Rare Bearded Capuchin (Sapajus libidinosus) Tool-Use Culture is Threatened by Land use Changes in Northeastern Brazil

Abstract

Animal traditions are increasingly threatened by human impact on natural habitats, posing a challenge to conservation policies. In northeastern Brazil, bearded capuchins (Sapajus libidinosus) inhabiting the Cerrado–Caatinga biome of Fazenda Boa Vista use stone hammers and anvils to crack open palm nuts and other encased foods. The same species inhabiting the mangroves of Morro do Boi ambush crabs and process them using wooden hammers and anvils. These traditions are gradually acquired by young capuchins exposed to the tool using activity of skilled older group members. Changes in land cover have threatened the persistence of this species, where these rare tool-use traditions occur. To assess land cover changes over the past 30 years, we analyzed a time series of remotely sensed imagery and quantified trends in land cover and agriculture across both study sites. We also developed a predictive model to forecast future changes in land cover by 2034. Our results show that agriculture increased by more than 300% in both sites from 1987 to 2017. If current trends continue in Morro do Boi, only 42% of forest (0.15 km2) will remain, which is insufficient to support the resident population of capuchins. In Fazenda Boa Vista, most of the land suitable for agriculture has already been used for that purpose. If private conservation efforts at Fazenda Boa Vista are to be effective through 2034, agricultural use should not be expanded any further. Imminent erosion and loss of natural vegetation will exacerbate the current situation, even if agriculture is not expanded. Our study is an example of the need for conservation to take behavioral traditions into account, as they are not widespread across the species distribution.

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

Fig. 1
Fig. 2
Fig. 3

References

  1. Adler-Golden, S., Berk, A., Bernstein, L. S., Richtsmeier, S., Acharya, P. K., et al.(1998). FLAASH, a MODTRAN4 atmospheric correction package for hyperspectral data retrievals and simulations. In Summaries of the Seventh JPL Airborne Earth Science Workshop (Vol. 1, pp. 9–14). Pasadena, CA: JPL Pub.

  2. Barrett, B. J., Monteza-Moreno, C. M., Dogandžić, T., Zwyns, N., Ibánez, A., & Crofoot, M. C. (2018). Habitual stone-tool-aided extractive foraging in white-faced capuchins, Cebus capucinus. Royal Society Open Science, 5(8), 181002. https://doi.org/10.1098/rsos.181002.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Benton, T. G., Vickery, J. A., & Wilson, J. D. (2003). Farmland biodiversity: is habitat heterogeneity the key? Trends in Ecology & Evolution, 18(4), 182–188. https://doi.org/10.1016/S0169-5347(03)00011-9.

    Article  Google Scholar 

  4. Bernard, E., Penna, L. A., & Araújo, E. (2014). Downgrading, downsizing, degazettement, and reclassification of protected areas in Brazil. Conservation Biology, 28(4), 939–950. https://doi.org/10.1111/cobi.12298.

    CAS  Article  PubMed  Google Scholar 

  5. Boesch, C. (1993). Aspects of transmission of tool-use in wild chimpanzees. In K. R. Gibson & T. Ingold (Eds.), Tools, language and cognition in human evolution (pp. 171–183). Cambridge: Cambridge University Press.

    Google Scholar 

  6. Boesch, C., & Boesch-Achermann, H. (2000). The chimpanzees of the Taï Forest: Behavioural ecology and evolution. New York: Oxford University Press.

    Google Scholar 

  7. Brakes, P., Dall, S. R., Aplin, L. M., Bearhop, S., Carroll, E. L., et al (2019). Animal cultures matter for conservation. Science, 363(6431), 1032–1034. https://doi.org/10.1126/science.aaw3557.

    CAS  Article  PubMed  Google Scholar 

  8. Canale, G. R., Guidorizzi, C. E., Kierulff, M. C. M., & Gatto, C. A. F. R. (2009). First record of tool use by wild populations of the yellow-breasted capuchin monkey (Cebus xanthosternos) and new records for the bearded capuchin (Cebus libidinosus). American Journal of Primatology, 71(5), 366–372. https://doi.org/10.1002/ajp.20648.

    Article  PubMed  Google Scholar 

  9. Chen, X., Ikeda, K., Yamakita, K., & Nasu, M. (1994). Three-dimensional modeling of GIS based on delaunay tetrahedral tessellations. In ISPRS Commission III symposium: Spatial information from digital photogrammetry and computer vision (Vol. 2357, pp. 132–139). International Society for Optics and Photonics. https://doi.org/10.1117/12.182859

  10. Cutrim, F. H. R. (2013). Padrão comportamental e uso de ferramentas em macacos-prego (Sapajus libidinosus) residentes em manguezal. Resource Document. Universidade de São Paulo. https://teses.usp.br/teses/disponiveis/47/47132/tde-09012014-163238/publico/cutrim_corrigida.pdf. Accessed 30 Dec 2019.

  11. Cutrim, F. H. R., & Izar, P. (2017). Uso de ferramentas e orçamento de atividades de macacos-prego (Sapajus libidinosus) residentes em manguezal no Maranhão. In A Primatologia no Brasil.1 ed. Pernambuco: EDUFPE, 2017 (Vol.14, pp. 132–152). Resource document. Federal University of Pernambuco. https://www3.ufpe.br/editora/UFPEbooks/Outros/primatologia_brasil_vol_14/. Accessed 10 Oct 2019.

  12. de Freitas, E. P., & Queirós, M. M. (2017). O circuito produtivo dos agrocombustíveis no Brasil sob a ordem do liberalismo transnacional: Do controle estatal à hegemonia corporativa. GEOUSP: Espaço e Tempo, 21(3), 771–792. https://doi.org/10.11606/issn.2179-0892.geousp.2017.114782

  13. de Moraes, B. L. C., da Silva Souto, A., & Schiel, N. (2014). Adaptability in stone tool use by wild capuchin monkeys (Sapajus libidinosus). American Journal of Primatology, 76(10), 967–977. https://doi.org/10.1002/ajp.22286.

    Article  PubMed  Google Scholar 

  14. de Oliveira Lopes, L. S., dos Santos, R. W. P., & Miguel Filho, M. A. (2012). Núcleo de desertificação de Gilbués (PI): causas e intervenções. GEOGRAFIA (Londrina), 20(2), 53–66. https://doi.org/10.5433/2447-1747.2011v20n2p53.

    Article  Google Scholar 

  15. de Paula Júnior, E. T. (2010). O Estrangeiro e a propriedade da terra no MAPITOBA, a última fronteira agrícola do Cerrado. Resource documento. Revista UFG, 12(9). https://www.revistas.ufg.br/revistaufg/article/view/48327. Accessed 9 Sept 2019.

  16. Ellison, A. M., & Farnsworth, E. J. (1996). Anthropogenic disturbance of Caribbean mangrove ecosystems: past impacts, present trends, and future predictions. Biotropica, 549–565. https://doi.org/10.2307/2389096

  17. El-Tantawi, A. M., Bao, A., Chang, C., & Liu, Y. (2019). Monitoring and predicting land use/cover changes in the Aksu-Tarim River Basin, Xinjiang-China (1990–2030). Environmental monitoring and assessment, 191(8), 480. https://doi.org/10.1007/s10661-019-7478-0.

    Article  PubMed  Google Scholar 

  18. EMBRAPA. (2019). Brazilian Agriculture Research Corporation. Resource document. EMBRAPA. https://www.embrapa.br/en/codigo-florestal/area-de-reserva-legal-arl/modulo-fiscal. Accessed 3 Jan 2020.

  19. Eshchar, Y., Izar, P., Visalberghi, E., Resende, B., & Fragaszy, D. M. (2016). When and where to practice: social influences on the development of nut-cracking in bearded capuchins (Sapajus libidinosus). Animal Cognition, 19, 605–618. https://doi.org/10.1007/s10071-016-0965-6.

    CAS  Article  PubMed  Google Scholar 

  20. Estrada, A., Garber, P. A., Mittermeier, R. A., Wich, S., Gouveia, S., et al (2018). Primates in peril: the significance of Brazil, Madagascar, Indonesia and the Democratic Republic of the Congo for global primate conservation. PeerJ, 6, e4869. https://doi.org/10.7717/peerj.4869.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Falótico, T., & Ottoni, E. B. (2014). Sexual bias in probe tool manufacture and use by wild bearded capuchin monkeys. Behavioural Processes, 108, 117–122. https://doi.org/10.1016/j.beproc.2014.09.036.

    Article  PubMed  Google Scholar 

  22. Falótico, T., & Ottoni, E. B. (2016). The manifold use of pounding stone tools by wild capuchin monkeys of Serra da Capivara National Park, Brazil. Behaviour, 153(4), 421–442. https://doi.org/10.1163/1568539X-00003357

  23. Falótico, T., Coutinho, P. H. M., Bueno, C. Q., Rufo, H. P., & Ottoni, E. B. (2018). Stone tool use by wild capuchin monkeys (Sapajus libidinosus) at Serra das Confusões National Park, Brazil. Primates, 59(4), 385–394. https://doi.org/10.1007/s10329-018-0660-0.

    Article  PubMed  Google Scholar 

  24. Falótico, T., Proffitt, T., Ottoni, E. B., Staff, R. A., & Haslam, M. (2019). Three thousand years of wild capuchin stone tool use. Nature Ecology & Evolution, 3, 1034–1038. https://doi.org/10.1038/s41559-019-0904-4.

    Article  Google Scholar 

  25. Ferreira, R. G., Jerusalinsky, L., Silva, T. C. F., de Souza Fialho, M., de Araújo Roque, A., et al (2009). On the occurrence of Cebus flavius (Schreber 1774) in the Caatinga, and the use of semi-arid environments by Cebus species in the Brazilian state of Rio Grande do Norte. Primates, 50(4), 357–362. https://doi.org/10.1007/s10329-009-0156-z.

    Article  PubMed  Google Scholar 

  26. Floriani, D. C., Fukuda, J. C., & Pinto, E. F. (2004). Lençóis Maranhenses National Park: the largest coastal dunes area in South America. Gerenciamento Costeiro Integrado, 2, 62–64.

  27. Fornaro, A. C. (2012). Logística e agronegócio globalizado no Estado do Tocantins: Um estudo sobre a expansão das fronteiras agrícolas modernas no território brasileiro. Resource document. Universidade Estadual de Campinas. http://repositorio.unicamp.br/bitstream/REPOSIP/286703/1/Fornaro_AlexandreCaselli1979-_M.pdfxx. Accessed 12 Nov 2019.

  28. Fragaszy, D. M., Visalberghi, E., & Fedigan, L. M. (2004a). The complete capuchin: The biology of the genus Cebus. Cambridge: Cambridge University Press. https://doi.org/10.5860/choice.42-4029.

    Google Scholar 

  29. Fragaszy, D., Izar, P., Visalberghi, E., Ottoni, E. B., & de Oliveira, M. G. (2004b). Wild capuchin monkeys (Cebus libidinosus) use anvils and stone pounding tools. American Journal of Primatology, 64(4), 359–366. https://doi.org/10.1002/ajp.20085.

    Article  PubMed  Google Scholar 

  30. Fragaszy, D. M., Eshchar, Y., Visalberghi, E., Resende, B., Laity, K., & Izar, P. (2017). Synchronized practice helps bearded capuchin monkeys learn to extend attention while learning a tradition. Proceedings of the National Academy of Sciences of the USA, 114, 7798–7805. https://doi.org/10.1073/pnas.1621071114.

    CAS  Article  PubMed  Google Scholar 

  31. Friess, D. A., Rogers, K., Lovelock, C. E., Krauss, K. W., Hamilton, S. E., et al (2019). The state of the world’s mangrove forests: past, present, and future. Annual Review of Environment and Resources, 44, 89–115. https://doi.org/10.1146/annurev-environ-101718-033302.

    Article  Google Scholar 

  32. Ganem, R. S., Drummond, J. A., & de Aandrade Franco, J. L. (2013). Conservation polices and control of habitat fragmentation in the Brazilian Cerrado biome. Ambiente & Sociedade, 16(3), 99–118. https://doi.org/10.1590/S1414-753X2013000300007.

    Article  Google Scholar 

  33. Garland, E. C., Goldizen, A. W., Lilley, M. S., Rekdahl, M. L., Garrigue, C., et al (2015). Population structure of humpback whales in the western and central South Pacific Ocean as determined by vocal exchange among populations. Conservation Biology, 29(4), 1198–1207. https://doi.org/10.1111/cobi.12492.

    Article  PubMed  Google Scholar 

  34. Gibbs, H. K., Rausch, L., Munger, J., Schelly, I., Morton, D. C., et al (2015). Brazil’s soy moratorium. Science, 347(6220), 377–378. https://doi.org/10.1126/science.aaa0181.

    CAS  Article  PubMed  Google Scholar 

  35. Goren-Inbar, N., Sharon, G., Melamed, Y., & Kislev, M. (2002). Nuts, nut cracking, and pitted stones at Gesher Benot Ya ‘aqov, Israel. Proceedings of the National Academy of Sciences of the USA, 99(4), 2455–2460. https://doi.org/10.1073/pnas.032570499.

    CAS  Article  PubMed  Google Scholar 

  36. Gumert, M. D., Kluck, M., & Malaivijitnond, S. (2009). The physical characteristics and usage patterns of stone axe and pounding hammers used by long-tailed macaques in the Andaman Sea region of Thailand. American Journal of Primatology, 71(7), 594–608. https://doi.org/10.1002/ajp.20694.

    Article  PubMed  Google Scholar 

  37. Gumert, M. D., & Malaivijitnond, S. (2012). Marine prey processed with stone tools by burmese long‐tailed macaques (Macaca fascicularis aurea) in intertidal habitats. American Journal of Physical Anthropology, 149(3), 447–457. https://doi.org/10.1002/ajpa.22143.

  38. ICMBio (2009). Instituto Chico Mendes, Ato Instrução Normativa 07 de 11 de dezembro de 2009. Resource document. http://www.icmbio.gov.br/portal/images/stories/o-que-somos/in072009.pdf. Accessed 15 March 2018.

  39. Izar, P., Verderane, M. P., Peternelli-dos-Santos, L., Mendonça-Furtado, O., Presotto, A., et al (2012). Flexible and conservative features of social systems in tufted capuchin monkeys: comparing the sociecology of Sapajus libidinosus and Sapajus nigritus. American Journal of Primatology, 74, 315–331. https://doi.org/10.1002/ajp.20968.

    Article  PubMed  Google Scholar 

  40. Izar, P., Resende, B. D., & Ferreira, R. G. (2018). Proximate causes of tool use in feeding in the genus Sapajus, La Primatología en Latino América 2 (Vol. 1, pp. 239–250). Altos de Pipe: Ediciones IVIC.

  41. Koops, K., Wrangham, R. W., Cumberlidge, N., Fitzgerald, M. A., van Leeuwen, K. L., et al (2019). Crab-fishing by chimpanzees in the Nimba Mountains, Guinea. Journal of Human Evolution, 133, 230–241. https://doi.org/10.1016/j.jhevol.2019.05.002.

    Article  PubMed  Google Scholar 

  42. Kühl, H. S., Boesch, C., Kulik, L., Haas, F., Arandjelovic, M., et al (2019). Human impact erodes chimpanzee behavioral diversity. Science, 363(6434), 1453–1455. https://doi.org/10.1126/science.aau4532.

    CAS  Article  PubMed  Google Scholar 

  43. Lapola, D. M., Martinelli, L. A., Peres, C. A., Ometto, J. P., Ferreira, M. E., et al (2014). Pervasive transition of the Brazilian land-use system. Nature Climate Change, 4(1), 27. https://doi.org/10.1038/nclimate2056.

    Article  Google Scholar 

  44. Lillesand, T., Kiefer, R. W., & Chipman, J. (2015). Remote sensing and image interpretation. Hoboken: John Wiley & Sons.

    Google Scholar 

  45. Lin, Y.-P., Chu, H.-J., Wu, C. F., & Verburg, P. H. (2011). Predictive ability of logistic regression, auto-logistic regression and neural network models in empirical land-use change modeling: a case study. International Journal of Geographical Information Science, 25(1), 65–87. https://doi.org/10.1080/13658811003752332.

    Article  Google Scholar 

  46. Luncz, L. V., Falótico, T., Pascual-Garrido, A., Corat, C., Mosley, H., & Haslam, M. (2016). Wild capuchin monkeys adjust stone tools according to changing nut properties. Scientific Reports, 6, 33089. https://doi.org/10.1038/srep33089.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. Malaivijitnond, S., Lekprayoon, C., Tandavanittj, N., Panha, S., Cheewatham, C., & Hamada, Y. (2007). Stone-tool usage by Thai long-tailed macaques (Macaca fascicularis). American Journal of Primatology, 69(2), 227–233. https://doi.org/10.1002/ajp.20342.

    Article  PubMed  Google Scholar 

  48. Mannu, M., & Ottoni, E. B. (2009). The enhanced tool-kit of two groups of wild bearded capuchin monkeys in the Caatinga: tool making, associative use, and secondary tools. American Journal of Primatology, 71(3), 242–251. https://doi.org/10.1002/ajp.20642.

    Article  PubMed  Google Scholar 

  49. Maxwell, S. L., Fuller, R. A., Brooks, T. M., & Watson, J. E. (2016). Biodiversity: the ravages of guns, nets and bulldozers. Nature News, 536(7615), 143. Resource document. https://www.nature.com/news/biodiversity-the-ravages-of-guns-nets-and-bulldozers-1.20381. Accessed 1 Nov 2019.

  50. McComb, K., Moss, C., Durant, S. M., Baker, L., & Sayialel, S. (2001). Matriarchs as repositories of social knowledge in African elephants. Science, 292(5516), 491–494. https://doi.org/10.1126/science.1057895.

    CAS  Article  PubMed  Google Scholar 

  51. McGrew, W.C. (2003). Ten dispatches from the chimpanzee culture wars. In F. B. De Waal & P. L. Tyack (Eds.), Animal social complexity: intelligence, culture, and individualized societies (pp. 419-439). Harvard University Press.

  52. McLachlan, A., & Defeo, O. (2017). The ecology of sandy shores. San Diego: Academic Press.

    Google Scholar 

  53. Mello-Théry, N. A. (2011). Conservation of natural areas in São Paulo. Estudos Avançados, 25(71), 175–188. Resource document. https://scholar.google.com/scholar?hl=en&as_sdt=0%2C21&q=Conservation+of+natural+areas+in+S%C3%A3o+Paulo&btnG=. Accessed 20 Dec 2019.

  54. Mendes, F. D. C., Cardoso, R. M., Ottoni, E. B., Izar, P., Villar, D. N. A., & Marquezan, R. F. (2015). Diversity of nutcracking tool sites used by Sapajus libidinosus in Brazilian Cerrado. American Journal of Primatology, 77(5), 535–546. https://doi.org/10.1002/ajp.22373.

    Article  PubMed  Google Scholar 

  55. Menezes, M. P. M. D., Berger, U., & Mehlig, U. (2008). Mangrove vegetation in Amazonia: a review of studies from the coast of Pará and Maranhão States, north Brazil. Acta Amazonica, 38(3), 403–420. https://doi.org/10.1590/S0044-59672008000300004.

    Article  Google Scholar 

  56. Nowak, K., Perkin, A., & Jones, T. (2009). Update on habitat loss and conservation status of the endangered Zanzibar red colobus on Uzi and Vundwe Islands (p. 22). Resource document. Department of Commercial Crops, Fruits, and Forestry. https://www.researchgate.net/profile/Andrew_Perkin3/publication/237601815_Update_on_Habitat_Loss_and_Conservation_Status_of_the_Endangered_Zanzibar_Red_Colobus_on_Uzi_and_Vundwe_Islands/links/543539b30cf2bf1f1f2831dc.pdf. Accessed 12 Nov 2019.

  57. Oliveira-Filho, A. T., & Ratter, J. A. (2002). Vegetation physiognomies and woody flora of the cerrado biome. In P. S. Oliveira & R. J. Marquis (Eds.), The cerrados of Brazil: Ecology and natural history of a neotropical savanna (pp. 91–120). New York: Columbia University Press.

    Google Scholar 

  58. Osborn, F. V. (2002). Capsicum oleoresin as an elephant repellent: field trials in the communal lands of Zimbabwe. Journal of Wildlife Management, 66, 674–677. https://doi.org/10.2307/3803133.

    Article  Google Scholar 

  59. Ottoni, E. B., & Izar, P. (2008). Capuchin monkey tool use: overview and implications. Evolutionary Anthropology, 17(4), 171–178. https://doi.org/10.1002/evan.20185.

    Article  Google Scholar 

  60. Presotto, A., Verderane, M. P., Biondi, L., Mendonça-Furtado, O., Spagnoletti, N., et al (2018). Intersection as key locations for bearded capuchin monkeys (Sapajus libidinosus) traveling within a route network. Animal Cognition, 21(3), 393–405. https://doi.org/10.1007/s10071-018-1176-0.

    CAS  Article  PubMed  Google Scholar 

  61. Rausch, L. L., Gibbs, H. K., Schelly, I., Brandão, A., Morton, D. C., et al (2019). Soy expansion in Brazil’s Cerrado. Conservation Letters. https://doi.org/10.1111/conl.12671.

  62. Rocha, C. E. R., & Foschiera, A. A. (2018). Expansão da produção agrícola no território do Matopiba: Territorialização de agentes econômicos do setor sojicultor em Porto Nacional–TO. Expansion of agricultural production in the territory of Matopiba: Territorializing of economic agents (...). Caderno de Geografia, 28(52), 145–165. https://doi.org/10.5752/p.2318-2962.2018v28n52pp.2318-2962.2018v28n52p145.

    Article  Google Scholar 

  63. Ryan, S. J. (2006). The role of culture in conservation planning for small or endangered populations. Conservation Biology, 20(4), 1321–1324. https://doi.org/10.1111/j.1523-1739.2006.00347.x.

    CAS  Article  PubMed  Google Scholar 

  64. Rylands, A. B., & Brandon, K. (2005). Brazilian protected areas. Conservation Biology, 19(3), 612–618. https://doi.org/10.1111/j.1523-1739.2005.00711.x.

    Article  Google Scholar 

  65. Santos, R. R. (2010). Uso de ferramentas por macacos-prego em manguezais. Resource document. Universidade Federal do Rio Grande do Norte. https://repositorio.ufrn.br/jspui/bitstream/123456789/17213/1/FerramentaMacacoPrego_Santos_2010.pdf. Accessed 12 Nov 2019.

  66. Santos, R. R., & Bridgeman, L. L. (2019). Mangrove-living primates in the Neotropics: An ecological review. In K. Nowak, I. Matsuda, & A. A. Barnett (Eds.), Primates in flooded habitats: Ecology and conservation (pp. 54–58). Cambridge: Cambridge University Press.

    Google Scholar 

  67. Santos, R. R., Araújo, A., Fragaszy, D. M., & Ferreira, R. G. (2019). The role of tools in the feeding ecology of bearded capuchins living in mangroves. In K. Nowak, I. Matsuda, & A. A. Barnett (Eds.), Primates in flooded habitats: Ecology and conservation (pp. 179–190). Cambridge: Cambridge University Press.

    Google Scholar 

  68. Silva, J. M. (2019). Seleção de ferramentas e caranguejos por macacos-prego (Sapajus libidinosus) em manguezal. Resource document. Research Gate. https://www.researchgate.net/publication/338228860_SELECAO_DE_FERRAMENTAS_E_CARANGUEJOS_POR_MACACOS-PREGO_Sapajus_libidinosus_EM_MANGUEZAL. https://doi.org/10.13140/RG.2.2.20422.22084

  69. Silva, D. C., Vieira, T. B., da Silva, J. M., & de Cassia Faria, K. (2018). Biogeography and priority areas for the conservation of bats in the Brazilian Cerrado. Biodiversity and Conservation, 27(4), 815–828. https://doi.org/10.1007/s10531-017-1464-z.

    Article  Google Scholar 

  70. Soane, B. D., & Van Ouwerkerk, C. (1994). Soil compaction problems in world agriculture. Developments in Agricultural Engineering, 11, 1–21. https://doi.org/10.1016/B978-0-444-88286-8.50009-X.

    Article  Google Scholar 

  71. Spagnoletti, N., Visalberghi, E., Presotto, A., Fragaszy, D., & Izar, P. (2011). Do wild bearded capuchin monkeys (Cebus libidinosus) select anvils and habitat when using stone tools? Folia Primatologica, 82, 345–346. https://doi.org/10.1016/j.jhevol.2011.02.010.

    Article  Google Scholar 

  72. Spagnoletti, N., Visalberghi, E., Verderane, M. P., Ottoni, O., Izar, P., & Fragaszy, D. (2012). Stone tool use in wild bearded capuchin monkeys, Cebus libidinosus: is it a strategy to overcome food scarcity? Animal Behaviour, 83, 1285–1294. https://doi.org/10.1016/j.anbehav.2012.03.002.

    Article  Google Scholar 

  73. Spagnoletti, N., Cardoso, T. C. M., Fragaszy, D., & Izar, P. (2017). Coexistence between humans and capuchins (Sapajus libidinosus): comparing observational data with farmers’ perceptions of crop losses. International Journal of Primatology, 38(2), 243–262. https://doi.org/10.1007/s10764-016-9926-9.

    Article  Google Scholar 

  74. United States Geological Survey (2019). Landsat missions. Resource document. USGS. https://www.usgs.gov/land-resources/nli/landsat. Accessed 10 Feb 2019.

  75. Vanucci, M. (2001). What is so special about mangroves? Brazilian Journal of Biology, 61(4), 599–603. https://doi.org/10.1590/S1519-69842001000400008.

    Article  Google Scholar 

  76. Verderane, M. P. (2010). Socioecologia de macacos-prego (Cebus libidinosus) em área de ecótono cerrado/caatinga. Resource document. Universidade de São Paulo https://teses.usp.br/teses/disponiveis/47/47132/tde-27072010-084124/publico/verderane_do.pdf. Accessed 10 Oct 2019.

  77. Verderane, M. P., Izar, P., Visalberghi, E., & Fragaszy, D. M. (2013). Socioecology of wild bearded capuchin monkeys (Sapajus libidinosus): an analysis of social relationships among female primates that use tools in feeding. Behaviour, 150(6), 659–689. https://doi.org/10.1163/1568539X-00003076.

    Article  Google Scholar 

  78. Visalberghi, E., Spagnoletti, N., Ramos da Silva, E. D., Andrade, F. R., Ottoni, E., et al (2009). Distribution of potential suitable hammers and transport of hammer tools and nuts by wild capuchin monkeys. Primates, 50(2), 95–104. https://doi.org/10.1007/s10329-008-0127-9.

    Article  PubMed  Google Scholar 

  79. Visalberghi, E., Haslam, M., Spagnoletti, N., & Fragaszy, D. (2013). Use of stone hammer tools and anvils by bearded capuchin monkeys over time and space: construction of an archeological record of tool use. Journal of Archaeological Science, 40(8), 3222–3232. https://doi.org/10.1016/j.jas.2013.03.021.

    Article  Google Scholar 

  80. Visalberghi, E., Sirianni, G., Fragaszy, D., & Boesch, C. (2015). Percussive tool use by Taï Western chimpanzees and Fazenda Boa Vista bearded capuchin monkeys: a comparison. Philosophical Transactions of the Royal Society B: Biological Sciences, 370(1682), 20140351. https://doi.org/10.1098/rstb.2014.0351.

    Article  Google Scholar 

  81. Whiten, A. (2017). Culture extends the scope of evolutionary biology in the great apes. Proceedings of the National Academy of Sciences, 114(30), 7790–7797. https://doi.org/10.1073/pnas.1620733114.

  82. Whitehead, H., Rendell, L., Osborne, R. W., & Würsig, B. (2004). Culture and conservation of non-humans with reference to whales and dolphins: review and new directions. Biological Conservation, 120(3), 427–437. https://doi.org/10.1016/j.biocon.2004.03.017.

  83. Zinn, Y. L., Lal, R., & Resck, D. V. (2005). Changes in soil organic carbon stocks under agriculture in Brazil. Soil and Tillage Research, 84(1), 28–40. https://doi.org/10.1016/j.still.2004.08.007.

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Joanna Setchell, and two anonymous reviewers for their valuable comments and suggestions on this manuscript. We thank the owners of Fazenda Boa Vista (FBV) (Marino Gomes de Oliveira and Maria C. Fonseca de Oliveira) for permission to conduct research and the field assistants Marino Junior, Renato, Arizomar, Marcos, Márcio, Mara, Jozimar, and Nonato. We thank Wagner Costa Ribeiro for his comments on an earlier version of the manuscript. We thank Gordon Martin for editing and comments.

Funding

This study was funded by NASA-Develop National Program granted to AP and CR. Salisbury University grant to AP. The University of Georgia grant to RS. EthoCebus research at FBV is funded by FAPESP (2011/21032-2; 2012/20107-1; 2013/192192) and CNPq (303306/2009-2) grants to PI, CAPES (017/2012; 20131537) grants to NS and MPV, FAPEMA UNIVERSAL (00613/15) to RRS.

Author information

Affiliations

Authors

Contributions

AP conceived and designed the study. AP and CR performed Fazenda Boa Vista land cover analysis. KS performed Morro do Boi land cover analysis. NS and MV conducted data collection at Fazenda Boa Vista. RRS conducted data collection at Morro do Boi. RS collaborated in writing the manuscript. MM and CR collaborated in imaging analysis. AP, PI, EV, and DF wrote the manuscript. All authors contributed with comments and provided editorial advise.

Corresponding author

Correspondence to Andréa Presotto.

Additional information

Handling Editor: Joanna M. Setchell

Electronic supplementary material

ESM 1

(PDF 1320 kb)

ESM 2

(KML 3 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Presotto, A., Remillard, C., Spagnoletti, N. et al. Rare Bearded Capuchin (Sapajus libidinosus) Tool-Use Culture is Threatened by Land use Changes in Northeastern Brazil. Int J Primatol 41, 596–613 (2020). https://doi.org/10.1007/s10764-020-00166-3

Download citation

Keywords

  • Animal culture
  • Bearded capuchins
  • Behavior
  • Forest fragmentation
  • Primate conservation
  • Primate traditions