Stable nitrogen isotope analysis of dentine serial sections elucidate sex differences in weaning patterns of wild chimpanzees (Pan troglodytes)

American Journal of Physical Anthropology

Volumn 153, Issue 4, 2014, Pages 635-642

  Fahy, Geraldine E ^a   Richards, Michael P ^a,b   Fuller, Benjamin T ^a,c   Deschner, Tobias ^a   Hublin, Jean Jacques ^a   Boesch, Christophe ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

human evolution; lactation; maternal investment; primatology

Indexed keywords

NITROGEN;

ANIMAL EXPERIMENT; ARTICLE; DECIDUOUS TOOTH; DENTIN; DENTITION; EVOLUTION; FEMALE; ISOTOPE ANALYSIS; MALE; MOLAR TOOTH; NONHUMAN; PAN TROGLODYTES; SEX DIFFERENCE; TOOTH DEVELOPMENT; TOOTH ROOT; WEANING;

HUMAN EVOLUTION; LACTATION; MATERNAL INVESTMENT; PRIMATOLOGY;

ANIMALS; ANTHROPOLOGY, PHYSICAL; BIOLOGICAL EVOLUTION; DENTIN; FEMALE; MALE; NITROGEN ISOTOPES; PAN TROGLODYTES; SEX CHARACTERISTICS; WEANING;

EID: 84895923018     PISSN: 00029483     EISSN: 10968644     Source Type: Journal    
DOI: 10.1002/ajpa.22464     Document Type: Article

References (72)

1. AlQuahtani SJ, Hector MP, Liversidge HM,. 2010. Brief communication: the London atlas of human tooth development and eruption. Am J Phys Anthropol 142: 481-490.
2. Anemone RL, Mooney MP, Siegel MI,. 1996. Longitudinal study of dental development in Chimpanzees of known chronological age: implications for understanding the age at death of Plio-Pleistocene Hominids. Am J Phys Anthropl 99: 119-133.
3. Anemone RL, Watts ES, Swindler DR,. 1991. Dental development of known age chimpanzees, Pan troglodytes (Primates, Pongidae). Am J Phys Anthropl 86: 229-241.
4. Baayen RH,. 2008. Analyzing linguistic data. Cambridge, UK: Cambridge University Press.
5. Baayen RH,. 2011. languageR: data sets and functions with "analyzing linguistic data: a practical introduction to statistics." R package version 1.4.
6. Bates D, Maechler M, Bolker B,. 2012. lme4: linear mixed-effects models using S4classes. R package version 0. 999999-0.
7. Boesch C,. 1997. Evidence for dominant wild female chimpanzees investing more in sons. Anim Behav 54: 811-815.
8. Boesch C, Boesch-Achermann H,. 2000. The chimpanzees of the Taï forest: behavioural ecology and evolution. Oxford, UK: Oxford University Press.
9. Boesch C, Kohou G, Néné H, Vigilant L,. 2006. Male competition and paternity in wild chimpanzees of the Täi forest. Am J Phys Anthropol 130: 103-115.
10. Bogin B,. 1999. Patterns of human growth. Cambridge: Cambridge University Press.
11. Burt NM, Garvie-Lok S,. 2013. A new method of dentine microsampling of deciduous teeth for stable isotope ratio analysis. J Arch Sci 40: 3854-3864.
12. Clark CB,. 1977. A preliminary report on weaning among chimpanzees of the Gombe National Park, Tanzania. In:, Chevalier-Skolnikoff S, Poirier FE, editors. Primate bio-social development: biological, social, and ecological determinants. New York: Garland Publishing.
13. Clark AB,. 1978. Sex ratio and local resource competition in a prosimian primate. Science 201: 163-165.
14. Clutton-Brock TH, Albon SD, Guinness FE,. 1986. Great expectations: dominance, breeding success and offspring sex ratios in red deer. Anim Behav 34: 460-471.
15. Clutton-Brock TH, Gaynor D, Kansky R, MacColl ADC, McIlrath G, Chadwick P, Brotherton PNM, O'riain JM, Manser M, Skinner JD,. 1988. Costs of cooperative behaviour in suricates (Suricata suricatta). Proc R Soc Lond Ser B Biol Sci 265: 185-190.
16. Dean MC,. 2010. Retrieving chronological age from dental remains of early fossil hominins to reconstruct human growth in the past. Philos Trans R Soc B Biol Sci 365: 3397-3410.
17. Dean MC, Cole TJ,. 2013. Human life history evolution explains dissociation between the timing of tooth eruption and peak rates of root growth. PloS One 8: 1-14.
18. Dean MC, Vesey P,. 2008. Preliminary observations on increasing root length during the eruptive phase of tooth development in modern humans and great apes. J Hum Evol 54: 258-271.
19. Demirjian A,. 1986. Dentition. In:, Faulkner F, Tanner JM, editors. Human growth: a comprehensive treatise. New York: Plenum Press. p 269-298.
20. Eerkens JW, Berget AG, Bartelink EJ,. 2011. Estimating weaning and early childhood diet from serial micro-samples of dentin collagen. J Arch Sci 38: 3101-3111.
21. Emery Thompson M, Muller MN, Wrangham RW,. 2012. The energetics of lactation and the return to fecundity in wild chimpanzees. Behav Ecol 23: 1234-1241.
22. Fahy GE, Richards M, Riedel J, Hublin JJ, Boesch C,. 2013. Stable isotope evidence of meat eating and hunting specialization in adult male chimpanzees. Proc Natl Acad Sci USA 110: 5829-5833.
23. Field AP,. 2005. Discovering statistics using SPSS, 2nd ed. London: Sage.
24. Fogel M, Tuross N, Owsley D,. 1989. Nitrogen isotope tracers of human lactation in modern and archaeological populations. Annual report of the Director, Geophysical Laboratory (1988-1989). 2150, 111e117.
25. Forstmeier W, Schielzeth H,. 2011. Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner's curse. Behav Ecol Sociobiol 65: 47-55.
26. Fox J, Weisberg S,. 2011. An R companion to applied regression, 2nd ed. Thousand Oaks: Sage.
27. Fränkl AC, Kohou GN, Boesch C,. 1996. Sex-specific maternal investment in wild chimpanzees (Pan troglodytes verus). [Unpublished] Diploma thesis, University of Basel, Switzerland.
28. Fuller BT, Fuller JL, Harris DA, Hedges RE,. 2006. Detection of breastfeeding and weaning in modern human infants with carbon and nitrogen stable isotope ratios. Am J Phys Anthropl 129: 279-293.
29. Fuller BT, Richards MP, Mays SA,. 2003. Stable carbon and nitrogen isotope variations in tooth dentine serial sections from Wharram Percy. J Arch Sci 30: 1673-1684.
30. Galdikas BMF, Wood JW,. 1990. Birth spacing patterns in humans and apes. Am J Phys Anthropol 83: 185-191.
31. Gavan JA,. 1953. Growth and development of the chimpanzee: a longitudinal and comparative study. Hum Biol 25: 93.
32. Gleiser I, Hunt EE,. 1955. The permanent mandibular first molar: its calcification, eruption and decay. Am J Phys Anthropl 13: 253-284.
33. Goodall J,. 1986. The chimpanzees of Gombe: patterns of behavior. Cambridge, MA, USA: Belknap Press of Harvard University Press.
34. Goodall J,. 1989. Gombe: highlights and current research. In:, Heltne P, Marquardt L, editors. Understanding chimpanzees. Cambridge: Harvard University Press. p 5e17.
35. Gray SJ,. 1996. Infant care and feeding. In:, Little MA, Leslie PW, editors. Nomadic Turkana: biobehavior and ecology of a Pastoralist society. Oxford, England: Oxford University Press.
36. Herring DA, Saunders SR, Katzenberg MA,. 1998. Investigating the weaning process in past populations. Am J Phys Anthropol 105: 425-439.
37. Hiraiwa M,. 1981. Maternal and alloparental care in a troop of free-ranging Japanese monkeys. Primates 22: 309-329.
38. Hiraiwa-Hasegawa M,. 1990. Maternal investment before weaning. In:, Nishida T, editor. The chimpanzees of the Manhale Mountains: sexual and life history strategies. Tokyo: The University of Tokyo Press. p 257-266.
39. Horvat J, Kraemer HC,. 1982. Behavioral changes during weaning in captive chimpanzees. Primates 23: 488-499.
40. Humphrey LT,. 2010. Weaning behavior in human evolution. Semin Cell Dev Biol 21: 453-461.
41. Kachel AF, Premo LS, Hublin JJ,. 2011. Grandmothering and natural selection revisited. Proc R Soc B Biol Sci 278: 1939-1941.
42. Katzenberg MA, Herring DA, Saunders SR,. 1996. Weaning and infant mortality: evaluating the skeletal evidence. Yrb Phys Anthropol 39: 177e199.
43. Kennedy GE,. 2005. From the ape's dilemma to the weanling's dilemma: early weaning and its evolutionary context. J Hum Evol 48: 123-145.
44. Kimura T, Hamada Y,. 1996. Growth of wild and laboratory born chimpanzees. Primates 37: 237e251.
45. Kuykendall KL, Mahoney CJ, Conroy GC,. 1992. Probit and survival analysis of tooth emergence ages in a mixed-longitudinal sample of chimpanzees (Pan troglodytes). Am J Phys Anthropol 89: 379-399.
46. Lee PC,. 1996. The meanings of weaning: growth, lactation, and life history. Evol. Anthropol. Issues News Rev 5: 87-98.
47. Marlowe FW,. 2001., Male contribution to diet and female reproductive success among foragers, Curr Anthropol 42: 755-760.
48. Matsuzawa T, Sakura O, Kimura T, Hamada Y, Sugiyama Y,. 1990. Case report on the death of a wild chimpanzee (Pan troglodytes verus). Primates 31: 635e641.
49. McGrew WC, Marchant LF, Nishida TE,. 1996. Great ape societies. Cambridge, United Kingdom: Cambridge University Press.
50. Nakamura M, Hayaki H, Hosaka K, Itoh N, Zamma K,. 2013. Orphaned male Chimpanzees die young even after weaning. Am J Phys Anthropol 153:139-143.
51. Nishida T, Hamai M, Hasegawa T, Hiraiwa-Hasegawa M, Hosaka K, Hunt KD, Itoh N, et al. 2003. Demography, female life history, and reproductive profiles among the chimpanzees of Mahale. Am J Primatol 59: 99-121.
52. Nishida T, Hasegawa T, Hayaki H, Takahata Y, Uehara S,. 1992. Meat-sharing as a coalition strategy by an alpha male chimpanzee. Top Primatol 1: 159-174.
53. Nowak RM,. 1999. Walker's mammals of the world. Baltimore, USA: Johns Hopkins University Press.
54. Oftedal OT, Boness DJ, Tedman RA,. 1987. The behavior, physiology and anatomy of lactation in the Pinnipedia. Curr Mammal 1: 175-245.
55. Reitsema LJ,. 2012. Introducing fecal stable isotope analysis in primate weaning studies. Am J Primatol 74: 926-939.
56. Richards MP, Mays S, Fuller BT,. 2002. Stable carbon and nitrogen isotope values of bone and teeth reflect weaning age at the Medieval Wharram Percy site, Yorkshire, UK. Am J Phys Anthropl 119: 205-210.
57. Schoeller DA,. 1999. Isotope fractionation: why aren't we what we eat? J Archaeol Sci 26: 667-673.
58. Sealy JC, Armstrong R, Schrire C,. 1995. Beyond lifetime averages: tracing life histories through isotopic analysis of different calcified tissues. Antiquity 69: 290-300.
59. Silk JB,. 1983. Local resource competition and facultative adjustment of sex ratios in relation to competitive abilities. Am Nat 121: 56-66.
60. Silk JB,. 1988. Social mechanisms of population regulation in a captive group of bonnet macaques (Macaca radiata). Am J Primatol 14: 111-124.
61. Smith H, Boesch C,. 2011. Mortality and the magnitude of the "wild effect" in chimpanzee tooth emergence. J Hum Evol 60: 34-46.
62. Stack MV,. 1967. Vertical growth rates of deciduous teeth. J Dent Res 46 (Supp 1): 879-882.
63. Stearns SC,. 1989. The evolutionary significance of phenotypic plasticity. Bioscience 39: 436-445.
64. Sugiyama Y,. 1994. Age-specific birth rate and lifetime reproductive success of chimpanzees at Bossou, Guinea. Am J Primatol 32: 311e318.
65. Trivers RL,. 1972. Parental investment and sexual selection. In:, Campbell B, editor. Sexual selection and the descent of man, 1871-1971. Chicago: Aldine-Atherton. p 136-179.
66. Trivers RL,. 1974. Parent-offspring conflict. Am Zool 14: 249-264.
67. Trivers RL, Willard DE,. 1973. Natural selection of parental ability to vary the sex ratio of offspring. Science 179: 90-92.
68. van Noordwijk MA, van Schaik CP,. 2005. Development of ecological competence in Sumatran orangutans. Am J Phys Anthropol 127: 79-94.
69. Vandeleest JJ, Mendoza SP, Capitano JP,. 2012. Birth timing and the mother-infant relationship predict variation in infant behavior and physiology. Dev Psychobiol 55:829-837.
70. Vigilant L, Hofreiter M, Siedel H, Boesch C,. 2001. Paternity and relatedness in wild chimpanzee communities. Proc Natl Acad Sci USA 98: 12890-12895.
71. Wright LE, Schwarcz HP,. 1999. Correspondence between stable carbon, oxygen and nitrogen isotopes in human tooth enamel and dentine: Infant diets at Kaminaljuyu. J Arch Sci 26: 1159-1170.
72. Zihlman AL, Bolter DR, Boesch C,. 2007. Skeletal and dental growth and development in chimpanzees of the Taï National Park, Côte D'Ivoire. J Zool 273: 63-73.