Abstract
Currently, it has been revealed that high levels of tolerance facilitate the occurrence of cooperative behavior in animals. This predicts that Japanese macaques (Macaca fuscata) would fail to solve cooperative food-retrieval tasks because of their low level of social tolerance. However, Japanese macaques exhibit regional differences in their levels of tolerance. In this study, we showed how inter-group difference in social tolerance could affect cooperation, by presenting a well-established cooperative rope-pulling task with two free-ranging groups of Japanese macaques that exhibit different levels of social tolerance. We used the task that required two macaques to pull both ends of a single rope simultaneously to obtain food rewards. We found that some macaques from the more tolerant group successfully solved the task, and one of them learned to wait for a partner when a partner was absent. In contrast, however, those of the less tolerant group almost never succeeded in the task. These results indicate that Japanese macaques possess the abilities to cooperate with conspecifics, but such abilities may be constrained in their typically despotic society.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adler GH, Levins R (1994) The island syndrome in rodent populations. Q Rev Biol 69(4):473–490. https://doi.org/10.1086/418744
Alia-Klein N, Goldstein RZ, Kriplani A, Logan J, Tomasi D, Williams B, Fowler JS (2008) Brain monoamine oxidase A activity predicts trait aggression. J Neurosci 28(19):5099–5104. https://doi.org/10.1523/jneurosci.0925-08.2008
Amici F, Aureli F, Call J (2008) Fission-fusion dynamics, behavioral flexibility, and inhibitory control in primates. Curr Biol 18(18):1415–1419. https://doi.org/10.1016/j.cub.2008.08.020
Asakawa-Haas K, Schiestl M, Bugnyar T, Massen JJ (2016) Partner choice in raven (Corvus corax) cooperation. PLoS One 11(6):e0156962. https://doi.org/10.1371/journal.pone.0156962
Boehm C (2012) Moral origins: the evolution of virtue, altruism, and shame. Basic Books, New York
Bowles S, Gintis H (2011) A cooperative species: human reciprocity and its evolution. Princeton University Press, Princeton
Burton JJ (1977) Absence de comportement coopératif spontané dans une troupe de Macaca fuscata en présence de pierres appêtées. Primates 18(2):359–366
Chaffin CL, Friedlen K, de Waal FBM (1995) Dominance style of Japanese macaques compared with rhesus and stumptail macaques. Am J Primatol 35(2):103–116. https://doi.org/10.1002/ajp.1350350203
Coussi-Korbel S, Fragaszy DM (1995) On the relation between social dynamics and social learning. Anim Behav 50(6):1441–1453. https://doi.org/10.1016/0003-3472(95)80001-8
Cronin KA, Snowdon CT (2008) The effects of unequal reward distributions on cooperative problem solving by cottontop tamarins (Saguinus oedipus). Anim Behav 75(1):245–257. https://doi.org/10.1016/j.anbehav.2007.04.032
de Waal FBM, Luttrell LM (1986) The similarity principle underlying social bonding among female rhesus monkeys. Folia Primatol 46(4):215–234. https://doi.org/10.1159/000156255
Drea CM, Carter AN (2009) Cooperative problem solving in a social carnivore. Anim Behav 78(4):967–977. https://doi.org/10.1016/j.anbehav.2009.06.030
Hare B (2017) Survival of the friendliest: Homo sapiens evolved via selection for prosociality. Annu Rev Psychol 68(68):155–186. https://doi.org/10.1146/annurev-psych-010416-044201
Hare B, Tomasello M (2005a) Human-like social skills in dogs? Trends Cogn Sci 9(9):439–444. https://doi.org/10.1016/j.tics.2005.07.003
Hare B, Tomasello M (2005b) The emotional reactivity hypothesis and cognitive evolution. Trends Cogn Sci 9(10):464–465. https://doi.org/10.1016/j.tics.2005.08.010
Hare B, Plyusnina I, Ignacio N, Schepina O, Stepika A, Wrangham R, Trut L (2005) Social cognitive evolution in captive foxes is a correlated by-product of experimental domestication. Curr Biol 15(3):226–230. https://doi.org/10.1016/j.cub.2005.01.040
Hare B, Melis AP, Woods V, Hastings S, Wrangham R (2007) Tolerance allows bonobos to outperform chimpanzees on a cooperative task. Curr Biol 17(7):619–623. https://doi.org/10.1016/j.cub.2007.02.040
Hill DA (2004) Intraspecific variation: implications for specific comparisons. In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: a model for the study of social organization. Cambridge University Press, Cambridge, pp 262–266
Hirata S, Fuwa K (2007) Chimpanzees (Pan troglodytes) learn to act with other individuals in a cooperative task. Primates 48(1):13–21. https://doi.org/10.1007/s10329-006-0022-1
Inoue-Murayama M, Inoue E, Watanabe K, Takenaka A, Murayama Y (2010) Behavior-related candidate genes in Japanese macaques. In: Nakagawa N, Nakamichi M, Sugiura H (eds) The Japanese macaques. Springer Japan, Tokyo, pp 293–301
Itoigawa N, Tanaka T, Ukai N, Fujii H, Kurokawa T, Koyama T, Imakawa S (1992) Demography and reproductive parameters of a free-ranging group of Japanese macaques (Macaca fuscata) at Katsuyama. Primates 33(1):49–68. https://doi.org/10.1007/bf02382762
Joly M, Micheletta J, De Marco A, Langermans JA, Sterck EHM, Waller BM (2017) Comparing physical and social cognitive skills in macaque species with different degrees of social tolerance. Proc R Soc B 284(1862):20162738
Koyama T, Fujii H, Yonekawa F (1981) Comparative studies of gregariousness and social structure among seven feral Macaca fuscata groups. In: Chiarelli AB, Corruccini RS (eds) Primate behavior and sociobiology. Springer, Berlin, Heidelberg, pp 52–63
Kutsukake N, Castles DL (2001) Reconciliation and variation in post-conflict stress in Japanese macaques (Macaca fuscata fuscata): testing the integrated hypothesis. Anim Cogn 4(3–4):259–268. https://doi.org/10.1007/s10071-001-0119-2
MacLean EL, Hare B, Nunn CL, Addessi E, Amici F, Anderson RC, Zhao Y (2014) The evolution of self-control. Proc Natl Acad Sci USA 111(20):E2140–E2148. https://doi.org/10.1073/pnas.1323533111
Massen JJM, Ritter C, Bugnyar T (2015) Tolerance and reward equity predict cooperation in ravens (Corvus corax). Sci Rep 5:15021. https://doi.org/10.1038/srep15021
Matsumura S (1999) The evolution of “egalitarian” and “despotic” social systems among macaques. Primates 40(1):23–31. https://doi.org/10.1007/bf02557699
Melis AP, Semmann D (2010) How is human cooperation different? Philos Trans R Soc B 365(1553):2663–2674. https://doi.org/10.1098/rstb.2010.0157
Melis AP, Hare B, Tomasello M (2006a) Chimpanzees recruit the best collaborators. Science 311(5765):1297–1300. https://doi.org/10.1126/science.1123007
Melis AP, Hare B, Tomasello M (2006b) Engineering cooperation in chimpanzees: tolerance constraints on cooperation. Anim Behav 72(2):275–286. https://doi.org/10.1016/j.anbehav.2005.09.018
Molesti S, Majolo B (2016) Cooperation in wild Barbary macaques: factors affecting free partner choice. Anim Cogn 19(1):133–146. https://doi.org/10.1007/s10071-015-0919-4
Moll H, Tomasello M (2007) Cooperation and human cognition: the Vygotskian intelligence hypothesis. Philos Trans R Soc B 362(1480):639–648. https://doi.org/10.1098/rstb.2006.2000
Mori A (1977) Intra-troop spacing mechanism of the wild Japanese monkeys of the Koshima troop. Primates 18(2):331–357. https://doi.org/10.1007/bf02383112
Nakagawa N (2010) Intraspecific differences in social structure of the Japanese macaques: a revival of lost legacy by updated knowledge and perspective. In: Nakagawa N, Nakamichi M, Sugiura H (eds) The Japanese macaques. Springer Japan, Tokyo, pp 271–290
Nakamichi M, Shizawa Y (2003) Distribution of grooming among adult females in a large, free-ranging group of Japanese macaques. Int J Primatol 24(3):607–625. https://doi.org/10.1023/a:1023744515134
Nakamichi M, Yamada K (2010) Lifetime social development in female Japanese macaques. In: Nakagawa N, Nakamichi M, Sugiura H (eds) The Japanese macaques. Springer Japan, Tokyo, pp 241–270
Nakamichi M, Fujii H, Koyama T (1983) Development of a congenitally malformed Japanese monkey in a free-ranging group during the first four years of life. Am J Primatol 5(3):205–210. https://doi.org/10.1002/ajp.1350050304
Nakamichi M, Itoigawa N, Imakawa S, Machida S (1995) Dominance relations among adult females in a free-ranging group of Japanese monkeys at Katsuyama. Am J Primatol 37(3):241–251. https://doi.org/10.1002/ajp.1350370306
Newman TK, Syagailo YV, Barr CS, Wendland JR, Champoux M, Graessle M et al (2005) Monoamine oxidase A gene promoter variation and rearing experience influences aggressive behavior in rhesus monkeys. Biol Psychiat 57(2):167–172. https://doi.org/10.1016/j.biopsych.2004.10.012
Ostojic L, Clayton NS (2014) Behavioural coordination of dogs in a cooperative problem-solving task with a conspecific and a human partner. Anim Cogn 17(2):445–459. https://doi.org/10.1007/s10071-013-0676-1
Petit O, Desportes C, Thierry B (1992) Differential probability of “coproduction” in two species of macaque (Macaca tonkeana, M. mulatta). Ethology 90(2):107–120. https://doi.org/10.1111/j.1439-0310.1992.tb00825.x
Petit O, Abegg C, Thierry B (1997) A comparative study of aggression and conciliation in three cercopithecine monkeys (Macaca fuscata, Macaca nigra, Papio papio). Behaviour 134(5–6):415–432. https://doi.org/10.1163/156853997x00610
Plotnik JM, Lair R, Suphachoksahakun W, de Waal FB (2011) Elephants know when they need a helping trunk in a cooperative task. Proc Natl Acad Sci USA 108(12):5116–5121. https://doi.org/10.1073/pnas.1101765108
Rajender S, Pandu G, Sharma JD, Gandhi KPC, Singh L, Thangaraj K (2008) Reduced CAG repeats length in androgen receptor gene is associated with violent criminal behavior. Int J Legal Med 122(5):367–372. https://doi.org/10.1007/s00414-008-0225-7
Rand DG, Nowak MA (2013) Human cooperation. Trends Cogn Sci 17(8):413–425. https://doi.org/10.1016/j.tics.2013.06.003
Seed AM, Jensen K (2011) Animal behaviour: large-scale cooperation. Nature 472(7344):424–425
Seed AM, Clayton NS, Emery NJ (2008) Cooperative problem solving in rooks (Corvus frugilegus). Proc Biol Sci 275(1641):1421–1429. https://doi.org/10.1098/rspb.2008.0111
Thierry B (2000) Covariation of conflict management patterns across macaque species. In: Aureli F, de Wall FBM (eds) Natural conflict resolution. University of California Press, Berkeley, pp 106–128
Thierry B (2007) Unity in diversity: lessons from macaque societies. Evol Anthropol 16(6):224–238. https://doi.org/10.1002/evan.20147
Thierry B, Aureli F, Nunn CL, Petit O, Abegg C, De Waal FBM (2008) A comparative study of conflict resolution in macaques: insights into the nature of trait covariation. Anim Behav 75:847–860. https://doi.org/10.1016/j.anbehav.2007.07.006
Tomasello M, Melis AP, Tennie C, Wyman E, Herrmann E (2012) Two key steps in the evolution of human cooperation: the interdependence hypothesis. Curr Anthropol 53(6):673–692. https://doi.org/10.1086/668207
Vail AL, Manica A, Bshary R (2014) Fish choose appropriately when and with whom to collaborate. Curr Biol 24(17):R791–R793
Acknowledgements
We express sincere appreciation for the managers of the Awajishima Monkey Center for their great support of our study. Y.K. personally thanks Prof. Sarah Brosnan and Dr. Teresa Romero for their great advice. We would also like to thank the members of the Department of Ethology, Graduate School of Human Sciences, Osaka University. This work was supported by Japan Society for the Promotion of Science (JSPS) KAKENHI Grant numbers 25780389, 23730705, 23370099. This study received approval from the animal experimentation committee of Graduate School of Human Sciences, Osaka University (DouJinka 25-8-0), and was conducted in accordance with the animal experimentation guidelines of Osaka University.
Author information
Authors and Affiliations
Contributions
YK designed and conducted the experiments, collected and analyzed the data, and wrote the paper; KY designed and conducted the experiments, collected the data, and helped draft the manuscript; MN helped design the experiment and draft the manuscript. All authors gave final approval for publication.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
About this article
Cite this article
Kaigaishi, Y., Nakamichi, M. & Yamada, K. High but not low tolerance populations of Japanese macaques solve a novel cooperative task. Primates 60, 421–430 (2019). https://doi.org/10.1007/s10329-019-00742-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10329-019-00742-z