Responses of Amazonian Forests to Land Use and Climate Change

PERSPECTIVES

effects: by creating labyrinths of forest roads, logging opens up areas for coloniz- A crisis in the making: ation by migrant settlers who use destruc- tive slash-and-burn farming methods7. responses of Amazonian forests Logging also allows a sharp increase in hunting, which can dramatically affect to land use and climate change some wildlife species. In the Malaysian state of Sarawak, for example, one logging camp was estimated to consume 33 000 kg William F. Laurance of wildlife meat each year8. In recent years, aggressive multi- At least three global-change phenomena are having major impacts on Amazonian national timber companies from Malaysia, forests: (1) accelerating deforestation and logging; (2) rapidly changing patterns of Indonesia and other Asian countries have forest loss; and (3) interactions between human land-use and climatic variability. moved rapidly into the Amazon, either by Additional alterations caused by climatic change, rising concentrations of atmospheric buying large forest tracts, purchasing in- carbon dioxide, mining, overhunting and other large-scale phenomena could also terests in local timber firms or signing long- have important effects on the Amazon ecosystem. Consequently, decisions regarding term forest leases (termed ‘concessions’). Amazon forest use in the next decade are crucial to its future existence. In 1996 alone, Asian companies invested more than $US 500 million in the Brazilian William Laurance is at the Biological Dynamics of Forest Fragments Project, timber industry9. Brazil’s national environ- National Institute for Research in the Amazon (INPA), CP 478, Manaus, AM 69011-970, Brazil mental protection agency, IBAMA, which ([email protected]), and the Biodiversity Program, National Museum of Natural History, is responsible for regulating logging, esti- Smithsonian Institution, Washington, DC 20560, USA. mates that multinational companies now own or control about 4.5 million ha of the Brazilian Amazon10. This figure exceeds12 he Amazon contains over half of the In addition to deforestation, logging million ha if Asian timber leases in Guyana, Tworld’s remaining tropical rainforest1. operations are expanding dramatically in Suriname and Bolivia are included11,12. Today, these forests are experiencing the Amazon. Logging can result in forest A striking feature of the Amazonian tim- rapid, unprecedented changes that will clearing but usually involves the selective ber industry is that illegal logging is ram- have major impacts on biodiversity, re- removal of valuable timber species, such as pant. A study by the Brazilian government gional hydrology and the global carbon mahogany (Swietenia spp.)5. Most direct in 1997 concluded that 80% of Amazonian cycle. Government policies and land-use impacts of logging result from the net- logging was illegal, and recent raids have patterns are changing so quickly that arti- works of roads, tracks and small clearings netted massive stocks of stolen timber13. cles written only a year ago could be seri- created during cutting operations, which IBAMA has only 80 environmental inspec- ously out of date. For this reason, this arti- cause collateral tree mortality, soil erosion tors to police its Amazonian forests14, an cle relies not just on published papers in and compaction, vine and grass invasions, area the size of western Europe. Aside refereed journals, but also on an eclectic and microclimatic changes associated from widespread illegal cutting, most legal mix of sources – news reports, reputable with disruption of the forest canopy6,7. In operations from the nearly 400 Brazilian newspaper articles, personal observations addition, logging has important indirect timber companies9 are poorly managed. and ongoing research. The focus here is on global-change phenomena, such as large- scale changes in land-use patterns and the global climate, and how these changes 3.0 affect and interact with the forests of the Amazon basin. 2.5 Accelerating deforestation and ha)

logging 6 2.0 Nowhere in the world is (absolute) for- 10 est destruction occurring faster than in the × Amazon1. In Brazilian Amazonia, which 1.5 encompasses two-thirds of the basin, the mean rate of forest clearing has accelerated in recent years – from about 1.1 million ha 1.0 per year in 1991, to nearly 1.5 million ha per year from 1992 to 1994, to just over 2.0 mil- Deforestation rate ( lion ha per year from 1995 to 1997 (Refs 0.5 2–4). These averages disguise consid- erable year-to-year variation (Fig. 1) – in 1995, for example, 2.9 million ha of 0.0 forest was destroyed4, an area the size of 1990 1991 1992Ð93 1994 1995 1996 1997 Belgium. Deforestation rates have also Year risen sharply in some other parts of the Amazon, such as in northeastern Bolivia Fig. 1. Rates of deforestation in the Brazilian Amazon since 1990 (compiled from Refs 2–4). Values do not where massive tracts of lowland forest include small (<6.25 ha) clearings, logged forest or areas affected by ground-fires. The actual value for are being cleared for industrial soybean 1997 could be higher than shown here because satellite data for that year have not yet been fully analysed. farms and cattle ranches (Fig. 2).

With a burgeoning population that now exceeds 1.5 million, Manaus is the hub of Brazil development in the central Amazon. The 1.0 number of timber mills near the city re- portedly increased from ten to nearly 100 in a recent five-year period14. Current ef- forts to link Manaus to Rondônia in southern Amazonia, by paving highway BR-319, 0.8 will provide greatly increased access to the region for migrant settlers and raise

ha) the alarming prospect that over the next 6

10 decade Amazonian forests could become

× Bolivia 0.6 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 0.4 of forest in Brazilian Amazonia that was

Deforestation rate ( fragmented (<100 km2 in area) or prone to edge effects (<1 km from the forest edge) Colombia was over 1.5 times larger than the area ac- 0.2 18 Venezuela tually deforested . Because about 12.9% Ecuador of the region has now been deforested3,4, Peru the total area affected by fragmentation, clearing and edge effects could comprise a Guyana 0.0 third of the Brazilian Amazon. This figure would rise considerably if logged forests 0 3 6 9 12 15 18 were included. Amazonian population (×106 persons) Synergistic effects of land use and Fig. 2. Relationship between population size and mean annual rate of tropical rainforest destruction in climatic variability seven Amazonian countries, during the decade of the 1980s (r 2 = 0.66). Population sizes are for Amazonian Intact rainforests are quite resistant to residents only. Losses of nonrainforest are not included in the deforestation rates (except Bolivia, which fires and climate fluctuations, but there has had varying classifications of its lowland forest). Data compiled from Ref 20. are alarming synergisms between human land-uses and natural climatic variability. There is no question, for example, that logged forests are increasingly susceptible For example, a government inspection of white-water rivers such as the Solimões to fires, especially during droughts. Log- 34 operations in Paragominas, Pará, con- and Amazon18, which contain relatively ging increases forest desiccation and fuel cluded that ‘the results were a disaster’ fertile sediments that are most suitable loads (from slash piles)22,23 and greatly in- and that not one was using accepted prac- for agriculture, and in parts of Colombia, creases access to slash-and-burn farmers tices to limit forest damage15. In a highly Venezuela, Peru, Ecuador, and Roraima and ranchers, which are the major sources controversial move that is opening an ad- (Brazil) in the western and northern of ignition. The combination of logging, ditional 14 million ha of forest to logging, Amazon20 (Fig. 2). migrant farmers and droughts are largely Brazil announced last year that it will grant However, this picture is rapidly chang- responsible for the massive fires that de- timber leases in 39 national forests16. This ing. Major new highways, powerlines and stroyed millions of hectares of Southeast unprecedented step was defended on the transportation projects are dissecting the Asian forests in 1982–1983 and 1997–1998 basis that the government could better heart of the basin, providing access to (Refs 24 and 25). control cutting under such leasing agree- areas once considered too remote for de- Fragmented forests are also vulnerable ments and could favor timber companies velopment. One of the most ambitious to fire and climatic vicissitudes. Fragmen- that were more responsible17. new highways, BR-174, runs from the city tation leads to a juxtaposition of forest rem- of Manaus in central Amazonia, north- nants with fire-prone pastures, farmlands Changing patterns of forest loss ward to the Venezuelan border, spanning and regrowth forests26. During the 1997– In recent decades, large-scale deforest- a distance of over 1000 km. Almost fully 1998 El Niño drought, fires lit by small- ation has been concentrated in the eastern graded and paved, it was initially pro- scale farmers swept through an estimated and southern portions of the Amazon basin moted as a surgical cut through the forest 3.4 million ha of fragmented and natural – to the east, in Pará, ramifying out from to provide direct access to Caribbean ports forest, savanna, regrowth and farmlands in the Brasilia–Belém highway, and to the and markets in Venezuela. However, on the northern Amazonian state of Roraima27. south, in the Brazilian states of Rondônia, 24 June 1997, Brazilian President Fernando Even in the absence of drought, Amazon Acre and Mato Grosso, and in northern Cardoso announced that six million ha of forest remnants experience sharply el- Bolivia18. In both areas, rapid forest con- land along the highway would be opened evated rates of tree mortality and damage, version has resulted from internationally to settlement and suggested that the area apparently as a result of increased desic- funded development projects, government- to be farmed would be ‘so colossal that it cation and wind turbulence near forest sponsored colonization schemes, cattle would double the nation’s agricultural pro- edges28. These changes lead to a substan- ranching, small-scale farming, logging and duction’21. This highway is already pro- tial loss of forest biomass29, which has been land speculation7,13,19. There has also been moting rapid forest clearing, especially estimated to produce 3–16 million tons of some forest clearing along rivers, especially within 100 km of Manaus. carbon emissions per year in the Brazilian

412 TREE vol. 13, no. 10 October 1998 PERSPECTIVES

Deforestation can also influence re- Box 1. Is the Amazon a carbon sink? gional climate. In the Amazon basin, at least Recent evidence suggests that intact Amazonian forests could be a major carbon sink and thus might help half of all precipitation originates from evapotranspiration40. Reduced evapotran- 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 spiration from large-scale deforestation biomass, about 50% of which is carbon, in response to rising CO2 concentrations and increased nitrogen could cause a 20% decline in Amazon rain- deposition in the biosphere52. fall, leading to lower humidity, higher sur- Studies using the micrometeorological technique of eddy-covariance, which measures whole-forest 52 53 face temperatures and greater dry-season fluxes of CO2, suggest that undisturbed forests in southern and central Amazonia are absorbing 1.0 and 5.8 tons of carbon per ha each year, respectively. If these study sites are representative, these values sug- severity38,40. In the basin’s highly seasonal gest Amazonian forests as a whole (about 5 × 106 km2) could be a major sink, absorbing from 0.5 to 2.9 southeastern arc, such changes could in- gigatonnes of carbon annually (1 gigatonne = 109 metric tons; global anthropogenic emissions of carbon crease the likelihood of fires and potentially are currently 7–8 gigatonnes per year52). The Amazon-sink hypothesis is consistent with some, but not all, 54 cause rainforest to be replaced by drought- CO2 atmospheric-transport models . These studies have significant limitations, but if intact forests in the Amazon do prove to be a major adapted deciduous forest or woodland. carbon sink, it will provide a powerful global incentive for forest conservation. As the area of cleared, Hydroelectric dams are likely to in- burned, logged and fragmented forest increases, the positive effects of the Amazonian sink would diminish crease dramatically in the Amazon. A to- accordingly. Areas that had formerly been carbon sinks would instead become sources of greenhouse gases. tal of 79 major (i.e. 100–13 000 megawatt) dams are planned in the Brazilian Amazon alone, nearly all in forested areas, and these could cause a 20-fold increase in the Amazon alone30. In drought years, the uncertainties in general circulation mod- 600 000 ha currently inundated by reser- negative effects of fragmentation could well els (GCMs) about how temperature and voirs41. In addition to destroying forest and increase. rainfall will change at regional scales37. degrading aquatic systems, dams require The threat from Amazonian fires is in- Tropical forests will probably be more access roads and powerline clearings, all creasing. Rainforests that are burnt once sensitive to changes in soil water avail- of which promote forest fragmentation. become increasingly prone to subsequent ability, resulting from the combined ef- fires because many trees are killed, and fects of shifts in temperature and rainfall, Mining and hunting fuel is introduced to the forest floor26. Over than to changes in temperature per se38. Today, even the remotest areas of the a four-month period last year, satellite Of particular concern in the Amazon are Amazon are being influenced by human ac- images revealed 44 734 separate fires in extensive forests along the basin’s south- tivities. Illegal gold-mining is widespread, the Amazon31, virtually all of them human- eastern arc – precisely where fires and with wildcat miners polluting streams with caused. Estimates of the total number of population pressure are greatest – which mercury (used to separate gold from sedi- fires in 1997 were 28–50% higher than in have strong dry seasons even in normal ments) and threatening indigenous Indians the previous year26,32. Smoke from forest years and are at the physiological limits of through intimidation and introductions of burning became so severe in regional cen- tropical rainforest39. These forests sur- new diseases. A recent government cen- ters such as Manaus and Boa Vista that vive the protracted dry season only by sus, for example, tallied more than 3000 airports were temporarily closed and lo- virtue of having deep root systems39, and illegal miners in the Yanomami Indian cal hospitals reported 40–100% rises in thus any reduction in soil water availabil- Reserve in northern Amazonia42. There the incidence of respiratory problems33. ity could be crucial. are also increasing numbers of major Archaeological evidence suggests that Some GCMs suggest that extreme mineral, oil and natural gas developments severe El Niño events have occurred four weather events, such as El Niño droughts sanctioned by Amazonian governments. times during the past two millennia, at and tropical storms, could increase in fre- Much of the remote Peruvian Amazon – 1500, 1000, 700 and 400 BP, resulting in cata- quency or severity as a result of global one of the world’s most biologically im- strophic fires in the Amazon34. A growing warming26,37,38. At the least, the probabil- portant areas – has been opened up for oil fear is that the combination of massive de- ity of warm weather events should rise and gas exploration, with multinational forestation, forest fragmentation, logging and the likelihood of cool weather events corporations such as Shell Oil investing and thousands of human ignition sources decline, simply because of higher mean hundreds of millions of dollars in the re- could eventually turn less severe but far temperatures37. gion43. Roads created for oil exploration more frequent El Niño events, such as the and development in Ecuador have caused 1982–1983 and 1997–1998 droughts, into Hydrological changes a sharp rise in forest colonization, land major catastrophes26,35. The continuing Major land-use changes profoundly speculation and commercial hunting44. fragmentation of large, undisturbed forest affect the way that water cycles through Hunting pressure is growing through- tracts, which act as natural firebreaks, is the ecosystem. In deforested landscapes, out the Amazon because of greater access particularly alarming26. moisture that would normally be recycled to forests and markets and the common to the atmosphere through evapotranspi- use of shotguns. Frequently exploited spe- Other large-scale phenomena ration or retained in vegetation is instead cies include larger primates, deer, tapirs, Atmospheric and climatic changes quickly released as increased runoff or peccaries, large rodents and top carnivores Amazonian forests could be affected subsurface flow38–40. Water yields fluc- (such as jaguars and pumas)45. Intensive in several ways by anthropogenic changes tuate widely, leading to increased flood- hunting can dramatically alter the struc- in climate and atmosphere. For example, re- ing, erosion and sedimentation during wet ture of animal communities, extirpate spe- cent evidence suggests that these forests periods, and reduced flows in dry times. cies with low reproductive rates45, and ex- might be responding to rising carbon di- These changes can have important effects acerbate effects of habitat fragmentation oxidelevels by exhibiting faster turnover36 on aquatic ecosystems. The Amazon main- on exploited species. Hunting could poten- and by accumulating biomass (Box 1), a stream at Iquitos, Peru, for example, never tially have diverse effects on rainforests – if phenomenon that could have important exceeded 26 m during its annual peak be- top carnivores are eliminated, for example, implications for the global carbon cycle. fore 1970 but has never peaked below 26 m populations of seed predators could in- The effects of global warming are diffi- since, almost certainly because of up- crease rapidly and reduce the abundance cult to predict, largely because of present stream deforestation7. of large-seeded tree species46.

TREE vol. 13, no. 10 October 1998 413 PERSPECTIVES

Recent government initiatives highways, rapid logging expansion and 9 Muggiati, A. and Gondim, A. (1996) To date, development in the Amazon the very limited capacity for enforcement Madeireiras, O Estado de S. Paulo (São Paulo, has been haphazard and often unregulated. in the remote Amazonian frontier. Prob- Brazil) 16 September Illegal logging and forest-clearing are ram- ably the most effective strategy for forest 10 Brasil, K. (1996) Madeireiras asiáticas pant, and there is growing concern about conservation is preventing the construc- desrespeitam leis no AM, O Estado de S. Paulo accelerating deforestation and the rapid tion of new highways into the Amazon, (São Paulo, Brazil) 14 August 11 Ito, T.M. and Loftus, M. (1997) Cutting and influx of aggressive Asian timber compa- which in the past have inevitably led to dealing, U.S. News and World Report 3 October nies. For example, the respected chief of large-scale forest destruction. International 12 Report by the Japan–Brazil Network (1995) IBAMA, Eduardo Martins, said in early concerns are clearly felt in Amazonian Japanese logging in Bolivia – an analytical 1997 that ‘multimillion dollar investments countries, and foreign initiatives to pro- review of the operations of Industria in the Amazonian logging industry would vide debt relief51 or carbon-offset funds2 in Maderera Suto Ltd and its social and spell disaster as things stand. We don’t return for tropical forest protection could environmental impacts, Rainforest Action want that kind of investment’14. help fund some conservation initiatives. Be- Network 26 April Recently, however, there have been cause the region is in a tremendous state of 13 Abramovitz, J. (1998) Taking a Stand: several promising developments. In De- flux, long-term trends in development and Cultivating a New Relationship with the World’s cember 1997, Brazilian President Cardoso forest conservation could be determined Forests, World Watch Institute, Washington DC announced an ambitious plan to increase in the near future. It is no exaggeration to 14 Anon. (1997) Malaysian loggers in the Amazon, Rainforest Action Network (Action the area of protected Amazonian forests suggest that the next ten years will be the Alert) 24 February 1997 by an additional 25 million ha. The initia- ‘Decade of Decision’ for the Amazon. 15 Walker, G. (1996) Kinder cuts, New Sci. tive, developed in concert with the World 151(2048), 40–42 Bank and the World Wide Fund for Nature Acknowledgements 16 Anon. (1997) Controle sobre florestas exige a (WWF), would nearly triple the total area I thank Philip Fearnside, Oliver Phillips, reforma do IBAMA, A Critica (Manaus, Brazil) of national parks or biological reserves, Yadvinder Malhi, Claude Gascon, 19 January from 3.8% to 10% of the Brazilian Amazon, Carlos Rittl, Emilio Bruna, 17 Christie, M. (1997) Green groups frown as by the year 2000 (Ref. 47). Although a very Bruce Williamson and four anonymous Brazil auctions off jungle, Reuters News positive development, the plan is likely referees for many useful comments on Agency 4 August the manuscript. This is publication 18 Skole, D. and Tucker, C.J. (1993) Tropical to face many logistical and political chal- number 207 in the Biological Dynamics lenges48, so its full implementation re- deforestation and habitat fragmentation in of Forest Fragments Project technical the Amazon: satellite data from 1978 to 1988, mains far from certain. series. Science 260, 1905–1910 In February 1998, important new en- 19 Fearnside, P.M. (1987) Causes of vironmental legislation was passed in References deforestation in the Brazilian Amazon, in Brazil49. Although somewhat weakened by 1 Whitmore, T.C. (1997) Tropical forest The Geophysiology of Amazonia: Vegetation amendments, the new law sets much stiffer disturbance, disappearance, and species and Climate Interactions (Dickson, R.F., ed.), penalties for illegal logging, hunting, pol- loss, in Tropical Forest Remnants: Ecology, pp. 37–61, John Wiley & Sons lution and other activities, and will dis- Management, and Conservation of Fragmented 20 Sarre, A., Filho, M.S. and Reis, M. (1996) The qualify offending companies or individuals Communities (Laurance W.F. and amazing Amazon, in International Tropical from government loans and tax incen- Bierregaard R.O., Jr, eds), pp. 3–12, Timber Organization (ITTO) Tropical Forest tives. Historically, offenders have largely The University of Chicago Press Update (Vol. 6 No. 4), pp. 3–7, ITTO ignored Brazilian environmental laws, and 2 Fearnside, P.M. (1997) Monitoring needs to 21 de Cassia, R. (1997) BR-174: FHC anuncia transform Amazonian forest maintenance into abertura de nova frontiera agrícola no norte, only 6% of the fines levied by IBAMA have a global warming–mitigation option, Mitigation Amazonas em Tempo (Manaus, Brazil) 49 actually be paid . Adap. Strategies Glob. Change 2, 285–302 25 June, p. A4 In March 1998, facing growing domestic 3 INPE (1996) Deforestation in Brazilian 22 Uhl, C. and Buschbacher, R. (1985) A and international concern over increasing Amazonia, 1992–1994, Instituto Nacional de disturbing synergism between cattle ranch deforestation and wildfires, the Brazilian Pesquisas Espaciais, e Ministério da Ciéncia e burning practices and selective tree government announced a plan to reduce Tecnologia, Brasilia, Brazil harvesting in the eastern Amazon, Biotropica the rate of Amazon forest destruction. 4 INPE (1998) Deforestation in Brazilian 17, 265–268 The plan focuses mainly on small farmers. Amazonia, 1995–1997, Instituto Nacional de 23 Uhl, C. and Kauffman, B. (1990) Deforestation, Elements of the plan include barring new Pesquisas Espaciais, e Ministério da Ciéncia e fire susceptibility, and potential tree settlements in virgin forests, settling land- Tecnologia, Brasilia, Brazil responses to fire in the eastern Amazon, less families in areas that have already been 5 Verissimo, A. et al. (1995) Extraction of a Ecology 71, 437–449 high-value natural resource from Amazonia: 24 Leighton, M. (1986) Catastrophic drought and cleared, and limiting land deeds to areas the case of mahogany, For. Ecol. Manage. 72, fire in Borneo tropical rain forest associated of less than 100 ha (Ref. 50). One obvious 39–60 with the 1982–1983 El Niño Southern concern in a plan of this nature is that in 6 Uhl, C. and Vieira, I.C.G. (1989) Ecological Oscillation Event, in Tropical Rain Forests and much of the Amazon soil fertility declines impacts of selective logging in the Brazilian the World Atmosphere (Prance, G.T., ed.), rapidly in cleared lands and requires ex- Amazon: a case study from the Paragominas pp. 75–102, Cambridge University Press tensive fallow periods for nutrient recov- region of the state of Pará, Biotropica 21, 25 Brown, N. (1998) Out of control: fires and ery35. Thus, if farmers are not permitted to 98–106 forestry in Indonesia, Trends Ecol. Evol. 13, 41 clear new areas of forest, expensive ferti- 7 Grieser Johns, A. (1997) Timber Production and 26 Nepstad, D.C. (1998) Origin, incidence, and lizers will probably be needed to maintain Biodiversity Conservation in Tropical Rain implications of Amazon fires, in US Global soil fertility. Forests, Cambridge University Press Change Research Program Seminar Series These initiatives suggest that the Bra- 8 Bennett, E.L. (1996) The inter-relationships of (30 March), US Global Change Program commercial logging, hunting, and wildlife in (Washington, DC) zilian government is growing increasingly Sarawak, and recommendations for forest 27 Barbosa, R.I. (1998) Avaliação Preliminar da serious about slowing the rate of Ama- management, in Effects of Logging on Wildlife Área dos Sistemas Naturais e Agroecossistemas zonian deforestation. It is far from certain in the Tropics [Proceedings of a conference Atingida por Incêndios no Estado de Roraima whether the new measures will be effec- sponsored by BOLFOR (Bolivia) and Wildlife (10.12.1997 a 30.04.98), Instituto Nacional de tive, however, given the region’s growing Conservation Society (New York)], Wildlife Pesquisas da Amazônia e Nucleo de Pesquisas population, development of major new Conservation Society de Roraima (Boa Vista, Roraima, Brazil)

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28 Laurance, W.F. et al. Rain forest 36 Phillips, O.L. and Gentry, A.H. (1994) 46 Terborgh, J. (1992) Maintenance of fragmentation and the dynamics of Increasing turnover through time in tropical diversity in tropical forests, Biotropica 24, Amazonian tree communities, Ecology forests, Science 261, 954–958 283–292 (in press) 37 Mahlman, J.D. (1997) Uncertainties in 47 Batmanian, G. (1998) President Cardoso 29 Laurance, W.F. et al. (1997) Biomass collapse projections of human-caused climate announces plan to conserve 10% of Brazil’s in Amazonian forest fragments, Science 278, warming, Science 278, 1416–1417 forests, in Rain Forest Pilot Program Update 1117–1118 38 Intergovernmental Panel on Climate Change (Vol. 6 No. 1), pp. 1 and 4, The World Bank 30 Laurance, W.F., Laurance, S.G. and (IPCC) (1996) Climate Change 1995. Impacts, (Washington, DC) Delamonica, P. Tropical forest Adaptations and Mitigation of Climate Change: 48 Anon. (1998) Brazil announces Amazon fragmentation and greenhouse gas Scientific Technical Analyses, Cambridge protection plan, United Press International emissions, For. Ecol. Manage. University Press. 29 April (in press) 39 Nepstad, D.C. et al. (1994) The role of deep 49 Schomberg, W. (1998) Brazil introduces new 31 Brown, P. (1998) Forest fires: setting the roots in the hydrological and carbon cycles law to protect environment, Reuters News world ablaze, The Guardian, of Amazonian forests and pastures, Nature Service 13 February London 20 March 372, 666–669 50 Schomberg, W. (1998) Brazil seeks to limit 32 Borges, B. (1997) Brazil considers logging 40 Salati, E. and Vose, P.B. (1984) Amazon basin: settler damage to rainforest, Reuters News national forests, Environment News Service a system in equilibrium, Science 225, 129–138 Service 19 March (Washington DC) 29 October 41 Fearnside, P.M. (1995) Hydroelectric dams in 51 Anon. (1998) House approves debt relief for 33 Anon. (1997) A rain forest imperiled, The New the Brazilian Amazon as sources of tropical forest conservation, Associated Press York Times (Editorial) 15 October “greenhouse” gases, Environ. Conserv. 22, 7–19 19 March 34 Meggers, B.J. (1994) Archeological evidence 42 Christie, M. (1997) Yanomami Indians appeal 52 Grace, J. et al. (1994) Carbon dioxide uptake for the impact of mega-Niño events on for help against invaders, Reuters News by an undisturbed tropical rain forest in Amazonia during the past two millennia, Service 31 August southwest Amazonia, 1992 to 1993, Science Clim. Change 28, 321–338 43 Soltani, A., and Osborne, T. (1997) Arteries for 270, 778–780 35 Fearnside, P.M. and Leal-Filho, N. Soil and Global Trade, Consequences for Amazonia, 53 Malhi, Y. et al. Carbon dioxide transfer over a development in Amazonia: lessons from the Amazon Watch (Malibu, California) central Amazonian rain forest, J. Geophys. Biological Dynamics of Forest Fragments 44 Holmes, B. (1996) The low-impact road, New Res. (in press) Project, in Lessons from Amazonia: The Sci. 151(2048), 43 54 Enting, I.G., Trudinger, C.M. and Francey, R.J. Ecology and Conservation of a Fragmented 45 Robinson, J. and Redford, K., eds (1991) (1995) A synthesis invasion of the Forest (Bierregaard, R.O., Jr et al., eds), Neotropical Wildlife Use and Conservation, concentration of delta-C-13 of atmospheric

Yale University Press (in press) The University of Chicago Press CO2, Tellus 47B, 35–53

process of signal evolution. We will place them in perspective by considering the fac- Sensory ecology, receiver biases and tors and processes that affect each stage of communication (Box 1) and the sequence sexual selection of evolutionary steps involved (Box 2). During mate choice, the receiver must John A. Endler detect, perceive, assess (extract information) and act upon the signal. Signal evo- Alexandra L. Basolo lution is biased and constrained by how these receiver processes can work, as well During courtship, signals are sent between the sexes, and received signals contain as by the biophysics of signal generation, information that forms the basis of decision making. Much is known about signal emission and transmission (Box 1). En- content, but less is known about signal design – what makes signals work vironmental conditions can affect signal efficiently? A consideration of design not only gives new insights into the evolution reception and perception, and signalling of signals (including novelty), but also allows the development of specific and behaviour determines the range of these testable predictions about the direction of evolution. Recently there has been conditions during communication. The increased interest in signal design, but this has resulted in some apparently functional relationships between these fac- divergent views in the literature. tors mean that changes in one will cause evolutionary changes in the others (Box 2). John Endler is at the Dept of Ecology, Evolution and Marine Biology, Known and predictable properties of the University of California, Santa Barbara, CA 93106, USA ([email protected]); environment, signals and neural systems Alexandra Basolo is at the Nebraska Behavior Biology Group, School of Biological Sciences, will bias the direction of evolution at each University of Nebraska-Lincoln, Lincoln, NE 68583, USA ([email protected]). stage9. We call the resulting process sensory drive (SD), and it provides a concep- tual framework for all the models (Box 2). rowing interest in signal design effi- (PB), sensory drive8,9 (SD), sensory ex- Gciency has produced some diverse and ploitation10,11 (SE), receiver psychology12,13 Models divergent views in the literature because (RP), hidden preference14 (HP) and per- Sensory drive various authors have emphasized different ceptual drive15 (PD). The classical sexual The SD model emphasizes the evolu- and partially overlapping components of selection models16–19 [Fisher process (FP), tionary processes and interactions, and the evolution of signals and signal recog- good genes and/or handicap and/or indi- the ecological determinants of signals and nition, giving them different names. Mod- rect benefits (GG) and direct benefits (DB)], sensory systems (Box 2). For example, els include pattern recognition and gen- differ in their aims; they emphasize signal environmental factors can affect signals, eral assessment programs1 (PRP and GAP), content rather than design efficiency. Each signalling site choice and timing20–23. The sensory traps2,3 (ST), pre-existing bias4–7 model encompasses a different part of the model also emphasizes that there are many