Tool user; Long-tailed macaques; Grooming network; Social position; Preferential associations
Abstract :
[en] While the nutritional benefits and social learning of tool use in primates have been widely studied, far less is known about how tool use is associated with social life. We investigated the social aspects of tool use in a hybrid population of long-tailed macaques (Macaca fascicularis aurea × M. f. fascicularis) on Koram Island, Thailand, comprising both stone tool users and non-users. To assess potential socio-demographic patterns, we examined whether tool use differed between sexes and whether it was related to variation in dominance rank. Using social network analyses, we assessed whether tool users differed in their associations outside foraging contexts by analyzing their grooming interactions and positions within the grooming network. Males were more likely to use tools than females, whereas rank was unrelated to tool use. Tool users and non-users showed similar social connectivity, grooming rates, and numbers of grooming partners. However, grooming networks indicated that non-tool users preferentially associated with other non-users, whereas tool users showed no affiliative bias. By integrating individual characteristics with social network data, this study provides insight into how tool-use behavior integrates into primate social systems, particularly in populations with substantial variation in technological behavior.
Disciplines :
Animal psychology, ethology & psychobiology
Author, co-author :
Giraud, Gwennan ; Max Planck Institute for Evolutionary Anthropology > Lise Meitner Research Group Technological Primates
O’Malley, Theo D. R.; Max Planck Institute for Evolutionary Anthropology > Lise Meitner Research Group Technological Primates
Reeves, Jonathan S.; Max Planck Institute for Evolutionary Anthropology > Lise Meitner Research Group Technological Primates ; George Washington University > Department of Anthropology > Center for the Advanced Study of Hominin Paleobiology ; Universidade do Algarve > Interdisciplinary Center for Archaeology and the Evolution of Human Behavior
Tan, Amanda; Durham University > Department of Anthropology
Sosa, Sebastian; Max Planck Institute for Evolutionary Anthropology > Department of Human Behavior, Ecology and Culture
Malaivijitnond, Suchinda; Chulalongkorn University > Faculty of Science > Department of Biology ; Chulalongkorn University > National Primate Research Center of Thailand
Luncz, Lydia V.; Max Planck Institute for Evolutionary Anthropology > Lise Meitner Research Group Technological Primates ; George Washington University > Department of Anthropology > Center for the Advanced Study of Hominin Paleobiology
Language :
English
Title :
Network analysis highlights socio-demographic patterns of stone tool-using primates
Huber L Huber L Tool use The Rational Animal 2024 Springer 43 89 10.1007/978-3-031-60803-2_3
Sanz CM Call J Boesch C Tool Use in Animals Cognition and Ecology 2013 Cambridge University Press 10.1017/CBO9780511894800
Shumaker RW Walkup KR Beck BB Burghardt GM Animal Tool Behavior: The Use and Manufacture of Tools by Animals 2011 The Johns Hopkins University Press
Washburn SL Tools and human evolution Sci. Am. 1960 203 62 75
Hunt GR Gray RD Taylor AH Sanz CM Call J Boesch C Why is tool rare in animals? Tool Use in Animals Cognition and Ecology 2013 Cambridge University Press 89 118
Biro D Haslam M Rutz C Tool use as adaptation Philos. Trans. R. Soc. B: Biol. Sci. 2013 368 20120408
Koops K Sanz C Progress and prospects in primate tool use and cognition Primate Cognitive Studies 2022 Cambridge University Press 238 259 10.1017/9781108955836.010
Günther MM Boesch C Energetic cost of nut-cracking behaviour in wild chimpanzees Hands of Primates 1993 Springer Vienna 109 129 10.1007/978-3-7091-6914-8_8
Izar P et al. Stone tools improve diet quality in wild monkeys Curr. Biol. 2022 32 4088 4092.e3 1:CAS:528:DC%2BB38XitFKgu73K 35985326
Lonsdorf EV Sex differences in the development of termite-fishing skills in the wild chimpanzees, Pan troglodytes schweinfurthii, of Gombe National Park, Tanzania Anim. Behav. 2005 70 673 683
Miller R et al. Decision-making flexibility in New Caledonian crows, young children and adult humans in a multi-dimensional tool-use task PLoS ONE 2020 15 1:CAS:528:DC%2BB3cXmt1WntLc%3D 32160191 7065838 e0219874
Spagnoletti N Visalberghi E Ottoni E Izar P Fragaszy D Stone tool use by adult wild bearded capuchin monkeys (Cebus libidinosus). Frequency, efficiency and tool selectivity J. Hum. Evol. 2011 61 97 107 21470663
Westergaard GC Liv C Rocca AM Cleveland A Suomi SJ Tufted capuchins (Cebus apella) attribute value to foods and tools during voluntary exchanges with humans Anim. Cogn. 2004 7 19 24 10.1007/s10071-003-0181-z 12884078
Yamakoshi G Dietary responses to fruit scarcity of wild chimpanzees at Bossou, Guinea: Possible implications for ecological importance of tool use Am. J. Phys. Anthropol. 1998 106 283 295 1:STN:280:DyaK1czlvFegtg%3D%3D 9696145
Koops K Visalberghi E van Schaik CP The ecology of primate material culture Biol. Lett. 2014 10 20140508 25392310 4261853
Kulahci IG Quinn JL Dynamic relationships between information transmission and social connections Trends Ecol. Evol. 2019 34 545 554 30902359
Caldwell CA Whiten A Scrounging facilitates social learning in common marmosets, Callithrix jacchus Anim. Behav. 2003 65 1085 1092
Coussi-Korbel S Fragaszy DM On the relation between social dynamics and social learning Anim. Behav. 1995 50 1441 1453
Harrison RA van Leeuwen EJC Whiten A Chimpanzees’ behavioral flexibility, social tolerance, and use of tool-composites in a progressively challenging foraging problem iScience 2021 24 102033 2021iSci..24j2033H 33521600 7820130
Coelho CG et al. Social learning strategies for nut-cracking by tufted capuchin monkeys (Sapajus spp.) Anim. Cogn. 2015 18 911 919 1:STN:280:DC%2BC2MnmvFyiuw%3D%3D 10.1007/s10071-015-0861-5 25800169
Ottoni EB De Resende BD Izar P Watching the best nutcrackers: What capuchin monkeys (Cebus apella) know about others’ tool-using skills Anim. Cogn. 2005 8 215 219 10.1007/s10071-004-0245-8 15719240
Tan AWY Hemelrijk CK Malaivijitnond S Gumert MD Young macaques (Macaca fascicularis) preferentially bias attention towards closer, older, and better tool users Anim. Cogn. 2018 21 551 563 10.1007/s10071-018-1188-9 29754253
Biro D et al. Cultural innovation and transmission of tool use in wild chimpanzees: Evidence from field experiments Anim. Cogn. 2003 6 213 223 10.1007/s10071-003-0183-x 12898285
Coelho CG Garcia-Nisa I Ottoni EB Kendal RL Social tolerance and success-biased social learning underlie the cultural transmission of an induced extractive foraging tradition in a wild tool-using primate Proc. Natl. Acad. Sci. 2024 121 e2322884121 1:CAS:528:DC%2BB2MXhsVCqtLk%3D 39556750 11621824
Reeves JS Tan A Malaivijitnond S Luncz LV Simulation and social network analysis provide insight into the acquisition of tool behaviour in hybrid macaques Proc. R. Soc. B Biol. Sci. 2023 290 20222276
Thierry B Unity in diversity: Lessons from macaque societies Evol. Anthropol. 2007 16 224 238
Altschul DM Whither dominance? An enduring evolutionary legacy of primate sociality Personal. Neurosci. 2024 7 38384663 10877274 e1
Dittus WPJ The social regulation of population density and age-sex distribution in the toque monkey Behaviour 1977 63 281 322
Altmann SA A field study of the sociobiology of Rhesus monkeys, Macaca mulatta Ann. N. Y. Acad. Sci. 1962 102 338 435 1962NYASA.102.338A 1:STN:280:DyaF383gsVaksQ%3D%3D 14012344
Gumert MD Payment for sex in a macaque mating market Anim. Behav. 2007 74 1655 1667
Gumert MD Grooming and infant handling interchange in Macaca fascicularis: The relationship between infant supply and grooming payment Int. J. Primatol. 2007 28 1059 1074 10.1007/s10764-007-9202-0
Horner V Proctor D Bonnie KE Whiten A de Waal FBM Prestige affects cultural learning in chimpanzees PLoS ONE 2010 5 2010PLoSO..510625H 20502702 2873264 e10625
Kendal R et al. Chimpanzees copy dominant and knowledgeable individuals: Implications for cultural diversity Evol. Hum. Behav. 2015 36 65 72 27053916 4820294
Overduin-de Vries AM de Vries H Vermande MM Reijntjes AHA Sterck EHM Both aggressive and affiliative behaviour facilitate resource access in high-ranking female long-tailed macaques (Macaca fascicularis) Behaviour 2020 157 267 287
Seyfarth RM A model of social grooming among adult female monkeys J. Theor. Biol. 1977 65 671 698 1977JThBi.65.671S 1:STN:280:DyaE2s3htFWhsQ%3D%3D 406485
van Noordwijk MA van Schaik CP Competition among female long-tailed macaques, Macaca fascicularis Anim. Behav. 1987 35 577 589
Barrett BJ et al. Habitual stone-tool-aided extractive foraging in white-faced capuchins, Cebus capucinus R. Soc. Open Sci. 2018 5 181002 2018RSOS..581002B 30225086 6124021
de Andrade Moura AC Lee PC Wild Capuchins show male-biased feeding tool use Int. J. Primatol. 2010 31 457 470 10.1007/s10764-010-9406-6
Falótico T Bueno CQ Ottoni EB Ontogeny and sex differences in object manipulation and probe tool use by wild tufted capuchin monkeys (Sapajus libidinosus) Am. J. Primatol. 2021 83 e23251 33666265
Goldsborough Z Crofoot MC Barrett BJ Male-biased stone tool use by wild white-faced capuchins (Cebus capucinus imitator) Am. J. Primatol. 2024 86 e23594 1:CAS:528:DC%2BB2cXotVentQ%3D%3D 38196199
Muhammad R et al. Influence of COVID-19 on the emergence of stone-tool use behavior in a population of common long-tailed macaques (Macaca fascicularis fascicularis) in Thailand Am. J. Primatol. 2023 10.1002/ajp.23580 38012960
Gumert MD Hoong LK Malaivijitnond S Sex differences in the stone tool-use behavior of a wild population of Burmese long-tailed macaques (Macaca fascicularis aurea) Am. J. Primatol. 2011 73 1239 1249 21905061
Dunbar RIM Functional significance of social grooming in primates Folia Primatol. 1991 57 121 131
Gumert MD Ho M-HR The trade balance of grooming and its coordination of reciprocation and tolerance in Indonesian long-tailed macaques (Macaca fascicularis) Primates 2008 49 176 185 10.1007/s10329-008-0089-y 18545935
Henzi SP Barrett L The value of grooming to female primates Primates 1999 40 47 59 10.1007/BF02557701
Snyder-Mackler N et al. Social status drives social relationships in groups of unrelated female rhesus macaques Anim. Behav. 2016 111 307 317 26769983 4707678
De la Fuente MF et al. Foraging networks and social tolerance in a cooperatively breeding primate (Callithrix jacchus) J. Anim. Ecol. 2021 91 138 153 34655252
Dubuc C Hughes KD Cascio J Santos LR Social tolerance in a despotic primate: Co-feeding between consortship partners in rhesus macaques Am. J. Phys. Anthropol. 2012 148 73 80 22415860 4167600
Krause J Croft DP James R Social network theory in the behavioural sciences: Potential applications Behav. Ecol. Sociobiol. 2007 62 15 27 1:STN:280:DC%2BB383ns1Ogtw%3D%3D 10.1007/s00265-007-0445-8 32214613 7079911
Sih A Hanser SF McHugh KA Social network theory: New insights and issues for behavioral ecologists Behav. Ecol. Sociobiol. 2009 63 975 988 10.1007/s00265-009-0725-6
Sueur C Jacobs A Amblard F Petit O King AJ How can social network analysis improve the study of primate behavior? Am. J. Primatol. 2011 73 703 719 21181869
Sosa S Social network analysis Encyclopedia of Animal Cognition and Behavior 2018 Springer
Mann J Stanton MA Patterson EM Bienenstock EJ Singh LO Social networks reveal cultural behaviour in tool-using dolphins Nat. Commun. 2012 3 980 2012NatCo..3.980M 10.1038/ncomms1983 22864573
Hobaiter C Poisot T Zuberbühler K Hoppitt W Gruber T Social network analysis shows direct evidence for social transmission of tool use in wild chimpanzees PLoS Biol. 2014 12 25268798 4181963 e1001960
Canteloup C Hoppitt W van de Waal E Wild primates copy higher-ranked individuals in a social transmission experiment Nat. Commun. 2020 11 459 2020NatCo.11.459C 1:CAS:528:DC%2BB3cXksFamt78%3D 10.1038/s41467-019-14209-8 31974385 6978360
Newman MEJ Mixing patterns in networks Phys. Rev. E 2003 67 2003PhRvE.67b6126N 1975193 1:STN:280:DC%2BD3s7itlOrtA%3D%3D 026126
Farine DR Measuring phenotypic assortment in animal social networks: Weighted associations are more robust than binary edges Anim. Behav. 2014 89 141 153
Borgeaud C Sosa S Bshary R Sueur C van de Waal E Intergroup variation of social relationships in wild vervet monkeys: A dynamic network approach Front. Psychol. 2016 7 1 10
Gumert MD Gursky S Supriatna J Dominance and reciprocity in the grooming relationships of female long-tailed macaques (Macaca fascicularis) in Indonesia Indonesian Primates 2010 Springer 309 341 10.1007/978-1-4419-1560-3
Sosa S The influence of gender, age, matriline and hierarchical rank on individual social position, role and interactional patterns in Macaca sylvanus at ‘La Forêt des Singes’: A multilevel social network approach Front. Psychol. 2016 7 529 27148137 4834345
Gumert MD Malaivijitnond S Marine prey processed with stone tools by Burmese long-tailed macaques (Macaca fascicularis aurea) in intertidal habitats Am. J. Phys. Anthropol. 2012 149 447 457 23042618
Malaivijitnond S et al. Stone-tool usage by Thai long-tailed macaques (Macaca fascicularis) Am. J. Primatol. 2007 69 227 233 17146796
Gumert MD et al. Prevalence of tool behaviour is associated with pelage phenotype in intraspecific hybrid long-tailed macaques (Macaca fascicularis aurea × M. f. fascicularis) Behaviour 2019 156 1083 1125
Tan AWY From play to proficiency: The ontogeny of stone-tool use in coastal-foraging long-tailed macaques (Macaca fascicularis) from a comparative perception-action perspective J. Comp. Psychol. 2017 131 89 114 28318292
Bunlungsup S et al. Morphological characteristics and genetic diversity of Burmese long-tailed macaques (Macaca fascicularis aurea) Am. J. Primatol. 2016 78 441 455 26670099
Altmann J Observational study of behavior: Sampling methods Behaviour 1974 49 227 266 1:STN:280:DyaE2c7mtlWmsQ%3D%3D 4597405
Datta S The acquisition of dominance among free-ranging rhesus monkey siblings Anim. Behav. 1988 36 754 772
van Noordwijk MA van Schaik CP The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques, Macaca fascicularis Primates 1999 40 105 130 10.1007/BF02557705 23179535
Clutton-Brock TH Huchard E Social competition and selection in males and females Philos. Trans. R. Soc. B Biol. Sci. 2013 368 20130074 1:STN:280:DC%2BC2c7gs1Chtw%3D%3D
Fedigan LM Dominance and reproductive success in primates Am. J. Phys. Anthropol. 1983 26 91 129
Kappeler PM Van Schaik CP Evolution of primate social systems Int. J. Primatol. 2002 23 707 740 10.1023/A:1015520830318
Sosa S Sueur C Puga-Gonzalez I Network measures in animal social network analysis: Their strengths, limits, interpretations and uses Methods Ecol. Evol. 2020 12 10 21
Barthélemy M Barrat A Pastor-Satorras R Vespignani A Characterization and modeling of weighted networks Phys. A Stat. Mech. Its Appl. 2005 346 34 43 2005PhyA.346..34B
Newman MEJ The structure and function of complex networks SIAM Rev. 2003 45 167 256 2003SIAMR.45.167N 2010377
Bonacich P Factoring and weighting approaches to status scores and clique identification J. Math. Sociol. 1972 2 113 120
Bonacich P Some unique properties of eigenvector centrality Soc. Netw. 2007 29 555 564
Bonacich P Lloyd P Eigenvector-like measures of centrality for asymmetric relations Soc. Netw. 2001 23 191 201
Brent LJN Friends of friends: Are indirect connections in social networks important to animal behaviour? Anim. Behav. 2015 103 211 222 25937639 4415378
Newman MEJ Analysis of weighted networks Phys. Rev. E 2004 70 056131–1 056131–9
R Development Core Team. R: A language and environment for statistical computing. Preprint at http://www.r-project.org/ (2013).
Bates D Mächler M Bolker B Walker S Fitting linear mixed-effects models using lme4 J. Stat. Softw. 2015 67 1
Brooks M et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling R J. 2017 9 378
McGillycuddy M Warton DI Popovic G Bolker BM Parsimoniously Fitting Large Multivariate Random Effects in glmmTMB J. Stat. Softw. 2025 112 1
Hartig, F. DHARMa: Residual Diagnostic for Hierarchical (Multi-Level/Mixed) Regression Models. R package. 53 Preprint at http://florianhartig.github.io/DHARMa/ (2020).
James G Witten D Hastie T Tibshirani R An Introduction to Statistical Learning. Robust SRAM Designs and Analysis 2013 Springer 103
Menard S Applied Logistic Regression Analysis 2002 SAGE Publications 10.4135/9781412983433
Fox, J. et al. The car Package. Companion to Applied Regression. 104 Preprint at http://ftp.uni-bayreuth.de/math/statlib/R/CRAN/doc/packages/car.pdf (2007).
Lüdecke D Ben-Shachar M Patil I Waggoner P Makowski D Performance: An R package for assessment, comparison and testing of statistical models J. Open Source Softw. 2021 6 2021JOSS..6.3139L 3139
Majolo B Ventura R Koyama NF Sex, rank and age differences in the Japanese Macaque (Macaca fuscata yakui) participation in inter-group encounters Ethology 2005 111 455 468
Sprague DS Age, dominance rank, natal status, and tenure among male macaques Am. J. Phys. Anthropol. 1998 105 511 521 1:STN:280:DyaK1c3ksVarsQ%3D%3D 9584892
Zhou, H., Yang, Y. & Qian, W. Tweedie gradient boosting for extremely unbalanced zero-inflated data. http://arxiv.org/abs/1811.10192 (2019).
Kulik L Amici F Langos D Widdig A Sex differences in the development of social relationships in rhesus macaques (Macaca mulatta) Int. J. Primatol. 2015 36 353 376 10.1007/s10764-015-9826-4 25983360 4430863
Noë R Hammerstein P Biological markets: Supply and demand determine the effect of partner choice in cooperation, mutualism and mating Behav. Ecol. Sociobiol. 1994 35 1 11 10.1007/BF00167053
Schino G Grooming, competition and social rank among female primates: A meta-analysis Anim. Behav. 2001 62 265 271
Wrangham RW An ecological model of female-bonded primate groups Behaviour 1980 75 262 300
de Lima VCC Ferreira RG Social network changes during the development of immature capuchin monkeys (Sapajus spp.) Primates 2021 10.1007/s10329-021-00918-6 34273030
Dunayer ES Berman CM Infant handling among primates Int. J. Comp. Psychol. 2018 31 1 31
Fedurek P Lehmann J The effect of excluding juveniles on apparent adult olive baboons (Papio anubis) social networks PLoS ONE 2017 12 28323851 5360227 e0173146
Giraud G et al. Effect of infant presence on social networks of sterilized and intact wild female Balinese macaques (Macaca fascicularis) Animals 2021 11 34573504 8466756 2538
Liao Z Sosa S Wu C Zhang P The influence of age on wild rhesus macaques’ affiliative social interactions Am. J. Primatol. 2018 80 e22733
Krause J Lusseau D James R Animal social networks: An introduction Behav. Ecol. Sociobiol. 2009 63 967 973 10.1007/s00265-009-0747-0
Wasserman S Faust K Social Network Analysis: Methods and Applications 1994 Cambridge University Press
Sosa S et al. A multilevel statistical toolkit to study animal social networks: the Animal Network Toolkit Software (ANTs) R package Sci. Rep. 2020 10 12507 2020NatSR.1012507S 1:CAS:528:DC%2BB3cXhsVOqtb%2FP 10.1038/s41598-020-69265-8 32719477 7385643
Solymos, P., Zawadzki, Z., Bengtsson, H. & R Core Team. pbapply: Adding Progress Bar to ‘*apply’ Functions. R package. Preprint at (2023).
Peel L Delvenne J-C Lambiotte R Multiscale mixing patterns in networks Proc. Natl. Acad. Sci. 2018 115 4057 4062 2018PNAS.115.4057P 3796427 1:CAS:528:DC%2BC1cXht1GgsLnP 29610344 5910813
Karimi F Oliveira M On the inadequacy of nominal assortativity for assessing homophily in networks Sci. Rep. 2023 13 21053 2023NatSR.1321053K 1:CAS:528:DC%2BB3sXisFSmtbvJ 10.1038/s41598-023-48113-5 38030623 10686992
Boesch C Boesch H Sex differences in the use of natural hammers by wild chimpanzees: A preliminary report J. Hum. Evol. 1981 10 585 593
Boesch C Boesch H Possible causes of sex differences in the use of natural hammers by wild chimpanzees J. Hum. Evol. 1984 13 415 440
Falótico T Ottoni EB Sexual bias in probe tool manufacture and use by wild bearded capuchin monkeys Behav. Proc. 2014 108 117 122
Reader SM Laland KN Primate innovation: Sex, age and social rank differences Int. J. Primatol. 2001 22 787 805 10.1023/A:1012069500899
Van Noordwijk MA Van Schaik CP Male migration and rank acquisition in wild long-tailed macaques (Macaca fascicularis) Anim. Behav. 1985 33 849 861
Goodall J The Chimpanzees of Gombe: Patterns of Behavior 1986 The Belknap Press of Harvard University Press
Jack KM Fedigan L Male dispersal patterns in white-faced capuchins, Cebus capucinus Anim. Behav. 2004 67 761 769
Harrison ND et al. Behavioural change during dispersal and its relationship to survival and reproduction in a cooperative breeder J. Anim. Ecol. 2021 90 2637 2650 34258771 8597146
Md-Zain BM et al. A comprehensive population survey and daily activity budget on long-tailed macaques of Universiti Kebangsaan Malaysia J. Biol. Sci. 2010 10 608 615
Lehmann J Korstjens AH Dunbar RIM Group size, grooming and social cohesion in primates Anim. Behav. 2007 74 1617 1629
Hambali K Ismail A Munir Md-Zain B Daily activity budget of long-tailed macaques (Macaca Fascicularis) in Kuala Selangor Nature Park Int. J. Basic Appl. Sci. IJBAS-IJENS 2012 12 47
van Noordwijk MA van Schaik CP Career moves: Transfer and rank challenge decisions by male long-tailed macaques Behaviour 2001 138 359 395 10.1163/15685390152032505
Luncz LV et al. Diversity of stone tools between long-tailed macaque populations Folia Primatol. 2020 91 309
Luncz LV et al. Group-specific archaeological signatures of stone tool use in wild macaques Elife 2019 8 1 21
