Advertisement

Primates

, Volume 59, Issue 4, pp 385–394 | Cite as

Stone tool use by wild capuchin monkeys (Sapajus libidinosus) at Serra das Confusões National Park, Brazil

  • Tiago Falótico
  • Paulo Henrique M. Coutinho
  • Carolina Q. Bueno
  • Henrique P. Rufo
  • Eduardo B. Ottoni
Original Article

Abstract

Capuchin monkeys (Sapajus spp.) are proficient tool users, and the use of stone tools occurs in several populations, mostly to crack open encased foods. Two well-studied Brazilian populations of Sapajus libidinosus inhabit Fazenda Boa Vista and Serra da Capivara National Park and present different behavioral sets regarding tool use. Serra das Confusões National Park (SCoNP) lies between those sites, but little is known about the capuchin monkey population that lives there. To begin unraveling the capuchin behavior in this area, we conducted a brief survey for tool use sites. We found indirect evidence that capuchin monkeys at SCoNP use stone hammers to crack open at least four species of seeds and fruits. Plant reproductive parts there are processed with stone tools in a similar pattern to the other sites. Further study is needed to directly observe tool use by capuchin monkeys at SCoNP, verify the occurrence of other possible types of tool use in this population, and thus fully compare their tool use repertoire to that of other populations.

Keywords

Tradition Culture Cebus libidinosus Nut-cracking Percussive technology Lithics 

Notes

Acknowledgements

This research was authorized by the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio authorization no. 37615-6). We thank park chief José W.P.L. Ribeiro (Mitinha) for logistical support, Bruno C. Polverini for taxonomic identification of the vegetation samples, Gergely A.J. Szabó for rock type identification, and Noemi Spagnoletti, Michael D. Gumert and William C. McGrew for helpful comments that improved the manuscript. The study was funded by grants from São Paulo Research Foundation (FAPESP) to TF (2013/05219-0) and EBO (2014/04818-0), and from CNPq to EBO (PQ, Aux. 443309/2014-0).

Supplementary material

10329_2018_660_MOESM1_ESM.xlsx (20 kb)
Supplementary material 1 (XLSX 20 kb)

References

  1. Boesch C, Boesch H (1983) Optimisation of nut-cracking with natural hammers by wild chimpanzees. Behaviour 83:265–286.  https://doi.org/10.1163/156853983X00192 CrossRefGoogle Scholar
  2. Bour R, Zaher H (2005) A new species of Mesoclemmys, from the open formations of northeastern Brazil (Chelonii, Chelidae). Papéis Avulsos de Zool (São Paulo) 45:295–311.  https://doi.org/10.1590/S0031-10492005002400001 CrossRefGoogle Scholar
  3. Canale GR, Guidorizzi CE, Kierulff MCM, Gatto CAFR (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). Am J Primatol 71:366–372.  https://doi.org/10.1002/ajp.20648 CrossRefPubMedGoogle Scholar
  4. Chalk J, Wright BW, Lucas PW et al (2015) Age-related variation in the mechanical properties of foods processed by Sapajus libidinosus. Am J Phys Anthropol 159:199–209.  https://doi.org/10.1002/ajpa.22865 CrossRefPubMedGoogle Scholar
  5. Cutrim FHR (2013) Padrão comportamental e uso de ferramentas em macacos-prego (Sapajus libidinosus) residentes em manguezal. PhD Thesis. Institute of Psychology, University of São Paulo. São Paulo.  https://doi.org/10.11606/t.47.2013.tde-09012014-163238
  6. Dal Vechio F, Teixeira M Jr, Recoder RS et al (2016) The herpetofauna of Parque Nacional da Serra das Confusões, state of Piauí, Brazil, with a regional species list from an ecotonal area of Cerrado and Caatinga. Biota Neotrop 16:e20150105.  https://doi.org/10.1590/1676-0611-BN-2015-0105 CrossRefGoogle Scholar
  7. De Moraes BLC, Da Silva Souto A, Schiel N (2014) Adaptability in stone tool use by wild capuchin monkeys (Sapajus libidinosus). Am J Primatol 76:967–977.  https://doi.org/10.1002/ajp.22286 CrossRefPubMedGoogle Scholar
  8. de Moura AC (2007) Stone banging by wild capuchin monkeys: an unusual auditory display. Folia Primatol 78:36–45.  https://doi.org/10.1159/000095684 CrossRefPubMedGoogle Scholar
  9. de Moura AC, Lee PC (2004) Capuchin stone tool use in caatinga dry forest. Science 306:1909–1910.  https://doi.org/10.1126/science.1102558 CrossRefPubMedGoogle Scholar
  10. Falótico T, Ottoni EB (2013) Stone throwing as a sexual display in wild female bearded capuchin monkeys, Sapajus libidinosus. PLoS one 8:e79535.  https://doi.org/10.1371/journal.pone.0079535 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Falótico T, Ottoni EB (2014) Sexual bias in probe tool manufacture and use by wild bearded capuchin monkeys. Behav Process 108:117–122.  https://doi.org/10.1016/j.beproc.2014.09.036 CrossRefGoogle Scholar
  12. Falótico T, Ottoni EB (2016) The manifold use of pounding stone tools by wild capuchin monkeys of Serra da Capivara National Park, Brazil. Behaviour 153:421–442.  https://doi.org/10.1163/1568539X-00003357 CrossRefGoogle Scholar
  13. Falótico T, Siqueira JO, Ottoni EB (2017a) Digging up food: excavation stone tool use by wild capuchin monkeys. Sci Rep 7:6278.  https://doi.org/10.1038/s41598-017-06541-0 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Falótico T, Spagnoletti N, Haslam M et al (2017b) Analysis of sea almond (Terminalia catappa) cracking sites used by wild Burmese long-tailed macaques (Macaca fascicularis aurea). Am J Primatol 79:e22629.  https://doi.org/10.1002/ajp.22629 CrossRefGoogle Scholar
  15. Ferraz EMN, Rodal MJN, Sampaio EVSB (2003) Physiognomy and structure of vegetation along an altitudinal gradient in the semi-arid region of northeastern Brazil. Phytocoenologia 33:71–92.  https://doi.org/10.1127/0340-269X/2003/0033-0071 CrossRefGoogle Scholar
  16. Ferreira RG, Emidio RA, Jerusalinsky L (2010) Three stones for three seeds: natural occurrence of selective tool use by capuchins (Cebus libidinosus) based on an analysis of the weight of stones found at nutting sites. Am J Primatol 72:270–275.  https://doi.org/10.1002/ajp.20771 CrossRefPubMedGoogle Scholar
  17. Fragaszy DM, Izar P, Visalberghi E et al (2004) Wild capuchin monkeys (Cebus libidinosus) use anvils and stone pounding tools. Am J Primatol 64:359–366.  https://doi.org/10.1002/ajp.20085 CrossRefPubMedGoogle Scholar
  18. Gregorin R, Carmignotto AP, Percequillo AR (2008) Quirópteros do Parque Nacional da Serra das Confusões, Piauí, nordeste do Brasil. Chiroptera Neotropical 14:366–383Google Scholar
  19. Gumert MD, Malaivijitnond S (2013) Long-tailed macaques select mass of stone tools according to food type. Phil Trans R Soc B 368:20120413.  https://doi.org/10.1098/rstb.2012.0413 CrossRefPubMedGoogle Scholar
  20. Gumert MD, 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. Am J Primatol 71:594–608.  https://doi.org/10.1002/ajp.20694 CrossRefPubMedGoogle Scholar
  21. Haslam M, Luncz LV, Staff RA et al (2016) Pre-Columbian monkey tools. Curr Biol 26:R521–R522.  https://doi.org/10.1016/j.cub.2016.05.046 CrossRefPubMedGoogle Scholar
  22. IBAMA (2003) Plano de manejo do Parque Nacional da Serra das Confusões—PI. Instituto Brasileiro do Meio Ambiente e Recursos Naturais Renováveis - IBAMA. https://www.icmbio.gov.br/portal/images/stories/imgs-unidades-coservacao/parna_serra_das_confusoes.pdf
  23. Luncz LV, Falótico T, Pascual-Garrido A et al (2016) Wild capuchin monkeys adjust stone tools according to changing nut properties. Sci Rep 6:33089.  https://doi.org/10.1038/srep33089 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Mannu M, Ottoni EB (2009) The enhanced tool-kit of two groups of wild bearded capuchin monkeys in the Caatinga: tool making, associative use, and secondary tools. Am J Primatol 71:242–251.  https://doi.org/10.1002/ajp.20642 CrossRefPubMedGoogle Scholar
  25. Mendes FDC, Cardoso RM, Ottoni EB et al (2015) Diversity of nutcracking tool sites used by Sapajus libidinosus in Brazilian Cerrado. Am J Primatol 77:535–546.  https://doi.org/10.1002/ajp.22373 CrossRefPubMedGoogle Scholar
  26. Oddi G, Batista W, Maiorano L et al (2017) Habitat use in capuchin monkeys (Sapajus spp.): a preliminary study in the Caatinga of Rio São Francisco Natural Monument (Bahia, Brazil). Folia Primatol 88:189–209.  https://doi.org/10.1159/000479129 CrossRefGoogle Scholar
  27. Olson DM, Dinerstein E, Wikramanayake ED et al (2001) Terrestrial ecoregions of the world: a new map of life on earth. Bioscience 51:933–938.  https://doi.org/10.1641/0006-3568(2001)051[0933:TEOTWA]2.0.CO;2 CrossRefGoogle Scholar
  28. Ottoni EB, Izar P (2008) Capuchin monkey tool use: overview and implications. Evol Anthropol 17:171–178.  https://doi.org/10.1002/evan.20185 CrossRefGoogle Scholar
  29. Ottoni EB, Mannu M (2001) Semifree-ranging tufted capuchins (Cebus apella) spontaneously use tools to crack open nuts. Int J Primatol 22:347–358.  https://doi.org/10.1023/A:1010747426841 CrossRefGoogle Scholar
  30. Peternelli-Dos-Santos L (2015) Parâmetros nutricionais da dieta de duas populações de macacos-prego: Sapajus libidinosus no ecótono Cerrado/Caatinga e Sapajus nigritus na Mata Atlântica. PhD Thesis. Institute of Psychology, University of São Paulo. São Paulo. doi:10.11606/t.47.2015.tde-10082015-110633Google Scholar
  31. Proffitt T, Luncz LV, Falótico T et al (2016) Wild monkeys flake stone tools. Nature 539:85–88.  https://doi.org/10.1038/nature20112 CrossRefPubMedGoogle Scholar
  32. Rocha VJ, Reis NRD, Sekiama ML (1998) Uso de ferramentas por Cebus apella (Linnaeus) (Primates, Cebidae) para obtenção de larvas de coleoptera que parasitam sementes de Syagrus romanzoffianum (Cham.) Glassm. (Arecaceae). Rev Bras Zool 15:945–950.  https://doi.org/10.1590/S0101-81751998000400012 CrossRefGoogle Scholar
  33. Silveira LF, Santos M (2012) Bird richness in Serra das Confusões National Park, Brazil: how many species may be found in an undisturbed caatinga? Rev Bras Ornitol 20:188–198Google Scholar
  34. Sirianni G, Visalberghi E (2013) Wild bearded capuchins process cashew nuts without contacting caustic compounds. Am J Primatol 75:387–393.  https://doi.org/10.1002/ajp.22119 CrossRefPubMedGoogle Scholar
  35. Spagnoletti N, Visalberghi E, Ottoni EB et al (2011) Stone tool use by adult wild bearded capuchin monkeys (Cebus libidinosus). Frequency, efficiency and tool selectivity. J Hum Evol 61:97–107.  https://doi.org/10.1016/j.jhevol.2011.02.010 CrossRefPubMedGoogle Scholar
  36. Van Schaik CP, Ancrenaz M, Borgen G et al (2003) Orangutan cultures and the evolution of material culture. Science 299:102–105.  https://doi.org/10.1126/science.1078004 CrossRefPubMedGoogle Scholar
  37. Veloso HP, Rangel-Filho ALR, Lima JCA (1991) Classificação da vegetação brasileira adaptada a um sistema universal. IBGE, Departamento de Recursos Naturais e Estudos Ambientais. Rio de Janeiro. https://biblioteca.ibge.gov.br/visualizacao/monografias/GEBIS%20-%20RJ/classificacaovegetal.pd
  38. Verderane MP, Visalberghi E, Izar P, Fragaszy DM (2013) Socioecology of wild bearded capuchin monkeys (Sapajus libidinosus): an analysis of social relationships among female primates that use tools in feeding. Behaviour 150:659–689.  https://doi.org/10.1163/1568539X-00003076 CrossRefGoogle Scholar
  39. Visalberghi E, Fragaszy DM (2013) The Etho-Cebus Project: Stone-tool use by wild capuchin monkeys. In: Sanz C, Sanz CM, Call J et al (eds) Tool use in animals: cognition and ecology. Cambridge University, Cambridge, pp 203–222CrossRefGoogle Scholar
  40. Visalberghi E, Fragaszy DM, Ottoni EB et al (2007) Characteristics of hammer stones and anvils used by wild bearded capuchin monkeys (Cebus libidinosus) to crack open palm nuts. Am J Phys Anthropol 132:426–444.  https://doi.org/10.1002/ajpa.20546 CrossRefPubMedGoogle Scholar
  41. Visalberghi E, Sabbatini G, Spagnoletti N et al (2008) Physical properties of palm fruits processed with tools by wild bearded capuchins (Cebus libidinosus). Am J Primatol 70:884–891.  https://doi.org/10.1002/ajp.20578 CrossRefPubMedGoogle Scholar
  42. Visalberghi E, Spagnoletti N, Ramos da Silva ED et al (2009) Distribution of potential suitable hammers and transport of hammer tools and nuts by wild capuchin monkeys. Primates 50:95–104.  https://doi.org/10.1007/s10329-008-0127-9 CrossRefPubMedGoogle Scholar
  43. Visalberghi E, Haslam M, Spagnoletti N, Fragaszy DM (2013) Use of stone hammer tools and anvils by bearded capuchin monkeys over time and space: construction of an archeological record of tool use. J Archaeol Sci 40:3222–3232.  https://doi.org/10.1016/j.jas.2013.03.021 CrossRefGoogle Scholar
  44. Visalberghi E, Albani A, Ventricelli M et al (2016) Factors affecting cashew processing by wild bearded capuchin monkeys (Sapajus libidinosus, Kerr 1792). Am J Primatol 78:799–815.  https://doi.org/10.1002/ajp.22545 CrossRefPubMedGoogle Scholar
  45. Westergaard GC, Fragaszy DM (1987) The manufacture and use of tools by capuchin monkeys (Cebus apella). J Comp Psychol 101:159–168.  https://doi.org/10.1037/0735-7036.101.2.159 CrossRefGoogle Scholar
  46. Whiten A, Goodall J, McGrew WC et al (1999) Cultures in chimpanzees. Nature 399:682–685.  https://doi.org/10.1038/21415 CrossRefPubMedGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Experimental Psychology, Institute of PsychologyUniversity of São PauloSão PauloBrazil
  2. 2.Neotropical Primates Research GroupSão PauloBrazil

Personalised recommendations