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effects: by creating labyrinths of forest roads, logging opens up areas for colonization by migrant settlers who use destructive slash-and-burn farming methods7. Logging also allows a sharp increase in hunting, which can dramatically affect some wildlife species. In the Malaysian state of Sarawak, for example, one logging camp was estimated to consume 33 000 kg of wildlife meat each year8. In recent years, aggressive multinational timber companies from Malaysia, Indonesia and other Asian countries have moved rapidly into the Amazon, either by buying large forest tracts, purchasing interests in local timber firms or signing longterm forest leases (termed concessions). In 1996 alone, Asian companies invested more than $US 500 million in the Brazilian timber industry9. Brazils national environmental protection agency, IBAMA, which is responsible for regulating logging, estimates that multinational companies now own or control about 4.5 million ha of the Brazilian Amazon10. This figure exceeds12 million ha if Asian timber leases in Guyana, Suriname and Bolivia are included11,12. A striking feature of the Amazonian timber industry is that illegal logging is rampant. A study by the Brazilian government in 1997 concluded that 80% of Amazonian logging was illegal, and recent raids have netted massive stocks of stolen timber13. IBAMA has only 80 environmental inspectors to police its Amazonian forests14, an area the size of western Europe. Aside from widespread illegal cutting, most legal operations from the nearly 400 Brazilian timber companies9 are poorly managed.

A crisis in the making: responses of Amazonian forests to land use and climate change
William F. Laurance
At least three global-change phenomena are having major impacts on Amazonian forests: (1) accelerating deforestation and logging; (2) rapidly changing patterns of forest loss; and (3) interactions between human land-use and climatic variability. Additional alterations caused by climatic change, rising concentrations of atmospheric carbon dioxide, mining, overhunting and other large-scale phenomena could also have important effects on the Amazon ecosystem. Consequently, decisions regarding Amazon forest use in the next decade are crucial to its future existence.
William Laurance is at the Biological Dynamics of Forest Fragments Project, National Institute for Research in the Amazon (INPA), CP 478, Manaus, AM 69011-970, Brazil (wfl@inpa.gov.br), and the Biodiversity Program, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA.

he Amazon contains over half of the worlds remaining tropical rainforest1. Today, these forests are experiencing rapid, unprecedented changes that will have major impacts on biodiversity, regional hydrology and the global carbon cycle. Government policies and land-use patterns are changing so quickly that articles written only a year ago could be seriously out of date. For this reason, this article relies not just on published papers in refereed journals, but also on an eclectic mix of sources news reports, reputable newspaper articles, personal observations and ongoing research. The focus here is on global-change phenomena, such as largescale changes in land-use patterns and the global climate, and how these changes affect and interact with the forests of the Amazon basin.

In addition to deforestation, logging operations are expanding dramatically in the Amazon. Logging can result in forest clearing but usually involves the selective removal of valuable timber species, such as mahogany (Swietenia spp.)5. Most direct impacts of logging result from the networks of roads, tracks and small clearings created during cutting operations, which cause collateral tree mortality, soil erosion and compaction, vine and grass invasions, and microclimatic changes associated with disruption of the forest canopy6,7. In addition, logging has important indirect

3.0

2.5 Deforestation rate (106 ha)

Accelerating deforestation and logging

Nowhere in the world is (absolute) forest destruction occurring faster than in the Amazon1. In Brazilian Amazonia, which encompasses two-thirds of the basin, the mean rate of forest clearing has accelerated in recent years from about 1.1 million ha per year in 1991, to nearly 1.5 million ha per year from 1992 to 1994, to just over 2.0 million ha per year from 1995 to 1997 (Refs 24). These averages disguise considerable year-to-year variation (Fig. 1) in 1995, for example, 2.9 million ha of forest was destroyed4, an area the size of Belgium. Deforestation rates have also risen sharply in some other parts of the Amazon, such as in northeastern Bolivia where massive tracts of lowland forest are being cleared for industrial soybean farms and cattle ranches (Fig. 2).
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2.0

1.5

1.0

0.5

0.0 1990 1991 199293 1994 Year Fig. 1. Rates of deforestation in the Brazilian Amazon since 1990 (compiled from Refs 2 4). Values do not include small (<6.25 ha) clearings, logged forest or areas affected by ground-fires. The actual value for 1997 could be higher than shown here because satellite data for that year have not yet been fully analysed. 1995 1996 1997

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With a burgeoning population that now exceeds 1.5 million, Manaus is the hub of development in the central Amazon. The number of timber mills near the city reportedly increased from ten to nearly 100 in a recent five-year period14. Current efforts to link Manaus to Rondnia in southern Amazonia, by paving highway BR-319, will provide greatly increased access to the region for migrant settlers and raise the alarming prospect that over the next decade Amazonian forests could become bisected by an expanding swath of deforestation and logging. These changing patterns of land use are causing widespread forest fragmentation. One key study found that by 1988 the area of forest in Brazilian Amazonia that was fragmented (<100 km2 in area) or prone to edge effects (<1 km from the forest edge) was over 1.5 times larger than the area actually deforested18. Because about 12.9% of the region has now been deforested3,4, the total area affected by fragmentation, clearing and edge effects could comprise a third of the Brazilian Amazon. This figure would rise considerably if logged forests were included.

Brazil 1.0

0.8 Deforestation rate (106 ha)

0.6

Bolivia

0.4

Colombia 0.2 Venezuela Ecuador Peru Guyana 0 3 6 9 12 15 18

0.0

Amazonian population (106 persons) Fig. 2. Relationship between population size and mean annual rate of tropical rainforest destruction in seven Amazonian countries, during the decade of the 1980s (r 2 = 0.66). Population sizes are for Amazonian residents only. Losses of nonrainforest are not included in the deforestation rates (except Bolivia, which has had varying classifications of its lowland forest). Data compiled from Ref 20.

Synergistic effects of land use and climatic variability

Intact rainforests are quite resistant to fires and climate fluctuations, but there are alarming synergisms between human land-uses and natural climatic variability. There is no question, for example, that logged forests are increasingly susceptible to fires, especially during droughts. Logging increases forest desiccation and fuel loads (from slash piles)22,23 and greatly increases access to slash-and-burn farmers and ranchers, which are the major sources of ignition. The combination of logging, migrant farmers and droughts are largely responsible for the massive fires that destroyed millions of hectares of Southeast Asian forests in 19821983 and 19971998 (Refs 24 and 25). Fragmented forests are also vulnerable to fire and climatic vicissitudes. Fragmentation leads to a juxtaposition of forest remnants with fire-prone pastures, farmlands and regrowth forests26. During the 1997 1998 El Nio drought, fires lit by smallscale farmers swept through an estimated 3.4 million ha of fragmented and natural forest, savanna, regrowth and farmlands in the northern Amazonian state of Roraima27. Even in the absence of drought, Amazon forest remnants experience sharply elevated rates of tree mortality and damage, apparently as a result of increased desiccation and wind turbulence near forest edges28. These changes lead to a substantial loss of forest biomass29, which has been estimated to produce 316 million tons of carbon emissions per year in the Brazilian
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For example, a government inspection of 34 operations in Paragominas, Par, concluded that the results were a disaster and that not one was using accepted practices to limit forest damage15. In a highly controversial move that is opening an additional 14 million ha of forest to logging, Brazil announced last year that it will grant timber leases in 39 national forests16. This unprecedented step was defended on the basis that the government could better control cutting under such leasing agreements and could favor timber companies that were more responsible17.

Changing patterns of forest loss

In recent decades, large-scale deforestation has been concentrated in the eastern and southern portions of the Amazon basin to the east, in Par, ramifying out from the BrasiliaBelm highway, and to the south, in the Brazilian states of Rondnia, Acre and Mato Grosso, and in northern Bolivia18. In both areas, rapid forest conversion has resulted from internationally funded development projects, governmentsponsored colonization schemes, cattle ranching, small-scale farming, logging and land speculation7,13,19. There has also been some forest clearing along rivers, especially

white-water rivers such as the Solimes and Amazon18, which contain relatively fertile sediments that are most suitable for agriculture, and in parts of Colombia, Venezuela, Peru, Ecuador, and Roraima (Brazil) in the western and northern Amazon20 (Fig. 2). However, this picture is rapidly changing. Major new highways, powerlines and transportation projects are dissecting the heart of the basin, providing access to areas once considered too remote for development. One of the most ambitious new highways, BR-174, runs from the city of Manaus in central Amazonia, northward to the Venezuelan border, spanning a distance of over 1000 km. Almost fully graded and paved, it was initially promoted as a surgical cut through the forest to provide direct access to Caribbean ports and markets in Venezuela. However, on 24 June 1997, Brazilian President Fernando Cardoso announced that six million ha of land along the highway would be opened to settlement and suggested that the area to be farmed would be so colossal that it would double the nations agricultural production21. This highway is already promoting rapid forest clearing, especially within 100 km of Manaus.

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Deforestation can also influence regional climate. In the Amazon basin, at least half of all precipitation originates from evapotranspiration40. Reduced evapotranspiration from large-scale deforestation could cause a 20% decline in Amazon rainfall, leading to lower humidity, higher surface temperatures and greater dry-season severity38,40. In the basins highly seasonal southeastern arc, such changes could increase the likelihood of fires and potentially cause rainforest to be replaced by droughtadapted deciduous forest or woodland. Hydroelectric dams are likely to increase dramatically in the Amazon. A total of 79 major (i.e. 10013 000 megawatt) dams are planned in the Brazilian Amazon alone, nearly all in forested areas, and these could cause a 20-fold increase in the 600 000 ha currently inundated by reservoirs41. In addition to destroying forest and degrading aquatic systems, dams require access roads and powerline clearings, all of which promote forest fragmentation. Mining and hunting Today, even the remotest areas of the Amazon are being influenced by human activities. Illegal gold-mining is widespread, with wildcat miners polluting streams with mercury (used to separate gold from sediments) and threatening indigenous Indians through intimidation and introductions of new diseases. A recent government census, for example, tallied more than 3000 illegal miners in the Yanomami Indian Reserve in northern Amazonia42. There are also increasing numbers of major mineral, oil and natural gas developments sanctioned by Amazonian governments. Much of the remote Peruvian Amazon one of the worlds most biologically important areas has been opened up for oil and gas exploration, with multinational corporations such as Shell Oil investing hundreds of millions of dollars in the region43. Roads created for oil exploration and development in Ecuador have caused a sharp rise in forest colonization, land speculation and commercial hunting44. Hunting pressure is growing throughout the Amazon because of greater access to forests and markets and the common use of shotguns. Frequently exploited species include larger primates, deer, tapirs, peccaries, large rodents and top carnivores (such as jaguars and pumas)45. Intensive hunting can dramatically alter the structure of animal communities, extirpate species with low reproductive rates45, and exacerbate effects of habitat fragmentation on exploited species. Hunting could potentially have diverse effects on rainforests if top carnivores are eliminated, for example, populations of seed predators could increase rapidly and reduce the abundance of large-seeded tree species46.

Box 1. Is the Amazon a carbon sink?

Recent evidence suggests that intact Amazonian forests could be a major carbon sink and thus might help slow, to some extent, the rapid anthropogenic increase in atmospheric carbon dioxide (CO2). The most likely mechanism is that Amazonian and possibly other tropical forests are growing faster and accumulating biomass, about 50% of which is carbon, in response to rising CO2 concentrations and increased nitrogen deposition in the biosphere52. Studies using the micrometeorological technique of eddy-covariance, which measures whole-forest fluxes of CO2, suggest that undisturbed forests in southern52 and central53 Amazonia are absorbing 1.0 and 5.8 tons of carbon per ha each year, respectively. If these study sites are representative, these values suggest Amazonian forests as a whole (about 5 10 6 km2) could be a major sink, absorbing from 0.5 to 2.9 gigatonnes of carbon annually (1 gigatonne = 10 9 metric tons; global anthropogenic emissions of carbon are currently 78 gigatonnes per year52). The Amazon-sink hypothesis is consistent with some, but not all, CO2 atmospheric-transport models54. These studies have significant limitations, but if intact forests in the Amazon do prove to be a major carbon sink, it will provide a powerful global incentive for forest conservation. As the area of cleared, burned, logged and fragmented forest increases, the positive effects of the Amazonian sink would diminish accordingly. Areas that had formerly been carbon sinks would instead become sources of greenhouse gases.

Amazon alone30. In drought years, the negative effects of fragmentation could well increase. The threat from Amazonian fires is increasing. Rainforests that are burnt once become increasingly prone to subsequent fires because many trees are killed, and fuel is introduced to the forest floor26. Over a four-month period last year, satellite images revealed 44 734 separate fires in the Amazon31, virtually all of them humancaused. Estimates of the total number of fires in 1997 were 2850% higher than in the previous year26,32. Smoke from forest burning became so severe in regional centers such as Manaus and Boa Vista that airports were temporarily closed and local hospitals reported 40100% rises in the incidence of respiratory problems33. Archaeological evidence suggests that severe El Nio events have occurred four times during the past two millennia, at 1500, 1000, 700 and 400 BP, resulting in catastrophic fires in the Amazon34. A growing fear is that the combination of massive deforestation, forest fragmentation, logging and thousands of human ignition sources could eventually turn less severe but far more frequent El Nio events, such as the 19821983 and 19971998 droughts, into major catastrophes26,35. The continuing fragmentation of large, undisturbed forest tracts, which act as natural firebreaks, is particularly alarming26.

uncertainties in general circulation models (GCMs) about how temperature and rainfall will change at regional scales37. Tropical forests will probably be more sensitive to changes in soil water availability, resulting from the combined effects of shifts in temperature and rainfall, than to changes in temperature per se38. Of particular concern in the Amazon are extensive forests along the basins southeastern arc precisely where fires and population pressure are greatest which have strong dry seasons even in normal years and are at the physiological limits of tropical rainforest39. These forests survive the protracted dry season only by virtue of having deep root systems39, and thus any reduction in soil water availability could be crucial. Some GCMs suggest that extreme weather events, such as El Nio droughts and tropical storms, could increase in frequency or severity as a result of global warming26,37,38. At the least, the probability of warm weather events should rise and the likelihood of cool weather events decline, simply because of higher mean temperatures37. Hydrological changes Major land-use changes profoundly affect the way that water cycles through the ecosystem. In deforested landscapes, moisture that would normally be recycled to the atmosphere through evapotranspiration or retained in vegetation is instead quickly released as increased runoff or subsurface flow3840. Water yields fluctuate widely, leading to increased flooding, erosion and sedimentation during wet periods, and reduced flows in dry times. These changes can have important effects on aquatic ecosystems. The Amazon mainstream at Iquitos, Peru, for example, never exceeded 26 m during its annual peak before 1970 but has never peaked below 26 m since, almost certainly because of upstream deforestation7.

Other large-scale phenomena

Atmospheric and climatic changes Amazonian forests could be affected in several ways by anthropogenic changes in climate and atmosphere. For example, recent evidence suggests that these forests might be responding to rising carbon dioxide levels by exhibiting faster turnover36 and by accumulating biomass (Box 1), a phenomenon that could have important implications for the global carbon cycle. The effects of global warming are difficult to predict, largely because of present
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Recent government initiatives
To date, development in the Amazon has been haphazard and often unregulated. Illegal logging and forest-clearing are rampant, and there is growing concern about accelerating deforestation and the rapid influx of aggressive Asian timber companies. For example, the respected chief of IBAMA, Eduardo Martins, said in early 1997 that multimillion dollar investments in the Amazonian logging industry would spell disaster as things stand. We dont want that kind of investment14. Recently, however, there have been several promising developments. In December 1997, Brazilian President Cardoso announced an ambitious plan to increase the area of protected Amazonian forests by an additional 25 million ha. The initiative, developed in concert with the World Bank and the World Wide Fund for Nature (WWF), would nearly triple the total area of national parks or biological reserves, from 3.8% to 10% of the Brazilian Amazon, by the year 2000 (Ref. 47). Although a very positive development, the plan is likely to face many logistical and political challenges48, so its full implementation remains far from certain. In February 1998, important new environmental legislation was passed in Brazil49. Although somewhat weakened by amendments, the new law sets much stiffer penalties for illegal logging, hunting, pollution and other activities, and will disqualify offending companies or individuals from government loans and tax incentives. Historically, offenders have largely ignored Brazilian environmental laws, and only 6% of the fines levied by IBAMA have actually be paid49. In March 1998, facing growing domestic and international concern over increasing deforestation and wildfires, the Brazilian government announced a plan to reduce the rate of Amazon forest destruction. The plan focuses mainly on small farmers. Elements of the plan include barring new settlements in virgin forests, settling landless families in areas that have already been cleared, and limiting land deeds to areas of less than 100 ha (Ref. 50). One obvious concern in a plan of this nature is that in much of the Amazon soil fertility declines rapidly in cleared lands and requires extensive fallow periods for nutrient recovery35. Thus, if farmers are not permitted to clear new areas of forest, expensive fertilizers will probably be needed to maintain soil fertility. These initiatives suggest that the Brazilian government is growing increasingly serious about slowing the rate of Amazonian deforestation. It is far from certain whether the new measures will be effective, however, given the regions growing population, development of major new highways, rapid logging expansion and the very limited capacity for enforcement in the remote Amazonian frontier. Probably the most effective strategy for forest conservation is preventing the construction of new highways into the Amazon, which in the past have inevitably led to large-scale forest destruction. International concerns are clearly felt in Amazonian countries, and foreign initiatives to provide debt relief51 or carbon-offset funds2 in return for tropical forest protection could help fund some conservation initiatives. Because the region is in a tremendous state of flux, long-term trends in development and forest conservation could be determined in the near future. It is no exaggeration to suggest that the next ten years will be the Decade of Decision for the Amazon. Acknowledgements
I thank Philip Fearnside, Oliver Phillips, Yadvinder Malhi, Claude Gascon, Carlos Rittl, Emilio Bruna, Bruce Williamson and four anonymous referees for many useful comments on the manuscript. This is publication number 207 in the Biological Dynamics of Forest Fragments Project technical series.
9 Muggiati, A. and Gondim, A. (1996) Madeireiras, O Estado de S. Paulo (So Paulo, Brazil) 16 September 10 Brasil, K. (1996) Madeireiras asiticas desrespeitam leis no AM, O Estado de S. Paulo (So Paulo, Brazil) 14 August 11 Ito, T.M. and Loftus, M. (1997) Cutting and dealing, U.S. News and World Report 3 October 12 Report by the JapanBrazil Network (1995) Japanese logging in Bolivia an analytical review of the operations of Industria Maderera Suto Ltd and its social and environmental impacts, Rainforest Action Network 26 April 13 Abramovitz, J. (1998) Taking a Stand: Cultivating a New Relationship with the Worlds Forests, World Watch Institute, Washington DC 14 Anon. (1997) Malaysian loggers in the Amazon, Rainforest Action Network (Action Alert) 24 February 1997 15 Walker, G. (1996) Kinder cuts, New Sci. 151(2048), 4042 16 Anon. (1997) Controle sobre florestas exige a reforma do IBAMA, A Critica (Manaus, Brazil) 19 January 17 Christie, M. (1997) Green groups frown as Brazil auctions off jungle, Reuters News Agency 4 August 18 Skole, D. and Tucker, C.J. (1993) Tropical deforestation and habitat fragmentation in the Amazon: satellite data from 1978 to 1988, Science 260, 19051910 19 Fearnside, P.M. (1987) Causes of deforestation in the Brazilian Amazon, in The Geophysiology of Amazonia: Vegetation and Climate Interactions (Dickson, R.F., ed.), pp. 3761, John Wiley & Sons 20 Sarre, A., Filho, M.S. and Reis, M. (1996) The amazing Amazon, in International Tropical Timber Organization (ITTO) Tropical Forest Update (Vol. 6 No. 4), pp. 37, ITTO 21 de Cassia, R. (1997) BR-174: FHC anuncia abertura de nova frontiera agrcola no norte, Amazonas em Tempo (Manaus, Brazil) 25 June, p. A4 22 Uhl, C. and Buschbacher, R. (1985) A disturbing synergism between cattle ranch burning practices and selective tree harvesting in the eastern Amazon, Biotropica 17, 265268 23 Uhl, C. and Kauffman, B. (1990) Deforestation, fire susceptibility, and potential tree responses to fire in the eastern Amazon, Ecology 71, 437449 24 Leighton, M. (1986) Catastrophic drought and fire in Borneo tropical rain forest associated with the 19821983 El Nio Southern Oscillation Event, in Tropical Rain Forests and the World Atmosphere (Prance, G.T., ed.), pp. 75102, Cambridge University Press 25 Brown, N. (1998) Out of control: fires and forestry in Indonesia, Trends Ecol. Evol. 13, 41 26 Nepstad, D.C. (1998) Origin, incidence, and implications of Amazon fires, in US Global Change Research Program Seminar Series (30 March), US Global Change Program (Washington, DC) 27 Barbosa, R.I. (1998) Avaliao Preliminar da rea dos Sistemas Naturais e Agroecossistemas Atingida por Incndios no Estado de Roraima (10.12.1997 a 30.04.98), Instituto Nacional de Pesquisas da Amaznia e Nucleo de Pesquisas de Roraima (Boa Vista, Roraima, Brazil)
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References
1 Whitmore, T.C. (1997) Tropical forest disturbance, disappearance, and species loss, in Tropical Forest Remnants: Ecology, Management, and Conservation of Fragmented Communities (Laurance W.F. and Bierregaard R.O., Jr, eds), pp. 312, The University of Chicago Press 2 Fearnside, P.M. (1997) Monitoring needs to transform Amazonian forest maintenance into a global warmingmitigation option, Mitigation Adap. Strategies Glob. Change 2, 285302 3 INPE (1996) Deforestation in Brazilian Amazonia, 19921994, Instituto Nacional de Pesquisas Espaciais, e Ministrio da Cincia e Tecnologia, Brasilia, Brazil 4 INPE (1998) Deforestation in Brazilian Amazonia, 19951997, Instituto Nacional de Pesquisas Espaciais, e Ministrio da Cincia e Tecnologia, Brasilia, Brazil 5 Verissimo, A. et al. (1995) Extraction of a high-value natural resource from Amazonia: the case of mahogany, For. Ecol. Manage. 72, 3960 6 Uhl, C. and Vieira, I.C.G. (1989) Ecological impacts of selective logging in the Brazilian Amazon: a case study from the Paragominas region of the state of Par, Biotropica 21, 98106 7 Grieser Johns, A. (1997) Timber Production and Biodiversity Conservation in Tropical Rain Forests, Cambridge University Press 8 Bennett, E.L. (1996) The inter-relationships of commercial logging, hunting, and wildlife in Sarawak, and recommendations for forest management, in Effects of Logging on Wildlife in the Tropics [Proceedings of a conference sponsored by BOLFOR (Bolivia) and Wildlife Conservation Society (New York)], Wildlife Conservation Society

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28 Laurance, W.F. et al. Rain forest fragmentation and the dynamics of Amazonian tree communities, Ecology (in press) 29 Laurance, W.F. et al. (1997) Biomass collapse in Amazonian forest fragments, Science 278, 11171118 30 Laurance, W.F., Laurance, S.G. and Delamonica, P. Tropical forest fragmentation and greenhouse gas emissions, For. Ecol. Manage. (in press) 31 Brown, P. (1998) Forest fires: setting the world ablaze, The Guardian, London 20 March 32 Borges, B. (1997) Brazil considers logging national forests, Environment News Service (Washington DC) 29 October 33 Anon. (1997) A rain forest imperiled, The New York Times (Editorial) 15 October 34 Meggers, B.J. (1994) Archeological evidence for the impact of mega-Nio events on Amazonia during the past two millennia, Clim. Change 28, 321338 35 Fearnside, P.M. and Leal-Filho, N. Soil and development in Amazonia: lessons from the Biological Dynamics of Forest Fragments Project, in Lessons from Amazonia: The Ecology and Conservation of a Fragmented Forest (Bierregaard, R.O., Jr et al., eds), Yale University Press (in press) 36 Phillips, O.L. and Gentry, A.H. (1994) Increasing turnover through time in tropical forests, Science 261, 954958 37 Mahlman, J.D. (1997) Uncertainties in projections of human-caused climate warming, Science 278, 14161417 38 Intergovernmental Panel on Climate Change (IPCC) (1996) Climate Change 1995. Impacts, Adaptations and Mitigation of Climate Change: Scientific Technical Analyses, Cambridge University Press. 39 Nepstad, D.C. et al. (1994) The role of deep roots in the hydrological and carbon cycles of Amazonian forests and pastures, Nature 372, 666669 40 Salati, E. and Vose, P.B. (1984) Amazon basin: a system in equilibrium, Science 225, 129138 41 Fearnside, P.M. (1995) Hydroelectric dams in the Brazilian Amazon as sources of greenhouse gases, Environ. Conserv. 22, 719 42 Christie, M. (1997) Yanomami Indians appeal for help against invaders, Reuters News Service 31 August 43 Soltani, A., and Osborne, T. (1997) Arteries for Global Trade, Consequences for Amazonia, Amazon Watch (Malibu, California) 44 Holmes, B. (1996) The low-impact road, New Sci. 151(2048), 43 45 Robinson, J. and Redford, K., eds (1991) Neotropical Wildlife Use and Conservation, The University of Chicago Press 46 Terborgh, J. (1992) Maintenance of diversity in tropical forests, Biotropica 24, 283292 47 Batmanian, G. (1998) President Cardoso announces plan to conserve 10% of Brazils forests, in Rain Forest Pilot Program Update (Vol. 6 No. 1), pp. 1 and 4, The World Bank (Washington, DC) 48 Anon. (1998) Brazil announces Amazon protection plan, United Press International 29 April 49 Schomberg, W. (1998) Brazil introduces new law to protect environment, Reuters News Service 13 February 50 Schomberg, W. (1998) Brazil seeks to limit settler damage to rainforest, Reuters News Service 19 March 51 Anon. (1998) House approves debt relief for tropical forest conservation, Associated Press 19 March 52 Grace, J. et al. (1994) Carbon dioxide uptake by an undisturbed tropical rain forest in southwest Amazonia, 1992 to 1993, Science 270, 778780 53 Malhi, Y. et al. Carbon dioxide transfer over a central Amazonian rain forest, J. Geophys. Res. (in press) 54 Enting, I.G., Trudinger, C.M. and Francey, R.J. (1995) A synthesis invasion of the concentration of delta-C-13 of atmospheric CO2, Tellus 47B, 3553

Sensory ecology, receiver biases and sexual selection

John A. Endler Alexandra L. Basolo
During courtship, signals are sent between the sexes, and received signals contain information that forms the basis of decision making. Much is known about signal content, but less is known about signal design what makes signals work efficiently? A consideration of design not only gives new insights into the evolution of signals (including novelty), but also allows the development of specific and testable predictions about the direction of evolution. Recently there has been increased interest in signal design, but this has resulted in some apparently divergent views in the literature.
John Endler is at the Dept of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, CA 93106, USA (endler@lifesci.ucsb.edu); Alexandra Basolo is at the Nebraska Behavior Biology Group, School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, NE 68583, USA (basolo@niko.unl.edu).

process of signal evolution. We will place them in perspective by considering the factors and processes that affect each stage of communication (Box 1) and the sequence of evolutionary steps involved (Box 2). During mate choice, the receiver must detect, perceive, assess (extract information) and act upon the signal. Signal evolution is biased and constrained by how these receiver processes can work, as well as by the biophysics of signal generation, emission and transmission (Box 1). Environmental conditions can affect signal reception and perception, and signalling behaviour determines the range of these conditions during communication. The functional relationships between these factors mean that changes in one will cause evolutionary changes in the others (Box 2). Known and predictable properties of the environment, signals and neural systems will bias the direction of evolution at each stage9. We call the resulting process sensory drive (SD), and it provides a conceptual framework for all the models (Box 2).

rowing interest in signal design efficiency has produced some diverse and divergent views in the literature because various authors have emphasized different and partially overlapping components of the evolution of signals and signal recognition, giving them different names. Models include pattern recognition and general assessment programs1 (PRP and GAP), sensory traps2,3 (ST), pre-existing bias47
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(PB), sensory drive8,9 (SD), sensory exploitation10,11 (SE), receiver psychology12,13 (RP), hidden preference14 (HP) and perceptual drive15 (PD). The classical sexual selection models1619 [Fisher process (FP), good genes and/or handicap and/or indirect benefits (GG) and direct benefits (DB)], differ in their aims; they emphasize signal content rather than design efficiency. Each model encompasses a different part of the

Models
Sensory drive The SD model emphasizes the evolutionary processes and interactions, and the ecological determinants of signals and sensory systems (Box 2). For example, environmental factors can affect signals, signalling site choice and timing2023. The model also emphasizes that there are many

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