in

Chimpanzees balance resources and risk in an anthropogenic landscape of fear

  • 1.

    Dirzo, R. et al. Defaunation in the anthropocene. Science 345, 401–406 (2014).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 2.

    Boivin, N. L. et al. Ecological consequences of human niche construction: examining long-term anthropogenic shaping of global species distributions. Proc. Natl. Acad. Sci. 113, 6388–6396 (2016).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 3.

    Newbold, T. et al. Global effects of land use on local terrestrial biodiversity. Nature 520, 45–50 (2015).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 4.

    Hagen, M. et al. Biodiversity, species interactions and ecological networks in a fragmented world. In Advances in Ecological Research Vol. 46 (eds Jacob, U. & Woodward, G.) 89–210 (Academic Press, Cambridge, 2012).

    Google Scholar 

  • 5.

    Gallego-Zamorano, J. et al. Combined effects of land use and hunting on distributions of tropical mammals. Conserv. Biol. 34, 1271–1280 (2020).

    PubMed  PubMed Central  Article  Google Scholar 

  • 6.

    Ellis, E. C. & Ramankutty, N. Putting people in the map: anthropogenic biomes of the world. Front. Ecol. Environ. 6, 439–447 (2008).

    Article  Google Scholar 

  • 7.

    Estrada, A., Raboy, B. E. & Oliveira, L. C. Agroecosystems and primate conservation in the tropics: a review. Am. J. Primatol. 74, 696–711 (2012).

    PubMed  Article  Google Scholar 

  • 8.

    Bhagwat, S. A., Willis, K. J., Birks, H. J. B. & Whittaker, R. J. Agroforestry: a refuge for tropical biodiversity?. Trends Ecol. Evol. 23, 261–267 (2008).

    PubMed  Article  Google Scholar 

  • 9.

    Galán-Acedo, C. et al. The conservation value of human-modified landscapes for the world’s primates. Nat. Commun. 10, 1–8 (2019).

    Article  CAS  Google Scholar 

  • 10.

    Arroyo-Rodríguez, V. et al. Designing optimal human-modified landscapes for forest biodiversity conservation. Ecol. Lett. 23, 1404–1420 (2020).

    PubMed  Article  Google Scholar 

  • 11.

    Kshettry, A., Vaidyanathan, S., Sukumar, R. & Athreya, V. Looking beyond protected areas: identifying conservation compatible landscapes in agro-forest mosaics in north-eastern India. Glob. Ecol. Conserv. 22, e00905 (2020).

    Article  Google Scholar 

  • 12.

    Osborn, F. V. & Hill, C. M. Techiques to reduce crop loss: human and technical dimensions in Africa. In People and Wildlife, Conflict or Co-existence? 72–85 (Cambridge University Press, Cambridge, 2005).

  • 13.

    McLennan, M. R. & Asiimwe, C. Cars kill chimpanzees: case report of a wild chimpanzee killed on a road at Bulindi, Uganda. Primates J. Primatol. 57, 377–388 (2016).

    Article  Google Scholar 

  • 14.

    Chapman, C. A. et al. Do food availability, parasitism, and stress have synergistic effects on red colobus populations living in forest fragments?. Am. J. Phys. Anthropol. 131, 525–534 (2006).

    PubMed  Article  Google Scholar 

  • 15.

    Goldberg, T. L., Gillespie, T. R., Rwego, I. B., Estoff, E. L. & Chapman, C. A. Forest fragmentation as cause of bacterial transmission among nonhuman primates, humans, and livestock, Uganda. Emerg. Infect. Dis. 14, 1375–1382 (2008).

    PubMed  PubMed Central  Article  Google Scholar 

  • 16.

    McLennan, M. R., Hyeroba, D., Asiimwe, C., Reynolds, V. & Wallis, J. Chimpanzees in mantraps: lethal crop protection and conservation in Uganda. Oryx 46, 598–603 (2012).

    Article  Google Scholar 

  • 17.

    Kalema-Zikusoka, G., Rubanga, S., Mutahunga, B. & Sadler, R. Prevention of Cryptosporidium and GIARDIA at the human/gorilla/livestock interface. Front. Public Health 6, (2018).

  • 18.

    Kenney, J., Allendorf, F. W., McDougal, C. & Smith, J. L. D. How much gene flow is needed to avoid inbreeding depression in wild tiger populations?. Proc. R. Soc. B Biol. Sci. 281, 20133337 (2014).

    Article  Google Scholar 

  • 19.

    Willems, E. P. & Hill, R. A. Predator-specific landscapes of fear and resource distribution: effects on spatial range use. Ecology 90, 546–555 (2009).

    PubMed  Article  PubMed Central  Google Scholar 

  • 20.

    Coleman, B. T. & Hill, R. A. Living in a landscape of fear: the impact of predation, resource availability and habitat structure on primate range use. Anim. Behav. 88, 165–173 (2014).

    Article  Google Scholar 

  • 21.

    Palmer, M. S., Fieberg, J., Swanson, A., Kosmala, M. & Packer, C. A ‘dynamic’ landscape of fear: prey responses to spatiotemporal variations in predation risk across the lunar cycle. Ecol. Lett. 20, 1364–1373 (2017).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 22.

    Laundré, J. W., Hernandez, L. & Ripple, W. J. The landscape of fear: ecological implications of being afraid. Open Ecol. J. 3, (2010).

  • 23.

    Theuerkauf, J. & Rouys, S. Habitat selection by ungulates in relation to predation risk by wolves and humans in the Białowieża Forest, Poland. For. Ecol. Manag. 256, 1325–1332 (2008).

    Article  Google Scholar 

  • 24.

    Ciuti, S. et al. Effects of humans on behaviour of wildlife exceed those of natural predators in a landscape of fear. PLoS ONE 7, e50611 (2012).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 25.

    Nowak, K., Wimberger, K., Richards, S. A., Hill, R. A. & le Roux, A. Samango monkeys (Cercopithecus albogularis labiatus) manage risk in a highly seasonal, human-modified landscape in Amathole Mountains, South Africa. Int. J. Primatol. 38, 194–206 (2017).

    PubMed  Article  Google Scholar 

  • 26.

    Suraci, J. P., Clinchy, M., Zanette, L. Y. & Wilmers, C. C. Fear of humans as apex predators has landscape-scale impacts from mountain lions to mice. Ecol. Lett. 22, 1578–1586 (2019).

    PubMed  Article  Google Scholar 

  • 27.

    Carter, N. H., Shrestha, B. K., Karki, J. B., Pradhan, N. M. B. & Liu, J. Coexistence between wildlife and humans at fine spatial scales. Proc. Natl. Acad. Sci. 109, 15360–15365 (2012).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 28.

    Carter, N. H., Jasny, M., Gurung, B. & Liu, J. Impacts of people and tigers on leopard spatiotemporal activity patterns in a global biodiversity hotspot. Glob. Ecol. Conserv. 3, 149–162 (2015).

    Article  Google Scholar 

  • 29.

    Lamb, C. T. et al. The ecology of human–carnivore coexistence. Proc. Natl. Acad. Sci. 117, 17876–17883. https://doi.org/10.1073/pnas.1922097117 (2020).

    CAS  Article  PubMed  Google Scholar 

  • 30.

    Bryson-Morrison, N., Tzanopoulos, J., Matsuzawa, T. & Humle, T. Activity and habitat use of chimpanzees (Pan troglodytes verus) in the anthropogenic landscape of Bossou, Guinea, West Africa. Int. J. Primatol. 38, 282–302 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  • 31.

    de Almeida-Rocha, J. M., Peres, C. A. & Oliveira, L. C. Primate responses to anthropogenic habitat disturbance: a pantropical meta-analysis. Biol. Conserv. 215, 30–38 (2017).

    Article  Google Scholar 

  • 32.

    Galán‐Acedo, C., Arroyo‐Rodríguez, V., Cudney‐Valenzuela, S. J. & Fahrig, L. A global assessment of primate responses to landscape structure. Biol. Rev. 94, 1605–1618 (2019).

    PubMed  Article  PubMed Central  Google Scholar 

  • 33.

    Garriga, R. M. et al. Factors influencing wild chimpanzee (Pan troglodytes verus) relative abundance in an agriculture-swamp matrix outside protected areas. PLoS ONE 14, e0215545 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 34.

    Hockings, K. J., Anderson, J. R. & Matsuzawa, T. Road crossing in chimpanzees: a risky business. Curr. Biol. 16, R668–R670 (2006).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 35.

    Estrada, A. et al. Impending extinction crisis of the world’s primates: why primates matter. Sci. Adv. 3, e1600946 (2017).

    ADS  PubMed  PubMed Central  Article  Google Scholar 

  • 36.

    IUCN SSC Primate Specialist Group. Regional action plan for the conservation of western chimpanzees (Pan troglodytes verus) 2020–2030. (2020).

  • 37.

    Kalan, A. K. et al. Environmental variability supports chimpanzee behavioural diversity. Nat. Commun. 11, 4451 (2020).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 38.

    Hockings, K. J., Anderson, J. R. & Matsuzawa, T. Socioecological adaptations by chimpanzees, Pan troglodytes verus, inhabiting an anthropogenically impacted habitat. Anim. Behav. 83, 801–810 (2012).

    Article  Google Scholar 

  • 39.

    McLennan, M. R. & Hockings, K. J. Wild chimpanzees show group differences in selection of agricultural crops. Sci. Rep. 4, 5956 (2014).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 40.

    Kalan, A. K. et al. Novelty response of wild African apes to camera traps. Curr. Biol.  29, 1211–1217.e3 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 41.

    Hockings, K. J. & McLennan, M. R. From forest to farm: systematic review of cultivar feeding by chimpanzees—management implications for wildlife in anthropogenic landscapes. PLoS ONE 7, e33391 (2012).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 42.

    Hockings, K. J., Anderson, J. R. & Matsuzawa, T. Use of wild and cultivated foods by chimpanzees at Bossou, Republic of Guinea: feeding dynamics in a human-influenced environment. Am. J. Primatol. 71, 636–646 (2009).

    PubMed  Article  PubMed Central  Google Scholar 

  • 43.

    McLennan, M. R. Diet and feeding ecology of chimpanzees (Pan troglodytes) in Bulindi, Uganda: foraging strategies at the forest–farm interface. Int. J. Primatol. 34, 585–614 (2013).

    Article  Google Scholar 

  • 44.

    McLennan, M. R. & Ganzhorn, J. U. Nutritional characteristics of wild and cultivated foods for chimpanzees (Pan troglodytes) in agricultural landscapes. Int. J. Primatol. 38, 122–150 (2017).

    Article  Google Scholar 

  • 45.

    Matthews, A. & Matthews, A. Survey of gorillas (Gorilla gorilla gorilla) and chimpanzees (Pan troglodytes troglodytes) in Southwestern Cameroon. Primates 45, 15–24 (2004).

    PubMed  Article  PubMed Central  Google Scholar 

  • 46.

    Morgan, D. et al. African apes coexisting with logging: comparing chimpanzee (Pan troglodytes troglodytes) and gorilla (Gorilla gorilla gorilla) resource needs and responses to forestry activities. Biol. Conserv. 218, 277–286 (2018).

    Article  Google Scholar 

  • 47.

    Krief, S. et al. Wild chimpanzees on the edge: nocturnal activities in croplands. PLoS ONE 9, e109925 (2014).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 48.

    Riley, E. P. & Priston, N. E. C. Macaques in farms and folklore: exploring the human–nonhuman primate interface in Sulawesi, Indonesia. Am. J. Primatol. 72, 848–854 (2010).

    PubMed  Article  PubMed Central  Google Scholar 

  • 49.

    Parathian, H. E., McLennan, M. R., Hill, C. M., Frazão-Moreira, A. & Hockings, K. J. Breaking through disciplinary barriers: human–wildlife interactions and multispecies ethnography. Int. J. Primatol. 39, 749–775. https://doi.org/10.1007/s10764-018-0027-9 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  • 50.

    Fuentes, A. & Gamerl, S. Disproportionate participation by age/sex classes in aggressive interactions between long-tailed macaques (Macaca fascicularis) and human tourists at Padangtegal monkey forest, Bali, Indonesia. Am. J. Primatol. 66, 197–204 (2005).

    PubMed  Article  Google Scholar 

  • 51.

    McLennan, M. R. & Hockings, K. J. The aggressive apes? Causes and contexts of great ape attacks on local persons. In Problematic Wildlife (ed. Angelici, F. M.) 373–394 (Springer, Cham, 2016). https://doi.org/10.1007/978-3-319-22246-2_18.

  • 52.

    Hill, C. M. & Webber, A. D. Perceptions of nonhuman primates in human–wildlife conflict scenarios. Am. J. Primatol. 72, 919–924 (2010).

    PubMed  Article  Google Scholar 

  • 53.

    McLennan, M. R. & Hill, C. M. Troublesome neighbours: changing attitudes towards chimpanzees (Pan troglodytes) in a human-dominated landscape in Uganda. J. Nat. Conserv. 20, 219–227 (2012).

    Article  Google Scholar 

  • 54.

    Mito, Y. & Sprague, D. S. The Japanese and Japanese monkeys: dissonant neighbors seeking accommodation in a shared habitat. In The Macaque Connection: Cooperation and Conflict Between Humans and Macaques (eds Radhakrishna, S. et al.) 33–51 (Springer, Berlin, 2013).

    Google Scholar 

  • 55.

    Morzillo, A., de Beurs, K. & Martin-Mikle, C. A conceptual framework to evaluate human-wildlife interactions within coupled human and natural systems. Ecol. Soc. 19, (2014).

  • 56.

    Martin, J. et al. Coping with human disturbance: spatial and temporal tactics of the brown bear (Ursus arctos). Can. J. Zool. 88, 875–883 (2010).

    Article  Google Scholar 

  • 57.

    Hockings, K. J. et al. Chimpanzees share forbidden fruit. PLoS ONE 2, e886 (2007).

    ADS  PubMed  PubMed Central  Article  Google Scholar 

  • 58.

    Duvall, C. S. Human settlement ecology and chimpanzee habitat selection in Mali. Landsc. Ecol. 23, 699 (2008).

    Article  Google Scholar 

  • 59.

    Hockings, K. J., Parathian, H., Bessa, J. & Frazão-Moreira, A. Extensive overlap in the selection of wild fruits by chimpanzees and humans: implications for the management of complex social-ecological systems. Front. Ecol. Evol. 8, (2020).

  • 60.

    Nowak, K., Hill, R. A., Wimberger, K. & le Roux, A. Risk-taking in samango monkeys in relation to humans at two sites in South Africa. In Ethnoprimatology: Primate Conservation in the 21st Century (ed. Waller, M. T.) 301–314 (Springer, Berlin, 2016).

    Google Scholar 

  • 61.

    INE. Recenseamento Geral da População e Habitação: População por Região, Sector e Localidades por Sexo Censo 2009. 160 (2009).

  • 62.

    Heinicke, S. et al. Characteristics of positive deviants in western chimpanzee populations. Front. Ecol. Evol. 7, (2019).

  • 63.

    Bersacola, E. Zooming in on Human-Wildlife Coexistence: Primate Community Responses in a Shared Agroforest Landscape in Guinea-Bissau (Oxford Brookes University, Oxford, 2020).

    Google Scholar 

  • 64.

    Bessa, J., Sousa, C. & Hockings, K. J. Feeding ecology of chimpanzees (Pan troglodytes verus) inhabiting a forest-mangrove-savanna-agricultural matrix at Caiquene-Cadique, Cantanhez National Park, Guinea-Bissau. Am. J. Primatol. 77, 651–665 (2015).

    PubMed  Article  Google Scholar 

  • 65.

    Hockings, K. J. et al. Leprosy in wild chimpanzees. bioRxiv 2020.11.10.374371 (2020) https://doi.org/10.1101/2020.11.10.374371.

  • 66.

    Hockings, K. J. & Sousa, C. Differential utilization of cashew—a low-conflict crop—by sympatric humans and chimpanzees. Oryx 46, 375–381 (2012).

    Article  Google Scholar 

  • 67.

    Calenge, C. The package adehabitat for the R software: a tool for the analysis of space and habitat use by animals. Ecol. Model. 197, 516–519 (2006).

    Article  Google Scholar 

  • 68.

    Schmid, F. & Schmidt, A. Nonparametric estimation of the coefficient of overlapping—theory and empirical application. Comput. Stat. Data Anal. 50, 1583–1596 (2006).

    MathSciNet  MATH  Article  Google Scholar 

  • 69.

    Ridout, M. S. & Linkie, M. Estimating overlap of daily activity patterns from camera trap data. J. Agric. Biol. Environ. Stat. 14, 322–337 (2009).

    MathSciNet  MATH  Article  Google Scholar 

  • 70.

    Hijmans, R. J. Raster: geographic data analysis and modeling. (2020).

  • 71.

    Khorozyan, I., Stanton, D., Mohammed, M., Al-Rail, W. & Pittet, M. Patterns of co-existence between humans and mammals in Yemen: some species thrive while others are nearly extinct. Biodivers. Conserv. 23, 1995–2013 (2014).

    Article  Google Scholar 

  • 72.

    Sousa, J., Barata, A. V., Sousa, C., Casanova, C. C. N. & Vicente, L. Chimpanzee oil-palm use in southern Cantanhez National Park, Guinea-Bissau. Am. J. Primatol. 73, 485–497 (2011).

    PubMed  Article  PubMed Central  Google Scholar 

  • 73.

    Tutin, C. E. G. et al. Foraging profiles of sympatric lowland gorillas and chimpanzees in the Lope Reserve, Gabon [and discussion]. Philos. Trans. Biol. Sci. 334, 179–186 (1991).

    ADS  CAS  Article  Google Scholar 

  • 74.

    Yamakoshi, G. Dietary responses to fruit scarcity of wild chimpanzees at Bossou, Guinea: possible implications for ecological importance of tool use. Am. J. Phys. Anthropol. 106, 283–295 (1998).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 75.

    Wilson, M. L., Hauser, M. D. & Wrangham, R. W. Chimpanzees (Pan troglodytes) modify grouping and vocal behaviour in response to location-specific risk. Behaviour 144, 1621–1653 (2007).

    Article  Google Scholar 

  • 76.

    Lindshield, S., Danielson, B. J., Rothman, J. M. & Pruetz, J. D. Feeding in fear? How adult male western chimpanzees (Pan troglodytes verus) adjust to predation and savanna habitat pressures. Am. J. Phys. Anthropol. 163, 480–496 (2017).

    PubMed  Article  PubMed Central  Google Scholar 

  • 77.

    Olson, D. M. et al. Terrestrial ecoregions of the world: a new map of life on Earth. Bioscience 51, 933–938 (2001).

    Article  Google Scholar 

  • 78.

    Sousa, J., Vicente, L., Gippoliti, S., Casanova, C. & Sousa, C. Local knowledge and perceptions of chimpanzees in Cantanhez National Park, Guinea-Bissau. Am. J. Primatol. 76, 122–134 (2014).

    PubMed  Article  PubMed Central  Google Scholar 

  • 79.

    Sharma, K. et al. Conservation and people: towards an ethical code of conduct for the use of camera traps in wildlife research. Ecol. Solut. Evid. 1, e12033 (2020).

    Article  Google Scholar 

  • 80.

    Sun, C. et al. Tree phenology in a tropical montane forest in Rwanda. Biotropica 28, 668–681 (1996).

    Article  Google Scholar 

  • 81.

    McLennan, M. R. Chimpanzee Ecology and Interactions with People in an Unprotected Human-Dominated Landscape at Bulindi, Western Uganda (Oxford Brookes University, Oxford, 2010).

    Google Scholar 

  • 82.

    Jenks, K. E. et al. Using relative abundance indices from camera-trapping to test wildlife conservation hypotheses—an example from Khao Yai National Park, Thailand. Trop. Conserv. Sci. 4, 113–131 (2011).

    ADS  Article  Google Scholar 

  • 83.

    O’Brien, T. G., Kinnaird, M. F. & Wibisono, H. T. Crouching tigers, hidden prey: sumatran tiger and prey populations in a tropical forest landscape. Anim. Conserv. Forum 6, 131–139 (2003).

    Article  Google Scholar 

  • 84.

    Rue, H., Martino, S. & Chopin, N. Approximate Bayesian inference for latent Gaussian models by using integrated nested Laplace approximations. J. R. Stat. Soc. Ser. B Stat. Methodol. 71, 319–392 (2009).

    MathSciNet  MATH  Article  Google Scholar 

  • 85.

    Blangiardo, M., Cameletti, M., Baio, G. & Rue, H. Spatial and spatio-temporal models with R-INLA. Spat. Spatio-Temporal Epidemiol. 4, 33–49 (2013).

    Article  Google Scholar 

  • 86.

    Cameletti, M., Lindgren, F., Simpson, D. & Rue, H. Spatio-temporal modeling of particulate matter concentration through the SPDE approach. AStA Adv. Stat. Anal. 97, 109–131 (2013).

    MathSciNet  MATH  Article  Google Scholar 

  • 87.

    Lindgren, F., Rue, H. & Lindström, J. An explicit link between Gaussian fields and Gaussian Markov random fields: the stochastic partial differential equation approach. J. R Stat. Soc. Ser. B Stat. Methodol. 73, 423–498 (2011).

    MathSciNet  MATH  Article  Google Scholar 

  • 88.

    Bakka, H. et al. Spatial modeling with R-INLA: a review. Wiley Interdiscip. Rev. Comput. Stat. 10, e1443 (2018).

    MathSciNet  Article  Google Scholar 

  • 89.

    Noor, A. M. et al. The changing risk of Plasmodium falciparum malaria infection in Africa: 2000–10: a spatial and temporal analysis of transmission intensity. Lancet 383, 1739–1747 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  • 90.

    Rue, H. et al. Bayesian computing with INLA: a review. Annu. Rev. Stat. Its Appl. 4, 395–421 (2017).

    ADS  Article  Google Scholar 

  • 91.

    Cressie, N. & Wikle, C. K. Statistics for Spatio-Temporal Data (Wiley, Hoboken, 2015).

    Google Scholar 

  • 92.

    Lindgren, F. & Rue, H. Bayesian spatial modelling with R-INLA. J. Stat. Softw. 63, 1–25 (2015).

    Article  Google Scholar 

  • 93.

    Spiegelhalter, D. J., Best, N. G., Carlin, B. P. & Linde, A. V. D. Bayesian measures of model complexity and fit. J. R. Stat. Soc. Ser. B Stat. Methodol. 64, 583–639 (2002).

    MathSciNet  MATH  Article  Google Scholar 

  • 94.

    R Core Team. R: A language and environment for statistical computing. (R Foundation for Statistical Computing, 2020).


  • Source: Ecology - nature.com

    An aggressive market-driven model for US fusion power development

    King Climate Action Initiative announces new research to test and scale climate solutions