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Comparisons of Limb Structural Properties in Free-ranging Chimpanzees from Kibale, Gombe, Mahale, and Taï Communities

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Primate Locomotion

Abstract

Structural characteristics of limb bones provide insight into how an animal dynamically loads its limbs during life. Cause-and-effect relationships between loading and the osteogenic response it elicits are complex. In spite of such complexities, cross-sectional geometric properties can be useful indicators of locomotor repertoires. Typical comparisons use primates that are distinguished by broad habitual locomotor differences, usually with samples garnered from several museum collections. Intraspecific variability is difficult to investigate in such samples because knowledge of their behavior or life histories, which are tools for interpreting intraspecific variability, is limited. Clearly, intraspecific variation both in morphology and behavior/life history exists. Here we expand an ongoing effort toward understanding intraspecific variation in limb structural properties by comparing free-ranging chimpanzees that have associated behavioral and life history data. Humeral and femoral data from 11 adult chimpanzees (Pan troglodytes) of Kibale National Park (Uganda) are compared to 29 adult chimpanzees from Gombe (Tanzania), Mahale Mountains (Tanzania), and Taï Forest (Côte d’Ivoire) National Park communities. Overall, limb structural morphology of Kibale chimpanzees most resembles limb structural morphology of Mahale chimpanzees. Shape ratios and percentage cortical areas of Kibale chimpanzees are most similar to non-Gombe chimpanzees, while Kibale structural properties, e.g., maximum rigidity, are most similar to non-Taï structural properties. Even after adding Kibale females, Taï females continue to stand out from females in other communities.

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Abbreviations

ANOVA:

analysis of variance

AP:

anteroposterior

BM:

body mass

%CA:

percentage cortical area of cross sections

CA:

cortical area

F:

femur

FMSID:

supero-inferior diameter of the femoral head

G:

Gombe

H:

humerus

HHMD:

maximum diameter of the humeral head

I max /I min :

maximum/minimum rigidity (principal moments of area) I x /I y second moments of area about anatomical planes

K:

Kibale

KS:

Kolmogorov-Smirnov

L:

bone length

LSD:

least significant difference

M:

Mahale

ML:

mediolateral

ROI:

region of interest

sI max :

normalized I max (maximal rigidity)

SD:

standard deviation

T:

Taï

TA:

total cross-sectional area

VOI:

volume of interest

References

  • Becquet C, Patterson N, Stone AC, Przeworksi M, Reich D (2007) Genetic structure of chimpanzee populations. PLoS Genetics 3, e66.

    Google Scholar 

  • Bhatavadekar NB, Daegling DJ, Rapoff AJ (2006) Application of an image-based weighted measure of skeletal loading stiffness to great ape mandibles. Am J Phys Anthropol 131:243–251.

    Article  PubMed  Google Scholar 

  • Biewener AA (2003) Animal Locomotion. Oxford University Press, Oxford.

    Google Scholar 

  • Boesch C, Boesch-Achermann H (2000) The Chimpanzees of the Taï Forest – Behavioural Ecology and Evolution. Oxford University Press, New York.

    Google Scholar 

  • Burr DB, Piotrowski G, Martin RB, Cook PN (1982) Femoral mechanics in the lesser bushbaby (Galago senegalensis): structural adaptations to leaping in primates. Anat Rec 202:419–429.

    Article  PubMed  CAS  Google Scholar 

  • Burr DB, Ruff CB, Johnson C (1989) Structural adaptations of the femur and humerus to arboreal and terrestrial environments in three species of macaque. Am J Phys Anthropol 79:357–367.

    Article  PubMed  CAS  Google Scholar 

  • Burr DB, Milgrom C, Fyhrie D, Forwood M, Nyska M, Finestone A, Hoshaw S, Saiag E, Simkin A (1996) In vivo measurement of human tibial strains during vigorous activity. Bone 18:405–410.

    Article  PubMed  CAS  Google Scholar 

  • Carlson KJ (2002) Shape and material properties of African pongid femora and humeri: their relationship to observed positional behaviors. PhD dissertation, Indiana University.

    Google Scholar 

  • Carlson KJ (2005) Investigating the form-function interface in African apes – relationships between principal moments of area and positional behaviors in femoral and humeral diaphyses. Am J Phys Anthropol 127:312–334.

    Article  PubMed  Google Scholar 

  • Carlson KJ, Demes B, Franz T (2005) Mediolateral forces associated with quadrupedal gaits of lemurids. J Zool (Lond) 266:261–273.

    Article  Google Scholar 

  • Carlson KJ, Doran-Sheehy DM, Hunt KD, Nishida T, Yamanaka A, Boesch C (2006) Locomotor behavior and long bone morphology in individual free-ranging chimpanzees. J Hum Evol 50:394–404.

    Article  PubMed  Google Scholar 

  • Carlson KJ, Grine FE, Pearson OM (2007) Robusticity and sexual dimorphism in the postcranium of modern hunter-gatherers from Australia. Am J Phys Anthropol 134:9–23.

    Article  PubMed  Google Scholar 

  • Carlson KJ, Judex S (2007) Increased non-linear locomotion alters diaphyseal bone shape. J Exp Biol 210:3117–3125.

    Article  PubMed  Google Scholar 

  • Carlson KJ, Sumner DR, Morbeck ME, Nishida T, Yamanaka A, Boesch C (2008) The role of non-behavioral factors in adjusting long bone diaphyseal structure in free-ranging chimpanzees. Int J Primatol 29:1401–1420.

    Article  PubMed  Google Scholar 

  • Carter ML, Pontzer H, Wrangham RW, Kerbis Peterhans J (2008) Skeletal pathology in Pan troglodytes schweinfurthii in Kibale National Park, Uganda. Am J Phys Anthropol 135:389–403.

    Article  Google Scholar 

  • Chapman CA, Chapman LJ, Wrangham R, Isabirye-Basuta G, Ben-David K (1997) Spatial and temporal variability in the structure of a tropical forest Afr J Ecol 35:287–302.

    Article  Google Scholar 

  • Currey JD (2002) Bones: Structure and Mechanics. Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Demes B, Jungers WL (1989) Functional differentiation of long bones in Lorises. Folia Primatol 52:58–69.

    Article  PubMed  CAS  Google Scholar 

  • Demes B, Jungers WL, Selpien K (1991) Body size, locomotion, and long bone cross-sectional geometry in Indriid primates. Am J Phys Anthropol 86:537–547.

    Article  PubMed  CAS  Google Scholar 

  • Demes B, Jungers WL (1993) Long bone cross-sectional dimensions, locomotor adaptations and body size in prosimian primates. J Hum Evol 25:57–74.

    Article  Google Scholar 

  • Demes B, Stern JT, Hausman MR, Larson SG, McLeod KJ, Rubin CT (1998) Patterns of strain in the Macaque ulna during functional activity. Am J Phys Anthropol 106:87–100.

    Article  PubMed  CAS  Google Scholar 

  • Demes B, Qin Y, Stern JT Jr, Larson SG, Rubin CT (2001) Patterns of strain in the Macaque tibia during functional activity. Am J Phys Anthropol 116:257–265.

    Article  PubMed  CAS  Google Scholar 

  • Demes B, Carlson KJ, Franz TM (2006) Cutting corners: the dynamics of turning behaviors in two primate species. J Exp Biol 209:927–937.

    Article  PubMed  Google Scholar 

  • Demes B, Carlson KJ (2009) Locomotor variation and bending regimes of capuchin limb bones. Am J Phys Anthropol 139:558–571.

    Google Scholar 

  • Devlin MJ, Lieberman DE (2007) Variation in estradiol level affects cortical bone growth in response to mechanical loading in sheep. J Exp Biol 210:602–613.

    Article  PubMed  CAS  Google Scholar 

  • Dial R, Bloodworth B, Lee A, Boyne P, Heys J (2004) The distribution of free space and its relation to canopy composition at six forest sites. Forest Sci 50:312–325.

    Google Scholar 

  • Gentry AH, Emmons LH (1987) Geographical variation in fertility, phenology, and composition of the understory of Neotropical forests. Biotropica 19:216–227.

    Article  Google Scholar 

  • Goodall J (1986) The Chimpanzees of Gombe. The Belknap Press of Harvard University Press, Cambridge, MA.

    Google Scholar 

  • Green DJ, Gordon AD, Richmond BG (2007) Limb-size proportions in Australopithecus afarensis and Australopithecus africanus. J Hum Evol 52:187–200.

    Article  PubMed  Google Scholar 

  • Griffin NL (2008) Bone architecture of the hominin second proximal pedal phalanx: a preliminary investigation. J Hum Evol 54:162–168.

    Article  PubMed  Google Scholar 

  • Gunji H, Shimizu D, Hosaka M, Huffman A, Kawanaka K, Matsumoto-Oda A, Nishida T (1998) Notes on some chimpanzee skeletons from the Mahale Mountains National Park, Tanzania. In: Nishida T (ed), Resource Use Patterns and Social Structure Among Chimpanzees. Nisshindo Printer, Kyoto, pp 113–130.

    Google Scholar 

  • Guy F, Brunet M, Schmittbuhl M, Viriot L (2003) New approaches in hominoid taxonomy: ­morphometrics. Am J Phys Anthropol 121:198–218.

    Article  PubMed  Google Scholar 

  • Haeusler M, McHenry HM (2007) Evolutionary reversals of limb proportions in early hominids? Evidence from KNM-ER 3735 (Homo habilis). J Hum Evol 53:383–405.

    Article  PubMed  Google Scholar 

  • Harms KE, Powers JS, Montgomery RA (2004) Variation in small sapling density, understory cover, and resource availability in four Neotropical forests. Biotropica 36:40–51.

    Google Scholar 

  • Holt B (2003) Mobility in Upper Paleolithic and Mesolithic Europe: evidence from the lower limb. Am J Phys Anthropol 122:200–215.

    Article  PubMed  Google Scholar 

  • Hunt KD (1992) Positional behavior of Pan troglodytes in the Mahale Mountains and Gombe Stream National Parks, Tanzania. Am J Phys Anthropol 87:83–105.

    Article  CAS  Google Scholar 

  • Hunt KD, McGrew WC (2002) Chimpanzees in the dry habitats of Assirik, Senegal and Semliki Wildlife Reserve, Uganda. In: Boesch C, Hohmann G, Marchant LF (eds), Behavioural Diversity in Chimpanzees and Bonobos. Cambridge University Press, Cambridge, pp 35–51.

    Chapter  Google Scholar 

  • Jungers WL, Burr DB, Cole MS (1998) Body size and scaling of long bone geometry, bone strength, and positional behavior in cercopithecoid primates. In: Strasser E, Fleagle J, Rosenberger A, McHenry HM (eds), Primate Locomotion – Recent Advances. Plenum Press, New York, pp 309–330.

    Google Scholar 

  • Lieberman DE, Polk JD, Demes B (2004) Predicting long bone loading from cross-sectional geometry. Am J Phys Anthropol 123:156–171.

    Article  PubMed  Google Scholar 

  • Lockwood CA, Kimbel WH, Lynch JM (2004) Morphometrics and hominoid phylogeny: support for a chimpanzee-human clade and differentiation among great ape subspecies. PNAS 101:4356–4360.

    Article  PubMed  CAS  Google Scholar 

  • Madar SI, Rose MD, Kelley J, MacLatchy L, Pilbeam D (2002) New Sivapithecus postcranial specimens from the Siwaliks of Pakistan. J Hum Evol 42:705–752.

    Article  PubMed  Google Scholar 

  • Marchi D, Sparacello VS, Holt BM, Formicola V (2006) Biomechanical approach to the reconstruction of activity patterns in Neolithic Western Liguria, Italy. Am J Phys Anthropol 131:447–455.

    Article  Google Scholar 

  • Marchi D (2007) Relative strength of the tibia and fibula and locomotor behavior in hominoids. J Hum Evol 53:647–655.

    Article  PubMed  Google Scholar 

  • Martin RB, Burr DB, Sharkey NA (1998) Skeletal Tissue Mechanics. Springer-Verlag, New York.

    Google Scholar 

  • Montgomery RA, Chazdon RL (2001) Forest structure, canopy architecture, and light transmittance in tropical wet forests. Ecology 82:2707–2718.

    Article  Google Scholar 

  • Morbeck ME, Zihlman AL, Sumner DR, Galloway A (1991) Poliomyelitis and skeletal asymmetry in Gombe chimpanzees. Primates 32:77–91.

    Article  Google Scholar 

  • Morbeck ME (1999) Life history of Gombe chimpanzees: the inside view from the skeleton. In: Strum SC, Lindburg DG, Hamburg D (eds), The New Physical Anthropology: Science, Humanism, and Critical Reflection. Prentice-Hall, Upper Saddle River, NJ, pp 18–31.

    Google Scholar 

  • Morbeck ME, Galloway A, Sumner DR (2002) Getting old at Gombe: skeletal aging in ­wild-ranging chimpanzees. In: Erwin J, Hof PR (eds), Aging in Nonhuman Primates Interdisciplinary Topics in Gerontology, Vol. 31. Karger, Basel/New York, pp 48–62.

    Google Scholar 

  • Nagurka ML, Hayes WC (1980) An interactive graphics package for calculating cross-sectional properties of complex shapes. J Biomech 13:59–64.

    Article  PubMed  CAS  Google Scholar 

  • Nishida T (1990) The Chimpanzees of the Mahale Mountains – Sexual and Life History strategies. University of Tokyo Press, Tokyo.

    Google Scholar 

  • Ohman JC (1993) Cross-sectional geometric properties from biplanar radiographs and computed tomography: functional application to the humerus and femur in hominoids. PhD dissertation, Kent State University.

    Google Scholar 

  • Pearson OM, Lieberman DE (2004) The aging of Wolff’s “Law”: ontogeny and responses to mechanical loading in cortical bone. Yrbk Phys Anthropol 47:63–99.

    Article  Google Scholar 

  • Polk JD, Demes B, Jungers WL, Biknevicius AR, Heinrich RE, Runestad JA (2000) A comparison of primate, carnivoran and rodent limb bone cross-sectional properties: are primates really unique? J Hum Evol 39:297–325.

    Article  PubMed  CAS  Google Scholar 

  • Pusey AE, Oehlert GW, Williams JM, Goodall J (2005) Influences of ecological and social factors on body mass of wild chimpanzees. Int J Primatol 26:3–31.

    Article  Google Scholar 

  • Robling AG, Warden SJ, Shultz KL, Beamer WG, Turner CH (2007) Genetic effects on bone mechanotransduction in congenic mice harboring bone size and strength quantitative trait loci. J Bone Miner Res 22:984–991.

    Article  PubMed  CAS  Google Scholar 

  • Ruff CB (1987) Structural allometry of the femur and tibia in Hominoidea and Macaca. Folia Primatol 48:9–49.

    Article  PubMed  CAS  Google Scholar 

  • Ruff CB (1989) New approaches to structural evolution of limb bones in primates. Folia Primatol 53:142–159.

    Article  PubMed  CAS  Google Scholar 

  • Ruff CB, Runestad JA (1992) Primate limb bone structural adaptations. Annu Rev Anthropol 21:407–433.

    Article  Google Scholar 

  • Ruff CB (1999) Skeletal structure and behavioral patterns of prehistoric Great Basin populations. In: Hemphill BE, Larsen CS (eds), Prehistoric Lifeways in the Great Basin Wetlands: Bioarchaeological Reconstruction and Interpretation. University of Utah Press, Salt Lake City, pp 290–320.

    Google Scholar 

  • Ruff CB (2002) Long bone articular and diaphyseal structure in Old World monkeys and apes I: Locomotor effects. Am J Phys Anthropol 119:305–342.

    Article  PubMed  Google Scholar 

  • Ruff CB, Holt B, Trinkaus E (2006) Who’s afraid of the big bad Wolff?: “Wolff’s Law” and bone functional adaptation. Am J Phys Anthropol 129:484–498.

    Article  PubMed  Google Scholar 

  • Ruff CB (2008) Femoral/humeral strength in early African Homo erectus. J Hum Evol 54:383–390.

    Article  PubMed  Google Scholar 

  • Schaffler MB, Burr DB, Jungers WL, Ruff CB (1985) Structural and mechanical indicators of limb specialization in primates. Folia Primatol 45:61–75.

    Article  PubMed  CAS  Google Scholar 

  • Smith RJ, Jungers WL (1997) Body mass in comparative primatology. J Hum Evol 32:523–559.

    Article  PubMed  CAS  Google Scholar 

  • Stock J, Pfeiffer S (2001) Linking structural variability in long bone diaphyses to habitual behaviors: foragers from southern African Later Stone Age and Andaman Islands. Am J Phys Anthropol 115:337–348.

    Article  PubMed  CAS  Google Scholar 

  • Sumner DR, Morbeck ME, Lobick JJ (1989) Apparent age-related bone loss among adult female Gombe chimpanzees. Am J Phys Anthropol 79:225–234.

    Article  PubMed  CAS  Google Scholar 

  • Sumner DR, Andriacchi TP (1996) Adaptation to differential loading: comparison of growth-related changes in cross-sectional properties of the human femur and humerus. Bone 19:121–126.

    Article  PubMed  CAS  Google Scholar 

  • Swartz SM, Bertram JEA, Biewener AA (1989) Telemetered in vivo strain analysis of locomotor mechanics of brachiating gibbons. Nature 342:270–272.

    Article  PubMed  CAS  Google Scholar 

  • Terranova CJ (1995a) Functional morphology of leaping behaviors in galagids: associations between loading, limb use and diaphyseal geometry. In: Atterman L, Izard MK, Doyle GA (eds), Creatures of the Dark: the Nocturnal Prosimians. Plenum Press, New York, pp 473–493.

    Google Scholar 

  • Terranova CJ (1995b) Leaping behaviors and the functional morphology of strepsirhine primate long bones. Folia Primatol 65:181–201.

    Google Scholar 

  • Turner CH, Hsieh YF, Muller R, Bouxsein ML, Baylink DJ, Rosen CJ, Grynpas MD, Donahue LR, Beamer WG (2000) Genetic regulation of cortical and trabecular bone strength and microstructure in inbred strains of mice. J Bone Miner Res 15:1126–1131.

    Article  PubMed  CAS  Google Scholar 

  • Wergedal JE, Sheng MH, Ackert-Bicknell CL, Beamer WG, Baylink DJ (2005) Genetic variation in femur extrinsic strength in 29 different inbred strains of mice is dependent on variations in femur cross-sectional geometry and bone density. Bone 36:111–122.

    Article  PubMed  Google Scholar 

  • Whitten A, Goodall J, McGrew WC, Nishida T, Reynolds V, Sugiyama Y, Tutin CEG, Wrangham RW, Boesch C (1999) Cultures in chimpanzees. Nature 399:682–685.

    Article  Google Scholar 

  • Xiong DH, Shen H, Xiao P, Guo YF, Long JR, Zhao LJ, Liu YZ, Deng HY, Li JL, Recker RR, Deng HW (2006) Genome-wide scan identified QTLs underlying femoral neck cross-sectional geometry that are novel studied risk factors of osteoporosis. J Bone Miner Res 21:424–437.

    Article  PubMed  CAS  Google Scholar 

  • Yamanaka A, Gunji H, Ishida H (2005) Curvature, length, and cross-sectional geometry of the femur and humerus in anthropoid primates. Am J Phys Anthropol 127:46–57.

    Article  PubMed  Google Scholar 

  • Zihlman AL, Stahl D, Boesch C (2008) Morphological variation in adult chimpanzees (Pan ­troglodytes verus) of the Taï National Park, Côte d’Ivoire. Am J Phys Anthropol 135:34–41.

    Article  PubMed  Google Scholar 

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Carlson, K.J. et al. (2011). Comparisons of Limb Structural Properties in Free-ranging Chimpanzees from Kibale, Gombe, Mahale, and Taï Communities. In: D'Août, K., Vereecke, E. (eds) Primate Locomotion. Developments in Primatology: Progress and Prospects. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-1420-0_9

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