Anthropogenic disturbance in tropical forests can double biodiversity loss from deforestation

Journal name:
Nature
Volume:
535,
Pages:
144–147
Date published:
DOI:
doi:10.1038/nature18326
Received
Accepted
Published online

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.

At a glance

Figures

  1. The conservation status of primary forests.
    Figure 1: The conservation status of primary forests.

    a, Conservation value in Paragominas (circles) and Santarém (triangles). b, Total loss of conservation value due to disturbance. c, Total loss of conservation value due to disturbance expressed as a proportion of the expected conservation value without disturbance. 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. There was no significant difference in conservation values between regions in the median response (F1;26 = 1.45, P = 0.24, analysis of covariance (ANCOVA)).

  2. Conservation value deficit over large spatial scales.
    Figure 2: Conservation value deficit over large spatial scales.

    a, Proportionate loss of conservation value (CV) from disturbance in Pará (median estimate; see Methods). Areas of endemism (AoE) are: Belém (BE), Guiana (GU), Rondônia (RO), Tapajós (TA) and Xingu (XI). These do not include the island of Marajó (MA). Grey shading denotes strictly protected areas. b, Proportionate loss of CV in Pará (PA) and its AoEs from forest loss and disturbance (median estimate). Error bars show the range over all approaches to estimating conservation value (see Methods). Numbers show disturbance relative to forest loss (percentage range over approaches).

  3. Response of forest birds to disturbance.
    Figure 3: Response of forest birds to disturbance.

    ad, The odds of detecting species groups along gradients of landscape (a, b) and within-forest (c, d) disturbance in Paragominas (a, c) and Santarém (b, d) (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. eh, Disturbance sensitivity of the species groups related to their mean range size (107 km2). Error bars shows s.e.m. Group colours correspond to groupings in ad. Black lines show significant relationships (P < 0.05, F-test) (see Methods).

  4. Response of large-stemmed plants to disturbance.
    Figure 4: Response of large-stemmed plants to disturbance.

    ad, The odds of detecting species groups along gradients of landscape (a, b) and within-forest (c, d) disturbance in Paragominas (a, c) and Santarém (b, d) (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. eh, Disturbance sensitivity of the species groups related to their mean wood density (g cm−3). Error bars show s.e.m. Group colours correspond to groupings in ad. Black lines show significant relationships (P < 0.05, F-test) (see Methods).

  5. Study design.
    Extended Data Fig. 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.

  6. Richness of forest species.
    Extended Data Fig. 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).

  7. Conservation value of primary forests measured by individual taxa.
    Extended Data Fig. 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).

  8. Range of conservation value estimates using three alternative sets of reference plots.
    Extended Data Fig. 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.

  9. The importance of hypothesis selected variables.
    Extended Data Fig. 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).

  10. The importance of PCA selected variables.
    Extended Data Fig. 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).

  11. The importance of step-wise selected variables.
    Extended Data Fig. 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).

  12. Responses of small-stemmed plants and dung beetles to disturbance.
    Extended Data Fig. 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.

Tables

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

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Author information

Affiliations

  1. Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, UK

    • Jos Barlow,
    • Gareth D. Lennox,
    • Erika Berenguer,
    • Julio Louzada,
    • Victor Hugo Fonseca Oliveira,
    • Luke Parry &
    • Juliana M. Silveira
  2. MCTI/Museu Paraense Emílio Goeldi, CP 399, Belém, Pará, CEP 66040-170, Brazil

    • Jos Barlow,
    • Alexander C. Lees,
    • Ima C. G. Vieira &
    • Nárgila G. Moura
  3. Universidade Federal de Lavras, Setor de Ecologia e Conservação. Lavras, Minas Gerais, CEP 37200-000, Brazil

    • Jos Barlow,
    • Julio Louzada,
    • Victor Hugo Fonseca Oliveira,
    • Rodrigo F. Braga &
    • Juliana M. Silveira
  4. EMBRAPA Amazônia Oriental. Belém, Pará, CEP 66095-100, Brazil

    • Joice Ferreira,
    • Thiago Moreira Cardoso,
    • Raimundo Cosme de Oliveira Jr &
    • Adriano Venturieri
  5. Cornell Lab of Ornithology, Cornell University, Ithaca, New York 14850, USA

    • Alexander C. Lees &
    • Nárgila G. Moura
  6. Institute for Applied Ecology, University of Canberra, Bruce, Australian Capital Territory 2617, Australia

    • Ralph Mac Nally &
    • James R. Thomson
  7. Arthur Rylah Institute for Environmental Research, Department of Environment, Land, Water and Planning, 123 Brown Street, Heidelberg, Victoria 3084, Australia

    • James R. Thomson
  8. Universidade de São Paulo, Escola Superior de Agricultura “Luiz de Queiroz”, Esalq/USP, Avenida Pádua Dias, 11, São Dimas, Piracicaba, SP, CEP 13418-900, Brazil

    • Silvio Frosini de Barros Ferraz &
    • Rodrigo Anzolin Begotti
  9. Universidade Federal do Pará (UFPA), Núcleo de Altos Estudos Amazonicos (NAEA), Av. Perimetral, Numero 1, Guamá, Belém-Pará, CEP 66075-750, Brazil

    • Luke Parry
  10. Universidade Federal de Viçosa, Departamento de Biologia Geral. Av. PH Rolfs s/n. Viçosa, Minas Gerais, CEP 36570-900, Brazil

    • Ricardo Ribeiro de Castro Solar
  11. Tropical Ecosystems and Environmental Sciences Group (TREES), Remote Sensing Division, National Institute for Space Research (INPE), Avenida dos Astronautas, 1.758, Jd. Granja, São José dos Campos, CEP 12227-010, SP, Brazil

    • Luiz E. O. C. Aragão
  12. College of Life and Environmental Sciences, University of Exeter, Exeter EX4 4RJ, UK

    • Luiz E. O. C. Aragão
  13. IMAZON, Rua Dom Romualdo de Seixas 1698, Edifício Zion, 11 andar, CEP 66055-200 Belém, PA, Brazil

    • Carlos M. Souza Jr,
    • Sâmia Serra Nunes &
    • João Victor Siqueira
  14. Instituto de Biociencias, Universidade de São Paulo, Rua do Matão, Travessa 14, 101, CEP 05508-090 São Paulo, Brazil

    • Renata Pardini
  15. Universidade Federal de Mato Grosso, Instituto de Biociencias, Departamento de Biologia e Zoologia. Av. Fernando Correa da Costa, 2367, Boa Esperança, CEP 78060-900, Cuiaba, MT, Brazil

    • Fernando Z. Vaz-de-Mello
  16. Instituto Socio Ambiental Serra do Mar (ISASM), Estrada Ribeirão das Voltas s/n, Lumiar, CEP 28616-010, Nova Friburgo, Brazil

    • Ruan Carlo Stulpen Veiga
  17. Stockholm Environment Institute, Linnégatan 87D, Box 24218, Stockholm 104 51, Sweden

    • Toby A. Gardner
  18. International Institute for Sustainability, Estrada Dona Castorina, 124, Horto, Rio de Janeiro, 22460-320, Brazil

    • Toby A. Gardner

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.

Competing financial interests

The authors declare no competing financial interests.

Corresponding author

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Author details

Extended data figures and tables

Extended Data Figures

  1. Extended Data Figure 1: Study design. (670 KB)

    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.

  2. Extended Data Figure 2: Richness of forest species. (290 KB)

    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).

  3. Extended Data Figure 3: Conservation value of primary forests measured by individual taxa. (206 KB)

    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).

  4. Extended Data Figure 4: Range of conservation value estimates using three alternative sets of reference plots. (130 KB)

    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.

  5. Extended Data Figure 5: The importance of hypothesis selected variables. (383 KB)

    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).

  6. Extended Data Figure 6: The importance of PCA selected variables. (382 KB)

    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).

  7. Extended Data Figure 7: The importance of step-wise selected variables. (376 KB)

    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).

  8. Extended Data Figure 8: Responses of small-stemmed plants and dung beetles to disturbance. (248 KB)

    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 Tables

  1. Extended Data Table 1: Policy interventions used to reduce deforestation and their effect on disturbance (329 KB)
  2. Extended Data Table 2: Forest loss and disturbance in Pará and its areas of endemism (309 KB)

Additional data