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Humid tropical vertebrates are at lower risk of extinction and population decline in forests with higher structural integrity

Nature Ecology & Evolution volume 6, pages 1840–1849 (2022)Cite this article

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Abstract

Reducing deforestation underpins global biodiversity conservation efforts. However, this focus on retaining forest cover overlooks the multitude of anthropogenic pressures that can degrade forest quality and imperil biodiversity. We use remotely sensed indices of tropical rainforest structural condition and associated human pressures to quantify the relative importance of forest cover, structural condition and integrity (the cumulative effect of condition and pressures) on vertebrate species extinction risk and population trends across the global humid tropics. We found that tropical rainforests of high integrity (structurally intact and under low pressures) were associated with lower likelihood of species being threatened and having declining populations, compared with forest cover alone (without consideration of condition and pressures). Further, species were more likely to be threatened or have declining populations if their geographic ranges contained high proportions of degraded forest than if their ranges contained lower proportions of forest cover but of high quality. Our work suggests that biodiversity conservation policies to preserve forest integrity are now urgently required alongside ongoing efforts to halt deforestation in the hyperdiverse humid tropics.

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Fig. 1: The relative importance of forest integrity, structural condition and forest cover on the odds of mammals, birds, reptiles and amphibians being threatened and having declining population trends.
Fig. 2: Predicted probabilities of tropical rainforest-obligate and rainforest-associated mammal, bird, reptile and amphibian species being threatened and having declining population trends.
Fig. 3: Predicted probabilites of rainforest-obligate mammals, birds, reptiles and amphibians being threatened and having declining population trends across the four biogeographic realms within the tropical rainforest biome.

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Data availability

All datasets used in this paper are openly available via the citations identified in the Methods. Processed spreadsheets can be accessed at Zenodo https://doi.org/10.5281/zenodo.7036360.

Code availability

Python and R code to replicate geospatial and statistical analyses can also be accessed through the same Zenodo repository https://doi.org/10.5281/zenodo.7036360. Additional Python code to process species range maps before raster overlay and tabulation of area can be accessed at https://doi.org/10.5281/zenodo.5525586.

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Acknowledgements

This work was funded by the NASA Biodiversity and Ecological Forecasting Program under the 2016 ECO4CAST solicitation through grant NNX17AG51G to A.J.H., J.E., S.J.G, P.A.J., J.E.M.W. and O.V., the NASA Global Ecosystem Dynamics Investigation (NNL15AA03 to S.J.G.) and the NASA GEO solicitation (80NSSC18K0338 to P.A.J.).

Author information

Authors and Affiliations

  1. Natural Resources and Environmental Studies Institute, University of Northern British Columbia, Prince George, British Columbia, Canada

    Rajeev Pillay, Jose Aragon-Osejo & Oscar Venter

  2. School of Earth and Environmental Sciences, The University of Queensland, Brisbane, Queensland, Australia

    James E. M. Watson & Brooke A. Williams

  3. Centre for Biodiversity and Conservation Science, The University of Queensland, Brisbane, Queensland, Australia

    James E. M. Watson & Brooke A. Williams

  4. Department of Ecology, Montana State University, Bozeman, MT, USA

    Andrew J. Hansen

  5. School of Informatics, Computing and Cyber Systems, Northern Arizona University, Flagstaff, AZ, USA

    Patrick A. Jantz, Patrick Burns & Scott J. Goetz

  6. Departamento de Biología, Facultad de Ciencias, Universidad Nacional de Colombia, Bogotá, Colombia

    Dolors Armenteras

  7. United Nations Development Programme, New York, NY, USA

    Scott C. Atkinson, Jamison Ervin, Christina Supples & Anne L. S. Virnig

  8. Rui Nabeiro Biodiversity Chair, MED Institute, Universidade de Évora, Évora, Portugal

    Pamela González-del-Pliego

  9. The Nature Conservancy, Missoula, MT, USA

    Nathaniel P. Robinson

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  1. Rajeev Pillay
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Contributions

R.P. conceived this study with O.V., J.E.M.W. and A.J.H. providing major inputs. J.A.O. and R.P. developed the Python code for geospatial analyses. P.A.J. simulated potential error in mapping canopy cover and height for SCI and FSII data. N.P.R. processed change in SCI and forest cover loss data. P.G.D.P. provided amphibian range maps not available in the IUCN Red List. R.P. performed all geospatial and statistical analyses and wrote the manuscript. O.V., J.E.M.W., A.J.H., S.J.G., P.A.J., P.B., C.S., D.A., B.A.W., P.G.D.P., J.A.O., N.P.R., S.C.A., J.E. and A.L.S.V. reviewed and edited manuscript drafts.

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Correspondence to Rajeev Pillay.

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Nature Ecology & Evolution thanks Daniele Baisero, Matthew Betts and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 The relative importance of forest integrity, structural condition, the human footprint or pressure, and forest cover on the odds of mammals, birds, reptiles, and amphibians being threatened and having declining population trends (for sample sizes, see Supplementary Table 1a).

Structural condition and human pressures considered together (that is, FSII) tended to be associated with lower odds of species extinction risk and declining population trends than either structural condition or human pressures individually. Point estimates represent median standardized odds ratios of species being threatened (circles) or having a declining population (squares), generated by exponentiating standardized coefficients (log odds) of 100 phylogenetic logistic regressions (Supplementary Table 3). The vertical dotted line represents an odds ratio of 1, denoting statistical non-significance. Error bars represent median 95% confidence intervals generated with 2,000 parametric bootstraps in each regression. Each regression was performed with one phylogenetic tree randomly drawn from 10,000 available trees for each taxonomic group. Separate models were parameterized for rainforest-obligate and rainforest-associated species for each response variable. Illustration credits: Steven Traver, Ferran Sayol, Birgit Szabo, and Jose Carlos Arenas-Monroy.

Extended Data Fig. 2 Predicted probabilities of tropical rainforest-obligate and associated mammal, bird, reptile, and amphibian species being threatened and having declining population trends as a function of two-way interactions between forest structural condition and integrity.

Species tended to be at higher risk of being threatened and having declining populations when high proportions of forest cover within their ranges were structurally intact but of low integrity (that is, under high human pressure) than when their ranges contained low proportions of forest cover in high structural condition and low human pressure. Median predicted probabilities were generated from 100 phylogenetic logistic regressions. See Supplementary Tables 1a and 6 for sample sizes and model estimates, respectively. Illustration credits: Steven Traver, Ferran Sayol, Birgit Szabo, and Jose Carlos Arenas-Monroy.

Extended Data Fig. 3 Predicted probabilities of rainforest-associated mammals, birds, reptiles, and amphibians being threatened and having declining population trends across the four biogeographic realms within the tropical rainforest biome.

The bar plots show the baseline probabilities in each realm estimated without consideration of either forest cover or integrity. The adjacent line plots show the probability of being threatened and having a declining population with increasing forest integrity after statistically controlling for the effects of forest cover (that is, among species with average area of forest cover within their ranges). Data points (1, threatened/declining; 0, not threatened/not declining) are vertically and horizontally jittered to reduce overlap. The bars and lines represent median predicted probabilities from 100 phylogenetic logistic regressions. Each regression was performed with one phylogenetic tree randomly drawn from 10,000 available trees for each taxonomic group. Error bars and the shaded areas of the lines represent median 95% confidence intervals generated with 2,000 parametric bootstraps in each regression. These results were mirrored in rainforest-obligate vertebrates (Fig. 3). See Supplementary Table 1b and Table 7 for sample sizes and model estimates, respectively. Illustration credits: Steven Traver, Ferran Sayol, Birgit Szabo, and Jose Carlos Arenas-Monroy.

Extended Data Fig. 4 Original and reclassified SCI and FSII datasets.

(a) The original SCI and FSII raster datasets from Hansen et al. 2019, 2020 and used in the main analyses presented here. The tropics lie between 23.5° N and 23.5° S latitudes (indicated by the dotted lines) but the tropical rainforest or humid tropical biome extends into the subtropics in some areas. (b) A reclassified SCI raster generated by simulating a + 20% error in canopy cover and height derived from multispectral satellite imagery (left). This +20% error reduced the number of pixels classified as high SCI (values 14–18), effectively simulating underestimates of canopy cover and height. (c) A reclassified SCI raster simulating a -20% error in canopy cover and height measurements (left). This -20% error increased the number of high SCI pixels, effectively simulating overestimates of canopy cover and height. See Supplementary Table 7 for original and reclassified thresholds of canopy cover and height. As with the original SCI, the Human Footprint was overlaid on both simulated SCI rasters to generate corresponding FSII rasters incorporating the assumed ±20% errors (b, c: right). All raster data were resampled from the original 30 m pixel resolution to 1 km (Methods). See Fig. 1 for model results estimated with the original datasets in Extended Data Fig. 4a, and Extended Data Figs. 5a, b for results estimated with the simulated datasets in Extended Data Figs. 4b, c.

Extended Data Fig. 5 Propagating simulated errors in mapping canopy cover and height with the SCI and FSII datasets to statistical models.

The relative importance of forest integrity, structural condition, and forest cover on the odds of mammals, birds, reptiles, and amphibians being threatened and having declining population trends. The underlying structural condition and integrity data for these analyses are a reclassified SCI raster generated by (a) simulating a + 20% error in canopy cover and height derived from multispectral satellite imagery. This +20% error reduced the number of pixels classified as high SCI (values 14–18), effectively simulating underestimates of canopy cover and height (Extended Data Fig. 4b) and (b) simulating a -20% error in canopy cover and height measurements. This -20% error increased the number of high SCI pixels, effectively simulating overestimates of canopy cover and height (Extended Data Fig. 4c). As with the original SCI, the Human Footprint was overlaid on both simulated SCI rasters to generate FSII rasters incorporating the assumed ±20% errors. Our overall conclusions remained robust to this simulated range of potential error in mapping canopy cover and height in the SCI and FSII datasets. Point estimates represent median standardized odds ratios of species being threatened (circles) or having a declining population (squares) generated by exponentiating standardized coefficients (log odds) of 100 phylogenetic logistic regressions. The vertical dotted line represents an odds ratio of 1, denoting statistical non-significance. Error bars represent median 95% confidence intervals generated with 2,000 parametric bootstraps in each regression. Each regression was performed with one phylogenetic tree randomly drawn from 10,000 available trees for each taxonomic group. Separate models were parameterized for rainforest-obligate and associated species for each response variable. See Supplementary Table 1a for sample sizes, Supplementary Table 8 for original and reclassified thresholds of canopy cover and height, and Supplementary Tables 9–10 for model estimates. Illustration credits: Steven Traver, Ferran Sayol, Birgit Szabo, and Jose Carlos Arenas-Monroy.

Extended Data Fig. 6 Pooling moderate structural condition and integrity forests with structurally intact and high-integrity forests.

The relative importance of forest integrity, structural condition, and forest cover on the odds of mammals, birds, reptiles, and amphibians being threatened and having declining population trends. In the main text, we calculated the area (km2) of structurally intact and high-integrity forests (SCI and FSII values 14–18), relative to the area of structurally degraded and low-integrity forests (SCI values 2–5 and FSII values 1–5) within species humid tropical ranges (Methods). Here, we conducted an additional analysis pooling the area of moderate structural condition and integrity forests (SCI and FSII values 6–13) with structurally intact and high-integrity forests and thereafter parameterizing an identical set of models as the main analyses. We were thus able to consider the entire gradient of forest quality when examining its effects on species extinction risk and declining populations. Our overall conclusions remained consistent, suggesting forests of moderate structural condition and integrity can have value for biodiversity conservation. Point estimates represent median standardized odds ratios of species being threatened (circles) or having a declining population (squares) generated by exponentiating standardized coefficients (log odds) of 100 phylogenetic logistic regressions. The vertical dotted line represents an odds ratio of 1, denoting statistical non-significance. Error bars represent median 95% confidence intervals generated with 2,000 parametric bootstraps in each regression. Each regression was performed with one phylogenetic tree randomly drawn from 10,000 available trees for each taxonomic group. Separate models were parameterized for rainforest-obligate and associated species for each response variable. See Supplementary Tables 1a and 11 for sample sizes and model estimates, respectively. Illustration credits: Steven Traver, Ferran Sayol, Birgit Szabo, and Jose Carlos Arenas-Monroy.

Extended Data Fig. 7 Alternative definitions of IUCN Threatened Status.

The relative importance of forest integrity, structural condition, and forest cover on the odds of mammals, birds, reptiles, and amphibians being threatened. In the main analyses, we considered a species to be threatened if it was classified in any one of the IUCN Red List categories Critically Endangered (CR), Endangered (EN) or Vulnerable (VU). Here, we performed additional analyses considering a species as threatened only if it was classified as (a) CR and (b) either CR or EN. For all analyses, we classified species in the Near Threatened and Least Concern categories as non-threatened. This allowed us to maintain the binary classification (threatened/non-threatened) of the response variable, which was necessary for the logistic regression analyses used in this paper. Our overall conclusions remained consistent across these different degrees of threat. Point estimates represent median standardized odds ratios of species being threatened, generated by exponentiating standardized coefficients (log odds) of 100 phylogenetic logistic regressions. The vertical dotted line represents an odds ratio of 1, denoting statistical non-significance. Error bars represent median 95% confidence intervals generated with 2,000 parametric bootstraps in each regression. Each regression was performed with one phylogenetic tree randomly drawn from 10,000 available trees for each taxonomic group. Separate models were parameterized for rainforest-obligate and associated species. See Supplementary Tables 13–14 for sample sizes and model estimates, respectively. Illustration credits: Steven Traver, Ferran Sayol, Birgit Szabo, and Jose Carlos Arenas-Monroy.

Extended Data Fig. 8 Excluding species designated as threatened under IUCN criteria A and B.

The relative importance of forest integrity, structural condition, and forest cover on the odds of mammals, birds, reptiles, and amphibians being threatened. These analyses were performed after excluding (a) 2,751 species listed as threatened in criterion B of the IUCN Red List of Threatened Species, and (b) 3,745 species listed as threatened in both criteria A and B of the IUCN Red List. We did not include declining population data in this analysis of potential circularity because the IUCN Red List criteria are not used for determining overall population trends. Point estimates represent median standardized odds ratios of species being threatened, generated by exponentiating standardized coefficients (log odds) of 100 phylogenetic logistic regressions. The vertical dotted line represents an odds ratio of 1, denoting statistical non-significance. Error bars represent median 95% confidence intervals generated with 2,000 parametric bootstraps in each regression. Each regression was performed with one phylogenetic tree randomly drawn from 10,000 available trees for each taxonomic group. Separate models were parameterized for rainforest-obligate and associated species. See Supplementary Tables 15–17 for sample sizes and model estimates. Illustration credits: Steven Traver, Ferran Sayol, Birgit Szabo, and Jose Carlos Arenas-Monroy.

Extended Data Fig. 9 Change in forest structural condition and forest cover loss.

The relative importance of change (degradation) in tropical rainforest structural condition and forest cover loss between 2012 and 2018 on the odds of mammal, bird, reptile, and amphibian species being threatened and having declining population trends. Point estimates represent median standardized odds ratios of species being threatened (circles) or having a declining population (squares) generated by exponentiating standardized coefficients (log odds) of 100 phylogenetic logistic regressions. The vertical dotted line represents an odds ratio of 1, denoting statistical non-significance. Error bars represent median 95% confidence intervals generated with 2,000 parametric bootstraps in each regression. Each regression was performed with one phylogenetic tree randomly drawn from 10,000 available trees for each taxonomic group. Separate models were parameterized for rainforest-obligate and associated species for each response variable. See Supplementary Tables 1a and 19 for sample sizes and model estimates, respectively. Illustration credits: Steven Traver, Ferran Sayol, Birgit Szabo, and Jose Carlos Arenas-Monroy.

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Pillay, R., Watson, J.E.M., Hansen, A.J. et al. Humid tropical vertebrates are at lower risk of extinction and population decline in forests with higher structural integrity. Nat Ecol Evol 6, 1840–1849 (2022). https://doi.org/10.1038/s41559-022-01915-8

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