Animal Cognition

, Volume 17, Issue 4, pp 891–899 | Cite as

Semi-wild chimpanzees open hard-shelled fruits differently across communities

  • Bruce Rawlings
  • Marina Davila-Ross
  • Sarah T. Boysen
Original Paper

Abstract

Researchers investigating the evolutionary roots of human culture have turned to comparing behaviours across nonhuman primate communities, with tool-based foraging in particular receiving much attention. This study examined whether natural extractive foraging behaviours other than tool selection differed across nonhuman primate colonies that had the same foods available. Specifically, the behaviours applied to open the hard-shelled fruits of Strychnos spp. were examined in three socially separate, semi-wild colonies of chimpanzees (Pan troglodytes) that lived under shared ecological conditions at Chimfunshi Wildlife Orphanage, and were comparable in their genetic makeup. The chimpanzees (N = 56) consistently applied six techniques to open these fruits. GLMM results revealed differences in the number of combined technique types to open fruits across the colonies. They also showed colony differences in the application of three specific techniques. Two techniques (full biting and fruit cracking) were entirely absent in some colonies. This study provides empirical evidence that natural hard-shelled fruit-opening behaviours are distinct across chimpanzee colonies, differences that most likely have not resulted from ecological and genetic reasons.

Keywords

Chimpanzee Extractive foraging Hard-shelled fruits Culture Social learning 

Supplementary material

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References

  1. Agostini L, Visalberghi E (2005) Social influences on the acquisition of sex-typical foraging patterns by juveniles in a group of wild tufted capuchin monkeys (Cebus nigritus). Am J Primatol 65:335–351. doi:10.1002/ajp.20120 PubMedCrossRefGoogle Scholar
  2. Bates D, Maechler M, Bolker B (2010) lme4: linear mixed effects models using S4 classes (R package version 0.999375-35). http://CRAN.R-project.org/package=lme4
  3. Biro D, Inoue-Nakamura N, Tonooka R, Yamakoshi G, Sous C, Matsuzawa T (2003) Cultural innovation and transmission of tool use in wild chimpanzees: evidence from field experiments. Anim Cogn 6:213–223. doi:10.1007/s10071-003-0183-x PubMedCrossRefGoogle Scholar
  4. Boesch C, Boesch H (1983) Optimisation of nut-cracking with natural hammers by wild chimpanzees. Behaviour 83:256–286. doi:10.1163/156853983X00192 CrossRefGoogle Scholar
  5. Boesch C, Boesch H (1984) Possible causes of sex differences in the use of natural hammers by wild chimpanzees. J Hum Evol 13:415–440. doi:10.1016/S0047-2484(84)80055-X CrossRefGoogle Scholar
  6. Boesch C, Boesch H (1990) Tool use and tool making in wild chimpanzees. Folia Primatol 54:1–15. doi:10.1371/journal.pone.0055768 CrossRefGoogle Scholar
  7. Bonnie KE, Horner V, Whiten A, de Waal FBM (2006) Spread of arbitrary customs among chimpanzees: a controlled experiment. Proc Roy Soc B 274:367–372. doi:10.1098/rspb2006.3733 CrossRefGoogle Scholar
  8. Byrne RW, Byrne JM (1991) Hand preferences in the skilled gathering tasks of mountain gorillas (Gorilla g. berengei). Cortex. 27:521–546. doi:10.1037/0012-1649.31.4.619 PubMedCrossRefGoogle Scholar
  9. Corp N, Byrne R (2002) The ontogeny of manual skill in wild chimpanzees: evidence from feeding on the fruit of saba florida. Behaviour 139:137–168CrossRefGoogle Scholar
  10. Crast J, Hardy JM, Fragaszy D (2010) Inducing traditions in captive capuchin monkeys (Cebus apella). Anim Behav 80:955–964. doi:10.1016/j.anbehav.2010.08.023 CrossRefGoogle Scholar
  11. Davila-Ross M, Allcock B, Thomas C, Bard KA (2011) Aping expressions? Chimpanzees produce distinct laugh types when responding to laughter of others. Emotion 11:1113–1120. doi:10.1037/a0022594 CrossRefGoogle Scholar
  12. Dindo M, Thierry B, Whiten A (2008) Social diffusion of novel foraging methods in brown capuchin monkeys (Cebus apella). Proc Roy Soc B 275:187–193. doi:10.1098/rspb2007.1318 CrossRefGoogle Scholar
  13. Fessler DM (2002) Dimorphic foraging behaviours and the evolution of hominid hunting. Riv Biol 95:429–453PubMedGoogle Scholar
  14. Galef BG Jr (2004) Approaches to the study of traditional behaviours of free-living animals. Learn Behav 32:53–61. doi:10.3758/BF03196006 CrossRefGoogle Scholar
  15. Goodall J (1986) The chimpanzees of Gombe: patterns of behaviour. Harvard University Press, CambridgeGoogle Scholar
  16. Gruber T, Muller M, Strimling P, Wrangham R, Zuberbuhler K (2009) Wild chimpanzees rely on cultural knowledge to solve an experimental honey acquisition task. Curr Biol 19:1806–1810. doi:10.1016/j.cub.2009.08.060 PubMedCrossRefGoogle Scholar
  17. Gruber T, Clay Z, Zuberbuhler K (2010) A comparison of bonobo and chimpanzee tool use; evidence for a female bias in the Pan linage. Anim Behav 80:1023–1033. doi:10.1016/j.anbehav.2010.09.005 CrossRefGoogle Scholar
  18. Hopper LM, Schapiro SJ, Lambeth SP, Brosnan SF (2011) Chimpanzees’ socially maintained food preferences indicate both conservatism and conformity. Anim Behav 81:1195–1202. doi:10.1016/j.anbehav.2011.03.002 CrossRefGoogle Scholar
  19. Horner V, Whiten A, Flynn E, de Waal FBM (2006) Faithful replication of foraging techniques along cultural transmission chains by chimpanzees and children. PNAS 103:13878–13883. doi:10.1073/pnas.0606015103 PubMedCentralPubMedCrossRefGoogle Scholar
  20. Inoue-Nakamura N, Matsuzawa T (1997) Development of stone tool use by wild chimpanzees (Pan troglodytes). J Comp Psychol 111:159–173. doi:10.1037/0735-7036.111.2.159 PubMedCrossRefGoogle Scholar
  21. Kendal RL, Custance DM, Kendal JR, Vale G, Stoinksi TS, Rakotomalala NL, Rasamimanana H (2010) Evidence for social learning in wild lemurs (Lemur catta). Learn Behav 38:220–234. doi:10.3758/LB.38.3.220 PubMedCrossRefGoogle Scholar
  22. Koops K, McGrew WC, Matsuzawa T (2010) Do chimpanzees (Pan troglodytes) use cleavers and anvils to fracture Treculia africana fruits? Preliminary data on a new form of percussive technology. Primates 51:175–178. doi:10.1007/s10329-009-0178-6 PubMedCrossRefGoogle Scholar
  23. Laland K, Janik VM (2007) The animal cultures debate. Trends Ecol Evol 21:542–547CrossRefGoogle Scholar
  24. Lonsdorf EV (2005) Sex differences in the development of termite-fishing in the wild chimpanzees Pan troglodytes schweinfurthii of Gombe National Park. Tanzania Anim Behav 70:673–683. doi:10.1016/j.tree.2006.06.005 CrossRefGoogle Scholar
  25. Lonsdorf EV, Eberly LE, Pusey AE (2004) Sex differences in learning in chimpanzees. Nature 428:715–716. doi:10.1038/428715a PubMedCrossRefGoogle Scholar
  26. Lucas PW, Gaskins JT, Lowry TK, Harrison ME, Morrogh-Bernard HC, Cheyne SM, Begley MR (2011) Evolutionary optimization of material properties of a tropical seed. J Roy Soc Interf 9:34–42. doi:10.1098/rsif 2011.0188CrossRefGoogle Scholar
  27. Luncz LV, Mundry R, Boesch C (2012) Evidence for cultural differences between neighboring chimpanzee communities. Curr Biol 22:922–926. doi:10.1016/j.cub.2012.03.031 PubMedCrossRefGoogle Scholar
  28. Mackinnon KC (2006) Food choice by juvenile capuchin monkeys Cebus capucinus in a tropical dry forest. Springer, New York. doi: 10.1007/0-387-25872-8_17
  29. Matsumoto-Oda A, Kasagula MB (2000) Preliminary study of feeding competition between baboons and chimpanzees in the Mahale Mountains National Park. Tanzania Af Stud Monogr 21:147–157Google Scholar
  30. McGrew WC (1979) Evolutionary implications of sex differences in chimpanzee predation and tool use. In: Hamburg DA, McCown E (eds). The Great Apes, Benjamin/Cummings Publishing, California, pp 441–463Google Scholar
  31. McGrew WC (1999) Manual laterality in anvil use: wild chimpanzees cracking Strychnos fruits. Laterality 4:79–87. doi:10.1080/03069887600760101 PubMedGoogle Scholar
  32. Nishida T, Turner L (1996) Food transfer between mother and infant chimpanzees of the Mahale Mountains National Park. Tanzania Int J Primatol 17:947–968. doi:10.1007/BF02735296 CrossRefGoogle Scholar
  33. Pruetz J, Bertolani P (2007) Savanna chimpanzees (Pan troglodytes verus) hunt with tools. Curr Biol 17:412–417. doi:10.1016/j.cub.2006.12.042 PubMedCrossRefGoogle Scholar
  34. R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  35. Reader SM, Biro D (2010) Experimental identification of social learning in wild animals. Learn Behav 33:265–283. doi:10.3758/LB.38.3.265 CrossRefGoogle Scholar
  36. Rosenberger AL, Hartwig WC (2011) New world monkeys. Encyclopedia of life sciences, Nature Publishing Group. Macmillan Reference Ltd. http://www.els.net
  37. Russon AE (1998) The nature and evolution of intelligence in orangutans (Pongo pygmaeus). Primates 39:485–503. doi:10.1007/BF02557571 CrossRefGoogle Scholar
  38. Schoning C, Humle T, Mobius Y, McGrew WC (2008) The nature of culture: technological variation in chimpanzee predation on army ants revisited. J Hum Evol 55:48–59. doi:10.1016/j.jhevol.2007.12.002 PubMedCrossRefGoogle Scholar
  39. Sterling E, Dierenfeld E, Ashborne C, Feistner A (1994) Dietary intake, food consumption and nutrient intake in wild and captive populations of Daubentonia madagascariensis. Folia Primatol 62:115–124PubMedCrossRefGoogle Scholar
  40. Stokes EJ, Byrne RW (2001) Cognitive capacities for behavioural flexibility in wild chimpanzees (Pan troglodytes): the effect of snare injury on complex manual food processing. Anim Cogn 4:11–28. doi:10.1007/s100710100082 CrossRefGoogle Scholar
  41. Tennie C, Call J, Tomasello M (2009) Ratcheting up the ratchet: on the evolution of cumulative culture. Philos Trans Roy Soc B 364:2405–2415. doi:10.1098/rstb2009.0052 CrossRefGoogle Scholar
  42. Tutin CEG, Baillie JEM, Dupain J., Gatti S, Maisels F, Stokes EJ, Morgan DB, Walsh PD (2008) Pan troglodytes ssp. troglodytes. In: IUCN 2013. IUCN Red List of Threatened SpeciesGoogle Scholar
  43. van de Waal E, Renevey N, Favre CM, Bshary R (2010) Selective attention to philopatric models causes directed social learning in wild vervet monkeys. Proc Roy Soc B. 277:2105–2111. doi:10.1098/rspb2009.2260 CrossRefGoogle Scholar
  44. van de Waal E, Claidièrea N, Whiten A (2013) Social learning and spread of alternative means of opening an artificial fruit in four groups of vervet monkeys. Anim Behav 85:71–76. doi:10.1016/j.anbehav.2012.10.008 CrossRefGoogle Scholar
  45. van Lawick-Goodall J, Van-Lawick H, Packer C (1973) Tool-use in free-living Baboons in the Gombe National Park. Tanzania Nat 241:212–213. doi:10.1038/241212a0 Google Scholar
  46. van Schaik CP, Knott CD (2001) Geographic variation in tool use on Neesia fruits in orangutans. Am J Phys Anthropol 11:331–342. doi:10.1002/ajpa.1045 Google Scholar
  47. van Schaik CP, Ancrenaz M, Borgen G, Galdikas B, Knott CD, Singleton L, Suzuki A, Utami SS, Merill M (2003) Orangutan cultures and the evolution of material culture. Science 299:102–105. doi:10.1126/science.1078004 PubMedCrossRefGoogle Scholar
  48. Whiten A, Goodall J, McGrew WC, Nishida T, Reynoldsk V, Sugiyama Y (1999) Culture in chimpanzees. Nature 399:15–19. doi:10.1038/21415 CrossRefGoogle Scholar
  49. Whiten A, Goodall J, McGrew W, Nishida T, Reynolds V, Sugiyama Y, Tutin C, Wrangham R, Boesch C (2001) Charting cultural variation in chimpanzees. Behaviour. 138:1481–1516. doi:10.1163/156853901317367717 Google Scholar
  50. Whiten A, Spiteri A, Horner V, Bonnie KE, Lambeth SP, Schapiro SJ, de Waal FBM (2007) Transmission of multiple traditions within and between groups. Curr Biol 17:1–6. doi:10.1016/j.cub.2007.05.031 CrossRefGoogle Scholar
  51. Wilson ML, Balmforth Z, Cox D, Davenport T, Hart J, Hicks C, Hunt KD, Kamenya S, Mitani JC, Moore J, Nakamura M, Nixon S, Plumptre AJ, Reynolds V (2008). Pan troglodytes ssp. schweinfurthii. In: IUCN 2013. IUCN red list of threatened speciesGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Bruce Rawlings
    • 1
  • Marina Davila-Ross
    • 1
  • Sarah T. Boysen
    • 2
  1. 1.Psychology Department, Centre for Comparative and Evolutionary PsychologyUniversity of PortsmouthPortsmouthUK
  2. 2.Department of PsychologyThe Ohio State UniversityColumbusUSA

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