Anthropogenic disturbance in tropical forests can double biodiversity loss from deforestation

Abstract

Concerted political attention has focused on reducing deforestation1,2,3, and this remains the cornerstone of most biodiversity conservation strategies4,5,6. However, maintaining forest cover may not reduce anthropogenic forest disturbances, which are rarely considered in conservation programmes6. These disturbances occur both within forests, including selective logging and wildfires7,8, and at the landscape level, through edge, area and isolation effects9. Until now, the combined effect of anthropogenic disturbance on the conservation value of remnant primary forests has remained unknown, making it impossible to assess the relative importance of forest disturbance and forest loss. Here we address these knowledge gaps using a large data set of plants, birds and dung beetles (1,538, 460 and 156 species, respectively) sampled in 36 catchments in the Brazilian state of Pará. Catchments retaining more than 69–80% forest cover lost more conservation value from disturbance than from forest loss. For example, a 20% loss of primary forest, the maximum level of deforestation allowed on Amazonian properties under Brazil’s Forest Code5, resulted in a 39–54% loss of conservation value: 96–171% more than expected without considering disturbance effects. We extrapolated the disturbance-mediated loss of conservation value throughout Pará, which covers 25% of the Brazilian Amazon. Although disturbed forests retained considerable conservation value compared with deforested areas, the toll of disturbance outside Pará’s strictly protected areas is equivalent to the loss of 92,000–139,000 km2 of primary forest. Even this lowest estimate is greater than the area deforested across the entire Brazilian Amazon between 2006 and 2015 (ref. 10). Species distribution models showed that both landscape and within-forest disturbances contributed to biodiversity loss, with the greatest negative effects on species of high conservation and functional value. These results demonstrate an urgent need for policy interventions that go beyond the maintenance of forest cover to safeguard the hyper-diversity of tropical forest ecosystems.

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Figure 1: The conservation status of primary forests.
Figure 2: Conservation value deficit over large spatial scales.
Figure 3: Response of forest birds to disturbance.
Figure 4: Response of large-stemmed plants to disturbance.

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Acknowledgements

This work was supported by grants from Brazil (CNPq 574008/2008-0, 458022/2013-6, and 400640/2012-0; Embrapa SEG:02.08.06.005.00; The Nature Conservancy – Brasil; CAPES scholarships) the UK (Darwin Initiative 17-023; NE/F01614X/1; NE/G000816/1; NE/F015356/2; NE/l018123/1; NE/K016431/1), Formas 2013-1571, and Australian Research Council grant DP120100797. Institutional support was provided by the Herbário IAN in Belém, LBA in Santarém and FAPEMAT. R.M. and J.R.T. were supported by Australian Research Council grant DP120100797. This is paper no. 49 in the Sustainable Amazon Network series.

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Authors

Contributions

T.A.G., J.F. and J.B. designed the research with additional input from E.B., A.C.L., S.F.B.F., J.L., V.H.F.O., L.P., R.R.C.S., I.C.G.V., L.E.O.C.A. and R.P. E.B., A.C.L., V.H.F.O., R.R.C.S, R.F.B., J.F., R.C.O., N.G.M. R.C.S.V., J.L., J.M.S and F.Z.V. collected the field data or analysed biological or soil samples. G.D.L. analysed the data, with input from J.B., J.R.T., R.M., A.C.L. and T.A.G. S.F.B.F., R.A.B., T.M.C., C.M.S., S.S.N., J.V.S., A.V. and T.A.G. processed the remote sensing data. J.B., G.D.L., J.F., A.C.L., R.M., J.R.T. and T.A.G. wrote the manuscript, with input from all authors.

Corresponding author

Correspondence to Jos Barlow.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Study design.

a, The location of Paragominas and Santarém within Pará. b, c, The distribution of study catchments (n = 36) within Paragominas and Santarém, respectively. d, The distribution of study plots (n = 175) in example catchments spanning the gradient of primary forest. Selected catchments are shown in red in a and b. e, Sampling design within each plot.

Extended Data Figure 2 Richness of forest species.

ac, The richness of forest species in secondary forests (SF), pastures (PA), and mechanised agricultural lands (AG) relative to the average richness of forest species in all undisturbed and disturbed primary forests (dashed line) in Paragominas (green) and Santarém (orange). Panels show the convex hull (a), automatic (b) and high basal area filters (c) used to classify forest species (see Methods).

Extended Data Figure 3 Conservation value of primary forests measured by individual taxa.

ad, Estimates of conservation value in the Paragominas (circles) and Santarém (triangles) study regions from large-stemmed plants (a) small-stemmed plants (b) birds (c) and dung beetles (d). Dashed lines show expectations without disturbance. Grey lines show all regressions, with the black solid line showing the median response (see Methods). Values were standardized across study regions and taxa. There was no significant difference between taxa in the median estimate (F3;117 = 1.36, P = 0.26, ANCOVA).

Extended Data Figure 4 Range of conservation value estimates using three alternative sets of reference plots.

Mean species density (de) is measured by: all disturbed and undisturbed plots in the least disturbed reference catchments (grey shaded region), all undisturbed plots throughout a region (green shaded region), and undisturbed plots in the reference catchments (purple shaded region). See Methods for details.

Extended Data Figure 5 The importance of hypothesis selected variables.

ah, Species AUCcv values for each variable in Paragominas (a, c, e, g) and Santarém (b, d, f, h) for large-stemmed plants (a, b), small-stemmed plants (c, d), birds (e, f) and beetles (g, h). Variable importance was measured by the mean AUCcv over all well-modelled species (see Methods). Variable colours denote group membership: green, orange and blue represent landscape disturbance, within-forest disturbance and natural variables, respectively (see Methods for variable descriptions). Letters show the results for multiple pair-wise comparisons of group means using Tukey’s range test. Variables which do not share a letter have significantly different mean importance (P < 0.05).

Extended Data Figure 6 The importance of PCA selected variables.

ah, Species’ AUCcv values for each variable in Paragominas (a, c, e, g) and Santarém (b, d, f, h) for large-stemmed plants (a, b), small-stemmed plants (c, d), birds (e, f) and beetles (g, h). Variable importance was measured by the mean AUCcv over all well-modelled species (see Methods). Variable colours denote group membership: green, orange and blue represent landscape disturbance, within-forest disturbance and natural variables, respectively (see Methods for variable descriptions). Letters show the results for multiple pair-wise comparisons of group means using Tukey’s range test. Variables which do not share a letter have significantly different mean importance (P < 0.05).

Extended Data Figure 7 The importance of step-wise selected variables.

ah, Species’ AUCcv values for each variable in Paragominas (a, c, e, g) and Santarém (b, d, f, h) for large-stemmed plants (a, b), small-stemmed plants (c, d), birds (e, f) and beetles (g, h). Variable importance is measured by the mean AUCcv over all well-modelled species (see Methods). Variable colours denote group membership: green, orange and blue represent landscape disturbance, within-forest disturbance and natural variables, respectively (see Methods for variable descriptions). Letters show the results for multiple pair-wise comparisons of group means using Tukey’s range test. Variables which do not share a letter have significantly different mean importance (P < 0.05).

Extended Data Figure 8 Responses of small-stemmed plants and dung beetles to disturbance.

ah, The odds of detecting small-stemmed plants (ad) and dung beetles (eh) species groups along gradients of landscape disturbance (a, b, e, f) and within-forest disturbance (c, d, g, h) in Paragominas (a, c, e, g) and Santarém (b, d, f, h) (see Methods). Species groups, shown by different coloured lines, are composed of species with similar disturbance responses (see Methods). Line thickness represents the relative size of the groups.

Extended Data Table 1 Policy interventions used to reduce deforestation and their effect on disturbance
Extended Data Table 2 Forest loss and disturbance in Pará and its areas of endemism

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Barlow, J., Lennox, G., Ferreira, J. et al. Anthropogenic disturbance in tropical forests can double biodiversity loss from deforestation. Nature 535, 144–147 (2016). https://doi.org/10.1038/nature18326

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