The ontogeny of the postcranial skeleton in saddle-back tamarins, Leontocebus fuscicollis and callimicos, Callimico goeldii (Callitrichidae, Primates)

Bernardo Urbani

doi:10.18778/1898-6773.86.2.01

Authors

Bernardo Urbani Behavioral Ecology and Sociobiology Unit, Leibniz Institute for Primate Research/German Primate Center, Göttingen, Germany; Center for Anthropology, Venezuelan Institute for Scientific Research, Caracas, Venezuela https://orcid.org/0000-0001-5392-9751

DOI:

https://doi.org/10.18778/1898-6773.86.2.01

Keywords:

allometry, growth, limb proportions, New World primates, ontogeny, postcranial skeleton

Abstract

Ontogenetic studies of callitrichid anatomy are limited to research focused mainly on postcranial skeleton of adults. The goal of this study is to compare the ontogeny of postcranial skeletal development in Goeldi’s monkeys (i.e., callimico; Callimico goeldii) with the corresponding data on saddle-back tamarins (Leontocebus fuscicollis). The intermembral, humerofemoral, brachial, crural, and ulna-radius indices of callimicos and saddle-back tamarins were calculated and compared among different age classes in order to assess the implications for their ecology and behavior. Ontogenetic trajectories, including age at growth cessation, were also calculated. It is shown that for a given hindlimb length, L. fuscicollis has longer forelimbs compared to C. goeldii, maintaining this proportion across all age classes. A relatively elongated forelimb observed in L. fuscicollis may have a mechanical role in reducing the force of impact when landing on large vertical substrates. In contrast, hindlimb length and pattern of hindlimb development (such as derived features of the ankle that enhance stability) in callimicos appear to play a critical role in propulsion during trunk-to-trunk leaping. These differences may affect niche partitioning, foraging strategies, and substrate use.

Downloads

Download data is not yet available.

References

Beck BB, Anderson D, Ogden J, Rettberg B, Brejla C, Scola R, Warneke M. 1982. Breeding the Goeldi’s monkey Callimico goeldii at Brookfield Zoo, Chicago. International Zoo Ybook, 22, 106–114.
View in Google Scholar

Berles P, Heymann EW, Golcher F, Nyakatura JA. 2022. Leaping and differential habitat use in sympatric tamarins in Amazonian Peru. J Mammal 103:I146–158.
View in Google Scholar

Bicca-Marques JC. 1999. Hand specialization, sympatry, and mixed-species associations in callitrichines. J Human Evol 36:349–378.
View in Google Scholar

Bicca-Marques JC, Calegaro-Marques CC, Pereira de Farias EM, de Oliveira Azevedo MA, Glauco de Araújo Santos F. 1997. Medidas morfométricas de Saguinus imperator imperator e Saguinus fuscicollis weddelli (Callithrichidae: Primates) em ambiente natural. In: Sousa MBC, Menezes AAL, editors. A Primatologia no Brasil – Volume 6. Natal (Brazil): EDUFRN/SBPr. 257–267.
View in Google Scholar

Bicca-Marques JC, Wojciechowski SA, Leigh SR. 1998. Heterochrony and size reduction in the dentition and hands of Callitrichinae. Am J Phys Anthropol Suppl. 26:111.
View in Google Scholar

Carroll JB. 1988. The stability of multifemale groups of Goeldi’s monkey Callimico goeldii in captivity. − Dodo, J. Jersey Wildlife Preserv Trust 25:37–43.
View in Google Scholar

Chiu CH, Hamrick MW. 2002. Evolution and development of the primate limb skeleton. Evol Anthropol 11:94–107.
View in Google Scholar

Cole TM, Falsetti AB, Harrill MS. 1988. Relationships between body size and dental, cranial, and postcranial variables in saddle-backed tamarins. Am J Phys Anthropol 75:197.
View in Google Scholar

Davis LC. 1996. Functional and phylogenetic implications of ankle morphology in Goeldi’s monkey (Callimico goeldii). In: Norconk MA, Rosenberger AL, Garber PA, editors. Adaptive Radiations of Neotropical Primates. New York: Plenum Press. 133–156.
View in Google Scholar

Dettling A, Pryce CR. 1999. Hormonal monitoring of age at sexual maturation in female Goeldi’s Monkeys (Callimico goeldii) in their family groups. Am J Primatol 48:77–83.
View in Google Scholar

Dettling A, Pryce CR. 2002. Functional morphology of the forelimb and long bones in the callitrichidae (Platyrrhini, Primates). Southern Illinois University.
View in Google Scholar

Falsetti AB, Cole TM. III. 1992. Relative growth of the postcranial skeleton in callitrichines. J Human Evol 23:79–92.
View in Google Scholar

Falsetti AB. 1987. Allometric aspects of size and shape variation in the postcranial skeleton of two South American tamarin groups. Am J Physical Anthropol 72:198.
View in Google Scholar

Fleagle JG. 1985. Size and adaptation in primates. In: Jungers WL, editor. Size and scaling in primate biology. New York: Plenum Press. 1–19.
View in Google Scholar

Garber PA, Leigh SR. 2001a. Patterns of positional behavior in mixed-species troops of Callimico goeldii, Saguinus labiatus, and Saguinus fuscicollis in northwestern Brazil. Am J Primatol 54:17–31.
View in Google Scholar

Garber PA, Leigh SR. 2001b. Scaling and size reduction in tamarins. Am J Physical Anthropol, Suppl. 32:68.
View in Google Scholar

Garber PA, Pruetz JD. 1995. Positional behavior in moustached tamarin monkeys: effects of habitat on locomotor variability and locomotor stability. J Human Evol 28:411–426.
View in Google Scholar

Garber PA, Leigh SR. 1997. Ontogenetic variation in small-bodied New World primates: Implications for patterns of reproduction and infant care. Fol Primatol 68:1–22.
View in Google Scholar

Garber PA, Teaford MF. 1986. Body weights in mixed species troops of Saguinus mystax mystax and Saguinus fuscicollis nigrifrons in Amazonian Peru. Am J Physical Anthropol 71:331–336.
View in Google Scholar

Garber PA. 1991. A comparative study of positional behavior in three species of tamarin monkeys. Primates, 32:219–230.
View in Google Scholar

Garber PA. 2007. Primate locomotor behavior and ecology. In: Campbell CJ, Fuentes A, MacKinnon KC, Pager M, Bearder SK, editors. Primates in perspective. Oxford University Press, New York, 543–560.
View in Google Scholar

Garber PA, Sallenave AS, Blomquist GE, Anzenberger G. 2009. A Comparative Study of the Kinematics of Trunk-to-Trunk Leaping in Callimico goeldii, Callithrix jacchus, and Cebuella pygmaea. In: Ford SM, Porter LM, Davis LC, editors. The Smallest Anthropoids. The Marmoset/Callimico Radiation. New York: Springer. 259–277.
View in Google Scholar

Gengozian N. 1969. Marmosets: their potential in experimental medicine. Ann NY Acad Sc, 162:336–362.
View in Google Scholar

Glassman DM. 1984. The relation of long bone diaphyseal length to chronological age in immature saddle-back tamarins, Saguinus fuscicollis. Primates 25:352–361.
View in Google Scholar

Gould SJ. 1977. Ontogeny and Phylogeny. The Belknap Press of Harvard University Press, Cambridge (Mass.), London.
View in Google Scholar

Hanihara T, Natori M. 1988. Numerical analysis of sexual dimorphism in Saguinus dentition. Primates 29:245–254.
View in Google Scholar

Hershkovitz P. 1977. Living New World monkeys. Vol. 1. Chicago: University of Chicago.
View in Google Scholar

Heymann EW, Buchanan-Smith HM. 2000. The behavioural ecology of mixed-species troops of callitrichine primates. Biol Rev 75:169–190.
View in Google Scholar

Heymann EW. 1997. The relationship between body size and mixed-species troops of tamarins (Saguinus spp.). Fol Primatol 68:287–295.
View in Google Scholar

Hofmann MI, Schradin C, Geissmann T. 2007. Radiographic evaluation of neonatal skeletal development in Callimico goeldii reveals closer similarity to Callithrix jacchus than to Saguinus oedipus. Am J Primatol 69:420–433.
View in Google Scholar

Jungers WL. 1985. Body size and scaling of limb proportions in primates. In: Jungers WL, editor. Size and scaling in primate biology. New York: Plenum Press. 345–381.
View in Google Scholar

Jurke MH, Pryce CR. 1994. Parental and infant behaviour during early periods of infant care in Goeldi’s monkey, Callimico goeldii. Animal Beh 48:1095–1112.
View in Google Scholar

Kimura T. 2003. Differentiation between fore-and hindlimb bones and locomotor behaviour in Primates. Fol Primatol 74:17–32.
View in Google Scholar

Leigh SR. 1994. Relations between captive and non-captive weights in anthropoid primates. Zoo Biol 13:21–43.
View in Google Scholar

Leigh SR. 1996a. Evolution of human growth spurts. Am J Phys Anthropol 101:455–474.
View in Google Scholar

Leigh SR. 1996b. Ontogeny and the evolution of body size dimorphism in primates. Anthropol (Brno) 33:17–28.
View in Google Scholar

Leigh SR, Shea BT. 1996. The ontogeny of body size variation in African apes. Am J Phys Anthropol 99:43–65.
View in Google Scholar

Martin RD. 1992. Goeldii and the dwarfs: the evolutionary biology of small New World monkeys. J Human Evol 22:367–393.
View in Google Scholar

Marroig G, Cheverud JM. 2009. Size and Shape in Callimico and Marmoset Skulls: Allometry and Heterochrony in the Morphological Evolution of Small Anthropoids. In: Ford SM, Porter LM, LC Davis, editors. The Smallest Anthropoids. The Marmoset/Callimico Radiation. New York: Springer. 331–353.
View in Google Scholar

Nelson AJ, Thompson JL. 1999. Growth and development in Neandertals and other fossil hominids: implications for the evolution of hominid ontogeny. In: Hoppa RD, Fitzgerald CM, editors. Human growth in the past. Studies from bones and teeth. Cambridge: Cambridge University Press. 88–110.
View in Google Scholar

Neusser M, Stanyon R, Bigoni F, Wienberg J, Mueller S. 2001. Molecular cytotaxonomy of New World monkeys (Platyrrhini) – Comparative analysis of five species by multi-color chromosome painting gives evidence for a classification of Callimico goeldii within the family of Callitrichidae. Cytogen Cell Genet 94:206–215.
View in Google Scholar

Palacios E, Wallace RB, Mollinedo JM, Heymann EW, Shanee S, Calouro AM, del Valle E, Mittermeier RA. 2021. Callimico goeldii. IUCN Red List Threatened Spec 2021: e.T3564A191700340.
View in Google Scholar

Polk JD. 2002. Adaptive and phylogenetic influences on musculoskeletal design in cercopithecine primates. J Exp Biol 205:3399–3412.
View in Google Scholar

Rylands AB, Heymann EW, Alfaro JL, Buckner JC, Roos C, Matauschek C, Jean P, Sampaio R, Mittermeier RA. 2016. Taxonomic review of the New World tamarins (Primates: Callitrichidae). Zool J Linnean Soc 177:1003–1028.
View in Google Scholar

Shea BT. 1995. Ontogenetic scaling and size correction in the comparative study of primate adaptations. Anthropol 33:1–16.
View in Google Scholar

Sodaro V. 2000. A review of hand-reared Goeldi’s monkey Callimico goeldii at Brookfield Zoo 1977–1997. Intl Zoo Ybook, 37:360–366.
View in Google Scholar

Terborgh J. 1983. Five New World primates. A study in comparative ecology. Princeton: Princeton University Press.
View in Google Scholar

Warneke M. 1998. Callimico goeldii, International Studbook. Chicago: Chicago Zoological Society.
View in Google Scholar

Warren RD, Crompton RH. 1998. Diet, body size and the energy costs of locomotion in saltatory primates. Fol Primatol 69:86–100.
View in Google Scholar

Yoneda M. 1984. Comparative studies on vertical separation, foraging behavior and traveling mode of saddle-backed tamarins (Saguinus fuscicollis) and red- chested moustached tamarins (Saguinus labiatus) in northern Bolivia. Primates 25:414–422.
View in Google Scholar