Manipulative repertoire of bonobos (Pan paniscus) in spontaneous feeding situation.


Journal

American journal of primatology
ISSN: 1098-2345
Titre abrégé: Am J Primatol
Pays: United States
ID NLM: 8108949

Informations de publication

Date de publication:
07 2022
Historique:
revised: 01 03 2022
received: 13 09 2021
accepted: 19 03 2022
pubmed: 14 4 2022
medline: 26 7 2022
entrez: 13 4 2022
Statut: ppublish

Résumé

Comparative behavioral studies of hand use amongst primate species, including humans, have been central in research on evolutionary mechanisms. In particular, the manipulative abilities of our closest relatives, the chimpanzee (Pan troglodytes), have been widely described in various contexts, showing a high level of dexterity both in zoo and in natural conditions. In contrast, the study of bonobos' manipulative abilities has almost exclusively been carried out in experimental contexts related to tool use. The objective of the present study is to describe the richness of the manipulative repertoire of zoo-housed bonobos, in a spontaneous feeding context including various physical substrates to gain a larger insight into our evolutionary past. Our study describes a great variety of grasping postures and grip associations in bonobos, close to the range of manipulative repertoire in chimpanzees, confirming that the two species are not markedly different in terms of cognitive and morphological constraints associated with food manipulation. We also observed differences in manipulative behaviors between juveniles and adults, indicating a greater diversity in grip associations and grasping postures used in isolation with age, and a sex-biased use of tools with females using tools more often than males. These results are consistent with the previous results in the Pan genus and reinforce the hypothesis that the evolutionary mechanisms underlying the flexibility of manipulative behaviors are shared by both species and that these ecological strategies would have already evolved in their common ancestor.

Identifiants

pubmed: 35417066
doi: 10.1002/ajp.23383
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e23383

Informations de copyright

© 2022 Wiley Periodicals LLC.

Références

Almécija, S., Moyà-Solà, S., & Alba, D. M. (2010). Early origin for human-like precision grasping: A comparative study of pollical distal phalanges in fossil hominins. PLoS One, 5(7), e11727. https://doi.org/10.1371/journal.pone.0011727
Almécija, S., Smaers, J. B., & Jungers, W. L. (2015). The evolution of human and ape hand proportions. Nature Communications, 6(1), 7717. https://doi.org/10.1038/ncomms8717
Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49(3/4), 227-267. https://doi.org/10.1163/156853974X00534
Bardo, A., Borel, A., Meunier, H., Guéry, J.-P., & Pouydebat, E. (2016). Behavioral and functional strategies during tool use tasks in bonobos. American Journal of Physical Anthropology, 161(1), 125-140. https://doi.org/10.1002/ajpa.23015
Bardo, A., Cornette, R., Borel, A., & Pouydebat, E. (2017). Manual function and performance in humans, gorillas, and orangutans during the same tool use task. American Journal of Physical Anthropology, 164(4), 821-836. https://doi.org/10.1002/ajpa.23323
Bardo, A., Pouydebat, E., & Meunier, H. (2015). Do bimanual coordination, tool use, and body posture contribute equally to hand preferences in bonobos? Journal of Human Evolution, 82, 159-169. https://doi.org/10.1016/j.jhevol.2015.02.015
Bardo, A., Vigouroux, L., Kivell, T. L., & Pouydebat, E. (2018). The impact of hand proportions on tool grip abilities in humans, great apes and fossil hominins: A biomechanical analysis using musculoskeletal simulation. Journal of Human Evolution, 125, 106-121. https://doi.org/10.1016/j.jhevol.2018.10.001
Beck, B. B. (1980). Animal tool behavior. Garland STPM Pub.
Bentley-Condit, V., & Smith, E. O. (2010). Animal tool use: Current definitions and an updated comprehensive catalog. Behaviour, 147(2), 185-32A. https://doi.org/10.1163/000579509X12512865686555
Biro, D., Inoue-Nakamura, N., Tonooka, R., Yamakoshi, G., Sousa, C., & Matsuzawa, T. (2003). Cultural innovation and transmission of tool use in wild chimpanzees: Evidence from field experiments. Animal Cognition, 6(4), 213-223. https://doi.org/10.1007/s10071-003-0183-x
Boesch, C., & Boesch, H. (1983). Optimisation of nut-cracking with natural hammers by wild chimpanzees. Behaviour, 83(3-4), 265-286. https://doi.org/10.1163/156853983X00192
Boesch, C., & Boesch, H. (1990). Tool use and tool making in wild chimpanzees. Folia Primatologica, 54(1-2), 86-99. https://doi.org/10.1159/000156428
Boose, K. J., White, F. J., & Meinelt, A. (2013). Sex differences in tool use acquisition in bonobos (Pan paniscus): Bonobo sex differences in tool use. American Journal of Primatology, 75(9), 917-926. https://doi.org/10.1002/ajp.22155
Breuer, T., Ndoundou-Hockemba, M., & Fishlock, V. (2005). First observation of tool use in wild gorillas. PLoS Biology, 3(11), e380. https://doi.org/10.1371/journal.pbio.0030380
Butterworth, G., & Itakura, S. (1998). Development of precision grips in chimpanzees. Developmental Science, 1(1), 39-43. https://doi.org/10.1111/1467-7687.00010
Byrne, G., & Suomi, S. J. (1996). Individual differences in object manipulation in a colony of tufted capuchins. Journal of Human Evolution, 31(3), 259-267. https://doi.org/10.1006/jhev.1996.0060
Byrne, R. W., Corp, N., & Byrne, J. M. (2001). Manual dexterity in the gorilla: Bimanual and digit role differentiation in a natural task. Animal Cognition, 4(3-4), 347-361. https://doi.org/10.1007/s100710100083
Christel, M. (1993). Grasping techniques and hand preferences in Hominoidea. In (Eds.) Preuschoft, H. & Chivers, D. J., Hands of Primates (pp. 91-108). Springer. https://doi.org/10.1007/978-3-7091-6914-8_7
Christel, M., Kitzel, S., & Niemitz, C. (1998). How precisely do bonobos (Pan paniscus) grasp small objects? ​30. https://doi.org/10.1023/A:1020319313219
Colwell, R. K., Mao, C. X., & Chang, J. (2004). Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology, 85(10), 2717-2727. https://doi.org/10.1890/03-0557
Corp, N., & Byrne, R. W. (2002). The ontogeny of manual skill in wild chimpanzees: Evidence from feeding on the fruit of Saba florida. Behaviour, 139, 137-168.
Crast, J., Fragaszy, D., Hayashi, M., & Matsuzawa, T. (2009). Dynamic in-hand movements in adult and young juvenile chimpanzees (Pan troglodytes). American Journal of Physical Anthropology, 138(3), 274-285. https://doi.org/10.1002/ajpa.20925
Diogo, R., Molnar, J. L., & Wood, B. (2017). Bonobo anatomy reveals stasis and mosaicism in chimpanzee evolution, and supports bonobos as the most appropriate extant mode l for the common ancestor of chimpanzees and humans. Scientific Reports, 7(1), 608. https://doi.org/10.1038/s41598-017-00548-3
Druelle, F., Schoonaert, K., Aerts, P., Nauwelaerts, S., Stevens, J. M. G., & D'Août, K. (2018). Segmental morphometrics of bonobos (Pan paniscus): Are they really different from chimpanzees (Pan troglodytes)? Journal of Anatomy, 233(6), 843-853. https://doi.org/10.1111/joa.12894
Feix, T., Kivell, T. L., Pouydebat, E., & Dollar, A. M. (2015). Estimating thumb-index finger precision grip and manipulation potential in extant and fossil primates. Journal of the Royal Society Interface, 12(106), 20150176. https://doi.org/10.1098/rsif.2015.0176
Fox, E. A., Sitompul, A. F., & van Schaik, C. P. (1999). Intelligent tool use in wild Sumatran orangutans. In (Eds.) Parker, S. T., Mitchell, R. W. & Miles, H. L., The mentalities of Gorillas and Orangutans (1st ed., pp. 99-116). Cambridge University Press. https://doi.org/10.1017/CBO9780511542305.005
Fragaszy, D. M., & Crast, J. (2016). Functions of the hand in primates, The evolution of the primate hand (pp. 313-344). Springer.
Furuichi, T., Sanz, C., Koops, K., Sakamaki, T., Ryu, H., Tokuyama, N., & Morgan, D. (2015). Why do wild bonobos not use tools like chimpanzees do? Behaviour, 152(3-4), 425-460. https://doi.org/10.1163/1568539X-00003226
Garber, P. A., Bicca-Marques, J. C., & Azevedo-Lopes, M. A. deO. (2009). Primate cognition: Integrating social and ecological information in decision-making. In (Eds.) Garber, P. A., Estrada, A., Bicca-Marques, J. C., Heymann, E. W. & Strier, K. B., South American Primates (pp. 365-385). Springer. https://doi.org/10.1007/978-0-387-78705-3_14
Goodall, J. (1964). Tool-using and aimed throwing in a community of free-living chimpanzees. Nature, 201(4926), 1264-1266. https://doi.org/10.1038/2011264a0
Greenfield, P. M. (1991). Language, tools and brain: The ontogeny and phylogeny of hierarchically organized sequential behavior. Behavioral and Brain Sciences, 14(4), 531-551. https://doi.org/10.1017/S0140525X00071235
Gruber, T., Clay, Z., & Zuberbühler, K. (2010). A comparison of bonobo and chimpanzee tool use: Evidence for a female bias in the Pan lineage. Animal Behaviour, 80(6), 1023-1033. https://doi.org/10.1016/j.anbehav.2010.09.005
Grueter, C. C., Robbins, M. M., Ndagijimana, F., & Stoinski, T. S. (2013). Possible tool use in a mountain gorilla. Behavioural Processes, 100, 160-162. https://doi.org/10.1016/j.beproc.2013.09.006
Harrison, T., & Rein, T. R. (2016). The hands of fossil non-hominoid anthropoids. The Evolution of the Primate Hand, ​455-483.
Hayashi, M., Takeshita, H., & Matsuzawa, T. (2006). Cognitive development in apes and humans assessed by object manipulation, Cognitive development in chimpanzees (pp. 395-410). Springer.
Hohmann, G., & Fruth, B. (2003). Culture in bonobos? Between-species and within-species variation in behavior. Current Anthropology, 44(4), 563-571. https://doi.org/10.1086/377649
Hopkins, W. D. (1995). Hand preferences for a coordinated bimanual task in 110 chimpanzees (Pan troglodytes): Cross-sectional analysis. Journal of Comparative Psychology, 109(3), 291-297. https://doi.org/10.1037/0735-7036.109.3.291
Ingmanson, E. J. (1996). Tool-using behavior in wild Pan paniscus: Social and ecological considerations. In A. E. Russon, K. A. Bard, & S. T. Parker (Eds.), Reaching into thought: The minds of the great apes (pp. 190-210). Cambridge University Press.
Inoue-Nakamura, N., & Matsuzawa, T. (1997). Development of stone tool use by wild chimpanzees (Pan troglodytes). Journal of Comparative Psychology, 111(2), 159-173. https://doi.org/10.1037/0735-7036.111.2.159
Jones, C. E., & Fragaszy, D. M. (2020). Compound grips in tufted capuchin monkeys (Sapajus spp and Sapajus libidinosus). American Journal of Primatology, 82(6), 23133. https://doi.org/10.1002/ajp.23133
Jones, L. A., & Lederman, S. J. (2006). Human hand function. Oxford University Press.
Jones-Engel, L. E., & Bard, K. A. (1996). Precision grips in young Chimpanzees. American Journal of Primatology, 391, 15-15.
Kano, T. (1982). The use of leafy twigs for rain cover by the pygmy chimpanzees of Wamba. Primates, 23(3), 453-457. https://doi.org/10.1007/BF02381327
Key, A., Merritt, S. R., & Kivell, T. L. (2018). Hand grip diversity and frequency during the use of Lower Palaeolithic stone cutting-tools. Journal of Human Evolution, 125, 137-158. https://doi.org/10.1016/j.jhevol.2018.08.006
Kinani, J. -F., & Zimmerman, D. (2015). Tool use for food acquisition in a wild mountain gorilla (Gorilla beringei beringei): Tool use in a Mountain Gorilla. American Journal of Primatology, 77(3), 353-357. https://doi.org/10.1002/ajp.22351
Kivell, T. L. (2015). Evidence in hand: Recent discoveries and the early evolution of human manual manipulation. Philosophical Transactions of the Royal Society, B: Biological Sciences, 370(1682), 20150105. https://doi.org/10.1098/rstb.2015.0105
Kivell, T. L., Kibii, J. M., Churchill, S. E., Schmid, P., & Berger, L. R. (2011). Australopithecus sediba hand demonstrates mosaic evolution of locomotor and manipulative abilities. Science, 333(6048), 1411-1417. https://doi.org/10.1126/science.1202625
van Leeuwen, T., Vanhoof, M. J. M., Kerkhof, F. D., Stevens, J. M. G., & Vereecke, E. E. (2018). Insights into the musculature of the bonobo hand. Journal of Anatomy, 233(3), 328-340. https://doi.org/10.1111/joa.12841
Lonsdorf, E. V. (2005). Sex differences in the development of termite-fishing skills in the wild chimpanzees, Pan troglodytes schweinfurthii, of Gombe National Park, Tanzania. Animal Behaviour, 70(3), 673-683.
Macfarlane, N. B. W., & Graziano, M. S. A. (2009). Diversity of grip in Macaca mulatta. Experimental Brain Research, 8, 14. https://doi.org/10.1007/s00221-009-1909-z
Makofske, B. (2011). Manual Dexterity. In (Eds.) Kreutzer, J. S., DeLuca, J. & Caplan, B., Encyclopedia of Clinical Neuropsychology (pp. 1522-1523). Springer. https://doi.org/10.1007/978-0-387-79948-3_1460
Marzke, M. W. (1997). Precision grips, hand morphology, and tools. American Journal of Physical Anthropology, 102(1), 91-110. https://doi.org/10.1002/(SICI)1096-8644(199701)102:1%3C91::AID-AJPA8%3E3.0.CO;2-G
Marzke, M. W. (2013). Tool making, hand morphology and fossil hominins. Philosophical Transactions of the Royal Society, B: Biological Sciences, 368(1630), 20120414. https://doi.org/10.1098/rstb.2012.0414
Marzke, M. W., Marchant, L. F., McGrew, W. C., & Reece, S. P. (2015). Grips and hand movements of chimpanzees during feeding in Mahale Mountains National Park, Tanzania: Chimpanzee Feeding Grips and Hand use in Mahale. American Journal of Physical Anthropology, 156(3), 317-326. https://doi.org/10.1002/ajpa.22651
Marzke, M. W., & Wullstein, K. L. (1996). Chimpanzee and human grips: A new classification with a focus on evolutionary morphology. International Journal of Primatology, 17(1), 117-139. https://doi.org/10.1007/BF02696162
Marzke, M. W., Wullstein, K. L., & Viegas, S. F. (1992). Evolution of the power (“squeeze”) grip and its morphological correlates in hominids. American Journal of Physical Anthropology, 89(3), 283-298. https://doi.org/10.1002/ajpa.1330890303
Matsuzawa, T. (2011). Education by master-apprenticeship, The Chimpanzees of Bossou and Nimba (pp. 201-208). Springer.
McGrew, W. (1979). Evolutionary implications of sex differences in chimpanzee predation and tool use. The Great Apes
McGrew, W. C. (2010). Chimpanzee Technology. Science, 328(5978), 579-580. https://doi.org/10.1126/science.1187921
Meulman, E. J. M., & van Schaik, C. P. (2013). Orangutan tool use and the evolution of technology. In (Eds.) Sanz, C., Call, J. & Boesch, C., Tool Use in Animals (pp. 176-202). Cambridge University Press. https://doi.org/10.1017/CBO9780511894800.012
Moore, R. (2013). Social learning and teaching in chimpanzees. Biology & Philosophy, 28(6), 879-901.
Napier, J. R. (1956). The prehensile movements of the human hand. The Journal of Bone and Joint Surgery. British, 38(4), 902-913. https://doi.org/10.1302/0301-620X.38B4.902
Napier, J. R. (1960). Studies of the hands of living primates. Proceedings of the Zoological Society of London, 134(4), 647-657. https://doi.org/10.1111/j.1469-7998.1960.tb05606.x
Neufuss, J., Humle, T., Cremaschi, A., & Kivell, T. L. (2017). Nut-cracking behaviour in wild-born, rehabilitated bonobos (Pan paniscus): A comprehensive study of hand-preference, hand grips and efficiency. American Journal of Primatology, 79(2):e22589-16. https://doi.org/10.1002/ajp.22589
Neufuss, J., Robbins, M. M., Baeumer, J., Humle, T., & Kivell, T. L. (2018). Manual skills for food processing by mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda. Biological Journal of the Linnean Society, 127(3), 543-562. https://doi.org/10.1093/biolinnean/bly071
Nishida, T., Kano, T., Goodall, J., McGrew, W. C., & Nakamura, M. (1999). Ethogram and ethnography of Mahale chimpanzees. Anthropological Science, 107(2), 141-188. https://doi.org/10.1537/ase.107.141
Osuna-Mascaró, A. J., Ortiz, C., Stolz, C., Musgrave, S., Sanz, C. M., Morgan, D. B., & Fragaszy, D. M. (2020). Dexterity and technique in termite fishing by chimpanzees (Pan troglodytes troglodytes) in the Goualougo Triangle, Republic of Congo. American Journal of Primatology, 83(1), e23215. https://doi.org/10.1002/ajp.23215
Pal, A., Kumara, H. N., Mishra, P. S., Velankar, A. D., & Singh, M. (2018). Extractive foraging and tool-aided behaviors in the wild Nicobar long-tailed macaque (Macaca fascicularis umbrosus). Primates, 59(2), 173-183. https://doi.org/10.1007/s10329-017-0635-6
Parker, S. T., & Gibson, K. R. (1979). A developmental model for the evolution of language and intelligence in early hominids. Behavioral and Brain Sciences, 2(3), 367-381. https://doi.org/10.1017/S0140525X0006307X
Parry, C. W. (1966). Rehabilitation of the hand. Butterworth.
Pouydebat, E., Gorce, P., Coppens, Y., & Bels, V. (2009). Biomechanical study of grasping according to the volume of the object: Human versus non-human primates. Journal of Biomechanics, 42(3), 266-272. https://doi.org/10.1016/j.jbiomech.2008.10.026
Pouydebat, E., Laurin, M., Gorce, P., & Bels, V. (2008). Evolution of grasping among anthropoids. Journal of Evolutionary Biology, 21(6), 1732-1743. https://doi.org/10.1111/j.1420-9101.2008.01582.x
Pouydebat, E., Reghem, E., Borel, A., & Gorce, P. (2011). Diversity of grip in adults and young humans and chimpanzees (Pan troglodytes). Behavioural Brain Research, 218(1), 21-28. https://doi.org/10.1016/j.bbr.2010.11.021
Pruetz, J. D., & Bertolani, P. (2007). Savanna chimpanzees, Pan troglodytes verus, hunt with tools. Current Biology, 17(5), 412-417. https://doi.org/10.1016/j.cub.2006.12.042
Richmond, B. G., Roach, N. T., & Ostrofsky, K. R. (2016). Evolution of the early hominin hand, The evolution of the primate hand (pp. 515-543). Springer.
Samuni, L., Lemieux, D., Lamb, A., Galdino, D., & Surbeck, M. (2021). Tool use behavior in three wild bonobo communities at Kokolopori. American Journal of Primatology, 84, e23342.
Sanz, C. M., & Morgan, D. B. (2013). Ecological and social correlates of chimpanzee tool use. Philosophical Transactions of the Royal Society, B: Biological Sciences, 368(1630), 20120416. https://doi.org/10.1098/rstb.2012.0416
van Schaik, C. P., Fox, E. A., & Sitompul, A. F. (1996). Manufacture and use of tools in wild sumatran orangutans: Implications for human evolution. Naturwissenschaften, 83(4), 186-188. https://doi.org/10.1007/s001140050271
Susman, R. L. (1998). Hand function and tool behavior in early hominids. Journal of Human Evolution, 35(1), 23-46. https://doi.org/10.1006/jhev.1998.0220
Takeshita, H., & Walraven, V. (1996). A comparative study of the variety and complexity of object manipulation in captive chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). Primates, 37(4), 423-441. https://doi.org/10.1007/BF02381377
Tocheri, M. W., Orr, C. M., Jacofsky, M. C., & Marzke, M. W. (2008). The evolutionary history of the hominin hand since the last common ancestor of Pan and Homo. Journal of Anatomy, 212(4), 544-562. https://doi.org/10.1111/j.1469-7580.2008.00865.x
Tonooka, R., & Matsuzawa, T. (1995). Hand preferences of captive chimpanzees (Pan troglodytes) in simple reaching for food. International Journal of Primatology, 16(1), 17-35. https://doi.org/10.1007/BF02700151
Toth, N., Schick, K. D., Savage-Rumbaugh, E. S., Sevcik, R. A., & Rumbaugh, D. M. (1993). Pan the tool-maker: Investigations into the stone tool-making and tool-using capabilities of a bonobo (Pan paniscus). Journal of Archaeological Science, 20(1), 81-91. https://doi.org/10.1006/jasc.1993.1006
Truppa, V., Carducci, P., & Sabbatini, G. (2019). Object grasping and manipulation in capuchin monkeys (genera Cebus and Sapajus). Biological Journal of the Linnean Society, 127(3), 563-582. https://doi.org/10.1093/biolinnean/bly131
VideoLan. (2020). VLC media player-3.0.8 Vetinari. https://www.videolan.org/vlc/releases/3.0.8.html
Visalberghi, E., Fragaszy, D. M., & Savage-Rumbaugh, S. (1995). Performance in a tool-using task by common chimpanzees (Pan troglodytes), bonobos (Pan paniscus), an orangutan (Pongo pygmaeus), and capuchin monkeys (Cebus apella). Journal of Comparative Psychology, 109(1), 52-60. https://doi.org/10.1037/0735-7036.109.1.52
Washburn, S. L. (1960). Tools and human evolution. Scientific American, 203(3), 62-75.
Wittiger, L., & Sunderland-Groves, J. L. (2007). Tool use during display behavior in wild cross river gorillas. American Journal of Primatology, 69(11), 1307-1311. https://doi.org/10.1002/ajp.20436
Won, Y. -J., & Hey, J. (2005). Divergence population genetics of chimpanzees. Molecular Biology and Evolution, 22(2), 297-307. https://doi.org/10.1093/molbev/msi017
Wood, B., Henry, A., & Baker, J., others. (2011). Wiley-Blackwell encyclopedia of human evolution', Wiley-Blackwell encyclopedia of human evolution (p. 852). Wiley-Blackwell.
Wrangham, R. W. (1980). An ecological model of female-bonded primate groups. Behaviour, 75, 262-300.

Auteurs

Caroline Gérard (C)

Eco-anthropologie (EA), Muséum National d'Histoire Naturelle, CNRS, Université de Paris, Paris, France.

Ameline Bardo (A)

Histoire Naturelle de l'Homme Préhistorique (HNHP), Muséum National d'Histoire Naturelle, CNRS, Université de Paris, Paris, France.
Skeletal Biology Research Centre, School of Anthropology and Conservation, University of Kent, Canterbury, UK.

Jean P Guéry (JP)

La Vallée des Singes, Romagne, France.

Emmanuelle Pouydebat (E)

Mécanismes Adaptatifs et Evolution (MECADEV), Muséum National d'Histoire Naturelle, CNRS, Paris, France.

Bruno Simmen (B)

Eco-anthropologie (EA), Muséum National d'Histoire Naturelle, CNRS, Université de Paris, Paris, France.

Victor Narat (V)

Eco-anthropologie (EA), Muséum National d'Histoire Naturelle, CNRS, Université de Paris, Paris, France.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH