ORIGINAL ARTICLE

A longitudinal study on hand and wrist skeletal maturationin chimpanzees (Pan troglodytes), with emphasis on growthin linear dimensions

Received: 11 September 2002 / Accepted: 16 February 2003 / Published online: 25 April 2003� Japan Monkey Centre and Springer-Verlag 2003

Abstract Skeletalmaturation in the chimpanzeehandandwrist (the RUS system; radius, ulna, and short bones) wasstudied both longitudinally and cross-sectionally. Matu-rity states were evaluated in each of the 13 bones of theRUS system based on the TW2 method (Tanner andWhitehouse method), and the RUS score was calculatedby the summation of scores for these bones. Individualvariation was examined by means of residual curves andpseudo-velocity curves of RUS score and anterior trunklength (ATL). Norms of the age change pattern in RUSskeletal maturation and the growth of ATL were deter-mined for each sex, and the relationships among ATLgrowth and skeletal and reproductive maturation wereexamined. We found a fairly good relationship betweenATL growth and RUS skeletal maturation. Comparisonof growth and development between humans and chim-panzees showed that growth characteristics are coupledwith each other at puberty in male chimpanzees and inboth sexes of humans. Although nutritional conditioninfluenced ATL growth in infancy, it had no effect on theRUSmaturational process. Social relationships appeared

to influence both ATL growth and RUS maturation.Analyses on relationships between RUS skeletal matura-tion, ATL growth, and reproductive maturation, showedthat RUS skeletal maturation is a good indicator of‘‘physiological age’’.

Keywords RUS Æ TW2 method Æ Skeletal growth andmaturation Æ Pan troglodytes Æ Longitudinal study

Introduction

Knowledge about growth and development in non-human primates is essential in considering the evolutionof biological characteristics in primates and the interre-lationships of species-specific life history, ecology, andlife-style (Leigh 1996; Winkler 1996; Leigh and Shea1996; Lee 1997). The body is composed of many differ-ent systems from the viewpoint of growth and develop-ment: somatometrical characters, dental development(formation and eruption), reproductive maturation, andskeletal maturation. Interrelationships between thegrowth, development, and maturation of these systemsfrom an evolutionary perspective have been discussed bya variety of researchers (e.g. Watts and Gavan 1982;Watts 1985, 1986; Leigh 1996). How thoroughly a sys-tem has been studied, however, varies. Tooth eruption,for example, has been studied in a diverse number ofprimate species (Simpson et al. 1991; Anemone et al.1991; Kuykendall et al. 1992; Nissen and Riesen 1964;Smith 1991; Smith et al. 1994), and growth in somato-metrical items, especially body mass, has been studied inmany species of lemurs, platyrrhines, and catarrhinesincluding humans (Gavan 1971; Smith et al. 1975;Cheverud et al. 1991; Leigh 1996; Leigh and Terranova1998; Hamada et al. 1999). Skeletal maturation, how-ever, has not been thoroughly studied (exceptions,Kimura and Hamada 1990, 1995, 1996; Watts 1971;Michejda 1987; Hamada et al. 1998; Nakai 2001), andthis is especially true of chimpanzees (Watts 1971;Marzke et al. 1996; Hamada et al. 1998).

Primates (2003) 44:259–271DOI 10.1007/s10329-003-0039-7

Yuzuru Hamada Æ Kaoru Chatani

Toshifumi Udono Æ Yasuhiro Kikuchi Æ Harumoto Gunji

Y. Hamada (&) Æ K. ChataniSection of Morphology, Primate Research Institute,Kyoto University, Inuyama, Aichi 484-8506, JapanE-mail: hamada@pri.kyoto-u.ac.jpTel.: +81-568-630521Fax: +81-568-615775

T. UdonoKumamoto Primate Park,Sanwa Kagaku Kenkyusho Co.,Nishikuroiwa 990, Misumi-cho,Uto-Gun, Kumamoto 869-3201, Japan

Y. KikuchiLaboratory of Anatomy,Saga Medical University,Nabeshima 5-1-1, Saga,Saga 849-8501, Japan

H. GunjiJapan Monkey Centre,Kanrin, Inuyama,Aichi 484-0081, Japan

Skeletal maturation has been studied by severalmethods, based mainly on the observation of epiphysealdevelopment and its fusion with the endophysis. Thedevelopment and fusion of the epiphysis is closelyrelated to growth in linear dimensions, and skeletalmaturation is regarded as a fundamental aspect ofmaturation in mammals.

Bone maturation has been evaluated by many meth-ods, including the fusion of epiphyses using dry bones(Kimura and Hamada 1990; Nakai 2001), the appear-ance of primary and secondary ossification centres usingradiographs (Nissen and Riesen 1949), and shapechanges and fusion of the epiphysis. There are a varietyof techniques for assessment of the latter method: theatlas method (Todd 1937; Owada and Sutow 1953;Greulick and Pyle 1959; Sugiura and Nakazawa 1976,for humans; Michejda 1987, for rhesus macaques andhumans), the scoring method based on observations ineach of the epiphyses or carpal bones (TW1 and TW2methods; Tanner et al. 1962, 1975), or a method com-bining both observation and measurement (Fels method;Roche et al. 1988). Some of these techniques are notapplicable to non-human primates but others are, forexample the RUS system (Radius, Ulna and Shortbones) of the TW methods, at least in the staging pro-cess.

The species ‘‘norm’’ of bone maturation is importantas a basic parameter of growth and development, andelucidation of the norm is an intermediate goal forcomparison between species. In order to establish aspecies norm, cross-sectional studies are necessary toobtain the outline and degree of variation among indi-viduals and longitudinal studies are necessary to revealthe systematic change of pace in growth and develop-ment as in, for example, the adolescent growth spurt(Tanner 1962). Such studies on great apes are difficult toconduct because the number of subjects accessible forgrowth study is limited and the period from birth tomaturity is quite long.

In applying the TW1 method, Watts (1971) gave thespecies norm of the RUS skeletal system for rhesusmacaques and chimpanzees. Although her study wasbased on longitudinal data, she determined the normfrom a cross-sectional analysis. In applying the TW2method on cross-sectional data, Hamada et al. (1998)presented distance and pseudo-velocity curves of RUSmaturation in chimpanzees. Although the curves looksimilar to those of humans, there are quantitative dif-ferences between the two species, for example, in dura-tion from the age at peak velocity to the age at fullmaturity.

A longitudinal study on chimpanzees is expected toestablish the norm, to highlight individual variation, topinpoint the causes of variation, and to find the mech-anism by which such causes originate. Growth anddevelopment are under the influence of various factors inchimpanzees (Hamada and Udono 2002), and theirinfluence is expressed by changes in the tempo andvelocity of growth and development.

In the present study, we tried to establish the speciesnorm of maturation in the RUS skeletal system and thegrowth of anterior trunk length (ATL) in chimpanzees,and we discuss whether RUS skeletal maturation servesas a good indicator of ‘‘physiological age’’.

Methods

Subjects

Chimpanzees (Pan troglodytes) reared at the Kumamoto PrimatePark of Sanwa-Kagaku (pharmaceutical) Co. (hereafter Sanwa)and at the Primate Research Institute of Kyoto University (PRI)were used for the study. Chronological ages were known for themajority of subjects, except for several older individuals who hadbeen imported without exact records of birth date. Their ages wereestimated from the records of inspection at their arrival. Underanaesthesia, somatometry and X-rays of hand and wrist bones weremade. Details of rearing conditions and environments, and themethod of anaesthesia have been described elsewhere (Hamadaet al. 1996, 1998; Hamada and Udono 2002). Our study satisfiedthe guidelines of care and use of experimental primates in Sanwaand PRI, and our research program was permitted by the ethicscommittees of each institute.

Subjects for the longitudinal study

We observed radiographs taken longitudinally from a total oftwelve chimpanzees (P. troglodytes, seven females and five males) atintervals of 6 months or less. The name of subjects, number ofradiographs, and period of observation are listed in Table 1. Birthdates, ages at reproductive maturation, and rearing conditions aredescribed in Hamada and Udono (2002).

Subjects for the cross-sectional study

Skeletal maturation and ATL was measured in a total of 82chimpanzees (48 females and 34 males, Table 2). Longitudinal datawere also included in the cross-sectional analyses. A total of 432sets of data were obtained (242 for females and 190 for males).Subjects who were not incorporated into the longitudinal study butwere measured and had radiographs taken more than once werenot paid special attention other than to obtain parameters for age

Table 1 Ages at the beginning and end of longitudinal data col-lection

Name Radiograph Anterior trunk length

Start End N Start End N

Female Fuku 0.25 10.99 22 0.25 10.99 23Inko 1.30 13.24 23 1.30 13.24 25Pan 0.00 12.45 34 0.00 17.02 39Pearl 1.30 13.24 15 1.30 13.24 15Popo 1.17 14.21 27 0.08 16.30 37Yoko 1.19 13.13 18 1.19 13.13 19Yoshie 0.57 12.51 25 0.57 12.52 25

Total 164 Total 183

Male Jiro 1.33 13.27 24 1.33 12.87 23Mizuo 0.36 12.30 25 0.36 12.30 25Nicky 1.53 13.47 24 1.53 13.47 25Reo 0.01 14.01 36 0.01 14.01 37Tick 1.52 13.46 24 1.52 13.46 25

Total 133 Total 135

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classes (for example, the median ATL for each age class) as will beexplained.

Evaluation of skeletal maturation

We followed the same protocol of X-ray filming of hand and wristbones as described by Hamada and his colleagues (1998). Followingstrictly the TW2 textbook (Tanner et al. 1975), we evaluated thedegree ofmaturity in each epiphyseal part of hand andwrist bones ofthe RUS system, that is, distal epiphyses of the radius and ulna, andepiphyses of metacarpals and phalanges of the first, third, and fifthfingers. The two observers (Y. Hamada and a technician) evaluatedthe stages more than once, and the most frequent stage was used asthe representative. The stages were determined from A to I for allbones except ulna which were from A to H. The total of maturityscores, which were listed for each of the epiphyses, for each of thestages, and for each sex in the textbook, was calculated. We describehereafter the total as the RUS score. A fully matured individual isevaluated as having a RUS score of 1,000.

We also analysed RUS skeletal maturation by simple scores,which were obtained as follows. Scores were given to each epiph-ysis, a score of 0 to stage A, 1 to stage B, etc, and 8 to stage I, andwere then totalled. The simple score was 103 at full maturity.

Anterior trunk length (ATL)

We measured the anterior trunk length, that is the distance fromthe cranial tip of the sternum to the cranial tip of the pubicsymphysis. We used an anthropometer and read up to the wholemillimetre (less than 1 mm was cut off).

Numerical analyses

Cross-sectional analysis for age change pattern in RUS scoreand ATL

Age-change pattern was first described from the cross-sectional dataof RUS score and ATL. The data were divided into age classes, andthen average age, and median, 10th and 90th percentiles of ATL orRUS score were obtained for each class. In cases of more than onedatum from the same individual, average age andRUS score or ATLwere calculated to represent the datum for that individual in the ageclass, to minimise the bias of a given individual. Curves of median,

10th and 90th percentiles against age were smoothed by theLoess.smooth function (S-Plus 4.0, MathSoft Co.).

Estimation of ages at ATL growth cessationand at RUS skeletal maturity

It is rather difficult to estimate the ages at which growth andmaturation cease, because there are inevitable measurement andobservation errors and the interval of observation varies. There-fore, researchers have adopted various ways to determine the ages.For example, Watts (1971) roughly gave the maturation age forchimpanzees as 12 years, many researchers determined by ‘‘rule ofthumb’’ or by ‘‘eyes’’ (Cheverud et al. 1991; Leigh 1996), and someused segmental regression analysis (Chen et al. 2000). Estimation ofthe age at ATL growth cessation in the present study was madefrom longitudinal data as follows: first, ‘‘adult size’’ was deter-mined, that is the maximal size was found in the data series, and themaximal ATL and ATLs of the two measurements closest to theage at the maximal ATL were averaged; second, the age was cal-culated by proportional allotment between two data, one of whichATL becomes larger than the adult size for the first time and an-other is the datum which is one measurement previous to that in thelongitudinal data series. For cross-sectional data, the age at whichATL growth ceases was estimated in the same way as that forlongitudinal data, regarding the median of age class as individualATL. As the age at ATL growth cessation is approximately12 years, the adult ATL for cross-sectional data was calculated bythe average of ATL from the data of 12 years of age or older.

Age at RUS skeletal maturity was determined for the longitu-dinal data series as the average of the first age (ith) at which theRUS score attained 1,000 and the age which is one observationprevious to that (i-1th) in the longitudinal data series. In caseswhere one RUS score was evaluated as 1,000 (ith radiograph) butthe score of the next radiograph (i+1th) was smaller than 1,000,and then the score attained 1,000 again (i+2th), age at RUSskeletal maturity was obtained by the average of age from i)1th toi+2th. Age at RUS skeletal maturity was estimated for cross-sec-tional data by logistic analysis as follows (an alternative of thesurvival or probit methods; Kuykendall et al. 1992): first, frequency(p) of individuals, whose scores are evaluated as 1,000, was calcu-lated for each age class from 7 to 12 years; second, logit was cal-culated as log [p/(1-p)]; and third, linear regression was calculatedbetween the logits and the ages of classes (e.g. 7.5 years of age forage class 7). In six age classes from 7 to 12, p in the age class 7 canbe 0 and/or p in the age class 12 can be 1. In such cases, the ageclass(es) with p of 0 or 1 was (were) not used in the calculation ofregression. When more than one data from the same individualwere included in an age class, we used one representative state forthat individual. It was counted as matured if the first age atmaturity of that individual was younger than the representative ageof the class. Although iteration method is recommended to calcu-late the parameters of regression (Sokal and Rohlf 1995), we usedthe least square method because the number of age classes was notlarge. Ages at which frequencies of RUS skeletal maturity are 0.1,0.5 and 0.9 were calculated from the regression function.

Longitudinal analysis of ATL and RUS score

Relative ATL (%ATL) was calculated for each subject for longi-tudinal analysis against its adult ATL. The curves of age change of%ATL and RUS-score were smoothed by Loess.smooth function.By the application of that function, we obtained 50 pairs of dis-tance parameters (age, score) or (age, %ATL), and we calculatedpseudo-velocity from two consecutive parameters as (score2 )score1)/(age2 – age1) or (%ATL2 ) %ATL1)/(age2 – age1). Residualcurves were used for the analysis of growth fluctuations. They werecalculated by the subtraction of %ATL or RUS score of the subjectfrom that obtained from cross-sectional data, and were smoothedby a multiple regression function (5th or 6th order; Excel, Micro-soft).

Table 2 Cross-sectional data obtained for anterior trunk lengths(ATL) and radiographs

Age (years) Female Male Total

0.00–0.99 21 23 441.00–1.99 24 17 412.00–2.99 23 14 373.00–3.99 23 15 384.00–4.99 16 14 305.00–5.99 12 12 246.00–6.99 13 14 277.00–7.99 15 10 258.00–8.99 18 13 319.00–9.99 17 13 3010.00–10.99 13 11 2411.00–11.99 13 11 2412.00–12.99 10 8 1813.00–14.99 12 11 2315.00–19.99 9 3 12‡20.00 3 1 4Total 242 190 432

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Establishment of species norm of growth and maturation

Combining the cross-sectional and longitudinal analyses, we triedto obtain the species norm of the velocity curves of RUS skeletalmaturation and ATL growth in chimpanzees. First, a global-fittingpseudo-velocity curve was obtained from the cross-sectional data.Second, a longitudinal curve was examined to find systematicfluctuations of smaller scale, which are often concealed by theaveraging in cross-sectional analysis (e.g. adolescent growth spurt;Tanner 1962). The great fluctuation, which is not found in thecross-sectional velocity curve, is considered to reflect the non-inherent influences on growth. Therefore, we observed residualcurves to pick up subjects who did not show great fluctuations intheir curves. We pooled their velocity parameters, and calculated acurve with the Loess.smooth function. Thus, the norm in thepresent study is by no means based on strict statistical procedures.It should be refined by the addition of longitudinal subjects andappropriate statistical procedures in the future.

Results

ATL growth curve and variationfrom cross-sectional analysis

Growth curves of anterior trunk length (ATL) formedian, 10th and 90th percentiles are shown in Fig. 1a.The median ATL curve of females looks to be a simpleparabolic and ATL appears to stop growing (matura-tion) at about 12 years of age. The age and ATL atmaturation in females are estimated as 11.77 years and470 mm, respectively, and the adult average ATL is489.85 mm (SD =27.22, n =33). As shown by thecurves of the 10th and 90th percentiles, variation is notwide.

The median ATL growth curve in males follows thesame trajectory of that in females from birth to 6 yearsof age, where the velocity of males becomes greater thanthat of females. The age and ATL at its maturation inmales are estimated as 12.10 years and about 510 mm,and the adult average ATL is 511.77 mm (SD =21.21,n=21). Sex difference in adult average ATLs is statisti-cally significant (p=0.15%, t-test). However, the ages at

which ATL ceased its growth do not significantly differbetween sexes. Thus, the small sex difference in ATL,around 5%, does not appear to be produced by thedifference in the growth period (bimaturism) but by thegreater velocity in males from 6 to 12 years of age, thatis, the preadult (adolescent) growth (Leigh 1996).

The pseudo-velocity curve of ATL starts with 50 mm/year in females (Fig. 1b, c), and then the velocitydecreases linearly with age until growth cessation. Thepace of decrease in velocity appears to become slower atthe age of six. In males, pseudo-velocity starts withabout 50 mm/year, and it rapidly decreases to about30 mm/year at 5 years of age. The pace of deceleration isslowed down in the period from 5 to 9 years of age, andthen it becomes faster again up to growth cessation.

Age change curve and variation in RUS skeletalmaturation from cross-sectional analysis

An age change curve was obtained for RUS skeletalmaturation from the cross-sectional data (Fig. 2a). Themedian RUS score in females linearly increases with ageuntil about 8 years of age, and then the pace of increasebecomes slower and attains 1,000 (maturity) at about12.5 years of age. The median curve in males starts froma similar score to that in females, increases at a slowerpace and passes below that of females. From about5 years of age, the velocity gradually increases and thecurve of males becomes closer to that of females.Therefore, sex difference is the widest, about a score of190, at the age of 5 years. The pace slows at about9 years of age and the RUS skeletal system attainsmaturity at about 12 years of age. The age at RUSmaturity in males appears to be a little younger than thatin females.

Deviation diagrams of 10th and 90th percentiles(Fig. 2b) showed that the widest variation is found atabout 6 years of age in both the 10th and 90th percen-tiles in females, and at about 9 years of age in males. The

Fig. 1a, b Anterior trunklength (ATL) growth curves.Line graph for males anddotted-line graph for females.a Distance curves of median,10th percentile, and 90thpercentile, and b pseudo-velocity curve obtained fromthe median curve of the distancegrowth

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deviation in the 10th percentile of females is the greatestamong either percentile of the two sexes.

Although the median curve of the RUS score in malesis located lower than that in females, it does not neces-sarily mean that males are less mature than females at agiven age. This is because the TW2 method producesdifferent scores for the same stage of a given epiphysisfor males and females. Therefore, RUS simple scoreswere compared between sexes to find that a similar resultwas obtained, that is, males are less mature than femalesof the same age in the immature period.

Age at RUS maturity was estimated by means oflogistic analysis (Table 3). Ages at which 90% of indi-viduals have attained a score of 1,000 are 12.17 and11.44 years in females and males, respectively. This re-sult supports the notion mentioned before that malesmay mature slightly earlier than females, but we mustwait for the accumulation of data to conclude so. It isimportant to remark here that the RUS skeletal systemmatures at almost the same age as ATL ceases itsgrowth.

Pseudo-velocity curves of the RUS score differ fairlywidely between sexes (Fig. 2c). The velocity of about100 increment/year is maintained from infancy toabout 8 years of age in females, and then it linearly

decreases with age. Thus, the curve in females iscomposed of two phases which are demarcated by theinflection point at 8 years of age. The curve in males,on the other hand, looks complicated. In earlierinfancy, the velocity is about 40 increment/year untilthe age of 2 years, and then it accelerates to about130 increment/year at 8 years of age. From 8 years, thevelocity decreases to 0 at about 12 years of age. Thus,the velocity curve is parabolic in general, but in detailthere are changes in pace at 2, 4, 6, 8, and 10 years ofage.

Longitudinal analysis on ages at RUS maturityand ATL growth cessation and growth fluctuations

Ages at RUS maturity and ATL growth cessation, andadult ATL estimated for each of the subjects longitudi-nally studied are listed in Table 4.

Fig. 2a–c Age change curves for the radius, ulna, and short bones(RUS) skeletal system. Line graph for males and dotted-line graphfor females. a Distance curves of median, 10th percentile, and 90thpercentile. b Deviation diagram between the median and 10thpercentile (lower half) and between median and 90th percentile(upper half). c Pseudo-velocity curve obtained from the parametersof the median distance curve

Table 4 Anterior trunk length (ATL; mm) at maturity and ages atmaturity of ATL and RUS (radius, ulna, short bones)

Name ATL RUS

mm Age Age

FemaleCross-sectional 487.5 12.10 12.50Longitudinal Fuku 450.7 10.41 10.86

Inko 517.0 11.93 10.62Pan 498.5 15.25 11.99Pearl 472.5 13.04 10.78Popo 503.4 11.39 11.28Yoko 478.0 11.52 9.95Yoshie 487.7 11.98 9.89Av. 486.83 12.217 10.767

MaleCross-sectional 509.5 11.77 11.91Longitudinal Jiro 526.0 12.87 11.13

Mizuo 518.0 10.73 10.58Nicky 512.4 10.53 10.85Reo 535.3 13.00 10.27Tick 516.8 11.66 9.83Av. 521.70 11.758 10.532

Table 3 Age at RUS maturity (RUS system = radius, ulna, andshort bones) as estimated by logistic analysis

Frequency Female Male

0.1 9.25 9.610.5 10.71 10.530.9 12.17 11.44

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General view of variation

We first examined whether there are common (consis-tent) fluctuations in residual curves of the RUS score.Wide individual variation may conceal systematic fluc-tuations in cross-sectional analysis. Some female indi-viduals have similar residual curves of RUS and %ATL.Their residuals tend to be great (Yoshie, Pan, Pearl, andPopo; Fig. 3a). Others show different patterns in the twodiagrams (Yoko, Fuku, and Inko; Fig. 3b). Of the latterindividuals, Yoko and Inko have small residuals inabsolute values both for RUS score and %ATL, that is,RUS matures and %ATL grow in a similar way to thestandard. Although residuals of %ATL are great inFuku (the maximum was 6% at about 4 years of age),her residuals of RUS score are negative but not great inabsolute value and the score becomes positive from4 years of age.

In males, Mizuo has grown fast, as shown by hisresidual curve of %ATL (Fig. 3c), but his skeletal matu-ration proceeds in a similar way to the cross-sectionalcurves. Tick and Nicky’s patterns of growth and skeletalmaturation are similar way to those of the cross-sectionalcurves (Fig. 3d). The age change pattern of theRUS scorein Jiro follows the cross-sectional curve, but his residualsof%ATLbecame greater in adolescence,)5%at 10 yearsof age. Reo shows similar residual curves to those of Pan,with great ups and downs (Fig. 3e).

Common features in longitudinal pseudo-velocity curvesin ATL and the establishment of the norm

The pseudo-velocity curve of ATL obtained fromcross-sectional analysis has two inflection points at 5and 9 years of age in males. However, this pattern isnot always found in the longitudinal curves (Fig. 4a);the inflection point at 5 years of age was not clearlyshown. Although the curve of Reo has an inflectionpoint at that age, as described above, his growth pat-tern cannot be regarded as standard. On the otherhand, the curves of Mizuo and Tick are considered tobe close to the standard. The inflection point is foundat 6 years of age when the rapid growth in infant andjuvenile periods has ceased. After that the velocityis maintained until 8 or 9 years of age, and then itdecreases rapidly.

In females, the cross-sectional pseudo-velocity curveis linear with a slight change of pace at about 6 yearsof age. Many individuals have curves similar to thecross-sectional curve (Fuku, Inko, Popo, and Yoshie),but the inflection at 6 years of age is not always found(Fig. 4b). In the other three individuals, like Pan inFig. 4b, velocities are smaller than that of the cross-sectional curve until about 6 years of age, and thenthey become larger (catch-up). It is probable that thepresence of such individuals produced the slightinflection point at that age in the cross-sectionalpseudo-velocity curve.

From these considerations, the males Mizuo andTick, and the females Fuku, Inko, Popo, and Yoshiewere picked to obtain the norms of velocity curves ofATL. The curves were calculated by the loess.smoothfunction applied to their velocity parameters pooled inthe two sexes (Fig. 5).

Fig. 3a–e Residual curves of RUS score and %ATL for longitu-dinal subjects from the cross-sectional median curve. Line graphsfor RUS maturation and dotted-line graphs for %ATL growth.a Deviations are well correlated with each other, in Pan (female).bDeviations are not correlated, in Inko (female). c Fast growth in amale, Mizuo. d Standard growth in a male, Nicky. e Delayedgrowth in the periadolescent period, in Reo (male)

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Common features in longitudinal pseudo-velocity curvesin RUS maturation and the establishment of the norm

The cross-sectional pseudo-velocity curve of the RUSscore is composed of acceleration and decelerationphases in males. Jiro, Mizuo, Nicky and Tick havesimilar curves (Fig. 6a). Considerable variation is foundin ages at the inflection points and at about 10 years ofage some individuals show great acceleration and othersdo not. Their velocity parameters were used for thecalculation of the norm curve.

In females, longitudinal pseudo-velocity curves of theRUS score look different from the cross-sectionalpseudo-velocity curve. The curves of Fuku, Inko, andYoshie are similar to each other (Fig. 6b). The age at thepeak and the height of the peak vary with individual.After 8 years of age, velocities in these three femalesdecrease rapidly, but the deceleration is suppressed orthe velocity is even accelerated in the period between 9and 11 years of age. If we consider the pattern found inmales to also underlie that of females, variations of thelongitudinal curves in females are explained withoutdifficulty. The velocity curve of females is not consideredto have a peak at about 8 years of age but between 4 and6 years of age, and has another variable inflection point

at about 10 years of age. The other three individuals(Pan, Pearl, and Popo), who were considered to havesuffered from environmental influences in their growthand development, are considered to have a deviatedpattern to their RUS pseudo-velocity curve. Theirparameters of pseudo-velocity were not, therefore, usedfor the calculation of species ‘‘norm’’, but those of Fuku,Inko, and Yoko were.

From these considerations, probable norms ofvelocity curves of the RUS score in the two sexes ofchimpanzees were obtained (Fig. 7).

Interrelationships between skeletal maturation,ATL growth, and reproductive maturation

The interrelationships between skeletal maturation,ATL growth, and reproductive maturation were exam-ined. The age of maturation is defined as the age atmenarche in females (see Table 1 of Hamada andUdono 2002) and the age at which the testicular sizereaches 100 cm3 (semi-maturation) in males. The aver-age RUS score and %ATL at menarche (average age=8.70 years, range 7.7–10.6) are 831.7 and 91.69%,respectively. The coefficient of correlation between age

Fig. 4 Longitudinal pseudo-velocity curves of ATL instandard and aberrant(influenced by environmentalfactors) subjects and cross-sectional curve: for males,Mizuo (standard) and Reo(aberrant; a), and for females,Inko (standard) and Pan(aberrant; b)

Fig. 5a, b Norm of the %ATLgrowth curves in chimpanzees.a Velocity curve and b distancecurve obtained from velocityparameters. Line graph formales and dotted-line graph forfemales

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at menarche and RUS score is 0.634, and that betweenage at menarche and %ATL is 0.662. In males, theaverage RUS score and %ATL at the age of testicularsemi-maturation (average age =8.70 years, range 7.7–9.8) are 721.1 and 91.02%, respectively. The coefficientof correlation between age at testicular semi-maturationand RUS score is 0.626, and that between age attesticular semi-maturation and %ATL is 0.839.

Factors causing variation and the evaluationof their influences

Nutrition The influence of the difference in nursery carefor younger infants was assessed, that is, the ATL andRUS score at the age of 1.5 years were compared be-tween groups of artificially-cared-for (bottle fed) andmaternally-cared-for (breast fed) individuals (Table 5).The average (SD) of RUS score residuals, from indi-vidual variation, are )11.63 (42.25) and )14.23 (36.86)

Fig. 7a, b Norm of the RUS-maturation curve inchimpanzees. a Velocity curveand b distance curve obtainedfrom velocity parameters. Linegraph for males and dotted-linegraph for females

Fig. 6a, b Longitudinal pseudo-velocity curves of RUS score instandard and aberrant(influenced by environmentalfactors) subjects and cross-sectional curve. a Males, Mizuo(standard) and Reo (aberrant);b females, Inko (standard) andPan (aberrant)

Table 5 Comparison of growth and development between mater-nally- and artificially-cared-for groups: %ATL-residual and RUS-residual at 1.5 years of age

Name %ATL-residual RUS-residual

Maternally-caredfor

Pearl )4.06 0.58Yoko )1.83 )46.05Reo )0.18 48.57Jiro )2.39 )3.60Tick )5.67 )57.66Average )2.825 )11.634SD 2.113 42.251

Artificially-caredfor

Popo 1.62 24.22Fuku R 3.60 )63.36Inko 0.52 )3.11Yoshie R 1.85 0.40Pan R 0.15 31.21Mizuo 1.33 )48.03Nicky 0.62 )40.92Average 1.384 )14.227SD 1.158 36.856

Difference inaverage p (t-test)

0.004 0.457

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in maternally- and artificially-cared-for groups, respec-tively, and the difference is not significant (t-test). On theother hand, averages of %ATL residuals are )2.83%(2.11) and 1.38% (1.16) in maternally- and artificially-cared-for groups, respectively, and the difference is sig-nificant (p <0.5%, t-test). Therefore, the difference incare, which perhaps reflects a nutritional difference, mayhave influenced ATL growth but not RUS maturation.

Social relationships Tick and Jiro were considered to bedifferently influenced by their social relationships inadolescence (Hamada and Udono 2002). Residual curvesboth of %ATL and RUS in Tick passed close to zero orwere a little positive. Tick matured skeletally at 9.8 yearsof age and ATL ceased growth at 11.66 years of age,attaining an adult size of 516.8 mm (Table 4). On theother hand, growth and skeletal maturation in Jiro wasdelayed in adolescence. Although his RUS residual dia-gram does not move widely apart from 0, he maturedskeletally as late as 11.13 years of age. The residual of%ATL became great from 7 to 10 years of age (maxi-mum deviation of )4.0%), and he attained his adult sizeof 526.0 mm at 12.87 years of age. The delay in skeletalmaturation was recovered by the rapid increase of scorein the latest period of growth (10–12 years of age; Fig. 8).

Environmental changes Three individuals reared at PRI,Pan, Popo and Reo, have experienced the same change inrearing environment after 2 years of age. Pan and Popowere separated from their mother soon after birth, andReo was separated at 2 years of age. After the separa-tion, they were reared together. The rearing environmentchanged from an indoor group cage to an indoor cagewith out-door ground (Hamada and Udono 2002), andthey were considered to be under similar environmentalinfluences as reflected by their similar residual curves of%ATL and RUS (see Fig. 3a for Pan and e for Reo).

Of the Sanwa chimpanzees, Pearl and Yoko experi-enced a significant environmental change; they wereleased to other institutes for bio-medical research. Yokodid not appear to have been heavily influenced by theenvironmental change, in comparison to Pearl, from herresidual diagrams of %ATL and RUS. She experiencedmenarche at 8.90 years of age, which is close to theaverage of 8.70 years. Pearl, as shown in Fig. 9, exhib-ited delayed growth of %ATL and maturation of RUSbefore she was leased, and just after she was returned toSanwa her growth and maturation states showed greatretardation (at maximum )9% in %ATL and)100 points in RUS score). The retardation in growthand maturation was also reflected by her age at menar-che, as old as 10.57 years. After her return to Sanwa,however, she caught up rapidly to complete her skeletalmaturation at nearly the average age of maturation forfemale chimpanzees (see Table 4).

Although most of the chimpanzees were reared in asocial group, there were a few individuals reared inindividual cages. They were the female Yoshie andmale Mizuo (see Fig. 3c). From the viewpoint ofgrowth and development, such individuals did notsuffer from environment. As shown in Table 4 by theRUS maturation and ATL growth scores, they ma-tured rather earlier than average.

Discussion

The chimpanzee (P. troglodytes) is the closest species tohumans in extant primates. Therefore, knowledge of itsgrowth and development, especially the establishment ofa species ‘‘norm’’, is important to understand the evo-lution of characteristic human growth and development.However, such knowledge is very scarce at present be-cause the population accessible for growth study is verysmall, as chimpanzees are large animals with a very longlife span and growth period. The collection of longitu-dinal data on a large scale is very difficult to realise, and

Fig. 8 Example showing the influence of social relationship on thepseudo-velocity curve of RUS maturation. Tick and Jiro grew up inthe same social troop and were socially ranked higher and lower,respectively. Arrows indicate the age at which their testes attained100 cm3 (semi-maturation)

Fig. 9 Example showing the influence of environmental change.Residual curve of Pearl, a female chimpanzee. Line graph for RUSmaturation and dotted-line graph for %ATL

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the ideal statistical analyses could not be made. There-fore, a combination of cross-sectional and longitudinalanalyses is necessary, as made in the present study.

Within the systems of growth, development and mat-uration, skeletal maturation is probably the least studiedsystem in chimpanzees (exceptions are Watts 1971; Mar-zke et al. 1996, on infants younger than 24 months of age;Matsuzawa et al. 1990, on wild chimpanzees; Hamadaet al. 1998). Based on radiographs collected at the Yerkeslaboratory, Watts (1971) presented the chimpanzee normof RUS skeletal maturation based on the TW1 method.However, her norm was elucidated from cross-sectionalanalysis. Therefore, her norm is considered to suffer fromaveraging (Tanner 1962). Analyses on longitudinalgrowth curves (distance and velocity) are needed.

The reason why longitudinal analyses are necessary isto discriminate systematic fluctuation from environ-mental fluctuation (noise) in the growth curves. Theintroduction of experimental settings to the growthstudy, that is, controlling the factors of the growthenvironment (e.g. nutrition), may facilitate the evalua-tion of environmental fluctuations. It also facilitatesdetermination of the reaction norm (Stearns 1981).However, as chimpanzees have a high intelligence, wemust refrain from causing them excessive stress in thecourse of growth research. Therefore, we must look intothe variations that are found when rearing in anuncontrolled environment. As anticipated, the variationbetween individuals is rather small in the present study.

It is possible to examine the details of local systematicfluctuation by the application of appropriate mathemat-ical models when the fluctuation patterns are known (forexample, a triple logistic function for the human heightgrowth curve; Bock et al. 1973). When we do not havesuch a priori knowledge of pattern, wemust make varioustrials to find the pattern. The adolescent (sub-adult)growth spurt is one of the possible systematic fluctuations.Watts (1971) used exponential function to smooth thegrowth curve, and she examined the spurt in chimpanzeesby finding a systematic deviation from the exponentialcurve. Leigh (1996) and Hamada and Udono (2002) ap-plied Loess’ smoothing function to discuss whetherchimpanzees and other species of primates have an ado-lescent growth spurt or not. However, we intended toexamine the systematic fluctuations within a wholegrowth period, and the adolescent spurt is just one ofthem.

Although the present study was based on asmall population of subjects reared under a standardisedenvironment, the norms of ATL growth andRUS skeletal maturation were established in chimpan-zees, combining the cross-sectional and longitudinalanalyses.

ATL growth in chimpanzees

Figure 5 shows the norm of ATL growth curves inchimpanzees. In the diagram, the early infantile period

from birth to 4 years of age has not been well elucidatedbecause of the paucity of data. Therefore the inflectionpoint at about 4 years of age is considered to be anartefact. This norm curve of ATL velocity in chimpan-zees is much different from the velocity growth curve ofhuman height, in which great changes of pace are found(see for example, Fig. 1.4 of Bogin 1999, p 29). Thevelocity curve of chimpanzees appears simple andalmost linear, and the velocity is highest in early infancyand it decreases until the cessation of growth. Detailedobservation showed that the curve in males is composedof three phases demarcated by two inflection points at 6and 8.5 years of age: (1) rapid deceleration from 0 to6 years of age, (2) slow deceleration from 6 to 8.5 yearsof age, and (3) rapid deceleration from 8.5 to 12 years ofage. In females, the curve is linear and phases are notclearly demarcated, but a slight inflection point is foundat about 8 years of age, where the pace of decelerationbecomes slower.

RUS skeletal maturation in chimpanzees

Based on the cross-sectional and longitudinal velocitycurves, the norm of the age change pattern of RUSskeletal maturation in chimpanzees was determined asshown in Fig. 7. In males, the norm velocity curve iscomposed of two phases: acceleration from early infancyto 8 years of age, and rapid deceleration from 8 to12 years of age. These major phases appear to be sepa-rated by additional inflection points at about 2, 4, 6, and10 years of age. Variation among individuals was foundin the heights and sharpness of peaks at 4 and 8 years ofage and the velocity at about 10 years of age (velocitycurves have a peak here in a couple of individuals).

The velocity curves of females are also composed oftwo phases with an inflection point at about 4 years ofage. Variation in velocity found at about 10 years of agewas wide, and some individuals had a sharp and highpeak in the velocity curve. The variation at 10 years ofage was found in both sexes, and it may reflect the finalstep of maturation at the distal epiphysis of radius (fromstage H to I) and/or ulna (from stage G to H). Thematurity score difference at the final step was fairlylarge, for example, in radius, 58 increments/year infemales and 75 in males. Therefore, it seems that thevariation of velocity curve at about 10 years of age isproduced by the variation of age at which the final stepsoccur. The shapes of velocity curves of the RUS scoreare similar between sexes, but the ages at the peak ofvelocity differ greatly (Fig. 7).

The velocity curve of chimpanzees differs greatlyfrom the incremental curve of the RUS score of humans(Fig. 9, p 16, of Tanner et al. 1975). The latter starts at1.5 years of age with 60 increment/year in males and95 increment/year in females. The annual incrementdecreases from that age to about 25 in the two sexes at4 years of age. In females from 4 to 8 years of age theannual increment is only slightly increased, and it

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accelerates steeply from 8.5 years of age to attain thepeak, at 14.5 years of age, of about 120 increment/year.The RUS skeletal system in females matures only1.5 years after the peak. As for males, small annualincrements of about 25 points/year in the infant andjuvenile period, are continued until 11.5 years of age.From that age they increase to reach the peak of about170 increment/year at 16.5 years of age, and shortlyafter that the RUS system matures (at 18.2 years of age).Thus, in humans, the maturation process is much sup-pressed in the juvenile period, much accelerated inadolescence, and ceases shortly after the peak. Thispattern looks similar to the velocity curve of height inhumans.

Comparison of skeletal maturation, growthof skeletal length, and reproductive maturationbetween chimpanzees and humans

The maturation of the RUS system and ATL growth arefast in infant and juvenile periods with a rather simplepattern in female chimpanzees. No inflection points inthe velocity curve were found in the period of puberty(6–8 years of age). On the other hand, in males,although the ATL grows at the same velocity as thatin females before puberty, the deceleration of growthwas weak in the period of puberty. Puberty is the periodin which reproductive maturation proceeds rapidly, asshown by the age change curve of testicular volume (seeFig. 4 of Hamada and Udono 2002). This weakerdeceleration of ATL velocity in males produces the sexdifference in ATL after the onset of puberty. In the caseof RUS skeletal maturation, a similar difference in agechange pattern was found. The maturation processes infemales were more advanced than those in males in theperiods of infant and juvenile (birth to about 6 years ofage). On the other hand, RUS scores are greatly in-creased in the early adolescent period in males. By dif-ferent velocity patterns, the two sexes mature at similarages at about 12 years. It appears that the delayedskeletal maturation in males gives the potential forgreater ATL growth than in females in early adolescence(6–8 years of age). The results lead to the hypothesis thatskeletal maturation, growth of skeletal length, andreproductive maturation are linked in early adolescencein male chimpanzees but not in females.

In humans, velocity curves of stature and the incre-mental curve of RUS skeletal maturation do not differmuch in pattern between the two sexes. Accelerations inthe two sexes are found to be coincident with the arrival ofpuberty both in the growth of skeletal length and inskeletal maturation. Ages at the peak of the incrementalcurve of RUS in humans are 14.5 and 16.5 years in fe-males and males, respectively (from Fig. 9, Tanner et al.1975). These ages are older than the ages at ‘‘peak heightvelocity’’ from the Harpenden Growth Research Project(Marshall 1974; 12.3 and 13.9 years of age for females andmales, respectively), by 2.2 and 2.6 years respectively. For

reproductive maturation, the age at genital stage 2 is11.5 years and that at genital stage 5 is 14.5 years, andthose at breast stages 2 and 5 are 11.0 and 14.0 years,respectively. Skeletal maturation, growth of skeletallength, and reproductive maturation are linked in earlyadolescence in both sexes in humans; the characteristicgrowth phenomena are found to be coincident with eachother. This coupling is produced by the control of repro-duction-related hormones (Bogin 1999). It is probablethat growth and development in adolescent chimpanzeesis under the control of reproduction-related hormone inmales, but not in females. Analysing body mass growth,Leigh (1996) also reported that chimpanzees show a ‘‘sub-adult’’ growth spurt in males but not in females.

From the above considerations, it is hominid femalesthat have evolved overall growth and maturation tocouple with puberty-related reproductive maturation.Male chimpanzees show rudimentary coupling.

Variation of growth and maturation in chimpanzees

Being based on a small population of subjects, we couldnot definitely explain the environmental influences ongrowth and maturation but some of them, nutrition,social relationship, and rearing environment, could beanalysed.

The difference in care was not reflected in RUSmaturation but in ATL growth as shown in Table 5.Wild infants (Gombe and Mahale populations; Ueharaand Nishida 1987; Pusey 1978) grow more slowly thanthose artificially reared (Grether and Yerkes 1940, onYerkes population; Hamada et al. 1996, on Sanwapopulations; see Fig. 2(1) of Hamada et al. 1996). In-fants cannot take foods independently and must rely onprovision by caretakers, and the condition of provisioninfluences the growth of body mass. The velocity of massgrowth in wild chimpanzees is comparable to that inartificially reared chimpanzees in the juvenile period(Hamada et al. 1996), though there is a rather widevariation in the juvenile growth of wild chimpanzeesaccording to the mother’s social rank in the troop (Puseyet al. 1997). Skeletal maturation in wild chimpanzees isthe future research subject (case report, Matsuzawa et al.1990).

Social relationships (or order in a hierarchy) influencethe growth of adolescent male chimpanzees. Tick andJiro were an example of this influence (Hamada andUdono 2002). The influence was also proved by theskeletal maturation data in the present study. Afterexperiencing puberty, the influence becomes significant.The ATL growth and RUS maturation in Jiro (lowranking male) were much delayed compared with thosein Tick (high ranking male). As a result, Jiro maturedlater than Tick. However, the influence was not toostrong for Jiro to reach his genetically determined adultsize.

Three PRI chimpanzees were reared in the same cageafter separation from their mother in early infancy.

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Although we could not identify the cause, they showedsimilar patterns of fluctuation in growth and matura-tion. Growth and maturation were much delayed in thejuvenile period and much accelerated (catch-up) inadolescence. One of the Sanwa chimpanzees, Pearl, whowas leased to another institute for a while, showed aconsiderable influence of rearing condition.

Chimpanzees are known to be highly social primates,and social deprivation could constitute severe stress andeffect growth and maturation. This is why rearing in asocial group is strongly recommended in the guidelinesof rearing and experimental use of primates. However, ifenough social contacts were provided, chimpanzeesreared in individual cages could grow well (Hamada andUdono 2002). Yoshie (female) and Mizuo (male) weresuch subjects, and they grew rapidly in %ATL andRUS. These examples may also stress the importance ofenough space or a refuge in a cage for chimpanzees toescape from excessive social conflict.

RUS skeletal maturation as a ‘‘physiological age’’

Here we consider only the intraspecific ‘‘physiologicalage’’. The issue of whether the RUS skeletal systemcould function as a physiological age across species ornot, especially between humans and chimpanzees, will bediscussed elsewhere from the perspective of life-historyevolution (e.g. Smith 1992) with comparable knowledgeof skeletal maturation of other species.

The stage of skeletal maturation has been regarded asthe physiological age or ‘‘biological age’’. Physiologicalage is expected to reflect the deviation of growth,accelerated or decelerated. This recognition is well ex-pressed by the title of the TW2 textbook that includesthe ‘‘prediction of adult height’’. The necessary condi-tions for such an ‘‘age’’ indicator are as follows: (1) aseries of many quantitative changes (stages) from birthto maturation, (2) the same order in the changes, (3) novariation in the state among matured individuals, and(4) the changes must reflect the variation in growth andmaturation in many other systems of growth. Theeruption of teeth possesses many of the necessary con-ditions, but the number of stages is limited and the orderof eruption is not always fixed (see Simpson et al. 1991).Physical dimension, such as stature, is also a good ‘‘age’’indicator but only when the adult dimension is known.

RUS skeletal maturation is considered to fulfil theconditions of a physiological age indicator. The increaseof RUS score starts at birth and ends at the same age orslightly younger than the age when ATL reaches theadult size. The age at RUS maturation is close to the ageat eruption of the last permanent teeth (maxillary thirdmolars), which is at 11.33 and 11.36 years of age infemales and males, respectively (Smith et al. 1994).It meets conditions 1–3. RUS skeletal maturationshowed fluctuation in parallel with ATL growth inindividuals with wide fluctuation (e.g. Pan and Reo). Thefact that the fluctuation in the former is also considered

to reflect various environmental influences shows thatRUS skeletal maturation also meets condition 4.

Acknowledgements We thank the staff of the Section of Morphol-ogy at PRI and of Sanwa Primate Park for their kind help andmany suggestions. We also thank Dr. I. Hayasaka (Director of theSanwa Primate Park) and Profs. T. Kimura and T. Matsuzawa whocontinuously encouraged us to follow the growth and developmentof chimpanzees. This research was supported by a grant-in-aid forCOE Research 2001, a grant-in-aid for Specially Promoted Re-search (COE) 2002, and grants-in-aid nos. 11833008 and 11304059from the Ministry of Education, Culture, Sports, Science andTechnology.

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