environmentally benign land use systems in an old forest frontier region. Agriculture, Ecosystems and Environment 97:151 165. Sherry, T. W. 2000. Shade coffee: a good brew even in small doses. The Auk 117:563 568. Shine, R., Ambariyanto, P. S. Harlow, and Mumpuni. 1999. Ecological attributes of two commercially-harvested python species in northern Sumatra. Journal of Herpetology 33:249 257. Siebert, S. F. 2002. From shade- to sun-grown perennial crops in Sulawesi, Indonesia: implications for biodiversity conservation and soil fertility. Biodiversity and Conservation 11:1889 1902. Singh, S. N., A. Verma, and L. Tyagi. 2003. Investigating options for attenuating methane emission from Indian rice fields. Environment International 29:547 553. Soto-Pinto, L., I. Perfecto, J. Castillo- Hernandez, and J. Caballero-Nieto. 2000. Shade effect on coffee production at the northern Tzeltal zone of the state of Chiapas, Mexico. Agriculture, Ecosystems and Environment 80:61 69. Soto-Pinto, L., Y. Romero-Alvarado, J. Caballero-Nieto, and G. S. Warnholtz. 2001. Woody plant diversity and structure of shade-grown coffee plantations in northern Chiapas, Mexico. Revista de Biologia Tropical 49:977 987. Soto-Pinto, L., I. Perfecto, and J. Caballero- Nieto. 2002. Shade over coffee: its effects on berry borer, leaf rust and spontaneous herbs in Chiapas, Mexico. Agroforestry Systems 55:37 45. Staver, C., F. Guharay, D. Monterroso, and R. G. Muschler. 2001. Designing pestsuppressive multistrata perennial crop systems: shade-grown coffee in Central America. Agroforestry Systems 53:151 170. Stork, N. E., and M. J. D. Brendell. 1990. Variation in the insect fauna of Sulawesi trees with season, altitude, and forest type. Pages 173 190 in W. J. Knight, and J. D. Holloway, editors. Insects and the rain forests of South East Asia. Royal Entomological Society, London. Tamisier, A., and P. Grillas. 1994. A review of habitat changes in the Camargue: an assessment of the effects of the loss of biological diversity on the wintering waterfowl community. Biological Conservation 70:39 47. Tilman, D., J. Fargione, B. Wolff, C. D Antonio, A. Dobson, R. Howarth, D. Schindler, W. H. Schlesinger, D. Simberloff, and D. Swackhamer. 2001. Forecasting agriculturally driven global environment change. Science 292:281 284. Torres, J. A. 1984. Diversity and distribution of ant communities in Puerto Rica. Biotropica 16:296 303. Tourenq, C., R. E. Bennetts, H. Kowalski, E. Vialet, J.-L. Lucchesi, Y. Kayser, and P. Isenmann. 2001. Are ricefields a good alternative to natural marshes for waterbird communities in the Camargue, southern France? Biological Conservation 100:335 343. Vallan, D. 2002. Effects of anthropogenic environmental changes on amphibian diversity in the rain forests of eastern Madagascar. Journal of Tropical Ecology 18:725 742. Van Bodegom P. M., P. H. Verburg A. Stein S. Adiningsih and H. A. C. D. Van Der Gon. 2002. Effects of interpolation and data resolution on methane emission estimates from rice paddies. Environmental and Ecological Statistics 9:5 26. Wilby, A., and M. B. Thomas. 2002. Natural enemy diversity and pest control: patterns of