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.
Similar content being viewed by others
References
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Gregorin R, Carmignotto AP, Percequillo AR (2008) Quirópteros do Parque Nacional da Serra das Confusões, Piauí, nordeste do Brasil. Chiroptera Neotropical 14:366–383
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
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
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
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
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
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
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
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
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
Ottoni EB, Izar P (2008) Capuchin monkey tool use: overview and implications. Evol Anthropol 17:171–178. https://doi.org/10.1002/evan.20185
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
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-10082015-110633
Proffitt T, Luncz LV, Falótico T et al (2016) Wild monkeys flake stone tools. Nature 539:85–88. https://doi.org/10.1038/nature20112
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
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 20:188–198
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
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
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
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
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
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 203–222
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
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
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
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
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
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
Whiten A, Goodall J, McGrew WC et al (1999) Cultures in chimpanzees. Nature 399:682–685. https://doi.org/10.1038/21415
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).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
About this article
Cite this article
Falótico, T., Coutinho, P.H.M., Bueno, C.Q. et al. Stone tool use by wild capuchin monkeys (Sapajus libidinosus) at Serra das Confusões National Park, Brazil. Primates 59, 385–394 (2018). https://doi.org/10.1007/s10329-018-0660-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10329-018-0660-0