Bone microstructure in juvenile chimpanzees

Bone Microstructure in Juvenile Chimpanzees

Dawn M. Mulhern1* and Douglas H. Ubelaker2

1Department of Anthropology, Fort Lewis College, Durango, CO 813012National Museum of Natural History, Smithsonian Institution, Washington, DC 20013

KEY WORDS osteon; Hominoidea; histomorphometry; primate

ABSTRACT The growth, development, and mainte-nance of bone are influenced by genetic and environ-mental variables. Understanding variability in bonemicrostructure among primates may help illuminatethe factors influencing the number and size of second-ary osteons. The purpose of this study is to assess thebone microstructure in 8 humeral and 12 femoral sec-tions of 12 juvenile chimpanzees, aged 2–15.3 years,and one adult chimp. Secondary osteons were countedand measured for 16 fields per section. Results indicatethat the femur exhibits a mean osteon population den-sity (OPD) of 4.46 6 2.34/mm2, mean Haversian canalarea of 0.0016 6 0.0007 mm2, and mean osteon area of0.033 6 0.006 mm2. The humerus has a mean OPD of4.72 6 1.57/mm2, mean Haversian canal area of 0.00136 0.0003 mm2, and mean osteon area of 0.033 6 0.005

mm2. Differences are not significant between the hu-merus and femur, possibly indicating similar mechani-cal demands during locomotion. Osteon population den-sity exhibits a moderate correlation with age (r 50.498) in the femur of the juvenile chimps, but theadult chimp has an OPD of 10.28/mm2, suggesting thatosteons likely accumulate with age. Females exhibithigher osteon densities in the periosteal envelope com-pared to males in the humerus, indicating more remod-eling during periosteal expansion. Overall similaritiesbetween chimpanzees and humans as well as previouslypublished data on Late Pleistocene hominids (Abbottet al.: Am J Phys Anthropol 99 [1996] 585–601) suggestthat bone microstructure has been stable throughouthuman evolution. Am J Phys Anthropol 140:368–375,2009. VVC 2009 Wiley-Liss, Inc.

Studies in bone histomorphometry have the potential toshed light on the variety of factors contributing to growth,development, and maintenance of bone tissue. Identifyingsimilarities and differences among species in bone micro-structure provides a basis for assessing the relative impor-tance of biological and environmental factors. In addition,identification of species-specific differences is important ina forensic context in cases of extreme fragmentation.Since nonhuman primates share the greatest genetic simi-larities with humans compared to other mammals, studiesof primate histomorphometry supply information aboutthe range of variability within Order Primates, serve asmodels for diseases affecting bone, illustrate microscopicdifferences due to biomechanical strain (such as straindue to locomotor pattern), and provide models for earlyhominid skeletal development.Early studies in bone histomorphometry focused on

describing variability among mammalian species. Mullerand Demarez (1934) reported Haversian canal diametersfor five apes (gorillas and chimpanzees) and one maca-que. Jowsey (1966) measured Haversian canal andosteon dimensions for two rhesus monkeys in a compara-tive mammalian study. Singh et al. (1974) quantified thenumber and size of primary canals and lacunae in asample of 12 nonhuman primates, including two galagos,four old world monkeys, five new world monkeys, andone gibbon. Schaffler and Burr (1984) studied percentosteonal bone and osteon density in 20 primates, includ-ing three prosimians, fifteen monkeys, and two chimpan-zees, to assess microscopic differences due to locomotorpattern. More recent studies focus on using primates asmodels for human pathology, such as osteoporosis. Przy-beck (1985) studied age changes in bone mass and boneremodeling dynamics in rib samples from 15 macaques.Burr (1992) studied femoral intracortical bone turnoverfor a sample of 54 immature and mature macaques to

assess their utility as models for skeletal pathology inhumans. Havill (2004) utilized 42 of Burr’s bone sam-ples, in addition to samples from another 33 older maca-ques to provide additional data on bone remodeling dy-namics and the applicability of macaque models to stud-ies of human aging and bone pathology. Lees andRamsay (1999) studied changes in trabeculae, bone for-mation rates, mineral apposition rate, and activation fre-quency with age in 28 cynomolgus monkeys to determinewhether they are appropriate models for perimenopausalskeletal changes. Mulhern and Ubelaker (2003) com-pared histological data for 12 juvenile humans and 12chimpanzees using Kerley’s (1965) method for age esti-mation to identify similarities and differences duringgrowth and development.The purpose of the present study is to expand on the

study by Mulhern and Ubelaker (2003) and provide addi-tional information regarding juvenile chimpanzee micro-structural variables, including osteon population density,Haversian canal area, and osteon area in the femur andhumerus. The results of this study will also be comparedwith published results for humans and nonhuman pri-mates. As outlined in Mulhern and Ubelaker (2003), inaddition to providing needed data on chimpanzee micro-structural variables, this study has the potential to con-tribute to a better understanding of the evolution of

*Correspondence to: Dawn M. Mulhern, Department of Anthropol-ogy, Fort Lewis College, 1000 Rim Drive, Durango, CO 81301, USA.E-mail: [email protected]

Received 21 May 2008; accepted 3 September 2008

DOI 10.1002/ajpa.20959Published online 11 May 2009 in Wiley InterScience

(www.interscience.wiley.com).

VVC 2009 WILEY-LISS, INC.

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 140:368–375 (2009)

human skeletal development as well as developmentaldifferences between apes and humans related to locomo-tor pattern. Chimpanzees experience more rapid skeletaland dental maturation compared to humans (Michejda,1980; Kuykendall, 1996) and also lack the adolescentgrowth spurt found in humans (Hamada and Udono,2002). Understanding how bone develops in chimpanzeeson a microstructural level allows a more holistic perspec-tive regarding growth and development in hominoids.

MATERIALS AND METHODS

In 1966, Kerley conducted a histological analysis of 30juvenile and adult chimpanzees of known age (Kerley,1966). He reported age-related changes in osteon numberand amount of circumferential lamellar bone, but he didnot provide specific quantitative data. In this study,twelve femoral and eight humeral midshaft cross sec-tions from Kerley’s sample were evaluated, including 12chimpanzees ranging in known age at death from 2 to15.3 years (Table 1). The femur from one adult chimpan-zee, 35 years of age, was also evaluated and results areprovided, since almost no data on adult chimpanzeeshave been published. The samples, prepared by Kerley,include undecalcified, ground thin sections from the mid-dle third of the diaphysis of each bone. It is unknownwhether the bones came from the right or left side.According to Kerley’s assessment of epiphyseal closure,

the humerus and femur were completely fused by about15 years; so, the chimpanzees in this study are consid-ered to be skeletally immature. Unfortunately, the sec-tions from Kerley’s adult sample were not housed withthe immature sections and their whereabouts wereunknown when this study was conducted. Histomorpho-metric data collected include the number of secondaryosteons and osteon fragments as well as Haversian canaland osteon areas.For each section, 16 fields were observed, including

fields adjacent to the periosteal and endosteal borders inthe following locations: anterior–posterior axis, mediolat-eral axis, anteriomedial–posteriolateral axis, and ante-riolateral–posteriomedial axis. Since the slides are notlabeled and therefore side is unknown, ‘‘medial’’ and ‘‘lat-eral’’ were used for recording purposes only. For this rea-son, comparisons within each bone section are limited tothe periosteal versus endosteal envelopes. Field sizesranged from 1.30 to 4.15 mm2 depending on the overallsize of the bone, but each field size was measured usingimage analysis software. The border of each field wasoutlined and the area calculated automatically. Haver-

sian canal areas and osteon areas were measured in thesame way. Osteon counts were conducted on the monitor,although they were sometimes viewed through themicroscope also for clarification. For future reference,individual osteons were numbered and areas wererecorded directly on the images captured. Morphometricanalysis was conducted at 1003 using a Leica DM LBstandard light microscope and Spot Insight color cameraand image capture software.The symbols for variables used follow Parfitt et al.

(1987) or Stout and Paine (1992, 1994). The followingvariables relating to secondary osteons were assessed:

1. Intact osteon density in number/mm2 (N.On): numberof secondary osteons per mm2 with at least 90% of theperimeter of the Haversian canal intact. At least halfof the osteon’s area had to be within the defined fieldto be counted.

2. Fragmentary osteon density in number/mm2

(N.On.Fg): number of osteon fragments or osteonswith 10% or more of the Haversian canal compro-mised by resorption. At least half of the fragment’sarea had to fall within the defined field to be counted.

3. Osteon population density (OPD): total number ofintact (N.On) and fragmentary (N.On.Fg) osteons.

4. Haversian canal area (H.Ar): average area of Haver-sian canals.

5. Osteon area (On.Ar): average area of osteons(including their Haversian canals). Osteons withround Haversian canals were measured to avoidmeasuring oblique osteons.

The total number of osteons measured varied among indi-viduals, but an average of 29 osteons (including both H.Arand On.Ar) were measured for each humeral section andan average of 47 were measured for each femoral section.Statistical analysis was conducted using SPSS 15.0.

Tests for normality and homogeneity of variances wereconducted and indicated that parametric tests are appro-priate, despite the small sample size. Independent Stu-dent’s t tests were used to compare count and area varia-bles between the periosteal and endosteal envelopes.Paired t tests were used to compare counts and areasbetween the humerus and femur for the eight individu-als represented by both bones. Pearson’s correlation coef-ficients were calculated to assess possible relationshipsbetween variables, and regression analyses were appliedto identify relationships between chronological age andhistomorphometric variables.

RESULTS

Morphometric data, including numbers of intactosteons (N.On), osteon fragments (N.On.Fg), osteon pop-ulation density (OPD), Haversian canal area (H.Ar), andosteon area (On.Ar), for each specimen are presented inTables 2 and 3 for the femur and humerus, respectively.Osteon population density ranges from 0.35/mm2 to 8.47/mm2 in the femur, with the lowest value occurring in a2-year-old chimp and the highest in a 7-year-old chimp.Haversian canal area ranges from 0.0011 to 0.0021 mm2

and osteon area ranges from 0.025 to 0.046 mm2 in thefemur. In the humerus, OPD ranges from 2.19 to 7.31mm2, Haversian canal area ranges from 0.0009 to 0.0017mm2, and osteon area ranges from 0.026 to 0.041 mm2.Summary data are presented by bone and by sex in

Table 4. Results for the femur include separate data for

TABLE 1. Sample age and sex distribution

Specimen Age (years) Sex

86 2.0 M113 2.0 F114 2.0 M66 5.0 M82 5.0 M57 7.0 M8 9.6 F

45 10.0 F11 12.0 F30 13.0 M1 13.4 F

18 15.3 MB 35.0 M

369BONE MICROSTRUCTURE IN JUVENILE CHIMPANZEES

American Journal of Physical Anthropology

the eight individuals also represented by the humerus.Overall, the femur and humerus exhibit similar OPDs of4.46 6 2.34/mm2 and 4.72 6 1.57/mm2, respectively. Theeight individuals represented by the humerus and femurhave a femoral OPD of 4.53 6 2.86/mm2. A paired t testbetween the eight individuals represented by both bonesshows no significant differences in osteon number.Figure 1 shows a comparison of values for OPD in thehumerus and femur for the eight individuals representedby both humerus and femur. The correlation coefficientfor OPD in the femur and humerus is r 5 0.547, indicat-ing that 29.9% of the variation in humeral OPD isexplained by the variation in femoral OPD. Overall,Haversian canal area is slightly larger in the femur(0.0016 6 0.0007 mm2) compared to the humerus(0.0013 6 0.0003 mm2), even when the subgroup of eightindividuals is isolated (0.0015 6 0.0003 mm2). Finally,mean osteon area is the same in the femur (0.033 60.006 mm2) and humerus (0.033 6 0.005 mm2) for the

TABLE 2. Histomorphometric variables by individual for the femur

SpecimenAge

(years) SexN.On

(number/mm2) SDN.On.Fg

(number/mm2) SDOPD

(number/mm2) SDH.Ar(mm2) SD

On.Ar(mm2) SD

86 2.0 M 0.35 0.83 0.00 0.00 0.35 0.83 0.0011 NA 0.025 NA113 2.0 F 4.35 2.20 0.25 0.52 4.60 2.28 0.0018 0.0010 0.036 0.017114 2.0 M 3.22 3.54 0.00 0.00 3.22 3.54 0.0019 0.0010 0.034 0.01566 5.0 M 2.82 2.29 0.09 0.23 2.91 2.41 0.0012 0.0005 0.033 0.01482 5.0 M 2.00 2.40 0.00 0.00 2.00 2.40 0.0015 0.0007 0.030 0.02157 7.0 M 8.08 4.76 0.39 0.50 8.47 5.09 0.0012 0.0009 0.032 0.0128 9.6 F 4.94 3.67 0.17 0.25 5.11 3.85 0.0016 0.0006 0.046 0.019

45 10.0 F 3.92 2.41 0.03 0.12 3.95 2.45 0.0013 0.0006 0.025 0.00811 12.0 F 8.22 3.80 0.22 0.39 8.44 3.49 0.0016 0.0013 0.032 0.01730 13.0 M 3.89 3.29 0.28 0.46 4.17 3.65 0.0021 0.0010 0.032 0.0131 13.4 F 5.01 3.57 0.23 0.31 5.24 3.78 0.0016 0.0006 0.031 0.013

18 15.3 M 4.91 3.85 0.11 0.26 5.02 4.02 0.0014 0.0008 0.037 0.019B 35.0 M 10.28 4.45 0.48 0.36 10.77 4.56 0.0012 0.0006 0.031 0.013

TABLE 3. Morphometric variables by individual for the humerus

SpecimenAge

(years) SexN.On


(number/mm2) SDOPD


On.Ar(mm2) SD

86 2.0 M 3.78 2.79 0.03 0.10 3.81 2.79 0.0011 0.0003 0.030 0.010113 2.0 F 6.88 5.16 0.44 0.82 7.31 5.58 0.0011 0.0004 0.033 0.015114 2.0 M 3.22 3.49 0.14 0.40 3.36 3.56 0.0013 0.0005 0.032 0.02082 5.0 M 2.19 2.42 0.00 0.00 2.19 2.42 0.0015 0.0008 0.041 0.01757 7.0 M 4.78 3.98 0.39 0.75 5.17 4.29 0.0016 0.0007 0.035 0.02145 10.0 F 5.24 2.47 0.05 0.12 5.29 2.52 0.0013 0.0006 0.033 0.01311 12.0 F 5.54 3.25 0.04 0.15 5.58 3.30 0.0009 0.0004 0.026 0.0121 13.4 F 4.73 2.80 0.31 0.45 5.04 3.07 0.0017 0.0010 0.039 0.023

TABLE 4. Summary data by bone and sex

Bone Sex n

Meanage

(years)N.On.


(number/mm2) SDOPD


On.Ar(mm2) SD

Femur F 5 9.4 5.29 1.70 0.18 0.09 5.47 1.73 0.0016 0.0002 0.034 0.008M 7 7.0 3.61 2.44 0.12 0.15 3.73 1.97 0.0015 0.0004 0.032 0.004Both 12 8.0 4.31 2.25 0.15 0.13 4.46 2.34 0.0016 0.0005 0.033 0.006Botha 8 6.7 4.39 2.73 0.14 0.15 4.53 2.86 0.0015 0.0003 0.031 0.004

Humerus F 4 9.4 5.60 0.92* 0.21 0.20 5.81 1.03* 0.0013 0.0004 0.033 0.005M 4 4.0 3.50 1.08* 0.14 0.18 3.64 1.23* 0.0014 0.0002 0.034 0.005Both 8 8.0 4.55 1.46 0.17 0.18 4.72 1.57 0.0013 0.0003 0.033 0.005

* Denotes P\ 0.05 between males and females.a Individuals also represented by humerus.

Fig. 1. Scatterplot of OPD in the femur and humerus.

370 D.M. MULHERN AND D.H. UBELAKER


entire sample and slightly lower in the femur (0.031 60.004 mm2) when the subgroup of eight individuals isisolated. Paired t tests indicate that Haversian canalarea and osteon area are not significantly differentbetween bones within the same individual.In the humerus, N.On and OPD are significantly dif-

ferent between males and females (P \ 0.05; Table 4).Osteon population density is 5.81 6 1.03/mm2 in femalesand 3.64 6 1.23/mm2 in males. Upon further inspectionof the data, these differences are due to differences inthe periosteal envelope (Table 5). Osteon population den-sity in the periosteal envelope is 5.23 6 1.16/mm2 infemales compared to 1.17 6 0.59/mm2 in males. Femalesalso exhibit a higher osteon density in the femur com-pared to males, but differences are not significant.Haversian canal area and osteon area do not differbetween the sexes.Table 6 shows the breakdown for each variable by en-

velope for the femur and humerus. Osteon populationdensity is significantly different between the periostealand endosteal envelopes in both the femur and humerus(P \ 0.05). In the femur, OPD is 3.19 6 2.03/mm2 in theperiosteal envelope and 5.85 6 3.08/mm2 in the endo-steal envelope. In the humerus, OPD is 3.20 6 2.33/mm2

in the periosteal envelope and 6.19 6 1.86/mm2 in theendosteal envelope. Haversian canal and osteon areas donot differ significantly between the periosteal and endo-steal envelopes in the femur or the humerus.Pearson’s correlation coefficients between age and his-

tomorphometric variables as well as between histomor-phometric variables for the femur and humerus are pre-sented in Table 7. None of the histomorphometric varia-bles exhibit significant correlations with age in thefemur or humerus. A scatterplot of age and osteon popu-lation density in the femur shows a somewhat linearpattern, with a correlation coefficient of 0.498 (see Fig.2). In the femur, age predicts 25% of the variation in

number of osteons and OPD and 12% of the variation inosteon fragments when using a linear model. OPD, H.Ar,and On.Ar do not show any significant correlations witheach other in the femur. Correlation coefficients forknown age and histomorphometric variables in the hu-merus are very low, and a scatterplot of OPD and ageshows that there is no clear pattern (see Fig. 3). In thehumerus, one pair of histomorphometric variables doesexhibit a significant relationship. Specifically, osteonarea and Haversian canal area show a significant posi-tive correlation (r 5 0.83; P \ 0.01), suggesting thatlarger osteons have larger canals in the humerus. Quad-ratic and cubic regression models do not provide appreci-ably better fits with the data, indicating that these vari-ables are generally poor predictors of age in juvenilechimpanzees. The small sample size may also be a factorin a lack of any discernible relationship.In addition to the present study, Table 8 shows com-

parative data for chimpanzees (Schaffler and Burr,1984), macaques (Havill, 2004), humans (Ericksen, 1991;

TABLE 5. Osteon counts by envelope in the humerus

Specimen Age (years) Sex

N.On (number/mm2) OPD (number/mm2)

Periosteal envelope Endosteal envelope Periosteal envelope Endosteal envelope

113 2.0 F 5.06 9.00 5.44 9.5045 10.0 F 5.50 5.03 5.50 5.1211 12.0 F 6.36 4.73 6.36 4.811 13.4 F 3.45 5.97 3.61 6.29Mean 9.4 5.09* 6.18 5.23* 6.43SD 5.1 1.22 1.95 1.16 2.1486 2.0 M 1.58 5.43 1.94 6.03114 2.0 M 0.46 5.97 0.64 6.0882 5.0 M 0.78 3.59 0.78 3.5957 7.0 M 1.31 7.37 1.31 8.06Mean 4.0 1.03* 5.59 1.17* 5.94SD 2.5 0.51 1.56 0.59 1.83

* P\ 0.01 between males and females.

TABLE 6. Mean histomorphometric variables by envelope for the humerus and femur

Bone n

Periostealenvelope(number/mm2)

Endostealenvelope(number/mm2)

Periostealenvelope (mm2)

Endostealenvelope (mm2)

Periostealenvelope(mm2)

Endostealenvelope(mm2)

OPD SD OPD SD H.Ar SD H.Ar SD On.Ar SD On.Ar SD

Femur 12 3.19 2.03* 5.85 3.08* 0.0015 0.0002 0.0015 0.0004 0.032 0.007 0.034 0.006Humerus 8 3.2 2.33* 6.19 1.86* 0.0012 0.0002 0.0014 0.0003 0.03 0.008 0.035 0.006

* P\ 0.05 for a Student’s t test between periosteal and endosteal envelopes within the same bone.

TABLE 7. Correlation coefficients for age andhistomorphometric variables for the femur and humerus

FemurAge

(years)OPD

(number/mm2)H.Ar(mm2)

On.Ar(mm2)

Age 1.000 0.498 0.146 0.164OPD 1.000 0.110 0.314HcA 1.000 0.348OA 1.000HumerusAge 1.000 0.222 0.244 0.058OPD 1.000 20.308 20.370HcA 1.000 0.863*OA 1.000

* P\ 0.01.



Jowsey, 1966; Burr et al., 1990; Pfeiffer et al., 2006; Mul-hern and Van Gerven, 1997), and Late Pleistocene homi-nids (Abbott et al., 1996) in femoral osteon number(N.On), OPD, Haversian canal area, and osteon area.The adult chimpanzee from the present study exhibitedan osteon population density of 10.77/mm2 compared to4.46/mm2 in the juvenile sample. Mean Haversian canaland osteon areas are slightly smaller in the adult thanthose observed for juvenile chimpanzees including anH.Ar of 0.0012 mm2 compared to 0.0015 mm2 and On.Arof 0.031 mm2 compared to 0.033 mm2.Using a t distribution comparison of two samples, ju-

venile chimpanzees have significantly larger osteonareas (0.033 6 0.006 mm2) compared to macaques (0.0246 0.006 mm2; P\ 0.001) although Haversian canal sizesare about the same (0.0014 6 0.0005 mm2 in macaquesand 0.0015 6 0.0003 mm2 in chimps), indicating thatchimpanzees have more bone per osteon.Compared to adult humans, the juvenile chimpanzees

in the present study exhibit fewer intact osteons, but theadult chimp is well within the range observed in adults.Compared to most of the human samples, the juvenilechimps exhibit significantly smaller Haversian canals (P\ 0.01). Only the difference in Haversian canal sizebetween the chimpanzees and the Holocene forager pop-ulation is not significant. Osteon area in the juvenilechimpanzees is more clearly in the range of human pop-ulations. The juvenile chimpanzees also exhibit signifi-cantly smaller Haversian canals (P \ 0.01) compared toa Late Pleistocene hominid sample, although osteon areaand osteon density are not significantly different.Percent osteonal refilling, which represents the pro-

portion of space within an osteon’s cement line that hasbeen filled in with bone, is similar in chimpanzees andhumans, with the chimp value of 95.4% falling justabove the upper end of the range observed for thehuman samples.

DISCUSSION

Chimpanzees

The accumulation of femoral osteons exhibits only amoderate linear relationship with age in immature chim-panzees (r 5 0.498 for OPD). This is likely affected bycortical drift, which erases previous bone turnover activ-

ity. This means that the effective age of the adult com-pacta is less than the chronological age of an individual(Frost, 1987). The weak association between chronologi-cal age and osteon density in immature chimpanzeesmay be due to modeling drifts and the fact that many ofthese individuals have not achieved the ‘‘birth’’ of theiradult compacta.Schaffler and Burr (1984) reported 7.4 secondary

osteons/mm2 in an adult chimpanzee and the presentstudy found 10.28 secondary osteons/mm2. Althoughthese data only represent two individuals, it is interest-ing to note that the mean number of secondary osteonsin immature chimps is 4.66/mm2, suggesting an overallpattern of accumulating osteons with age, as seen inhumans. This pattern of increased osteon density withage in chimpanzees is reported by Kerley (1965), but notquantified. Additional studies on adult chimpanzees arenecessary to further assess this relationship.The presence of more secondary osteons in the endo-

steal compared to periosteal bone in juvenile chimpan-zees is likely due to the older mean tissue age in thatportion of the cortex. Osteon density and size do not dif-fer between the humerus and femur in the presentstudy, revealing histologically similar bone in the fore-limbs and hindlimbs. These results suggest that mechan-ical demands may be similar for both bones during loco-motion in juvenile chimpanzees.Females exhibit more osteons than males in the femur

and humerus (with significant differences in the hu-merus only). The femur did demonstrate a moderaterelationship between OPD and age; so, the lower meanage in the male femoral sample could explain this dis-crepancy. In the humerus, no relationship between ageand OPD was found, arguing against the lower malemean age as an explanation for the observed difference.However, given the small sample size, this must be con-sidered. The significant differences in the humerus arerestricted to the periosteal envelope, possibly suggestingmore pronounced mechanical stress and loading duringperiosteal expansion in this group of females comparedto the males.

Chimpanzee and macaque

Juvenile chimpanzees exhibit fewer, but larger osteonsin the femur compared to juvenile macaques. In the

Fig. 2. Scatterplot of chronological age and OPD in thefemur.

Fig. 3. Scatterplot of chronological age and OPD in thehumerus.



present study, chimpanzees exhibited an average OPD of4.46/mm2, H.Ar of 0.0016 mm2, and On.Ar of 0.033 mm2

compared to an OPD of 6.89/mm2, H.Ar of 0.0014 mm2,and On.Ar of 0.024 mm2 in a sample of 34 immaturemacaques (Havill, 2004). Haversian canal size is similarin these two taxa; so, this may reflect an adaptation togreater strain in the chimpanzee femur due to mechani-cal loading during locomotion, with fewer osteons, butmore bone volume per osteon. Schaffler and Burr (1984)found that suspensory and bipedal primates exhibit ahigher percent osteonal bone compared to arboreal andterrestrial quadrupeds, probably due to mechanicalstrain on the hindlimbs when walking or braking.Although the juvenile chimpanzees exhibited lowerosteon densities compared to macaques (Havill, 2004),they also exhibit more bones per osteon; so, this couldresult in more secondary bone throughout the cortex.

Chimpanzee and human

Osteon density does not exhibit a strong relationshipwith age in juvenile chimpanzees. A lack of age-relatedchange in osteon density is also found in subadulthumans. A recent study by Rauch et al. (2007) found nochange in osteon density or dimensions with age in asample of 56 iliac crest samples from individuals between1.5 and 22.9 years. Streeter (2005) found no correlationbetween osteon density and age in a sample of humansubadult ribs. In adult humans, osteon density has beencorrelated with age in modern and archaeological popula-tions (Currey, 1964; Kerley, 1965; Stout and Lueck, 1995;Mulhern and Van Gerven, 1997, Mulhern, 2000). Thelack of a demonstrable relationship between osteon den-sity and age in juvenile chimpanzees could be related toactive drift that erases previous remodeling activity. Asmentioned previously, the cessation of active drift deter-mines the age of the effective birth of the adult compacta.In humans, a gradual decline in the rate of bone driftoccurs between about 14 and 19 years with the onset ofskeletal maturity (Frost, 1987). In chimpanzees, thislikely occurs earlier, since skeletal maturity is reachedsooner. This means that in a given bone, a chimpanzeelikely exhibits older compacta than an age-matchedhuman. In a previous comparison of this juvenile chim-panzee sample with Kerley’s (1965) sample of 12 humansubadults, results showed that osteon density was 27%higher in the chimps compared to humans, although thedifference was not statistically significant (Mulhern andUbelaker, 2003). The lack of a strong age associationbetween osteon density and chronological age in juvenilechimpanzees suggests an overall pattern of developmentsimilar to that reported for juvenile humans.The overall similarities between chimpanzees and

humans suggest that the femur does not exhibit signifi-cant differences due to locomotor pattern. Without compa-rable data on the humerus, it is impossible to discuss dif-ferences that may be present in the upper limb. Certainly,both species experience mechanical strain in the femurduring growth and development as well as throughoutadulthood during locomotion, although strains in theupper limb would differ significantly after human infantsbegin walking. If humans do differ significantly in bonemicrostructure between the humerus and femur, then thesimilarity between the humerus and femur observed in ju-venile chimpanzees may be related to locomotor pattern.If not, then bone microstructure in the limbs may be moreheavily influenced by other factors.

TABLE

8.Com

para

tivehistomorphom

etricdata

forthefemur

Taxon

Age

NN.O

n(number/m

m2)

SD

OPD

(number/m

m2)

SD

HcA

(mm

2)

SD

On.Ar

(mm

2)

SD

%O

Ref

aStudy

Macaque

\6yea

rs34

6.89

3.05

0.0014

0.0005

0.024

0.006

94.2

Havill,2004

Macaque

[6yea

rs41

9.00

3.36

0.0015

0.0005

0.024

0.005

93.8

Havill,2004

Chim

panzee

Immature

17.70

Sch

affler

andBurr,1984

Chim

panzee

Adult

17.40

Sch

affler

andBurr,1984

Chim

panzee

2–15.3

yea

rs12

4.31

2.25

4.46

2.34

0.0015

0.0003

0.033

0.006

95.4

Presentstudy

Chim

panzee

35yea

rs1

10.28

10.77

0.0012

0.031

Presentstudy

Human

20–97yea

rs319

4.96–15.69b

Erick

sen,1991

Human

Adult

26

0.0024c

0.039c

93.8

Jow

sey,

1966

Human(H

olocen

eforagers)

Adult

15

0.0019

0.0014

0.036

0.016

94.7

Pfeifferet

al.,2006

Human(18th

century)

25–50yea

rs20

0.0037

0.0039

0.045

0.022

91.8

Pfeifferet

al.,2006

Human(19th

century)

17–81yea

rs20

0.0032

0.0019

0.035

0.017

90.9

Pfeifferet

al.,2006

Human(m

edieval)

20–501

yea

rs43

5.76–10.68b

9.28–13.42b

0.0021

0.0007

0.038

0.007

94.5

MulhernandVan

Gerven

,1997

Human(prehistoricmales)

21–60yea

rs28

6.80–7.45b

0.0023

0.0009

0.034

0.010

93.2

Burr

etal.,1990

Human

(prehistoricfemales)

21–60yea

rs23

5.53–7.06b

0.0024

0.0008

0.041

0.009

94.1

Burr

etal.,1990

Hom

inid

(Late

Pleistocene)

18–501

yea

rs10

3.37

1.01

0.0021

0.0006

0.028

0.008

92.5

Abbottet

al.,1996

a%

Osteonalrefilling5

OA-H

cA/O

A.

bRangeof

mea

nvalues

reportedbydecade.

cCalculatedfrom

perim

eter.



Osteon density for the adult chimpanzee from thepresent study and the chimpanzee studied by Schafflerand Burr (1984) falls within the range for human adults(Burr et al., 1990; Ericksen, 1991; Mulhern and VanGerven, 1997). Although these data should be consideredwith caution at present, the higher osteon densities in theadult chimps compared to juvenile chimps suggest thatthe overall pattern of an accumulation of osteons with ageseen in humans may be found in chimpanzees as well.Comparing Haversian canal and osteon areas between

chimpanzees and humans is problematic, since the pres-ent study is focused on juvenile chimpanzees and datafor osteon dimensions in humans comes from adults.Although several studies have documented age-relatedchanges in Haversian canal area in humans (Singh andGunberg, 1970; Thompson, 1980), a number of studieshave found no significant relationship between osteondimensions and age, including samples with both suba-dults and adults (Frost, 1963; Mulhern and Van Gerven,1997; Mulhern, 2000; Pfeiffer, 1998; Rauch et al., 2007).It is unknown at present whether chimpanzees exhibitany age-related changes in osteon dimensions, but it isnot unlikely that they follow a similar pattern tohumans. Even so, the following discussion should be con-sidered within this context.The juvenile chimpanzees in the present study exhibit

significantly smaller Haversian canals compared to mostof the comparative human groups. Osteon areas, however,are within the range of modern adult humans, althoughat the smaller end of the range. In addition, percentosteonal refilling is similar in the chimpanzee and humansamples, indicating that, despite any differences in overalldimensions, chimpanzees and humans exhibit a similarbalance of bone formation and resorption.Abbott et al. (1996) found smaller and fewer osteons

and therefore slower bone turnover in a sample of LatePleistocene humans compared to recent humans. Smallosteon sizes were attributed to less vigorous osteoclasticactivity at the cellular level, indicating a lower metabolicrate for skeletal remodeling. The possibility of nutri-tional and disease stress as contributing factors was alsosuggested. According to the Abbott et al. (1996) study,low osteon densities in the Late Pleistocene groups couldbe attributed to high bone strains during adulthood thatdepressed remodeling rates or to a biologically deter-mined lower setpoint for bone response. While osteondensity in the juvenile chimps is comparable to thatobserved for the Late Pleistocene hominids, osteon den-sities for the adult chimps suggest that this may be anage-related phenomenon, with chimpanzees attaininghigher densities as adults. Since Haversian canal areaand osteon area do not appear to be significantly affectedby age-related changes, it is interesting to note thatwhile Haversian canal sizes are significantly different,with chimpanzees exhibiting smaller canals, osteon sizesare smaller in the Late Pleistocene sample, but differen-ces are not significant, resulting in slightly greater bonevolume per osteon in the chimpanzees. Specifically,osteonal refilling in the Late Pleistocene sample was92.5% compared to 95.4% in the chimpanzees.The overall similarities between chimpanzee and Late

Pleistocene and human histomorphometrics observed inthe present study indicate that underlying genetic fac-tors influencing the general patterns of osteon densityand size during growth and development may not havechanged much during the course of human evolution andsupport the idea that populational differences are pri-

marily responses to mechanical factors related to activityand differences in patterns of growth. The effect of activ-ity pattern on bone microstructure in humans is not wellunderstood. Burr et al. (1990) attributed greater osteondensities in males and smaller Haversian canals infemales to an active lifestyle in a Native American popu-lation from Pecos, New Mexico. Mulhern and VanGerven (1997) observed greater osteon densities in malesand larger osteons in females in the femur in a samplefrom Kulubnarti, Nubia, but Mulhern (2000) did notobserve any differences between males and females inthe rib for the same population, potentially indicatingdifferent responses in males and females to mechanicaldemands or to different types of loading on the femur inmales and females. However, in a recent study compar-ing rib and femur histomorphometry, Pfeiffer et al.(2006) found no clear relationship between osteon dimen-sions and physical activity in three human populations,suggesting that the relationship between bone micro-structure and aspects of lifestyle are complex.

CONCLUSIONS

1. In general, histomorphometric variables do not demon-strate a strong relationship with age in juvenile chim-panzees. This pattern has been reported in juvenilehumans, indicating that chimpanzees and humans fol-low a similar pattern of histological development.

2. Juvenile chimpanzees do not exhibit differences inhistomorphometric variables between the humerusand femur, suggesting similar mechanical demandsduring locomotion.

3. Juvenile female chimpanzees exhibit higher N.On andOPD in the periosteal envelope of the humerus com-pared to males, possibly suggesting greater remodel-ing during periosteal expansion in this group offemales compared to males.

4. Chimpanzees exhibit larger, but fewer osteons com-pared to juvenile macaques. These differences mayreflect differences in mechanical demands, with greaterloading on the chimpanzee femur during locomotion.

5. Haversian canal areas are significantly smaller in ju-venile chimpanzee femoral bone compared to mostadult human samples, but the amount of bonereplaced per osteon is comparable.

6. Overall, histomorphometric variables are similarbetween chimpanzees, Late Pleistocene hominids, andmodern humans, suggesting continuity in skeletal de-velopment and microstructure during human evolu-tion, despite differences in locomotor pattern.

ACKNOWLEDGMENTS

The authors thank the Armed Forces Institute of Pa-thology of the National Museum of Health and Medicinein Washington, DC, for the loan of Ellis Kerley’s chim-panzee bone thin sections.

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Bone microstructure in juvenile chimpanzees