A multi-level society comprised of one-male and multi-male core units in an African colobine (Colobus angolensis ruwenzorii)


Autoři: Samantha M. Stead aff001;  Julie A. Teichroeb aff001
Působiště autorů: Department of Anthropology, University of Toronto Scarborough, Toronto, Ontario, Canada aff001;  School of the Environment, University of Toronto, Toronto, Ontario, Canada aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0217666

Souhrn

Several mammalian species exhibit complex, nested social organizations, termed multi-level or modular societies. Multi-level societies comprise stable core units that fission and fuse with one another in a hierarchical manner, forming groups that vary in size over time. Among nonhuman primates, these social systems have been confirmed in several African papionin and Asian colobine species. We use data from August 2017 to July 2018 on individually-recognized Rwenzori Angolan colobus living near Lake Nabugabo, Uganda to document the first multi-level society in an African colobine. The study band comprised up to 135 individuals organized into 12 socially and spatially distinct core units that ranged in size from 4 to 23 individuals. These core units showed a strong affinity to one another, spending roughly 75% of their time together. Core units fissioned and fused non-randomly with one another throughout the day, leading to different combinations of core units being observed. Using association indices between core units, we employed hierarchical cluster analyses and permutation tests to show that some core units associated preferentially into clans. Thus, we confirm three tiers of social organization for Rwenzori Angolan colobus: core unit, clan, and band. The social organization of this subspecies is unlike any reported previously in a nonhuman primate, with about half the core units containing a single adult male and the others containing multiple reproductive adult males. The discovery of a unique primate multi-level society in a novel lineage could allow for a better understanding of the evolution of these complex social systems across the Animal Kingdom. Preliminary data show males transfer within the band and females transfer outside of the band, which is proposed for hominin multi-level societies. This subspecies could thus also provide insight into the selective pressures underlying multi-level societies in our own lineage.

Klíčová slova:

Animal sociality – Lakes – Permutation – Primates – Social systems – Colobus – Baboons – Human evolution


Zdroje

1. Kappeler PM, van Schaik CP. Evolution of primate social systems. Int J Primatol. 2002; 23: 707–740.

2. Clutton-Brock T. Mammalian societies. Hoboken: John Wiley & Sons; 2016.

3. Wrangham RW. An ecological model of female bonded primate groups. Behaviour. 1980; 75: 262–300.

4. van Schaik CP. The ecology of social relationships amongst female primates. In: Standen V, Foley RA, editors. Comparative Socioecology. Oxford: Blackwell Scientific; 1989. pp. 195–218.

5. Isbell LA. Contest and scramble competition: Patterns of female aggression and ranging behaviour among primates. Behav Ecol. 1991; 2: 143–155.

6. Sterck EHM, Watts DP, van Schaik CP. The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol. 1997; 41: 291–309.

7. Crockett CM, Janson CH. Infanticide and group size in red howlers. In: van Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge: Cambridge University Press; 2000. pp. 75–89.

8. Aureli F, Schaffner CM, Boesch C, Bearder SK, Call J, Chapman CA, et al. Fission-fusion dynamics new research frameworks. Curr Anthropol. 2008; 49: 627–654.

9. Grueter CC, Qi X, Li B, Li M. Multilevel societies. Curr Biol. 2017; 27: R979–R1001. doi: 10.1016/j.cub.2017.09.010

10. Grueter CC, Matsuda I, Zhang P, Zinner D. Multilevel societies in primates and other mammals: Introduction to the special issue. Int J Primatol. 2012; 33: 993–1001. doi: 10.1007/s10764-012-9614-3 23024443

11. Snyder-Mackler N, Beehner JC, Bergman TJ. Defining higher levels in the multilevel societies of geladas (Theropithecus gelada). Int J Primatol. 2012; 33: 1054–1068.

12. Schreier AL, Swedell L. The socioecology of network scaling ratios in the multilevel society of hamadryas baboons (Papio hamadryas hamadryas). Int J Primatol. 2012; 33: 1069–1080.

13. Wittemyer G, Douglas-Hamilton I, Getz WM. The socioecology of elephants: Analysis of the processes creating multitiered social structures. Anim Behav. 2005; 69: 1357–1371.

14. Couzin ID. Behavioral ecology: Social organization in fission-fusion societies. Curr Biol. 2006; 16: R169–R171. doi: 10.1016/j.cub.2006.02.042 16527735

15. VanderWaal KL, Wang H, McCowan B, Fushing H, Isbell LA. Multilevel social organization and space use in reticulated giraffe (Giraffa camelopardalis). Behav Ecol. 2014; 25: 17–26.

16. Rubenstein DI, Hack M. Natural and sexual selection and the evolution of multi- level societies: Insights from zebras with comparisons to primates. In: Kappeler PM, van Schaik CP, editors. Sexual selection in primates: New and comparative perspectives. Cambridge: Cambridge University Press; 2004. pp. 266–277.

17. Hoogland J. The black-tailed prairie dog: Social life of a burrowing mammal. Chicago: University of Chicago Press, Chicago, 1995)

18. Feh C, Munkhtuya B, Enkhbold S, Sukhbaatar T. Ecology and social structure of the Gobi khulan Equus hemionus subsp. in the Gobi B National Park, Mongolia. Biol Cons. 2001; 101: 51–61.

19. Whitehead H, Antunes R, Gero S, Wong SNP, Engelhaupt D, Rendell L. Multilevel societies of female sperm whales (Physeter macrocephalus) in the Atlantic and Pacific: Why are they so different? Int J Primatol. 2012; 33: 1142–1164.

20. Connor RC, Smolker RA, Richards AF. Two levels of alliance formation among male bottlenose dolphins. Proc Nat Acad Sci. 1992; 89: 987–990. doi: 10.1073/pnas.89.3.987 11607275

21. Tavares SB, Samarra FIP, Miller PJO. A multilevel society of herring-eating killer whales indicates adaptation to prey. Behav Ecol. 2017; 28: 500–514.

22. Kirkpatrick RC, Grueter CC. Snub-nosed monkeys: Multilevel societies across varied environments. Evol Anthropol. 2010; 19: 98–113.

23. Grueter CC, Li D, Ren B, Wei F, Li M. Deciphering the social organization and structure of wild Yunnan snub-nosed monkeys (Rhinopithecus bieti). Folia Primatol. 2017; 88: 358–383. doi: 10.1159/000480503 29041006

24. Yeager CP. Proboscis monkey (Nasalis larvatus) social organization: Intergroup patterns of association. Am J Primatol. 1991; 26: 133–137.

25. Schreier AL, Swedell L. The fourth level of social structure in a multi-level society: Ecological and social functions of clans in hamadryas baboons. Am J Primatol. 2009; 71: 948–955. doi: 10.1002/ajp.20736 19670312

26. Fischer J, Kopp GH, Pesco FD, Goffe A, Hammerschmidt K, Kalbitzer U, et al. Charting the neglected West: The social system of Guinea baboons. Am J Phys Anthropol. 2017; 162: 15–31. doi: 10.1002/ajpa.23144 28105722

27. Galat-Luong A, Galat G, Hagall S. The social and ecological flexibility of Guinea baboons: Implications for Guinea baboons social organization and male strategies. In: Swedell L, Leig S, editors. Reproduction and fitness in baboons: Behavioral, ecological and life history perspectives. New York: Springer; 2006. pp. 105–121.

28. Patzelt A, Kopp GH, Ndao I, Kalbitzer U, Zinner D, Fischer J. Male tolerance and male-male bonds in a multilevel primate society. Proc Natl Acad Sci USA. 2014; 111: 14740–14745. doi: 10.1073/pnas.1405811111 25201960

29. Rodseth L, Wrangham R, Harrigan A, Smuts B. The human community as a primate society. Curr Anthropol. 1991; 32: 221–254.

30. Swedell L, Plummer T. A Papionin multilevel society as a model for hominin social evolution. Int J Primatol. 2012; 33: 1165–1193.

31. Zhou WX, Sornette D, Hill RA, Dunbar RIM. Discrete hierarchical organization of social group sizes. Proc Biol Sci. 2005; 272: 439–444. doi: 10.1098/rspb.2004.2970 15734699

32. Hamilton MJ, Milne BT, Walker RS, Burger O, Brown JH. The complex structure of hunter-gatherer social networks. Proc Biol Sci. 2007; 274: 2195–2202. doi: 10.1098/rspb.2007.0564 17609186

33. Bowler M, Knogge C, Heymann EW, Zinner D. Multilevel societies in new world primates? Flexibility may characterize the organization of Peruvian red uakaris (Cacajao calvus ucayalii). Int J Primatol. 2012; 33: 1110–1124. doi: 10.1007/s10764-012-9603-6 23024445

34. Astaras C, Mühlenberg M, Waltert M. Note on drill (Mandrillus leucophaeus) ecology and conservation status in Korup National Park, Southwest Cameroon. Am J Primatol. 2008; 70: 306–310. doi: 10.1002/ajp.20489 17922527

35. Rogers ME, Aberneth KA, Fontaine B, Wickings J, White LJT, Tutin CEG. Ten days in the life of a mandrill horde in the Lope Reserve, Gabon. Am J Primatol. 1996; 40: 217–313.

36. Hongo S. New evidence from observations of progressions of mandrills (Mandrillus sphinx): a multilevel or non-nested society? Primates. 2014; 55: 473–481. doi: 10.1007/s10329-014-0438-y 25091875

37. Fashing PJ, Mulindahabi F, Gakima JB, Masozera M, Mununura I, Plumptre AJ, Nguyen N. Activity and ranging patterns of Colobus angolensis ruwenzorii in Nyungwe Forest, Rwanda: possible costs of large group size. Int J Primatol. 2007; 28: 529−550.

38. Grueter CC, Chapais B, Zinner D. Evolution of multilevel social systems in nonhuman primates and humans. Int J Primatol. 2012; 33: 1002–1037. doi: 10.1007/s10764-012-9618-z 23024444

39. Cui L-W, Huo S, Zhong T, Xiang Z-F, Xiao W, Quan R-C. Social organization of black-and-white snub-nosed monkeys (Rhinopithecus bieti) at Deqin, China. Am J Primatol. 2008; 70: 169–174. 17894403

40. Pines M, Saunders J, Swedell L. Alternative routes to the leader male role in a multi-level society: Follower vs. solitary male strategies and outcomes in hamadryas baboons. Am J Primatol. 2011; 73: 679–691. doi: 10.1002/ajp.20951 21433048

41. Snyder-Mackler N, Alberts SC, Bergman TJ. Concessions of an alpha male? Cooperative defence and shared reproduction in multi-male primate groups. Proc Roy Soc B. 2012; 279: 3788–3795.

42. Qi X-G, Garber PA, Ji W, Huang Z-P, Huang K, Zhang P, Guo S-T, Wang X-W, He G, Zhang P, Li B-G. Satellite telemetry and social modeling offer new insights into the origin of primate multilevel societies. Nat Comm. 2014; 5: 5296.

43. Shimooka Y. Seasonal variation in association patterns of wild spider monkeys (Ateles belzebuth belzebuth) at La Macarena, Colombia. Primates. 2003; 44: 83–90. doi: 10.1007/s10329-002-0028-2 12687471

44. Alexander RD. The evolution of social behavior. Ann Rev Ecol Syst. 1974; 5: 325–383.

45. van Schaik CP. Why are diurnal primates living in groups? Behaviour. 1983; 87: 120–144.

46. Link A, Di Fiore A. Effects of predation risk on the grouping patterns of white‐bellied spider monkeys (Ateles belzebuth belzebuth) in Western Amazonia. Am J Phys Anthropol. 2013; 150: 579–590. doi: 10.1002/ajpa.22230 23504960

47. Treves A, Chapman CA. Conspecific threat, predation avoidance, and resource defense: Implications for grouping in langurs. Behav Ecol Sociobiol. 1996; 39: 43–53.

48. Hamilton WD. Geometry for the selfish herd. J Theor Biol. 1971; 31: 295–311. doi: 10.1016/0022-5193(71)90189-5 5104951

49. Schreier AL, Swedell L. Ecology and sociality in a multilevel society: ecological determinants of spatial cohesion in Hamadryas baboons. Am J Phys Anthropol. 2012; 148: 580–588. doi: 10.1002/ajpa.22076 22552956

50. Rubenstein DI. Ecology and sociality in horses and zebras. In: Rubenstein DI, Wrangham RW, editors. Ecological aspects of social evolution. Princeton: Princeton University Press; 1986. pp. 282–302.

51. Grueter CC, van Schaik CP. Evolutionary determinants of modular societies in colobines. Behav Ecol. 2010; 21: 63–71.

52. Xiang Z-F, Yang B-H, Yu Y, Yao H, Grueter CC, Garber PA, Li M. Males collectively defend their one-male units against bachelor males in a multi-level primate society. Am J Primatol. 2014; 76: 609–617. doi: 10.1002/ajp.22254 24375453

53. Pappano DJ, Snyder-Mackler N, Bergman TJ, Beehner JC. Social ‘predators’ within a multilevel primate society. Anim Behav. 2012; 84: 653–658.

54. Oates JF. The natural history of African colobines. In: Davies AG, Oates JF, editors. Colobine monkeys: Their ecology, behaviour and evolution. UK: Cambridge University Press; 1994. pp. 75–128.

55. Fimbel C, Vedder A, Dierenfeld E, Mulindahabi F. An ecological basis for large group size in Colobus angolensis in the Nyungwe Forest, Rwanda. Afr J Ecol. 2001; 39: 83–92.

56. Miller A, Uwingeneye G, Kaplin B, Judge D, Grueter CC. The anatomy of a supergroup of Colobus angolensis ruwenzorii supergroups in Nyungwe National Park, Rwanda. 27th meeting of the International Primatological Society Congress; 2018.

57. Fashing PJ. African colobine monkeys: Their behavior, ecology and conservation. In: Campbell CJ, Fuentes A, MacKinnon KC, Bearder SK, Stumpf RM, editors. Primates in perspectives. 2nd ed. New York: Oxford University Press; 2011. pp. 203–229.

58. Arseneau-Robar TJM, Joyce MM, Stead SM, Teichroeb JA. Proximity and grooming patterns reveal opposite-sex bonding in Rwenzori Angolan colobus monkeys (Colobus angolensis ruwenzorii). Primates. 2018; 59: 267–279. doi: 10.1007/s10329-017-0643-6 29270880

59. Teichroeb JA, Bridgett GR, Corriveau A, Twinomugisha D. The immediate impact of selective logging on Angolan colobus (Colobus angolensis ruwenzorii) at Lake Nabugabo, Uganda. In: Behie AM, Teichroeb JA, Malone N, editors. Primate research and conservation in the Anthropocene. UK: Cambridge University Press. In Press.

60. Altmann J. Observational study of behavior: Sampling methods. Behaviour. 1974; 49: 227–265. 4597405

61. Oates JF. The social life of a black and white colobus monkey, Colobus guereza. Z Tierpsychol. 1977; 45: 1–60. 414475

62. Fashing PJ. Male and female strategies during intergroup encounters in guerezas (Colobus guereza): Evidence for resource defense mediated through males and a comparison with other primates. Behav Ecol Sociobiol. 2001; 50: 219–230.

63. Sicotte P, Macintosh AJ. Inter-group encounters and male incursions in Colobus vellerosus in central Ghana. Behaviour. 2004; 141: 533–554.

64. Whitehead H. Analyzing animal societies: Quantitative methods for vertebrate social analysis. Chicago: Chicago University Press; 2008.

65. Sokal RR, Rohlf FJ. The comparison of dendrograms by objective methods. Taxon. 1962; 11: 33–40.

66. Whitehead H. SOCPROG programs: Analyzing animal social structures. Behav Ecol Sociobiol. 2009; 63: 765–778.

67. Bejder L, Fletcher D, Bräger S. A method for testing association patterns of social animals. Anim Behav. 1998; 56: 719–725. doi: 10.1006/anbe.1998.0802 9784222

68. Whitehead H. Programs for analyzing social structure. Website handbook. 1999.

69. Sicotte P. Female mate choice in mountain gorillas. In: Robbins MM, Sicotte P, Stewart KJ, editors. Mountain gorillas: Three decades of research at Karisoke. Cambridge: Cambridge University Press; 2001. pp. 59–87.

70. Dunbar RIM, Dunbar P. Social dynamics of gelada baboons. In: Kuhn H, Luckett WP, Noback CR, Schultz AH, Starck D, Szalay FS, editors. Contributions to primatology. Switzerland: Karger; 1975. pp.157.

71. Swedell L. African papionins: Diversity of social organization and ecological flexibility. In: Campbell CJ, Fuentes A, MacKinnon KC, Bearder SK, Stumpf RM, editors. Primates in perspective. 2nd ed. New York: Oxford University Press; 2011. pp. 241–277.

72. Swedell L, Saunders J. Infant mortality, paternity certainty, and female reproductive strategies in hamadryas baboons. In: Swedell L, Leigh S, editors. Reproduction and fitness in baboons: Behavioral, ecological, and life history perspectives. New York: Springer; 2006. pp. 19–51.

73. Swedell L. Affiliation among females in wild Hamadryas baboons (Papio hamadryas hamadryas). Int J Primatol. 2002; 23: 1205–1226.

74. Zhang P, Li B-G, Qi X-G, MacIntosh AJJ, Watanabe K. A proximity-based social network of a group of Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Int J Primatol. 2012; 33: 1081–1095.

75. Ren RM, Yan KH, Xia SZ, Jin HY, Qiu JJ, Romero T. Social behavior of a captive group of golden snub-nosed langur Rhinopithecus roxellana. Zool Stud. 2010; 49: 1–8.

76. Zhao DP, Li BG, Li YH, Wada K. Extra-unit sexual behaviour among wild Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains of China. Folia Primatol. 2005; 76: 172–176. doi: 10.1159/000084379 15900104

77. Zhang P, Watanabe K, Li BG, Tan CL. Social organization of the Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling mountains of China. Primates. 2006; 47: 374–382. doi: 10.1007/s10329-006-0178-8 16625309

78. Zhang P, Watanabe K, Li BG. Female social dynamics in a provisioned free-ranging band of the Sichuan snub-nosed monkey (Rhinopithecus roxellana) in the Qinling Mountains, China. Am J Primatol. 2008; 70: 1–10.

79. Yao H, Liu X, Stanford C, Yang J, Huang T, Wu F, Li Y. Male dispersal in a provisioned multilevel group of Rhinopithecus roxellana in Shennongjia Nature Reserve, China. Am J Primatol. 2011; 73: 1280–1288. doi: 10.1002/ajp.21000 21898518

80. Qi X-G, Li B-G, Garber PA, Ji W. Watanabe K. Social dynamics of the golden snub-nosed monkey (Rhinopithecus roxellana): Female transfer and one-male unit succession. Am J Primatol. 2009; 71: 670–679. doi: 10.1002/ajp.20702 19434626

81. Hobaiter C, Samuni L, Mullins C, Akankwasa WJ, Zuberbuhler K. Variation in hunting behaviour in neighbouring chimpanzee communities in the Budongo forest, Uganda. PLoS One. 2017; 12: e0178065. doi: 10.1371/journal.pone.0178065 28636646

82. Zuberbuhler K, Jenny D. Leopard predation and primate evolution. J Human Evol. 2002; 43: 873–886.

83. Mitani JC, Sander WJ, Lwanga JS, Windfelder TL. Predatory behavior of crowned hawk-eagles (Stephanoaetus coronatus) in Kibale National Park, Uganda. Behav Ecol Sociobiol. 2001; 49: 187–195.

84. Kirkpatrick C. The Asian Colobines. In: Campbell CJ, Fuentes A, MacKinnon KC, Bearder SK, Stumpf RM, editors. Primates in perspective. 2nd ed. New York: Oxford University Press; 2011. pp.189–202.

85. de Silva S, Wittemyer G. 2012. A comparison of social organization in Asian elephants and African savannah elephants. Int J Primatol. 2012; 33: 1125–1141.

86. Harris TR. Between-group contest competition for food in a highly folivorous population of black and white colobus monkeys (Colobus guereza). Behav Ecol Sociobiol. 2006; 61: 317–329.

87. Korstjens AH, Nijssen EC, Noë R. Intergroup relationships in western black-and-white colobus, Colobus polykomos polykomos. Int J Primatol. 2005; 26: 1267–1289.

88. Teichroeb JA, Sicotte P. Cascading competition: the seasonal strength of scramble influences between-group contest in a folivorous primate. Behav Ecol Sociobiol. 2018; 72: 6.

89. Chapais B. Primeval kinship: How pair-bonding gave birth to human society. Cambridge: Harvard University Press; 2008

90. Chapais B. Monogamy, strongly bonded groups, and the evolution of human social structure. Evol Anthropol. 2013; 22: 52–65. doi: 10.1002/evan.21345 23585378

91. Grueter CC, Matsuda I, Zhang P, Zinner D. Multilevel societies in primates and other mammals: introduction to the special issue. Int J Primatol. 2012; 33: 993–1001. doi: 10.1007/s10764-012-9614-3 23024443

92. Alvarez HP. Residence groups among hunter-gatherers: A view of the claims and evidence for patrilocal bands. In: Chapais B, Berman CM, editors. Kinship and behavior in primates. Oxford: Oxford University Press; 2004. pp. 420–442.

93. Rodseth L, Novak SA. The social modes of men. Hum Nat. 2000; 11: 335–366. doi: 10.1007/s12110-000-1007-1 26193657

94. Tiger L. Men in groups. New York: Routledge; 1969.

95. Rodseth L, Wrangham RW, Harrigan AM, Smuts BB, Dare R, Fox R et al. The human community as a primate society [and comments]. Curr Anthropol. 1991; 32: 221–254.

96. Chapais B. The deep structure of human society: primate origins and evolution. In: Kappeler P, Silk J, editors. Mind the gap. Heidelberg: Springer; 2010. pp. 19–51.


Článek vyšel v časopise

PLOS One


2019 Číslo 10