Abstract
Global biodiversity loss is a critical environmental crisis, yet the lack of spatial data on biodiversity threats has hindered conservation strategies1. Theory predicts that abrupt biodiversity declines are most likely to occur when habitat availability is reduced to very low levels in the landscape (10–30%)2,3,4. Alternatively, recent evidence indicates that biodiversity is best conserved by minimizing human intrusion into intact and relatively unfragmented landscapes5. Here we use recently available forest loss data6 to test deforestation effects on International Union for Conservation of Nature Red List categories of extinction risk for 19,432 vertebrate species worldwide. As expected, deforestation substantially increased the odds of a species being listed as threatened, undergoing recent upgrading to a higher threat category and exhibiting declining populations. More importantly, we show that these risks were disproportionately high in relatively intact landscapes; even minimal deforestation has had severe consequences for vertebrate biodiversity. We found little support for the alternative hypothesis that forest loss is most detrimental in already fragmented landscapes. Spatial analysis revealed high-risk hot spots in Borneo, the central Amazon and the Congo Basin. In these regions, our model predicts that 121–219 species will become threatened under current rates of forest loss over the next 30 years. Given that only 17.9% of these high-risk areas are formally protected and only 8.9% have strict protection, new large-scale conservation efforts to protect intact forests7,8 are necessary to slow deforestation rates and to avert a new wave of global extinctions.
Access options
Subscribe to Journal
Get full journal access for 1 year
$199.00
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
from$8.99
All prices are NET prices.
References
- 1.
Joppa, L. N. et al. Filling in biodiversity threat gaps. Science 352, 416–418 (2016)
- 2.
Newbold, T. et al. Has land use pushed terrestrial biodiversity beyond the planetary boundary? A global assessment. Science 353, 288–291 (2016)
- 3.
Andrén, H. Effects of habitat fragmentation of birds and mammals in landscapes with different proportions of suitable habitat: a review. Oikos 71, 355–366 (1994)
- 4.
Betts, M. G., Forbes, G. J. & Diamond, A. W. Thresholds in songbird occurrence in relation to landscape structure. Conserv. Biol. 21, 1046–1058 (2007)
- 5.
Barlow, J. et al. Anthropogenic disturbance in tropical forests can double biodiversity loss from deforestation. Nature 535, 144–147 (2016)
- 6.
Hansen, M. C. et al. High-resolution global maps of 21st-century forest cover change. Science 342, 850–853 (2013)
- 7.
Peres, C. A. Why we need megareserves in Amazonia. Conserv. Biol. 19, 728–733 (2005)
- 8.
Gibson, L. et al. Primary forests are irreplaceable for sustaining tropical biodiversity. Nature 478, 378–381 (2011)
- 9.
Brooks, T. M. et al. Global biodiversity conservation priorities. Science 313, 58–61 (2006)
- 10.
Kareiva, P., Watts, S., McDonald, R. & Boucher, T. Domesticated nature: shaping landscapes and ecosystems for human welfare. Science 316, 1866–1869 (2007)
- 11.
Mendenhall, C. D., Karp, D. S., Meyer, C. F., Hadly, E. A. & Daily, G. C. Predicting biodiversity change and averting collapse in agricultural landscapes. Nature 509, 213–217 (2014)
- 12.
Fahrig, L. When does fragmentation of breeding habitat affect population survival? Ecol. Modell. 105, 273–292 (1998)
- 13.
Phalan, B., Onial, M., Balmford, A. & Green, R. E. Reconciling food production and biodiversity conservation: land sharing and land sparing compared. Science 333, 1289–1291 (2011)
- 14.
Wilson, E. O. Half-Earth: Our Planet’s Fight For Life. (W. W. Norton & Company, 2016)
- 15.
International Union for Conservation of Nature World Congress. Motion 48: Protection of primary forests, including intact forest landscapes. (2016)
- 16.
Tracewski, Ł. et al. Toward quantification of the impact of 21st-century deforestation on the extinction risk of terrestrial vertebrates. Conserv. Biol. 30, 1070–1079 (2016)
- 17.
International Union for Conservation of Nature. IUCN red list of threatened species. Version 2016.3 http://www.iucnredlist.org (2017)
- 18.
BirdLife International and NatureServe. Bird Species Distribution Maps of the World Version 5.0 (BirdLife International, 2015)
- 19.
Kim, D.-H. et al. Global, Landsat-based forest-cover change from 1990 to 2000. Remote Sens. Environ. 155, 178–193 (2014)
- 20.
Tilman, D., May, R. M., Lehman, C. L. & Nowak, M. A. Habitat destruction and the extinction debt. Nature 371, 65–66 (1994)
- 21.
Wearn, O. R., Reuman, D. C. & Ewers, R. M. Extinction debt and windows of conservation opportunity in the Brazilian Amazon. Science 337, 228–232 (2012)
- 22.
Sanderson, E. W. et al. The human footprint and the last of the wild. Bioscience 52, 891–904 (2002)
- 23.
Hanski, I. Metapopulation dynamics. Nature 396, 41–49 (1998)
- 24.
Brooks, T. M. et al. Habitat loss and extinction in the hotspots of biodiversity. Conserv. Biol. 16, 909–923 (2002)
- 25.
Balmford, A. Extinction filters and current resilience: the significance of past selection pressures for conservation biology. Trends Ecol. Evol. 11, 193–196 (1996)
- 26.
Ripple, W. J. et al. Bushmeat hunting and extinction risk to the world’s mammals. R. Soc. Open Sci. 3, 160498 (2016)
- 27.
Benítez-López, A. et al. The impact of hunting on tropical mammal and bird populations. Science 356, 180–183 (2017)
- 28.
Bellard, C., Genovesi, P. & Jeschke, J. M. Global patterns in threats to vertebrates by biological invasions. Proc. R. Soc. Lond. B 283, 20152454 (2016)
- 29.
Clavel, J., Julliar, R. & Devictor, V. Worldwide decline of specialist species: toward a global functional homogenization. Front. Ecol. Environ. 9, 222–228 (2011)
- 30.
Betts, M. G. et al. A species-centered approach for uncovering generalities in organism responses to habitat loss and fragmentation. Ecography 37, 517–527 (2014)
- 31.
Potapov, P. et al. The last frontiers of wilderness: tracking loss of intact forest landscapes from 2000 to 2013. Sci. Adv. 3, e1600821 (2017)
- 32.
Potapov, P. et al. Mapping the world’s intact forest landscapes by remote sensing. Ecol. Soc. 13, 51 (2008)
- 33.
Olson, D. M. et al. Terrestrial ecoregions of the world: a new map of life on Earth: a new global map of terrestrial ecoregions provides an innovative tool for conserving biodiversity. Bioscience 51, 933–938 (2001)
- 34.
IUCN and UNEP-WCMC. The World Database on Protected Areas (WDPA) http://www.protectedplanet.net/terms (2015)
- 35.
Butchart, S. H. et al. Improvements to the red list index. PLoS ONE 2, e140 (2007)
- 36.
Butchart, S. H. et al. Measuring global trends in the status of biodiversity: red list indices for birds. PLoS Biol. 2, e383 (2004)
- 37.
Hoffmann, M. et al. The changing fates of the world’s mammals. Phil. Trans. R. Soc. Lond. B 366, 2598–2610 (2011)
- 38.
BirdLife International. IUCN Red List for birds. http://www.birdlife.org (2017)
- 39.
Böhm, M. et al. The conservation status of the world’s reptiles. Biol. Conserv. 157, 372–385 (2013)
- 40.
Wildlife Conservation Society and Center for International Earth Science Information Network, Columbia University. Last of the Wild, v2: Global Human Footprint Dataset (Geographic). http://dx.doi.org/10.7927/H4M61H5F (2005)
- 41.
Venter, O. et al. Sixteen years of change in the global terrestrial human footprint and implications for biodiversity conservation. Nat. Commun. 7, 12558 (2016)
- 42.
Venter, O. et al. Data from: Global terrestrial Human Footprint maps for 1993 and 2009. http://dx.doi.org/10.5061/dryad.052q5 (2016)
- 43.
ESRI. ArcGIS Desktop: Release 10.1 (Environmental Systems Research Institute, 2012)
- 44.
R Core Team. R: A Language and Environment for Statistical Computing. http://www.R-project.org/ (2013)
- 45.
Seligman, M. Rborist: extensible, parallelizable implementation of the random forest algorithm. https://cran.r-project.org/web/packages/Rborist/index.html (2015)
- 46.
Hurlbert, A. H. & Jetz, W. Species richness, hotspots, and the scale dependence of range maps in ecology and conservation. Proc. Natl Acad. Sci. USA 104, 13384–13389 (2007)
- 47.
Augustin, N. H., Mugglestone, M. A. & Buckland, S. T. An autologistic model for the spatial distribution of wildlife. J. Appl. Ecol. 33, 339–347 (1996)
- 48.
Dormann, C. F. Assessing the validity of autologistic regression. Ecol. Modell. 207, 234–242 (2007)
- 49.
Bivand, R. et al. spdep: spatial dependence: weighting schemes, statistics and models. https://cran.r-project.org/web/packages/spdep/index.html (2017)
- 50.
Pike, N. Using false discovery rates for multiple comparisons in ecology and evolution. Methods Ecol. Evol. 2, 278–282 (2011)
- 51.
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289–300 (1995)
- 52.
Swets, J. A. Signal Detection Theory and ROC Analysis in Psychology and Diagnostics: Collected Papers (Psychology Press, 2014)
- 53.
United Nations. United Nations Statistics Division. Standard Country and Area Codes Classifications (M49). http://unstats.un.org/unsd/methods/m49/m49regin.htm (2013)
- 54.
Bahn, V. & McGill, B. J. Testing the predictive performance of distribution models. Oikos 122, 321–331 (2013)
- 55.
Gilleland, M. E. verification: weather forecast verification utilities. https://cran.r-project.org/web/packages/verification/index.html (2015)
- 56.
Dray, S., Legendre, P. & Peres-Neto, P. R. Spatial modelling: a comprehensive framework for principal coordinate analysis of neighbour matrices (PCNM). Ecol. Modell. 196, 483–493 (2006)
- 57.
Lee, D. CARBayes: an R package for Bayesian spatial modelling with conditional autoregressive priors. J. Stat. Softw. 55, 13 (2013)
- 58.
McMillen, D. McSpatial: nonparametric spatial data analysis. https://cran.r-project.org/web/packages/McSpatial/index.html (2013)
- 59.
Klier, T. & McMillen, D. P. Clustering of auto supplier plants in the United States. J. Bus. Econ. Stat. 26, 460–471 (2012)
- 60.
Cardillo, M. et al. Multiple causes of high extinction risk in large mammal species. Science 309, 1239–1241 (2005)
- 61.
Bates, D. M. lme4: Mixed-effects modeling with R. http://lme4.r-forge.r-project.org/book (2010)
- 62.
Ives, A. R. & Garland, T. Jr. Phylogenetic logistic regression for binary dependent variables. Syst. Biol. 59, 9–26 (2010)
- 63.
Petersen, R. et al. Mapping Tree Plantations with Multispectral Imagery: Preliminary Results for Seven Tropical Countries. (World Resources Institute, 2016)
- 64.
MacDicken, K. G. Global Forest Resources Assessment 2015: what, why and how? For. Ecol. Manage. 352, 3–8 (2015)
- 65.
Giam, X. et al. Reservoirs of richness: least disturbed tropical forests are centres of undescribed species diversity. Proc. R. Soc. Lond. B 279, 67–76 (2012)
- 66.
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005)
Acknowledgements
Funding from the National Science Foundation (NSF-DEB-1457837) and the College of Forestry IWFL Professorship in Forest Biodiversity Research to M.G.B. supported this research. We are grateful for comments from A. Hadley, U. Kormann, J. Bowman, C. Epps and C. Mendenhall on earlier versions of this manuscript.
Author information
Author notes
- Matthew G. Betts
- & Christopher Wolf
These authors contributed equally to this work.
Affiliations
Forest Biodiversity Research Network, Department of Forest Ecosystems and Society, Oregon State University, Corvallis, Oregon 97331, USA
- Matthew G. Betts
- , Christopher Wolf
- , William J. Ripple
- , Ben Phalan
- & Taal Levi
Global Trophic Cascades Program, Department of Forest Ecosystems and Society, Oregon State University, Corvallis, Oregon 97331, USA
- Matthew G. Betts
- , Christopher Wolf
- & William J. Ripple
Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK
- Ben Phalan
- & Stuart H. M. Butchart
Department of Fisheries and Wildlife, Oregon State University, Corvallis, Oregon 97331, USA
- Kimberley A. Millers
- & Taal Levi
Oregon Cooperative Fish and Wildlife Research Unit, Department of Fisheries and Wildlife, Oregon State University, Corvallis, Oregon 97331, USA
- Adam Duarte
BirdLife International, David Attenborough Building, Pembroke Street, Cambridge CB2 3QZ, UK
- Stuart H. M. Butchart
Authors
Search for Matthew G. Betts in:
Search for Christopher Wolf in:
Search for William J. Ripple in:
Search for Ben Phalan in:
Search for Kimberley A. Millers in:
Search for Adam Duarte in:
Search for Stuart H. M. Butchart in:
Search for Taal Levi in:
Contributions
M.G.B., C.W., S.H.M.B., W.J.R. and T.L. conceived the study, C.W., M.G.B. and T.L. analysed the data, and M.G.B. and C.W. wrote the first draft of the paper with subsequent editorial input from C.W., B.P., S.H.M.B., K.A.M. and A.D.
Competing interests
The authors declare no competing financial interests.
Corresponding authors
Correspondence to Matthew G. Betts or Christopher Wolf.
Reviewer Information Nature thanks J. Barlow, L. Gibson and the other anonymous reviewer(s) for their contribution to the peer review of this work.
Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended data
Extended data figures
- 1.
Receiver operating characteristic (ROC) curves for the models predicting status of forest exclusive species.
- 2.
Model results for models fit by class (mammals, amphibians, birds) and for all classes together (All).
- 3.
Sensitivity analysis results.
- 4.
Estimated standardized coefficients for each model term (with 95% confidence intervals as error bars) when a quadratic forest loss × cover2 interaction (forest loss × cover2) is included in the model.
- 5.
The effect of forest loss (for 2% additional loss) in relation to total forest cover using quadratic models.
- 6.
Results of multiple spatial models (estimates and 95% confidence intervals as error bars) for forest exclusive species when status (that is, whether or not a species is threatened) is used as the response.
- 7.
Relationship between forest loss 1990–2000 (from ref. 34) and 2000–2014 (from ref. 7).
- 8.
Country-level forest net loss (that is, change in percentage forest cover) for the 1990–2000 and 2000–2015 periods according to the Food and Agriculture Organization’s (FAO) Global Forest Resources Assessment.
- 9.
Sensitivity of our results to alternative categories of threat.
- 10.
Maps showing the methods used to quantify historical forest loss.
Supplementary information
PDF files
- 1.
Supplementary Information
This file contains Supplementary Tables 1-5.
Rights and permissions
To obtain permission to re-use content from this article visit RightsLink.
About this article
Further reading
-
The exceptional value of intact forest ecosystems
Nature Ecology & Evolution (2018)
-
Social-ecological outcomes of agricultural intensification
Nature Sustainability (2018)
-
Land-use change interacts with climate to determine elevational species redistribution
Nature Communications (2018)
-
Cattle-driven forest disturbances impact ensemble composition and activity levels of insectivorous bats in Mediterranean wood pastures
Agroforestry Systems (2018)
-
Multi-criteria spatial identification of carnivore conservation areas under data scarcity and conflict: a jaguar case study in Sierra Nevada de Santa Marta, Colombia
Biodiversity and Conservation (2018)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.