Espitia-Contreras, Jenny Paola 
ORCID: https://orcid.org/0000-0003-4212-7133, Fedigan, Linda M. and Turner, Sarah E.
(2020)
Social grooming efficiency and techniques are influenced by manual impairment in free-ranging Japanese macaques (Macaca fuscata).
PLOS ONE, 15
(2).
e0228978.
ISSN 1932-6203
Preview |
Text (application/pdf)
1MBTurner-PLoS-2020.pdf - Published Version Available under License Creative Commons Attribution. |
Official URL: http://dx.doi.org/10.1371/journal.pone.0228978
Abstract
Animals born with physical impairments may particularly require behavioural flexibility and innovation to survive and carry out social activities, such as grooming. Studies on free-ranging Japanese macaques on Awaji Island, Japan, have shown that individuals with congenital limb malformations exhibited compensatory behaviours while grooming, such as increased mouth and elbow use for removing ectoparasites. The aim of this study is to explore disabled and nondisabled grooming techniques to determine whether and to what extent disabled monkeys develop novel grooming techniques, and if there is disability-associated variation in grooming efficiency. We hypothesized that modified grooming techniques used by disabled monkeys fulfilled the social and relaxing functions of grooming, however, that grooming by manually impaired individuals may still carry a hygienic cost to the recipients. Grooming behavioural data were collected by video in 2007 on 27 adult females (11 with CLMs). With a detailed grooming-related ethogram, we transcribed 216 2-minute continuous grooming video samples. We analyzed the data using generalized linear mixed effects models in R. We found that monkeys with manual impairment were less efficient groomers, as measured by removal and movement efficiency during grooming. However, there were no significant differences associated with the number of grooming movements per sample among the focal animals. Additionally, with a behavioural sequential analysis, we isolated 8 distinct grooming techniques and 3 novel disability-specific movements. Our results indicate that innovation and modification of movement types does not entirely compensate for manual disability, and that manual impairment carries a cost to the hygienic function of grooming. However, for the grooming recipient, the experience of being groomed by a disabled or nondisabled groomer is likely similar, and through movement compensation, disabled monkeys are able to engage in the social aspect of grooming without incurring any disability-associated costs.
| Divisions: | Concordia University > Faculty of Arts and Science > Geography, Planning and Environment |
|---|---|
| Item Type: | Article |
| Refereed: | Yes |
| Authors: | Espitia-Contreras, Jenny Paola and Fedigan, Linda M. and Turner, Sarah E. |
| Journal or Publication: | PLOS ONE |
| Date: | 2020 |
| Funders: |
|
| Digital Object Identifier (DOI): | 10.1371/journal.pone.0228978 |
| ID Code: | 986927 |
| Deposited By: | Krista Alexander |
| Deposited On: | 26 Jun 2020 14:15 |
| Last Modified: | 26 Jun 2020 14:15 |
References:
1.Audet J-N, Lefebvre L. What’s flexible in behavioral flexibility? Behav Ecol. 2017 Aug 1;28(4):943–7.2.Reader SM, Laland KN. Primate Innovation: Sex, Age and Social Rank Differences. Int J Primatol. 2001 Oct;22(5):787–805.
3.Fusco G, Minelli A. Phenotypic plasticity in development and evolution: facts and concepts. Philos Trans R Soc Lond B Biol Sci. 2010 Feb 27;365(1540):547–56. pmid:20083631
4.Byrne RW, Stokes EJ. Effects of Manual Disability on Feeding Skills in Gorillas and Chimpanzees. Int J Primatol. 2002 Jun;23(3):539–54.
5.Stokes E, Byrne R. Cognitive capacities for behavioural flexibility in wild chimpanzees (Pan troglodytes): The effect of snare injury on complex manual food processing. Anim Cogn. 2001 1;4(1):11–28.
6.Turner SE, Fedigan L, Matthews H, Nakamichi M. Disability, Compensatory Behavior, and Innovation in Free-Ranging Adult Female Japanese Macaques (Macaca Fuscata). Am J Primatol. 2012 1;74(9):788–803. pmid:22549480
7.Arlet ME, Carey JR, Molleman F. Species, age and sex differences in type and frequencies of injuries and impairments among four arboreal primate species in Kibale National Park, Uganda. Primates. 2009 Jan;50(1):65–73. pmid:19067112
8.Carey JR, Pinter-Wollman N, Wyman M, Müller H-G, Molleman F, Zhang N. A search for principles of disability using experimental impairment of Drosophila melanogaster. Exp Gerontol. 2007 Mar 1;42(3):166–72. pmid:17118600
9.Lovell NC. An evolutionary framework for assessing illness and injury in nonhuman primates. Am J Phys Anthropol. 1991;34(S13):117–55.
10.Isakov A, Buchanan SM, Sullivan B, Ramachandran A, Chapman JKS, Lu ES, et al. Recovery of locomotion after injury in Drosophila melanogaster depends on proprioception. J Exp Biol. 2016 Jun 1;219(11):1760–71.
11.Ang MYL, Shender MA, Ross SR. Assessment of behavior and space use before and after forelimb amputation in a zoo-housed chimpanzee (Pan troglodytes). Zoo Biol. 2016 Dec 15;36(1):5–10. pmid:27981610
12.Sugiyama Y, Kurita H, Matsui T, Kimoto S, Egawa J. Congenital malformations in Japanese macaques (Macaca fuscata) at Takasakiyama. Primates. 2014 Apr 1;55(2):303–11. pmid:24474604
13.Yoshihiro S, Goto S, Minezawa M, Muramatsu M, Saito Y, Sugita H, et al. Frequency of occurrence, morphology, and causes of congenital malformation of limbs in the Japanese monkey. Ecotoxicol Environ Saf. 1979 Dec 1;3(4):458–70. pmid:119627
14.Turner SE, Fedigan LM, Matthews HD, Nakamichi M. Social consequences of disability in a nonhuman primate. J Hum Evol. 2014 Mar 1;68:47–57. pmid:24508353
15.Turner SE, Fedigan L, Nobuhara H, Nobuhara T, Matthews H, Nakamichi M. Monkeys with disabilities: Prevalence and severity of congenital limb malformations in Macaca fuscata on Awaji Island. Primates. 2008 1;49(3):223–6. pmid:18386117
16.Grueter CC, Bissonnette A, Isler K, van Schaik CP. Grooming and group cohesion in primates: implications for the evolution of language. Evol Hum Behav. 2013 Jan;34(1):61–8.
17.Ueno M, Nakamichi M. Grooming facilitates huddling formation in Japanese macaques. Behav Ecol Sociobiol. 2018 Jun;72(6):98.
18.Zamma K. Grooming site preferences determined by lice infection among Japanese macaques in Arashiyama. Primates. 2002 Mar 1;43(1):41–9. pmid:12091746
19.Keverne EB, Martensz ND, Tuite B. Beta-endorphin concentrations in cerebrospinal fluid of monkeys are influenced by grooming relationships. Psychoneuroendocrinology. 1989 Jan 1;14(1):155–61.
20.Aureli F, Yates K. Distress prevention by grooming others in crested black macaques. Biol Lett. 2010 Feb 23;6(1):27–9. pmid:19710054
21.Hammerstein P, Noë R. Biological trade and markets. Philos Trans R Soc Lond B Biol Sci. 2016 Feb 5;371(1687):20150101. pmid:26729940
22.Kaburu SSK, Newton-Fisher NE. Egalitarian despots: hierarchy steepness, reciprocity and the grooming-trade model in wild chimpanzees, Pan troglodytes. Anim Behav. 2015 Jan 1;99:61–71.
23.Schino G, Aureli F. The relative roles of kinship and reciprocity in explaining primate altruism. Ecol Lett. 2010 Jan;13(1):45–50. pmid:19840082
24.Schino G, di Sorrentino EP, Tiddi B. Grooming and coalitions in Japanese Macaques (Macaca fuscata): Partner choice and the time frame of reciprocation. J Comp Psychol. 2007 May;121(2):181–8. pmid:17516796
25.Gumert MD. Payment for sex in a macaque mating market. Anim Behav. 2007 Dec 1;74(6):1655–67.
26.Onishi K, Yamada K, Nakamichi M. Grooming-related feeding motivates macaques to groom and affects grooming reciprocity and episode duration in Japanese macaques (Macaca fuscata). Behav Processes. 2013 Jan;92:125–30. pmid:23206904
27.Tanaka I. Matrilineal distribution of louse egg-handling techniques during grooming in free-ranging Japanese macaques. Am J Phys Anthropol. 1995 Oct 1;98(2):197–201. pmid:8644879
28.Tanaka I. Social diffusion of modified louse egg-handling techniques during grooming in free-ranging Japanese macaques. Anim Behav. 1998 Nov;56(5):1229–36. pmid:9819340
29.Altmann J. Observational Study of Behavior: Sampling Methods. Behaviour. 1974;49(3):227–66. pmid:4597405
30.Friard O, Gamba M. BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol Evol. 2016 1;7(11):1325–30.
31.Bates D, Mächler M, Bolker B, Walker S. Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw. 2015 Oct 7;67(1):1–48.
32.Dussault CF, Fugère V, Lamy T, Taranu Z. Workshop 7: Generalized linear mixed models [Internet]. 2019 [cited 2019 Feb 27]. https://qcbs.ca/wiki/r_workshop7
33.Shoukri MM, Asyali MH, VanDorp R, Kelton DE. The Poisson Inverse Gaussian Regression Model in the Analysis of Clustered Counts Data. J Data Sci. 2004;2:17–32.
34.Crawley MJ. The R Book. Wiley Publishing; 2012.
35.McElroy EJ, McBrayer LD, Williams SC, Anderson RA, Reilly SM. Sequential analyses of foraging behavior and attack speed in ambush and widely foraging lizards. Adapt Behav. 2012 Feb;20(1, SI):16–31.
36.Roger Bakeman, Quera V. Sequential analysis and observational methods for the behavioral sciences. Cambridge: Cambridge University Press; 2011.
37.Ryu H, Graham KE, Sakamaki T, Furuichi T. Long-sightedness in old wild bonobos during grooming. Current Biology. 2016;26: R1131–R1132. pmid:27825444
38.Schino G, Ventura R, Troisi A. Grooming among female Japanese macaques: distinguishing between reciprocation and interchange. Behav Ecol. 2003 Nov 1;14(6):887–91.
Repository Staff Only: item control page
Download Statistics
Download Statistics