Extinction Debt and Windows of Conservation Opportunity in the Brazilian Amazon

Growing Extinction Debt Predicting, and potentially preventing, extinction is a central goal of conservation biology. Wearn et al. (p. 228; see the Perspective by Rangel) describe a mathematical approach for predicting the time lags in extinction following habitat loss. The model was applied to the highly biodiverse Brazilian Amazon region, and used to reconstruct the spatial and temporal patterns of extinction and the accumulation of extinction debt from 1970 through to the present, and to extrapolate to 2050 under four deforestation scenarios. The Amazon basin sits at a critical point: Few species have been driven extinct to date, but an extinction debt is rapidly accumulating, which could lead to an increasing rate of extinction in the next four decades. Deforestation scenarios predict species extinction rates and identify targets of conservation efforts. Predicting when future species extinctions will occur is necessary for directing conservation investments but has proved difficult. We developed a new method for predicting extinctions over time, accounting for the timing and magnitude of habitat loss. We applied this to the Brazilian Amazon, predicting that local extinctions of forest-dependent vertebrate species have thus far been minimal (1% of species by 2008), with more than 80% of extinctions expected to be incurred from historical habitat loss still to come. Realistic deforestation scenarios suggest that local regions will lose an average of nine vertebrate species and have a further 16 committed to extinction by 2050. There is a window of opportunity to dilute the legacy of historical deforestation by concentrating conservation efforts in areas with greatest debt.

[1]  I. Turner Species loss in fragments of tropical rain forest: a review of the evidence. , 1996 .

[2]  J. Karr Avian Extinction on Barro Colorado Island, Panama: A Reassessment , 1982, The American Naturalist.

[3]  C. Peres,et al.  Rapid avifaunal collapse along the Amazonian deforestation frontier , 2006 .

[4]  S. Pimm,et al.  Forest losses predict bird extinctions in eastern North America. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[5]  B. Soares-Filho,et al.  Modelling conservation in the Amazon basin , 2006, Nature.

[6]  Philip C. Stouffer,et al.  Rates of species loss from Amazonian forest fragments , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[7]  M. Nowak,et al.  Habitat destruction and the extinction debt , 1994, Nature.

[8]  A. Suarez,et al.  Extinction and Colonization of Birds on Habitat Islands , 2001 .

[9]  G. Dutson,et al.  Extinction and conservation on Cebu , 1995, Nature.

[10]  James E. Hines,et al.  A Large-Scale Deforestation Experiment: Effects of Patch Area and Isolation on Amazon Birds , 2007, Science.

[11]  M. Soulé,et al.  RESPONSE OF RODENTS TO HABITAT FRAGMENTATION IN COASTAL SOUTHERN CALIFORNIA , 1997 .

[12]  Bai-Lian Li,et al.  Habitat Destruction and the Extinction Debt Revisited , 1996 .

[13]  J. Ragle,et al.  IUCN Red List of Threatened Species , 2010 .

[14]  M. V. Sluys,et al.  Prediction of threatened tetrapods based on the species–area relationship in Atlantic Forest, Brazil , 2005 .

[15]  T. Brooks,et al.  Deforestation and bird extinctions in the Atlantic forest , 1999 .

[16]  Philip C. Stouffer,et al.  Local Extinctions of Terrestrial Insectivorous Birds in a Fragmented Landscape near Manaus, Brazil , 1999 .

[17]  John H. Lawton,et al.  BEETLE SPECIES RESPONSES TO TROPICAL FOREST FRAGMENTATION , 1998 .

[18]  J. Terborgh Preservation of Natural Diversity: The Problem of Extinction Prone Species , 1974 .

[19]  Barry W. Brook,et al.  Catastrophic extinctions follow deforestation in Singapore , 2003, Nature.

[20]  R. Holt,et al.  A Survey and Overview of Habitat Fragmentation Experiments , 2000 .

[21]  L. P. Koh,et al.  A century of avifaunal turnover in a small tropical rainforest fragment , 2005 .

[22]  Rômulo Ribon,et al.  Bird Extinctions in Atlantic Forest Fragments of the Viçosa Region, Southeastern Brazil , 2003 .

[23]  H. Tan,et al.  A Century of Plant Species Loss from an Isolated Fragment of Lowland Tropical Rain Forest , 1996 .

[24]  C. Safinya,et al.  Self-assembly and protein stability , 1994, Nature.

[25]  G. Halffter,et al.  Temporal shifts in dung beetle community structure within a protected area of tropical wet forest: a 35-year study and its implications for long-term conservation , 2008 .

[26]  T. Lovejoy,et al.  Effects of forest fragmentation on amazonian understory bird communities , 1989 .

[27]  S. Hubbell,et al.  How many tree species are there in the Amazon and how many of them will go extinct? , 2008, Proceedings of the National Academy of Sciences.

[28]  P. Raven,et al.  Biodiversity: Extinction by numbers , 2000, Nature.

[29]  W. Newmark Insularization of Tanzanian Parks and the Local Extinction of Large Mammals , 1996 .

[30]  R. Primack,et al.  Plant species lost in an isolated conservation area in Metropolitan Boston from 1894 to 1993. , 1996 .

[31]  Kenneth J Feeley,et al.  Extinction risks of Amazonian plant species , 2009, Proceedings of the National Academy of Sciences.

[32]  G. Kattan,et al.  Forest Fragmentation and Bird Extinctions: San Antonio Eighty Years Later , 1994 .

[33]  B. Wilcox Supersaturated Island Faunas: A Species-Age Relationship for Lizards on Post-Pleistocene Land-Bridge Islands , 1978, Science.

[34]  R. May,et al.  Uncertainties in extinction rates , 1994, Nature.

[35]  D. Vallan Influence of forest fragmentation on amphibian diversity in the nature reserve of Ambohitantely, highland Madagascar , 2000 .

[36]  C. Peres,et al.  Disturbance‐Mediated Mammal Persistence and Abundance‐Area Relationships in Amazonian Forest Fragments , 2007, Conservation biology : the journal of the Society for Conservation Biology.

[37]  W. Newmark,et al.  Extinction of mammal populations in Western North American national parks , 1995 .

[38]  L. P. Koh,et al.  Long‐Term Avifaunal Impoverishment in an Isolated Tropical Woodlot , 2006, Conservation biology : the journal of the Society for Conservation Biology.

[39]  L. P. Costa,et al.  The question of scale in threat analysis: a case study with Brazilian mammals , 1999 .

[40]  H. Tan,et al.  A Study of Plant Species Extinction in Singapore: Lessons for the Conservation of Tropical Biodiversity , 1994 .

[41]  A. Lynam,et al.  Differential responses of small mammals to fragmentation in a Thailand tropical forest , 1999 .

[42]  Helene C. Muller-Landau,et al.  The Future of Tropical Forest Species , 2006 .

[43]  W. Laurance Ecological Correlates of Extinction Proneness in Australian Tropical Rain Forest Mammals , 1991 .

[44]  L. Durrell Natural Change and Human Impact in Madagascar , 1998, Biodiversity & Conservation.

[45]  P. Ehrlich,et al.  Mammal Population Losses and the Extinction Crisis , 2002, Science.

[46]  Ilkka Hanski,et al.  Slow response of plant species richness to habitat loss and fragmentation. , 2005, Ecology letters.

[47]  Rodolfo Dirzo,et al.  Global State of Biodiversity and Loss , 2003 .

[48]  W. D. Robinson,et al.  Long‐Term Changes in the Avifauna of Barro Colorado Island, Panama, a Tropical Forest Isolate , 1999 .

[49]  N. Myers The Sinking Ark: A New Look at the Problem of Disappearing Species , 1979 .

[50]  J. Diamond,et al.  Bird Survival in an Isolated Javan Woodland: Island or Mirror? , 1987 .

[51]  Mark V. Lomolino,et al.  Ecology’s most general, yet protean 1 pattern: the species‐area relationship , 2000 .

[52]  C. Leck Avian Extinctions in an Isolated Tropical Wet-Forest Preserve, Ecuador , 1979 .

[53]  S. Goodman,et al.  The effects of forest fragmentation and isolation on insectivorous small mammals (Lipotyphla) on the Central High Plateau of Madagascar , 2000 .

[54]  H. Hillebrand,et al.  The imprint of the geographical, evolutionary and ecological context on species-area relationships. , 2006, Ecology letters.

[55]  Dar A. Roberts,et al.  Studies of land-cover, land-use, and biophysical properties of vegetation in the Large Scale Biosphere Atmosphere experiment in Amazonia , 2003 .

[56]  E. Willis Populations and Local Extinctions of Birds on Barro Colorado Island, Panama , 1974 .

[57]  C. Haddad,et al.  Habitat Split and the Global Decline of Amphibians , 2007, Science.

[58]  B. Zimmerman,et al.  Relevance of the equilibrium theory of island biogeography and species-area relations to conservation with a case from Amazonia , 1986 .

[59]  K. Gaston,et al.  The species–area relationship does not have an asymptote! , 2001 .

[60]  R. Dial Extinction or miscalculation? , 1994, Nature.

[61]  J. Diamond,et al.  Biogeographic kinetics: estimation of relaxation times for avifaunas of southwest pacific islands. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

[62]  P. Fearnside Deforestation in Brazilian Amazonia: History, Rates, and Consequences , 2005 .

[63]  W. Newmark A land-bridge island perspective on mammalian extinctions in western North American parks , 1987, Nature.

[64]  R. Macarthur,et al.  The Theory of Island Biogeography , 1969 .

[65]  M. B. Christiansen,et al.  Species loss in a forest bird community near Lagoa Santa in southeastern Brazil , 1997 .

[66]  Thomas M. Brooks,et al.  Time Lag between Deforestation and Bird Extinction in Tropical Forest Fragments , 1999 .

[67]  T. Case,et al.  Natural and Unnatural Extinction Rates of Reptiles on Islands , 1988, The American Naturalist.

[68]  Luis Miguel Renjifo Composition Changes in a Subandean Avifauna after Long‐Term Forest Fragmentation , 1999 .

[69]  A. Balmford,et al.  Atlantic forest extinctions , 1996, Nature.

[70]  William F. Laurance,et al.  The Future of the Brazilian Amazon , 2001, Science.

[71]  W. Wright,et al.  Bird declines over 22 years in forest remnants in southeastern Australia: Evidence of faunal relaxation? , 2006 .

[72]  P. Legendre,et al.  On Species-Area Relations , 1996, The American Naturalist.

[73]  T. Brooks Extinctions: consider all species , 2011 .

[74]  J. D. Pilgrim,et al.  Wilderness and biodiversity conservation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[75]  B. Soares-Filho,et al.  The End of Deforestation in the Brazilian Amazon , 2009, Science.

[76]  G. Cowlishaw Predicting the Pattern of Decline of African Primate Diversity: an Extinction Debt from Historical Deforestation , 1999 .

[77]  T. Larsen Forest butterflies in West Africa have resisted extinction… so far (Lepidoptera: Papilionoidea and Hesperioidea) , 2008, Biodiversity and Conservation.

[78]  S. Budiansky Extinction or miscalculation? , 1994, Nature.

[79]  J. L. Gittleman,et al.  The Future of Biodiversity , 1995, Science.

[80]  Kevin J. Gaston,et al.  Taxonomic and regional uncertainty in species-area relationships and the identification of richness hotspots , 2008, Proceedings of the National Academy of Sciences.

[81]  W. Newmark Tropical forest fragmentation and the local extinction of understory birds in the eastern Usambara Mountains, Tanzania , 1991 .

[82]  S. Hubbell,et al.  Species–area relationships always overestimate extinction rates from habitat loss , 2011, Nature.

[83]  E. Tjørve Shapes and functions of species–area curves: a review of possible models , 2003 .

[84]  T. Brooks,et al.  Deforestation Predicts the Number of Threatened Birds in Insular Southeast Asia , 1997 .

[85]  M. Hermy,et al.  Does the heathland flora in north-western Belgium show an extinction debt? , 2006 .

[86]  R. Ricklefs,et al.  The roles of island area per se and habitat diversity in the species-area relationships of four Lesser Antillean faunal groups , 1999 .

[87]  G. Asner,et al.  Cloud cover in Landsat observations of the Brazilian Amazon , 2001 .

[88]  A. Chiarello,et al.  Effects of fragmentation of the Atlantic forest on mammal communities in south-eastern Brazil , 1999 .

[89]  R. Wyman Population decline is a long way off. , 2011, Nature.

[90]  P. Stouffer,et al.  Twenty years of understorey bird extinctions from Amazonian rain forest fragments: consistent trends and landscape‐mediated dynamics , 2009 .

[91]  J. Barlow,et al.  The value of primary, secondary and plantation forests for Amazonian birds. , 2007 .

[92]  T. Givnish,et al.  Ecological Determinants of Species Loss in Remnant Prairies , 1996, Science.

[93]  Colin R. Trainor Changes in bird species composition on a remote and well-forested Wallacean Island, South-East Asia , 2007 .

[94]  P. Pyšek,et al.  Changes in composition and structure of urban flora over 120 years: a case study of the city of Plzeň , 2003 .

[95]  N. Sodhi,et al.  Heavy Extinctions of Forest Avifauna in Singapore: Lessons for Biodiversity Conservation in Southeast Asia , 2000, Conservation biology : the journal of the Society for Conservation Biology.

[96]  B. Klinkenberg,et al.  Forest loss with urbanization predicts bird extirpations in Vancouver , 2005 .

[97]  I. Hanski,et al.  Deforestation and apparent extinctions of endemic forest beetles in Madagascar , 2007, Biology Letters.

[98]  Douglas T. Bolger,et al.  Reconstructed Dynamics of Rapid Extinctions of Chaparral‐Requiring Birds in Urban Habitat Islands , 1988 .

[99]  M. Hermy,et al.  Plant species loss in an urban area (Turnhout, Belgium) from 1880 to 1999 and its environmental determinants , 2004 .

[100]  J. Metzger,et al.  Brazilian law: full speed in reverse? , 2010, Science.

[101]  J. Willig,et al.  Early Human Occupation IN Far Western North America: The Clovis-Archaic Interface , 1988 .

[102]  A. Báldi,et al.  Extinction debt of Hungarian reserves: A historical perspective , 2006 .

[103]  Earl D. McCoy,et al.  The Statistics and Biology of the Species-Area Relationship , 1979, The American Naturalist.

[104]  M. Rosenzweig,et al.  Species Diversity in Space and Time , 1995 .

[105]  C. E. Grelle Predicting extinction of mammals in the Brazilian Amazon , 2005, Oryx.

[106]  World Conservation Union , 1999 .

[107]  Jeremy P. Bird,et al.  Integrating spatially explicit habitat projections into extinction risk assessments: a reassessment of Amazonian avifauna incorporating projected deforestation , 2012 .

[108]  F. Achard,et al.  Determination of Deforestation Rates of the World's Humid Tropical Forests , 2002, Science.

[109]  G. Daily,et al.  Countryside Biogeography of Neotropical Mammals: Conservation Opportunities in Agricultural Landscapes of Costa Rica , 2003 .

[110]  James H. Brown Mammals on Mountaintops: Nonequilibrium Insular Biogeography , 1971, The American Naturalist.

[111]  David M. Stoms,et al.  Extinction rates under nonrandom patterns of habitat loss , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[112]  E. Willis,et al.  A revised list of birds of Barro Colorado Island, Panama , 1979 .