What limits tool use in nonhuman primates? Insights from tufted capuchin monkeys (Sapajus spp.) and chimpanzees (Pan troglodytes) aligning three-dimensional objects to a surface

Abstract

Perceptuomotor functions that support using hand tools can be examined in other manipulation tasks, such as alignment of objects to surfaces. We examined tufted capuchin monkeys’ and chimpanzees’ performance at aligning objects to surfaces while managing one or two spatial relations to do so. We presented six subjects of each species with a single stick to place into a groove, two sticks of equal length to place into two grooves, or two sticks joined as a T to place into a T-shaped groove. Tufted capuchins and chimpanzees performed equivalently on these tasks, aligning the straight stick to within 22.5° of parallel to the groove in approximately half of their attempts to place it, and taking more attempts to place the T stick than two straight sticks. The findings provide strong evidence that tufted capuchins and chimpanzees do not reliably align even one prominent axial feature of an object to a surface, and that managing two concurrent allocentric spatial relations in an alignment problem is significantly more challenging to them than managing two sequential relations. In contrast, humans from 2 years of age display very different perceptuomotor abilities in a similar task: they align sticks to a groove reliably on each attempt, and they readily manage two allocentric spatial relations concurrently. Limitations in aligning objects and in managing two or more relations at a time significantly constrain how nonhuman primates can use hand tools.

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Notes

  1. 1.

    Recent molecular analysis has revealed that capuchin monkeys, formerly identified as the single genus Cebus, are two genera, with the robust (tufted) forms (including apella, libidinosus, xanthosternos, and several other species) now recognized as the genus Sapajus, and the gracile forms retained as the genus Cebus (Lynch Alfaro et al. 2012a, b). Because colonies of tufted capuchin monkeys held in the USA are derived from animals imported from the wild prior to the elevation of subspecies of Cebus apella to true species, and more recently, to a species in the genus Sapajus, distinct from Cebus, monkeys in these colonies are now recognized as unknown combinations of species and hybrids of the genus Sapajus, rather than as C. apella.

References

  1. Bentley-Condit VK, Smith EO (2010) Animal tool use: current definitions and an updated comprehensive catalog. Behaviour 147(2):185–221, A1–A32

    Google Scholar 

  2. Bernstein N (1967) The coordination and regulation of movement. Pergamon Press, New York

    Google Scholar 

  3. Bernstein N (1996) On dexterity and its development. In: Latash M, Turvey M, Bernstein N (eds) Dexterity and its development. Lawrence Erlbaum, Mahway, pp 3–237

    Google Scholar 

  4. Biro D, Sousa C, Matsuzawa T (2006) Ontogeny and cultural propagation of tool use by wild chimpanzees at Bossou, Guinea: case studies in nut-cracking and leaf-folding. In: Matsuzawa T, Tomonaga M, Tanaka M (eds) Cognitive development in chimpanzees. Springer, New York, pp 476–508

    Google Scholar 

  5. Bril B, Smaers J, Steele J, Rein R, Nonaka T, Dietrich G, Biryukova E, Hirata S, Roux V (2012) Functional mastery of percussive technology in nut-cracking and stone-flaking actions: experimental comparison and implications for the evolution of the human brain. Phil Trans R Soc B 367(1585):59–74

    PubMed  Article  Google Scholar 

  6. Call J (2010) Trapping the minds of apes: causal knowledge and inferential reasoning about object–object interactions. In: Lonsdorf E, Ross S, Matsuzawa T (eds) The mind of the chimpanzee. Chicago University Press, Chicago, pp 75–84

    Google Scholar 

  7. Cox RFA, Smitsman AW (2006) The planning of tool-to-object relations in young children. Dev Psychobiol 48:178–186

    PubMed  Article  Google Scholar 

  8. Falotico T (2011) Uso de ferramentas por macacos-prego (Sapajus libidinosus) do parque nacional Serra da capivara - PI [Doctoral Thesis]. Universidade de São Paulo, São Paulo, Brazil

  9. Fragaszy DM (1998) How non-human primates use their hands. In: Connolly K (ed) The psychobiology of the hand. Cambridge University Press, Cambridge, pp 77–96

    Google Scholar 

  10. Fragaszy D, Cummins-Sebree S (2005) Relational spatial reasoning by a nonhuman: the example of capuchin monkeys. Behav Cogn Neurosci Rev 4:282–306

    PubMed  Article  Google Scholar 

  11. Fragaszy D, Izar P, Visalberghi E, Ottoni EB, Gomes de Oliveira M (2004) Wild capuchin monkeys (Cebus libidinosus) use anvils and stone pounding tools. Am J Primatol 64:359–366

    PubMed  Article  Google Scholar 

  12. Fragaszy DM, Stone BW, Scott NM, Menzel C (2011) How tufted capuchin monkeys (Cebus apella spp.) and common chimpanzees (Pan troglodytes) align objects to surfaces: insights into spatial reasoning and implications for tool use. Am J Primatol 73:1012–1030

    PubMed Central  PubMed  Google Scholar 

  13. Fragaszy DM, Liu Q, Wright BW, Allen A, Brown C, Visalberghi E (2013) Bearded capuchin monkeys (Sapajus libidinosus) strategically place nuts in a stable position during nut-cracking. PLoS One 8(2):e56182. doi:10.1371/journal.pone.0056182

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  14. Gangopadhyay N, Madary M, Spicer F (eds) (2010) Perception, action and consciousness. Oxford University Press, Oxford

    Google Scholar 

  15. Jeannerod M (1997) The cognitive neuroscience of action. Blackwell, Cambridge

    Google Scholar 

  16. Jones LA, Lederman SJ (2006) Human hand function. Oxford University Press, New York

    Google Scholar 

  17. Lacreuse A, Fragaszy DM (1997) Manual exploratory procedures and asymmetries for a haptic search task: a comparison between capuchins (Cebus apella) and humans. Laterality 2:247–266

    CAS  PubMed  Google Scholar 

  18. Lederman SJ, Klatzky RL (1987) Hand movements: a window into haptic object recognition. Cogn Psychol 19:342–368

    CAS  PubMed  Article  Google Scholar 

  19. Lederman SJ, Klatzky RL (2004) Haptic identification of common objects: effects of constraining the manual exploration process. Percep Psychophys 66:618–628

    Article  Google Scholar 

  20. Lockman JJ (2000) A perception-action perspective on tool use development. Child Dev 71:137–144

    CAS  PubMed  Article  Google Scholar 

  21. Lynch Alfaro JW, Boubli JP, Olson LE, Di Fiore A, Wilson B, Gutiérrez-Espeleta GA, Chiou KL, Schulte M, Neitzel S, Ross V, Schwochow D, Nguyen MTT, Farias I, Janson CH, Alfaro ME (2012a) Explosive Pleistocene range expansion leads to widespread Amazonian sympatry between robust and gracile capuchin monkeys. J Biogeogr 39:272–288

    Article  Google Scholar 

  22. Lynch Alfaro JW, de Sousa e Silva J Jr, Rylands AB (2012b) How different are robust and gracile capuchin monkeys? An argument for the use of Sapajus and Cebus. Am J Primatol 74:273–286

    Article  Google Scholar 

  23. Marzke M (1997) Precision grips, hand morphology, and tools. Am J Phys Anthro 102:91–110

    CAS  Article  Google Scholar 

  24. McCarty ME, Clifton RK, Collard RR (2001) The beginnings of tool use by infants and toddlers. Infancy 2:233–256

    Article  Google Scholar 

  25. Michaels CF, Weier S, Harrison SJ (2007) Using vision and dynamic touch to perceive the affordances of tools. Perception 36:750–772

    PubMed  Article  Google Scholar 

  26. Milner AD, Goodale MA (1995) The visual brain in action. Oxford University Press, Oxford

    Google Scholar 

  27. Milner AD, Goodale MA (2008) Two visual systems re-viewed. Neuropsychologia 46:774–785

    CAS  PubMed  Article  Google Scholar 

  28. Örnkloo H, von Hofsten C (2007) Fitting objects into holes: on the development of spatial cognition skills. Dev Psychol 43:404–416

    PubMed  Article  Google Scholar 

  29. Pan J, Kennedy EH, Pickering T, Menzel CR, Stone BW, Fragaszy DM (2011) Development of maze navigation by tufted capuchins (Cebus apella). Behav Process 86:206–215

    Article  Google Scholar 

  30. Penn D, Povinelli D (2007) Causal cognition in human and nonhuman animals: a comparative, critical review. Annu Rev Psychol 58:97–118

    PubMed  Article  Google Scholar 

  31. Roux V, Bril B (2005) Stone knapping: the necessary conditions for a uniquely hominin behaviour. McDonald Institute Monographs, Cambridge

    Google Scholar 

  32. Sanz CM, Morgan DB (2009) Flexible and persistent tool-using strategies in honey-gathering by wild chimpanzees. Int J Primatol 30:411–427

    Article  Google Scholar 

  33. Sanz C, Boesch C, Call J (eds) (2012) Tool-use: cognitive requirements and ecological determinants. Cambridge University Press, Cambridge

    Google Scholar 

  34. Shumaker RW, Walkup KR, Beck BB (2011) Animal tool behavior: the use and manufacture of tools by animals. Johns Hopkins University Press, Baltimore

    Google Scholar 

  35. Souto A, Bione CBC, Bastos M, Bezerra BM, Fragaszy D, Schiel N (2011) Critically endangered blonde capuchins fish for termites and use new techniques to accomplish the task. Biol Lett. doi:10.1098/rsbl.2011.0034

    Google Scholar 

  36. Street SY, James KH, Jones SS, Smith LB (2011) Vision for action in toddlers: the posting task. Child Dev 82:2083–2094

    PubMed Central  PubMed  Article  Google Scholar 

  37. Teleki G (1974) Chimpanzee subsistence technology: materials and skills. J Hum Evol 3:575–584

    Article  Google Scholar 

  38. Turvey MT (1996) Dynamic touch. Am Psychol 51:1134–1152

    CAS  PubMed  Article  Google Scholar 

  39. Vásques P, Cano M, Acuña C (2000) Discrimination of line orientation in humans and monkeys. J Neurophysiol 83:2639–2648

    Google Scholar 

  40. Wakita M (2008) Orientation perception in rhesus monkeys (Macaca mulatta). Anim Cogn 11:535–545

    PubMed  Article  Google Scholar 

  41. Wakita M (2012) Monkeys perceive the orientation of objects relative to the vertical axis. Anim Cogn 15:1205–1209

    PubMed  Article  Google Scholar 

Download references

Acknowledgments

Supported by NIH Grants HD060563 and HD056352 to Georgia State University. The contents of this article do not necessarily represent the official views of NIH. We thank John Kelly, Jennifer Schaeffer and Jamie Russell for assistance with testing.

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Correspondence to Dorothy M. Fragaszy.

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la Cour, L.T., Stone, B.W., Hopkins, W. et al. What limits tool use in nonhuman primates? Insights from tufted capuchin monkeys (Sapajus spp.) and chimpanzees (Pan troglodytes) aligning three-dimensional objects to a surface. Anim Cogn 17, 113–125 (2014). https://doi.org/10.1007/s10071-013-0643-x

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Keywords

  • Tool use
  • Spatial reasoning
  • Sapajus
  • Pan troglodytes
  • Alignment
  • Posting task