Cranial ontogeny and sexual dimorphism in two new world monkeys: Alouatta caraya (Atelidae) and Cebus apella (Cebidae)

Journal of Morphology

Volumn 272, Issue 6, 2011, Pages 744-757

  Flores, David ^a   Casinos, Adrià ^b  

^a MUSEO ARGENTINO DE CIENCIAS NATURALES BERNARDINO RIVADAVIA   (Argentina)

^b UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Cranial ontogeny; Primates; Sexual dimorphism

Indexed keywords

ALOUATTA; ANIMAL; ARTICLE; CEBUS; FEMALE; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; MALE; SEXUAL DEVELOPMENT; SKULL;

ALOUATTA; ANIMALS; CEBUS; FEMALE; MALE; SEX CHARACTERISTICS; SKULL;

ALOUATTA; ALOUATTA CARAYA; CEBIDAE; CEBUS; CEBUS APELLA; PLATYRRHINI; PRIMATES;

EID: 79955659483     PISSN: 03622525     EISSN: 10974687     Source Type: Journal    
DOI: 10.1002/jmor.10947     Document Type: Article

References (68)

1. Bezanson MF. 2005. Leap, bridge, or ride? Ontogenetic influences on positional behavior in Cebus and Alouatta. In: Estrada P, Garber A, Pavelka MSM, Luecke L, editors. New Perspectives in the Study of Mesoamerican Primates: Distribution, Ecology, Behavior, and Conservation. New York: Springer. pp 333-348.
2. Blanco MB, Godfrey LR. 2006. Craniofacial sexual dimorphismin Alouatta palliata, the mantled howling monkey. J Zool 270: 268-276.
3. Cole TM. 1992. Postnatal heterochrony of the masticatory apparatus in Cebus apella and Cebus albifrons. J Hum Evol 23: 253-282.
4. Corner BD, Richtsmeier JT. 1991. Morphometric analysis of craniofacial growth in Cebus apella. Am J Phys Anthropol 84: 323-342.
5. Crockett CM. 1987. Diet, dimorphism and demography: Perspectives from howlers to hominids. In: Kinzev WG, editor. The Evolution of Human Behavior: Primate Models. New York: State University of New York Press. pp 115-135.
6. Emerson SB, Bramble DM. 1993. Scaling, allometry and skull design. In: Hanken J, Hall BK, editors. The Skull. Chicago: The University of Chicago Press. pp 384-416.
7. Flores D, Giannini N, Abdala F. 2006. Comparative postnatal ontogeny of the skull in the Australidelphian Metatherian Dasyurus albopunctatus (Marsupialia: Dasyuromorpha: Dasyuridae). J Morphol 267: 426-440.
8. Flores DA, Abdala F, Giannini NP. 2010. Cranial ontogeny of Caluromys philander (Didelphidae, Caluromyinae): A qualitative and quantitative approach. J Mammal 91: 539-550.
9. Galliari C. 1985. Dental eruption in captive-born Cebus apella: From birth to 30 months old. Primates 26: 506-510.
10. Garber PA, Leigh SR. 1997. Ontogenetic variation in small-bodied New World primates: Implications for patterns of reproduction and infant care. Folia Primatol 68: 1-22.
11. Gavan JA, Swinldler DR. 1966. Growth rates and phylogeny in primates. Am J Phys Anthropol 24: 181-190.
12. Giannini N, Abdala F, Flores D. 2004. Comparative postnatal ontogeny in the skull of Dromiciops gliroides (Marsupialia: Microbiotheriidae). Am Mus Novit 3640: 1-17.
13. Giannini N, Segura V, Giannini MI, Flores D. 2010. A quantitative approach to the cranial ontogeny of the puma. Mamm Biol 75: 547-554.
14. Glander KE. 1980. Reproduction and population growth in free-ranging mantled howling monkeys. Am J Phys Anthropol 53: 25-36.
15. Gould SJ. 1977. Ontogeny and Phylogeny. Cambridge: Belknap Press. 501p.
16. Hartwig HC. 1995. Effect of life history on the squirrel monkey (Platyrrhini, Saimiri) cranium. Am J Phys Anthropol 97: 435-449.
17. Huxley JS. 1932. Problems of Relative Growth. London: Methuen. 302 p.
18. Janson CH, Boinski S. 1992. Morphological and behavioral adaptations for foraging in generalist Primates: The case of the Cebines. Am J Phys Anthropol 88: 483-498.
19. Jarman P. 1983. Mating system and sexual dimorphism in large terrestrial mammalian herbivores. Biol Rev 58: 485-520.
20. Jolicouer P. 1963a. The multivariate generalization of the allometry equation. Biometrics 19: 497-499.
21. Jolicouer P. 1963b. The degree of generality of robustness in Martes americana. Growth 27: 1-27.
22. Jones AL, DeGusta D, Turner SP, Campbell CJ, Milton K. 2000. Craniometric variation in a population of mantled howler monkeys (Alouatta palliata): Evidence of size selection in females and growth in dentally mature males. Am J Phys Anthropol 113: 411-434.
23. Jungers WL, German RZ. 1981. Ontogenetic and interspecific skeletal allometry in nonhuman primates: Bivariate versus multivariate analysis. Am J Phys Anthropol 55: 195-202.
24. Klingenberg CP. 1998. Heterochrony and allometry: The analysis of evolutionary change in ontogeny. Biol Rev 73: 79-123.
25. Laird AK. 1965. Dynamics of relative growth. Growth 29: 249-263.
26. Lande R. 1979. Quantitative genetic analysis of multivariate evolution, applied to brain: Body size allometry. Evolution 33: 402-416.
27. Leigh SR. 1992. Patterns of variation in the ontogeny of primate body size dimorphism. J Hum Evol 23: 27-50.
28. Leigh SR. 2004. Brain growth, life history, and cognition in primate and human evolution. Am J Primatol 62: 139-164.
29. Lumer H, Schultz AH. 1947. Relative growth of the limb segments and tail in Ateles geoffroyi and Cebus capucinus. Hum Biol 19: 53-67.
30. Manly BFJ. 1997. Randomization, Bootstrap, and Monte Carlo Methods in Biology, 2nd ed. New York: Chapman & Hall. 399 p.
31. Marroig G. 2007. When size makes a difference: Allometry, life-history and morphological evolution of capuchins (Cebus) and squirrels (Saimiri) monkeys (Cebinae, Platyrrhini). BMC Evol Biol 7: 20.
32. Martin RD. 1983. Human Brain Evolution in an Ecological Context (52nd James Arthur Lecture on the Evolution of the Human Brain). New York: American Museum of Natural History. 58 p.
33. Martin RD. 1996. Scaling of the mammalian brain: The maternal energy hypothesis. News Physiol Sci 11: 149-156.
34. Masterson TJ. 1997. Sexual dimorphism and interspecific cranial form in two Capuchin species: Cebus albifrons and C. apella. Am J Phys Anthropol 104: 487-511.
35. Milton K. 1980. The Foraging Strategy of Howler Monkeys: A Study in Primate Economics. New York: Columbia University Press. 165 p.
36. O'Higgins P, Moore WJ, Johnson DR, McAndrew TJ, Flinn RM. 1990. The variability of patterns of sexual dimorphism in the primate skull. Experientia 46: 670-672.
37. O'Higgins P, Chadfield P, Jones N. 2001. Facial growth and the ontogeny of morphological variation within and between the primates Cebus apella and Cercocebus torquatus. J Zool 254: 337-357.
38. Plavcan JM. 1993. Canine size and shape in male anthropoid primates. Am J Phys Anthropol 92: 201-216.
39. Plavcan JM. 2001. Sexual dimorphism in primate evolution. Yearb Phys Anthropol 44: 25-53.
40. Plavcan JM. 2002. Taxonomic variation in the patterns of craniofacial dimorphism in primates. J Hum Evol 42: 579-608.
41. Plavcan JM, Gomez AM. 1993. Dental scaling in Callitrichinae. Int J Primatol 14: 177-192.
42. Plavcan JM, van Schaik CP. 1992. Intrasexual competition and canine dimorphism in anthropoid primates. Am J Phys Anthropol 87: 461-477.
43. Plavcan JM, van Schaik CP. 1997. Intrasexual competition and body weight dimorphism in anthropoid primates. Am J Phys Anthropol 103: 37-68.
44. Quenouille MH. 1956. Notes on bias in estimation. Biometrika 43: 353-360.
45. R Development Core Team. 2004. R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Available at:
46. Ralls K. 1977. Sexual dimorphism in mammals: Avian models and unanswered questions. Am Nat 111: 918-938.
47. Ravosa MJ. 1991. The ontogeny of cranial sexual dimorphism in two Old World monkeys: Macaca fascicularis (Cercopithecinae) and Nasalis larvatus (Colobinae). Int J Primatol 12: 403-426.
48. Ravosa MJ. 1992. Allometry and heterochrony in extant and extinct Malagasy primates. J Hum Evol 23: 197-217.
49. Ravosa MJ. 2007. Cranial ontogeny, diet, and ecogeographic variation in African Lorises. Am J Primatol 69: 59-73.
50. Ravosa MJ, Ross CF. 1994. Craniodental allometry and heterochrony in two howler monkeys: Alouatta seniculus and A. palliata. Am J Primatol 33: 277-299.
51. Riska B, Atchley WR. 1985. Genetics of growth predicts patterns of brain-size evolution. Science 229: 668-671.
52. Schaefer K, Mitteroecker P, Gunz P, Bernhard B, Bookstein FL. 2004. Craniofacial sexual dimorphism patterns and allometry among extant hominids. Ann Anat 186: 471-478.
53. Schultz AH. 1960. Age changes and variability in skulls and teeth of the central American monkeys Alouatta, Cebus, and Ateles. Proc Zool Soc Lond 133: 337-390.
54. Schultz AH. 1962. Metric age changes and sex differences in primate skulls. J Morphol Anthropol 52: 239-255.
55. Shea BT. 1983. Allometry and heterochrony in the African apes. Am J Phys Anthropol 62: 275-289.
56. Shea BT. 1986. Ontogenetic approaches to sexual dimorphism in anthropoids. Hum Evol 1: 97-110.
57. Shea BT. 1992. Ontogenetic scaling of skeletal proportions in the talapoin monkeys. J Hum Evol 23: 283-307.
58. Shea BT, Gomez AM. 1998. Tooth scaling and evolutionary dwarfism: An investigation of allometry in human pygmies. Am J Phys Anthropol 77: 117-132.
59. Shea BT, Hammer RE, Brinster RL. 1987. Growth allometry of the organs in giant transgenic mice. Endocrinology 121: 1924-1930.
60. Sokal RR, Rohlf FJ. 1995. Biometry, 3rd ed. New York: W.H. Freeman. 887p.
61. Stahl WR, Malinow MR, Maruffo CA, Locker Pope B, Depaoli R. 1968. Growth and age estimation of howler monkeys. Biology of the howler monkey. Bibl Primatol 7: 59-80.
62. Tanner JM. 1988. Human growth and constitution. In: Harrison GA, Tanner JM, Pilbeam DR, Baker PT, editors. Human Biology, 3rd ed. Oxford: Oxford University Press. pp 339-435.
63. Terborgh J. 1983. Five New World Primates: A Study in Comparative Ecology. Princeton: Princeton University Press. 260p.
64. Thorington RW. 1967. Feeding and activity of Cebus and Saimiri in a Colombian forest. In: Stark D, Schneider L, Kuhn HJ, editors. Progress in Primatology. Stuttgart: Gustav Fisher. pp 180-184.
65. Thorington RW, Rudran R, Mack D. 1979. Sexual dimorphism of Alouatta seniculus and observations on capture techniques. In: Eisenberg JF, editor. Vertebrate Ecology in the Northern Neotropics. Washington, DC: Smithsonian Institution Press. pp 97-106.
66. Thorington RW, Ruiz JC, Eisenberg JF. 1984. A study of a black howling monkey (Alouatta caraya) population in Northern Argentina. Am J Primatol 6: 357-366.
67. Wayne RK. 1986. Cranial morphology of domestic and wild canids: The influence of development on morphological change. Evolution 40: 243-261.
68. Wiley RH. 1974. Evolution of social organization and life history patterns among grouse. Q Rev Biol 49: 201-226.