Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Occurrence dynamics of mammals in protected tropical forests respond to human presence and activities

Nature Ecology & Evolution volume 7, pages 1092–1103 (2023)Cite this article

Subjects

Abstract

Protected areas (PAs) play a vital role in wildlife conservation. Nonetheless there is concern and uncertainty regarding how and at what spatial scales anthropogenic stressors influence the occurrence dynamics of wildlife populations inside PAs. Here we assessed how anthropogenic stressors influence occurrence dynamics of 159 mammal species in 16 tropical PAs from three biogeographic regions. We quantified these relationships for species groups (habitat specialists and generalists) and individual species. We used long-term camera-trap data (1,002 sites) and fitted Bayesian dynamic multispecies occupancy models to estimate local colonization (the probability that a previously empty site is colonized) and local survival (the probability that an occupied site remains occupied). Multiple covariates at both the local scale and landscape scale influenced mammal occurrence dynamics, although responses differed among species groups. Colonization by specialists increased with local-scale forest cover when landscape-scale fragmentation was low. Survival probability of generalists was higher near the edge than in the core of the PA when landscape-scale human population density was low but the opposite occurred when population density was high. We conclude that mammal occurrence dynamics are impacted by anthropogenic stressors acting at multiple scales including outside the PA itself.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Distribution of study locations.
Fig. 2: Effect of habitat- and human pressure-related covariates on colonization and survival probability for habitat specialists and generalists.
Fig. 3: Mean predicted colonization probability for specialists and generalists in relation to habitat- and human pressure-related covariates.
Fig. 4: Density plot for species-specific β coefficients for colonization probability.
Fig. 5: Density plot for species-specific β coefficients for survival probability.

Data availability

Covariates included in our model are based on publicly available data and extracted values are in a Figshare repository (https://doi.org/10.6084/m9.figshare.21947300), as well as the R script to subset and organize the data. The detection non-detection matrix is also available from Figshare and raw camera-trap data from the TEAM Network are available on the Wildlife Insights platform (wildlifeinsights.org).

Code availability

All code to reproduce the analysis has been archived on Figshare (https://doi.org/10.6084/m9.figshare.21947300).

References

  1. Tilman, D. et al. Future threats to biodiversity and pathways to their prevention. Nature 546, 73 (2017).

    Article  CAS  PubMed  Google Scholar 

  2. Brondizio, E., Settele, J. & Díaz, S. 2019 Global Assessment Report on Biodiversity and Ecosystem Services (IPBES, 2019).

  3. Hansen, M. C. et al. High-resolution global maps of 21st-century forest cover change. Science 342, 850–853 (2013).

    Article  CAS  PubMed  Google Scholar 

  4. Pillay, R. et al. Tropical forests are home to over half of the world’s vertebrate species. Front. Ecol. Environ. https://doi.org/10.1002/fee.2420 (2021).

  5. Gray, C. L. et al. Local biodiversity is higher inside than outside terrestrial protected areas worldwide. Nat. Commun. 7, 12306 (2016).

  6. Bowyer, R. T., Boyce, M. S., Goheen, J. R. & Rachlow, J. L. Conservation of the world’s mammals: status, protected areas, community efforts, and hunting. J. Mammal. 100, 923–941 (2019).

    Article  Google Scholar 

  7. Collen, B., Ram, M., Zamin, T. & McRae, L. The tropical biodiversity data gap: addressing disparity in global monitoring. Trop. Conserv. Sci. 1, 75–88 (2008).

    Article  Google Scholar 

  8. Gonzalez, A. et al. Estimating local biodiversity change: a critique of papers claiming no net loss of local diversity. Ecology 97, 1949–1960 (2016).

    Article  PubMed  Google Scholar 

  9. Durant, S. M., Bashir, S., Maddox, T. & Laurenson, M. K. Relating long‐term studies to conservation practice: the case of the Serengeti Cheetah Project. Conserv. Biol. 21, 602–611 (2007).

    Article  PubMed  Google Scholar 

  10. Rosenblatt, E. et al. Detecting declines of apex carnivores and evaluating their causes: an example with Zambian lions. Biol. Conserv. 180, 176–186 (2014).

    Article  Google Scholar 

  11. MacKenzie, D. I. et al. Occupancy Estimation and Modeling: Inferring Patterns and Dynamics of Species Occurrence (Elsevier, 2017).

  12. Miguet, P., Jackson, H. B., Jackson, N. D., Martin, A. E. & Fahrig, L. What determines the spatial extent of landscape effects on species? Landsc. Ecol. 31, 1177–1194 (2016).

    Article  Google Scholar 

  13. DeFries, R. et al. From plot to landscape scale: linking tropical biodiversity measurements across spatial scales. Front. Ecol. Environ. 8, 153–160 (2010).

    Article  Google Scholar 

  14. Chandler, R. & Hepinstall-Cymerman, J. Estimating the spatial scales of landscape effects on abundance. Landsc. Ecol. 31, 1383–1394 (2016).

    Article  Google Scholar 

  15. Zeller, K. A. et al. Sensitivity of landscape resistance estimates based on point selection functions to scale and behavioral state: pumas as a case study. Landsc. Ecol. 29, 541–557 (2014).

    Article  Google Scholar 

  16. Beaudrot, L. et al. Local temperature and ecological similarity drive distributional dynamics of tropical mammals worldwide. Glob. Ecol. Biogeogr. 28, 976–991 (2019).

    Article  Google Scholar 

  17. Laurance, W. F. et al. Averting biodiversity collapse in tropical forest protected areas. Nature 489, 290–294 (2012).

    Article  CAS  PubMed  Google Scholar 

  18. DeFries, R., Karanth, K. K. & Pareeth, S. Interactions between protected areas and their surroundings in human-dominated tropical landscapes. Biol. Conserv. 143, 2870–2880 (2010).

    Article  Google Scholar 

  19. Fletcher, R. J. Jr et al. Is habitat fragmentation good for biodiversity? Biol. Conserv. 226, 9–15 (2018).

    Article  Google Scholar 

  20. Fahrig, L. et al. Is habitat fragmentation bad for biodiversity? Biol. Conserv. 230, 179–186 (2019).

    Article  Google Scholar 

  21. Clavel, J., Julliard, R. & Devictor, V. Worldwide decline of specialist species: toward a global functional homogenization? Front. Ecol. Environ. 9, 222–228 (2011).

    Article  Google Scholar 

  22. Devictor, V. et al. Defining and measuring ecological specialization. J. Appl. Ecol. 47, 15–25 (2010).

    Article  Google Scholar 

  23. Brotons, L., Mönkkönen, M. & Martin, J. L. Are fragments islands? Landscape context and density–area relationships in boreal forest birds. Am. Nat. 162, 343–357 (2003).

    Article  PubMed  Google Scholar 

  24. Öckinger, E. et al. Life-history traits predict species responses to habitat area and isolation: a cross-continental synthesis. Ecol. Lett. 13, 969–979 (2010).

    PubMed  Google Scholar 

  25. Zurell, D. et al. Spatially explicit models for decision‐making in animal conservation and restoration. Ecography https://doi.org/10.1111/ecog.05787 (2021).

  26. MacKenzie, D. I., Nichols, J. D., Hines, J. E., Knutson, M. G. & Franklin, A. B. Estimating site occupancy, colonization, and local extinction when a species is detected imperfectly. Ecology 84, 2200–2207 (2003).

    Article  Google Scholar 

  27. Cooke, R. S. C., Eigenbrod, F. & Bates, A. E. Projected losses of global mammal and bird ecological strategies. Nat. Commun. 10, 2279 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  28. Semper-Pascual, A. et al. Occupancy winners in tropical protected forests: a pantropical analysis. Proc. R. Soc. B 289, 20220457 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  29. Morante-Filho, J. C., Faria, D., Mariano-Neto, E. & Rhodes, J. Birds in anthropogenic landscapes: the responses of ecological groups to forest loss in the Brazilian Atlantic forest. PLoS ONE 10, e0128923 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  30. Newbold, T. et al. A global model of the response of tropical and sub-tropical forest biodiversity to anthropogenic pressures. Proc. R. Soc. B 281, 20141371 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  31. Hanski, I. Metapopulation dynamics. Nature 396, 41–49 (1998).

    Article  CAS  Google Scholar 

  32. Opdam, P. Metapopulation theory and habitat fragmentation: a review of holarctic breeding bird studies. Landsc. Ecol. 5, 93–106 (1991).

    Article  Google Scholar 

  33. Fahrig, L. Effects of habitat fragmentation on biodiversity. Ann. Rev. Ecol. Evol. Syst. 34, 487–515 (2003).

    Article  Google Scholar 

  34. Villalva, P. & Palomares, F. A continental approach to jaguar extirpation: a tradeoff between anthropic and intrinsic causes. J. Nat. Conserv. 66, 126145 (2022).

    Article  Google Scholar 

  35. Espinosa, S., Celis, G. & Branch, L. C. When roads appear jaguars decline: Increased access to an Amazonian wilderness area reduces potential for jaguar conservation. PLoS ONE 13, e0189740 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  36. Cai, J., Jiang, Z., Zeng, Y., Li, C. & Bravery, B. D. Factors affecting crop damage by wild boar and methods of mitigation in a giant panda reserve. Eur. J. Wildl. Res. 54, 723–728 (2008).

    Article  Google Scholar 

  37. Emmons, L. Dasyprocta punctata. The IUCN Red List of Threatened Species 2016 (IUCN, 2016); https://doi.org/10.2305/IUCN.UK.2016-2.RLTS.T89497686A78319610.en

  38. Bowkett, A. E. et al. Distribution and genetic diversity of the endangered Abbott’s duiker Cephalophus spadix in the Udzungwa Mountains, Tanzania. Endanger. Species Res. 24, 105–114 (2014).

    Article  Google Scholar 

  39. Benítez-López, A. et al. The impact of hunting on tropical mammal and bird populations. Science 356, 180–183 (2017).

    Article  PubMed  Google Scholar 

  40. Maxwell, S. L. et al. Area-based conservation in the twenty-first century. Nature 586, 217–227 (2020).

    Article  CAS  PubMed  Google Scholar 

  41. Semper-Pascual, A. et al. How do habitat amount and habitat fragmentation drive time-delayed responses of biodiversity to land-use change. Proc. R. Soc. B 288, 20202466 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  42. Thornton, D. H., Branch, L. C. & Sunquist, M. E. The relative influence of habitat loss and fragmentation: do tropical mammals meet the temperate paradigm. Ecol. Appl. 21, 2324–2333 (2011).

    Article  PubMed  Google Scholar 

  43. Cudney-Valenzuela, S. J. et al. Does patch quality drive arboreal mammal assemblages in fragmented rainforests. Perspect. Ecol. Conserv. 19, 61–68 (2021).

    Google Scholar 

  44. Benítez-López, A., Santini, L., Schipper, A. M., Busana, M. & Huijbregts, M. A. Intact but empty forests? Patterns of hunting-induced mammal defaunation in the tropics. PLoS Biol. 17, e3000247 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  45. Jerozolimski, A. & Peres, C. A. Bringing home the biggest bacon: a cross-site analysis of the structure of hunter-kill profiles in Neotropical forests. Biol. Conserv. 111, 415–425 (2003).

    Article  Google Scholar 

  46. Luskin, M. S., Christina, E. D., Kelley, L. C. & Potts, M. D. Modern hunting practices and wild meat trade in the oil palm plantation-dominated landscapes of Sumatra, Indonesia. Hum. Ecol. 42, 35–45 (2014).

    Article  Google Scholar 

  47. Sunquist, M. & Sunquist, F. Wild Cats of the World (Univ. Chicago Press, 2017).

  48. Di Bitetti, M. S., Paviolo, A., De Angelo, C. D. & Di Blanco, Y. E. Local and continental correlates of the abundance of a neotropical cat, the ocelot (Leopardus pardalis). J. Trop. Ecol. 24, 189–200 (2008).

  49. Guharajan, R. et al. Sustainable forest management is vital for the persistence of sun bear Helarctos malayanus populations in Sabah, Malaysian Borneo. For. Ecol. Manag. 493, 119270 (2021).

    Article  Google Scholar 

  50. Harrison, R. D. et al. Impacts of hunting on tropical forests in Southeast Asia. Conserv. Biol. 30, 972–981 (2016).

    Article  PubMed  Google Scholar 

  51. Pires Mesquita, G., Domingo Rodríguez‐Teijeiro, J. & Nascimento Barreto, L. Patterns of mammal subsistence hunting in eastern Amazon, Brazil. Wildl. Soc. Bull. 42, 272–283 (2018).

    Article  Google Scholar 

  52. Rovero, F., Mtui, A. S., Kitegile, A. S. & Nielsen, M. R. Hunting or habitat degradation? Decline of primate populations in Udzungwa Mountains, Tanzania: an analysis of threats. Biol. Conserv. 146, 89–96 (2012).

    Article  Google Scholar 

  53. BIEBER, C. & RUF, T. Population dynamics in wild boar Sus scrofa: ecology, elasticity of growth rate and implications for the management of pulsed resource consumers. J. Appl. Ecol. 42, 1203–1213 (2005).

    Article  Google Scholar 

  54. O’Brien, T. G. et al. Camera trapping reveals trends in forest duiker populations in African National Parks. Remote Sens. Ecol. Conserv. 6, 168–180 (2020).

    Article  Google Scholar 

  55. Beaudrot, L. et al. Standardized assessment of biodiversity trends in tropical forest protected areas: the end is not in sight. PLoS Biol. 14, e1002357 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  56. Gerland, P. et al. World population stabilization unlikely this century. Science 346, 234–237 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Crooks, K. R. et al. Quantification of habitat fragmentation reveals extinction risk in terrestrial mammals. Proc. Natl Acad. Sci. USA 114, 7635–7640 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Rovero, F. & Ahumada, J. The Tropical Ecology, Assessment and Monitoring (TEAM) Network: an early warning system for tropical rain forests. Sci. Total Environ. 574, 914–923 (2017).

    Article  CAS  PubMed  Google Scholar 

  59. Devarajan, K., Morelli, T. L. & Tenan, S. Multi-species occupancy models: review, roadmap, and recommendations. Ecography 43, 1612–1624 (2020).

    Article  Google Scholar 

  60. MacKenzie, D. et al. Occupancy Estimation and Modeling: Inferring Patterns and Dynamics of Species Occurrence (Elsevier, 2006).

  61. Broms, K. M., Hooten, M. B., Johnson, D. S., Altwegg, R. & Conquest, L. L. Dynamic occupancy models for explicit colonization processes. Ecology 97, 194–204 (2016).

    Article  PubMed  Google Scholar 

  62. Hockings, M., Dudley, N., MacKinnon, K., Whitten, T. & Leverington, F. Reporting Progress in Protected Areas: A Site-level Management Effectiveness Tracking Tool (World Bank/WWF, 2003).

  63. Neilson, E. W., Avgar, T., Burton, A. C., Broadley, K. & Boutin, S. Animal movement affects interpretation of occupancy models from camera‐trap surveys of unmarked animals. Ecosphere 9, e02092 (2018).

    Article  Google Scholar 

  64. de Valpine, P. et al. Programming with models: writing statistical algorithms for general model structures with NIMBLE. J. Comput. Graph. Stat. 26, 403–413 (2017).

    Article  Google Scholar 

  65. Gelman, A. et al. Bayesian Data Analysis (Chapman and Hall/CRC, 2013).

  66. Harris, I., Jones, P. D., Osborn, T. J. & Lister, D. H. Updated high-resolution grids of monthly climatic observations—the CRU TS3.10 Dataset. Int. J. Climatol. 34, 623–642 (2014).

    Article  Google Scholar 

  67. Fick, S. E. & Hijmans, R. J. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).

    Article  Google Scholar 

  68. Hollister, J. W. elevatr: Access elevation data from various APIs. R package version 0.4.1 https://CRAN.R-project.org/package=elevatr/ (2021).

  69. Faurby, S. et al. PHYLACINE 1.2: the phylogenetic atlas of mammal macroecology. Ecology 99, 2626 (2018).

    Article  PubMed  Google Scholar 

  70. Anile, S. & Devillard, S. Study design and body mass influence RAIs from camera trap studies: evidence from the Felidae. Anim. Conserv. 19, 35–45 (2016).

    Article  Google Scholar 

  71. Schiavina, M. et al. GHSL Data Package 2022: Public Release GHS P2022 (Publications Office of the European Union, 2022); https://data.europa.eu/doi/10.2760/19817

  72. Protected Planet: The World Database on Protected Areas (WDPA) and World Database on Other Effective Area-based Conservation Measures (UNEP-WCMC & IUCN, 2022); www.protectedplanet.net

  73. Pesaresi, M. & Politis, P. GHS-BUILT-S R2022A—GHS Built-up Surface Grid, Derived From Sentinel2 Composite and Landsat, Multitemporal (1975–2030) (European Commission, Joint Research Centre, 2022); http://data.europa.eu/89h/d07d81b4-7680-4d28-b896-583745c27085

Download references

Acknowledgements

This work was made possible by the TEAM Network, a collaboration between Conservation International, the Smithsonian Tropical Research Institute and the Wildlife Conservation Society. We thank all current and previous TEAM site managers and all people and institutions involved in fieldwork. This work was supported by the Research Council of Norway (project NFR301075 to A.S.P., D.S. and R.B.). L.B. was also supported by the National Science Foundation grant (DEB-2213568)

Author information

Authors and Affiliations

  1. Faculty of Environmental Sciences and Natural Resource Management, Norwegian University of Life Sciences, Ås, Norway

    Asunción Semper-Pascual, Douglas Sheil, Pierre Dupont, Soumen Dey & Richard Bischof

  2. Forest Ecology and Forest Management Group, Wageningen University and Research, Wageningen, the Netherlands

    Douglas Sheil

  3. Center for International Forestry Research, Bogor, Indonesia

    Douglas Sheil

  4. Program in Ecology & Evolutionary Biology, Department of BioSciences, Rice University, Houston, TX, USA

    Lydia Beaudrot

  5. Moore Center for Science, Conservation International, Arlington, VA, USA

    Jorge Ahumada

  6. Institute of Tropical Forest Conservation, Mbarara University of Science and Technology, Kabale, Uganda

    Emmanuel Akampurira & Robert Bitariho

  7. Conflict Research Group, Ghent University, Ghent, Belgium

    Emmanuel Akampurira

  8. Facultad de Ciencias, Universidad Autónoma de San Luis Potosí, San Luis Potosí, Mexico

    Santiago Espinosa

  9. Escuela de Biología, Pontificia Universidad Católica del Ecuador, Quito, Ecuador

    Santiago Espinosa

  10. Smithsonian Tropical Research Institute, Ancon, Republic of Panama

    Patrick A. Jansen

  11. Wildlife Ecology & Conservation Group, Wageningen University and Research, Wageningen, the Netherlands

    Patrick A. Jansen

  12. Biogeography of Conservation and Macroecology Laboratory, Institute of Biological Sciences, Universidade Federal do Pará, Pará, Brazil

    Marcela Guimarães Moreira Lima

  13. Department of Wildlife Management, College of African Wildlife Management, Mweka, Tanzania

    Emanuel H. Martin

  14. Department of Ecological Dynamics, Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany

    Badru Mugerwa

  15. Faculty VI—Planning Building Environment, Institute of Ecology, Technische Universität Berlin, Berlin, Germany

    Badru Mugerwa

  16. Department of Biology, University of Florence, Florence, Italy

    Francesco Rovero

  17. MUSE-Museo delle Scienze, Trento, Italy

    Francesco Rovero

  18. Museu Paraense Emílio Goeldi, Belém, Brazil

    Fernanda Santos

  19. International Gorilla Conservation Programme, Musanze, Rwanda

    Eustrate Uzabaho

Authors
  1. Asunción Semper-Pascual
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Douglas Sheil
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lydia Beaudrot
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pierre Dupont
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Soumen Dey
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jorge Ahumada
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Emmanuel Akampurira
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Robert Bitariho
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Santiago Espinosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Patrick A. Jansen
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Marcela Guimarães Moreira Lima
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Emanuel H. Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Badru Mugerwa
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Francesco Rovero
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Fernanda Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Eustrate Uzabaho
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Richard Bischof
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

D.S. and R. Bischof accessed funding. A.S.P., D.S. and R. Bischof conceptualized the study. A.S.P. developed and performed the analyses. R. Bischof, P.D. and S.D. contributed to the analyses. A.S.P. wrote the manuscript with support from R. Bischof, D.S. and L.B. Camera-trap data collection in the TEAM study areas was carried out by D.S., J.A., E.A., R. Bitariho, S.E., P.A.J., M.G.M.L., E.H.M., B.M., F.R., F.S. and E.U. The manuscript was finalized by A.S.P., with input and approval from all authors.

Corresponding author

Correspondence to Asunción Semper-Pascual.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Ecology & Evolution thanks Ana Benítez-López, Nicolas Deere and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Methods 1–4, Figs. 1–13 and Tables 1–4.

Reporting Summary

Peer Review File

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Semper-Pascual, A., Sheil, D., Beaudrot, L. et al. Occurrence dynamics of mammals in protected tropical forests respond to human presence and activities. Nat Ecol Evol 7, 1092–1103 (2023). https://doi.org/10.1038/s41559-023-02060-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-023-02060-6

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing