Abstract
Callitrichids are small Neotropical primates and, due to their cooperative breeding system, infants are of particular interest in research on social dynamics. Although a few studies have investigated the role of helpers in this type of system, there is still a lack of research in field studies seeking to determine whether there is a relationship between the number of helpers (adults) in a social group and the motor development of infants. With that in mind, four groups of wild marmosets (Callithrix jacchus) were observed and the motor behaviors of 1 to 4 month-old infants were recorded. To investigate the influence of the adult:infant ratio on motor diversity, used as an indicator of motor development, we ran a GLMM with a Gaussian distribution and found that: (i) in groups with fewer adults, 2-month-old infants show earlier motor diversity; (ii) motor diversity increases with age regardless of the ratio of adult males per infant; (iii) in groups with more adult females per infant, the motor diversity of 2-month-old infants is significantly lower compared to 3-month-old infants. Although adult callitrichid males play an important role in the care of their offspring, the presence of females appears to be a key factor in motor development at this early stage in the study groups. In a cooperative breeding system, the lack of helpers seems to drive the development of independence in infants, resulting in earlier development.
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References
Adolph, KE, Robinson SR (2015). Motor development. In: Lerner RM, Liben LS, Mueller U (ed.) Handbook of child psychology and developmental science. Vol 2, Cognitive Processes, 7th edition. Hoboken, NJ: John Wiley & Sons, Inc. p. 113 – 157.
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267. https://doi.org/10.1163/156853974x00534
Animal Behaviour (2003) Guidelines for the treatment of animals in behavioural research and teaching. Anim Behav 62:249–255. https://doi.org/10.1016/j.anbehav.2011.10.031
Barbosa MN, Silva Mota MT (2013) Alloparental responsiveness to newborns by nonreproductive, adult male, common marmosets (Callithrix jacchus). Am J Primatol 75:145–152. https://doi.org/10.1002/ajp.22092
Berman CM, Rasmussen KLR, Suomi SJ (1997) Group size, infant development and social networks in free-ranging rhesus monkeys. Anim Behav 53:405–421. https://doi.org/10.1006/anbe.1996.0321
Bezerra BM, Souto AS, Schiel N (2007) Infanticide and cannibalism in a free-ranging plurally breeding group of common marmosets (Callithrix jacchus). Am J Primatol 69:945–952. https://doi.org/10.1002/ajp.20394
Burkart JM (2015) Opposite effects of male and female helpers on social tolerance and proactive prosociality in callitrichid family groups. Sci Rep 5:9622. https://doi.org/10.1038/srep09622
CPRH 2022. http://www2.cprh.pe.gov.br/uc/apa-aldeia-beberibe/. Accesses in April 24th 2022.
De La Fuente MF, Sueur C, Garber PA, Bicca-Marques JC, Souto A, Schiel N (2021) Foraging networks and social tolerance in a cooperatively breeding primate (Callithrix jacchus). J Anim Ecol 1:1–17. https://doi.org/10.1111/1365-2656.13609
Digby LJ, Ferrari SF, Saltzman W. (2011) Callitrichines: The role of competition in cooperatively breeding species. In: Campbell, et al., (eds.) Primates in Perspective (2nd edition). New York: Oxford University Press, pp. 91–107.
Dunbar RIM, Carron PM, Shultz S (2018) Primate social group sizes exhibit a regular scaling pattern with natural attractors. Biol Lett 14:20170490. https://doi.org/10.1098/rsbl.2017.0490
Ford SM, Porter LM, Davis LC. (eds). (2009). The smallest Anthropoids. Developments in Primatology: Progress and Prospects. Boston: Springer
Fragaszy DM, Bard K (1997) Comparison of development and life history in Pan and Cebus. Int J Primatol 18:683–701. https://doi.org/10.1023/A:1026339712071
De La Fuente MF, Schiel N, Bicca-Marques JC, Caselli CB, Souto A, Garber PA (2019) Balancing contest competition, scramble competition, and social tolerance at feeding sites in wild common marmosets (Callithrix jacchus). Am J Primatol e22964. https://doi.org/10.1002/ajp.22964
Garber PA (1997) One for all and breeding for one: cooperation and competition as a tamarin reproductive strategy. Evol Anthropol 5:187–199. https://doi.org/10.1002/(sici)1520-6505(1997)5:6%3c187::aid-evan1%3e3.0.co;2-a
Gunhold T, Massen JJM, Schiel N, Souto A, Bugnyar T (2014) Memory, transmission and persistence of alternative foraging techniques in wild common marmosets. Anim Behav 91:79–91. https://doi.org/10.1016/j.anbehav.2014.02.023
Hinde RA, Spencer-Booth Y (1968) Review lecture—the study of mother-infant interaction in captive group-living rhesus monkeys. Proc R Soc B: Biol Sci 169:177–201. https://doi.org/10.1098/rspb.1968.0005
Holmes J (2014) John Bowlby and attachment theory (Second edition). Routledge, Taylor & Francis Group, p 272
Huang J, Cheng X, Zhang S, Chang L, Li X, Liang Z, Gong N (2020) Having infants in the family group promotes altruistic behavior of marmoset monkeys. Curr Biol 30:4047–4055. https://doi.org/10.1016/j.cub.2020.07.045
Ingram JC (1977) Interactions between parents and infants, and the development of independence in the common marmosets (Callithrix jacchus). Anim Behav 25:811–827. https://doi.org/10.1016/0003-3472(77)90035-5
Isler K, van Schaik CP (2012) Allomaternal care, life history and brain size evolution in mammals. J Hum Evol 63:52–63. https://doi.org/10.1016/j.jhevol.2012.03.009
Jablonski NG (2021) Social and affective touch in primates and its role in the evolution of social cohesion. Neuroscience 464:117–125. https://doi.org/10.1016/j.neuroscience.2020.11.024
Koenig A (1995) Group Size, Composition, and Reproductive Success in Wild Common Marmosets (Callithrix jacchus). Am J Primatol 35:311–317. https://doi.org/10.1002/ajp.1350350407
Kostan KM, Snowdon CT (2002) Attachment and social preferences in cooperatively-reared cotton-top tamarins. Am J Primatol 57:131–139. https://doi.org/10.1002/ajp.10040
Lehmann J, Korstjens AH, Dunbar RIM (2007) Group size, grooming and social cohesion in primates. Anim Behav 74:1617–1629. https://doi.org/10.1016/j.anbehav.2006.10.025
Lehner PN (1996) Handbook of ethological methods. Cambridge University Press, Cambridge
Lenth R (2016) Least-squares means: the R package lsmeans. J Stat Softw 69:1–33. https://doi.org/10.18637/jss.v069.i01
van Londen WM, Juffer F, van IJzendoorn MH (2007) Attachment, Cognitive, and Motor Development in Adopted Children: Short-term Outcomes after International Adoption. J Pediatr Psychol 32:1249–1258. https://doi.org/10.1093/jpepsy/jsm062
Maestripieri D (2018) Maternal influences on primate social development. Behav Ecol Sociob 72:1–12
Maestripieri D, Hoffman CL, Anderson GM, Carter CS, Higley JD (2009) Mother–infant interactions in free-ranging rhesus macaques: relationships between physiological and behavioral variables. Physiol Behav 96:613–619. https://doi.org/10.1016/j.physbeh.2008.12.016
Malukiewicz J, Boere v, Oliveira MAB, D’Arc M, Ferreira JVA, French J, Housman G, Souza CI, Jerusalinsky L, Melo FR, Valença-Montenegro MM, Moreira SB, Silva IO, Pacheco FS, Rogers J, Pissinatti A, del Rosario RCH, Ross C, Ruiz-Miranda CR, Pereira LCM, Schiel N, Silva FFR, Souto A, Šlipogor V, Tardif S (2020) An introduction to the Callithrix genus an overview of recent advances in marmoset research. ILAR J 61: 110–138. https://doi.org/10.1093/ilar/ilab027
Markham AC, Gesquiere LR (2017) Costs and benefits of group living in primates: an energetic perspective. Philos Trans R Soc B 372:20160239. https://doi.org/10.1098/rstb.2016.0239
Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB (2012) The evolution of primate societies. The University of Chicago Press, Chicago and London, p 730
Ngo V, Gorman JC, De La Fuente MF, Souto A, Schiel N, Miller CT (2022) Active vision during prey capture in wild marmoset monkeys. Curr Biol 32:1–6. https://doi.org/10.1016/j.cub.2022.06.028
Pinheiro J, Bates D, DebRoy S, Sarkar, D e R Core Team (2019) nlme: Linear and nonlinear mixed effects models. R package version 3.1‐137. Retrieved from: https://CRAN.R‐project.org/package=nlme
R Core Team (2021) R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Retrieved from: https://www.R‐project.org/
Rapaport LG (2011) Progressive parenting behavior in wild golden lion tamarins. Behav Ecol 22:745–754. https://doi.org/10.1093/beheco/arr055
Rapaport LG, Brown GR (2008) Social influences on foraging behavior in young nonhuman primates: learning what, where, and how to eat. Evol Anthropol 17:189–201. https://doi.org/10.1002/evan.20180
Rothe H, Darms K, Koenig A, Radespiel U, Juenemann B (1993) Long-term study of infant-carrying behavior in captive common marmosets (Callithrix jacchus): Effect of nonreproductive helpers on the parents’ carrying performance. Int J Primatol 14:79–93. https://doi.org/10.1007/BF02196504
Saito A, Izumi A, Nakamura K (2011) Development of infant common marmosets’ (Callithrix jacchus) preference for their parents over adults from another group. Primates 52:43–50. https://doi.org/10.1007/s10329-010-0205-7
Santos CV, Martins MM (2000) Parental care in the buffy-tufted-ear marmoset (Callithrix aurita) in wild and captive groups. Rev Bras Biol 60:667–672. https://doi.org/10.1590/S0034-71082000000400018
van Schaik CP, Isler K (2012) Life-history evolution in primates. In: Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB. The evolution of primate societies. Chicago and London: The University of Chicago Press, p. 220–244. https://doi.org/10.5167/uzh-71056
Schiel N, Huber L (2006) Social influences on the development of foraging behavior in free-living common marmosets (Callithrix jacchus). Am J Primatol 68:1150–1160. https://doi.org/10.1002/ajp.20284
Schiel N, Souto A (2017) The common marmoset: an overview of its natural history, ecology and behavior. Dev Neurobiol 77:244–262. https://doi.org/10.1002/dneu.22458
Schiel N, Souto A, Huber L, Bezerra BM (2010) Hunting strategies in wild common marmosets are prey and age dependent. Am J Primatol 72:1039–1046. https://doi.org/10.1002/ajp.20860
Šlipogor V, Massen JJM, Schiel N, Souto A, Bugnyar T (2021) Temporal consistency and ecological validity of personality structure in common marmosets (Callithrix jacchus): a unifying field and laboratory approach. Am J Primatol 83:e23229. https://doi.org/10.1002/ajp.23229
Souto A, Bezerra BM, Schiel N, Huber L (2007) Saltatory search in free-living Callithrix jacchus: environmental and age influences. Int J Primatol 28:881–893. https://doi.org/10.1007/s10764-007-9165-1
Stoinski TS, Beck B, Bloomsmith MA, Maple TL (2003). A behavioral comparison of captive-born, reintroduced golden lion tamarins and their wild-born offspring. Anim Behav 140:137–160. https://doi.org/10.1163/156853903321671479
Tardif SD, Harrison ML, Simek MA (1993) Communal infant care in marmosets and tamarins: relation to energetics, ecology, and social organization. In: Rylands AB (ed) Marmosets and tamarins: systematics, behaviour, and ecology. Oxford University Press, New York, pp 220–234
Tardif SD, Smucny DA, Abbott DH, Mansfield K, Schultz-Darken N, Yamamoto ME (2003) Reproduction in captive common marmosets (Callithrix jacchus). Comp Med 53:364–368
Tardif SD, Araújo A, Arruda MF, French JA, Sousa MBC, Yamamoto ME (2008) Reproduction and aging in marmosets and tamarins. Interdisc Top Gerontol 36:29–48. https://doi.org/10.1159/isbn.978-3-8055-8523-1
Terborgh J, Janson CH (1996) The socioecology of primate groups. Annu Rev Ecol Evol Syst 17:111–136. https://doi.org/10.1146/annurev.es.17.110186.000551
Vochteloo JD, Timmermans PJA, Duijghuisen JAH, Vossen JMH (1993) Effects of reducing the mother's radius of action on the development of mother–infant relationships in longtailed macaques. Anim Behav 45:603–12
Wang Y, Fang Q, Gong N (2014) Motor assessment of developing common marmosets. Neurosci Bull 30:387–393. https://doi.org/10.1007/s12264-013-1395-y
Whiten A, van de Waal E (2018) The pervasive role of social learning in primate lifetime development. Behav Ecol Sociobiol 72:80. https://doi.org/10.1007/s00265-018-2489-3
Yamamoto ME, Albuquerque FS, Lopes NA, Ferreira ES (2008) Differential infant carrying in captive and wild common marmosets (Callithrix jacchus). Acta Ethol 11:95–99. https://doi.org/10.1007/s10211-008-0046-1
Yamamoto ME, Box HO (1997) The role of non-reproductive helpers in infant care in captive Callithrix jacchus. Ethol 103:760–771. https://doi.org/10.1111/j.1439-0310.1997.tb00184.x
Yamamoto ME (1993) From dependence to sexual maturity: the behavioural ontogeny of Callitrichidae. In: Rylands AB (ed.) Marmosets and tamarins: systematics, behaviour, and ecology. New York: Oxford University Press. p 235–254. https://doi.org/10.1007/BF02735808
Yamamoto ME (2005) Infant care in Callitrichids: cooperation and competition. Annu Rev Biomed Sci 7:149-160. 10.5016/48
Young JW, Shapiro LJ (2018) Developments in development: What have we learned from primate locomotor ontogeny? Am J Phys Anthropol 165:37–71. https://doi.org/10.1002/ajpa.23388
Ziegler TE, Sosa ME, Colman RJ (2017) Fathering style influences health outcome in common marmoset (Callithrix jacchus) offspring. PLoS ONE 12:e0185695. https://doi.org/10.1371/journal.pone.0185695
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer. https://doi.org/10.1007/978-0-387-87458-6
Acknowledgements
We are very thankful to Bruna M. Bezerra for her assistance in data collection. This study was funded by CAPES (Coordination for the Improvement of Higher Education Personnel) through a PhD scholarship granted to Nicola Schiel and a master’s scholarship for Alexandre Malta.
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The study was funded by the Coordination for the Improvement of Higher Education Personnel (CAPES), through a scholarship granted to NS and AM.
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Conception: AS, CC, MFDF, NS; design of the study: CC, MFDF, NS; sampling: NS; data analysis: CC and MFDF; writing of the article: all authors. All authors have read and approved the final version of the article.
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The present research study was conducted in compliance with the guidelines for the ethical treatment of animals in behavioral research and teaching (Animal Behaviour, 2003; v.65; p 249–255), as well as with the ethical principles for the treatment of non-human primates, established by the American Society of Primatologists.
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Malta, A., Caselli, C., Souto, A. et al. Number of adult females in a group affects infant motor development of a cooperative breeding primate (Callithrix jacchus). Primates 63, 683–689 (2022). https://doi.org/10.1007/s10329-022-01016-x
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DOI: https://doi.org/10.1007/s10329-022-01016-x