PRIMATES, 40(3): 439-452, July 1999 439

A d o l e s c e n t G r o w t h and D e v e l o p m e n t in Japanese M a c a q u e s

(Macacafuscata): Punc tua t ed A d o l e s c e n t G r o w t h

Spur t by Season

YUZURU I-IAMADA, SEIJI HAYAKAWA, JURI SUZUKI, and SATOSHI OHKURA

Kyoto University

ABSTRACT. Adolescent growth of Japanese macaques (Macaca fuscata) was studied. Their growth is composed both of a seasonal cycle of acceleration and deceleration and of linear increases. There is a major growth spurt in linear dimension and body weight at the beginning of the breeding season of the third and fourth year of life in females and males respectively, when they mature reproductively. They show additional accelerated growth in the following year(s). These growth spurts, in total, are considered to correspond with the adolescent growth spurt in humans. Adolescent growth of Japanese macaques is characterized by a punctuation by slower growth and a later start, which is considered to be the product of adaptation to a strongly seasonal environment.

Key Words: Adolescence; Adolescent growth spurt; Japanese macaques; Macacafuscata; Adapti'{e growth pattern.

INTRODUCTION

The first and major interest in the growth and development of non-human primates is whether they have an "adolescent growth spurt" corresponding to that of Homo sapiens. Although growth and development in non-human primates have been studied in a variety of species, it has not always been possible to examine adolescent growth and development into detail. The paucity of comparative studies makes the evolutionary consideration of the characteristic human adolescent growth and development difficult. LEIGH (1996) demonstrated spurts in body weight for many species of non-human primates. Researchers of human growth differ in their interpretation of the growth spurt in linear dimensions. For example, BOGIN (1993) regards it as an exclusive characteristic of humans. In contrast other authors (e.g. TANNER, 1962) regard the human pattern as common to primates or to some anthropoids.

Using longitudinal measurements, WATTS and GAVAN (WATTS • GAVAN, 1982; WATTS, 1985, 1986) demonstrate a spurt in linear dimension for rhesus monkeys (Macaca mulatta) and chim- panzees (Pan troglodytes). TANNER et al. (1990) showed that there was a significant acceleration in growth of linear dimensions for female rhesus monkeys. These reports, however, have not satisfied those researchers who hold the view that the spurt is exclusively human (BOGIN, 1993), as the magnitude of acceleration is too small and/or individual variation is wide. There are other reports that make the issue more confusing. For example, the cross-sectional study of HAMADA (1994) demonstrated that Japanese macaques have a spurt in linear dimensions, while other reports indicate that chimpanzees do not have a clear spurt (GAVAN, 1953, 1971; GAVAN & SWINDLER, 1966; HAMADA et al., 1996b).

The reason for this controversy about the adolescent spurt growth in non-human primates is that the design of experiments has not been suitable to demonstrate the spurt. Periods of whole

440 Y. HAMADA et al.

growth and of adolescence are much shorter in non-human primates than in humans, therefore, finding a rapid change needs frequent measurements and a special method of data analysis. TANNER et al. (1990), for example, measured their animals every three month, and used a simple incremental curve. WATTS and GAVAN (1982) used an exponential function, and they described adolescent growth as the systematic positive deviation of the original growth curve from the curve estimated from that function.

Desirable design of such a study with M. fuscata includes first the frequent measurement and secondly the use of suitable way of data analysis, ideally with measurements of less than a month. Suitable curve fitting or smoothing algorisms have recently been developed, and pro- gram packages such as SAS or S-Plus offer an easy access to these analyses. For example, Spline function (HAMADA et al., 1996a), or Loess function (LEIGH, 1992; HAMADA et al., 1998) have been applied to the study of growth in human and non-human primates. These analytical methods are not based on global fitting, which often gives a systematic deviation, but on local fitting and are thought to be better adapted to the changes OCCUlTing during adolescent growth and development.

We planned a longitudinal growth study project on Japanese macaques (Macaca fuscata), which is composed of sections dealing with somatometry, endocrinology, and skeletal matura- tion. Somatometrical data were collected every second week. Although the number of subjects was limited, longitudinal data analyses gives an insight into the norm and variation of adoles- cent growth and development in this species. We analyzed not only linear dimensions but also body weight, skinfold thickness, testis and teat size to monitor physical change in adolescence. Based on these results, we discuss whether Japanese macaques have an adolescent growth spurt and the characteristics of their growth pattern.

SUBJECTS AND METHODS

SUBJECTS

Ten Japanese macaques (five males and five females) reared at the Primate Research Institute of Kyoto University, were studied. They were born in 1992 and 1993, and the individuals were referred by their number registered at the Primate Research Institute: Nos. 1412, 1428, 1439, 1459, and 1470 for males; and Nos. 1433, 1447, 1458, 1460, and 1469 for females. As Japanese macaques are strict seasonal breeders, the birth dates of all subjects were from April to June. The study period extended from April 1995 to April 1998. All of the macaques were thus just less than 3 years of age at their enrollment in the project. As Japanese macaques have a wide geographical variation in physical dimensions (HAMADA et ah, 1996b), subjects were chosen from Wakasa and Takahama troops, which are known to have similar body dimensions that are close to the average for Japanese macaques. Their diet consisted of commercial monkey-chow, fed everyday in standardized volume according to body weight, with supplements of sweet potatoes and vegetables. The monkeys were kept together in group cages with both outdoor and indoor access.

External expression of reproductive states was observed and recorded photographically; an endocrinological profile was used to show the detail of their sexual maturation (SuzuKI, in prep.). Menarche was only observed in two of the females; however three female monkeys became pregnant and gave birth during the study period. Infants were separated from their mothers in the first week of life. The state of swelling of the sexual skin (peri-anal part of body) and the color of the face were observed in the females.

Adolescent Growth of Japanese Monkeys 441

MEASUREMENTS

The monkeys were measured somatometrically every second week under anesthesia, using a 2:1 volumetric mixture of ketamine hydrochloride (Ketalar 50, Sankyo Co. Ltd.) and xylazine hydrochloride (Selactar 2%, Bayer Co. Ltd.), in the dose of 0.15 cc/kg BW. Sitting height, thigh length, leg length, body weight, length and width of testis, and teat were measured to the near- est millimeter with an anthropometer and a sliding caliper. We used the sum of sitting height, thigh length, and leg length as a surrogate for heights (stature).

Testicular and teat volumes were analyzed. Approximating the testis as an ellipsoid, testicular volume (TV) was calculated as TV= 1/6. pi-L. W 2, in which pi, L, and W stand for the circular constant, length and width of the testis respectively. Approximating the teat as a cylinder, we calculated teat volume (MV) as M V = 1/4. pi. L. W 2. As teat measurements were only started in the second year of the present project, a detailed examination could not be made on its age change, but MV appears to indicate the state of sexual maturity.

Skinfold thickness was measured using Lange-type skinfold caliper (GPM Co. Ltd.) to the nearest 0.2 mm at five body sites: caudal aspect of upper arm (triceps), cranial aspect of thigh (quadriceps), belly lateral to the umbilicus, subscapular, and suprailiac. Summed thickness was analyzed.

ANALYSES

Distance growth curves were obtained using Loess smoothing function of S-Plus 4 (Mathsoft, Co. Ltd.). Coordinate values obtained for the distance growth curve were used to calculate the pseudo-velocity, that is the ratio between two neighboring coordinates, (xl, yl) and (x2, y2), as V l = ( y 2 - y l ) / ( x z - x l ) . A pseudo-velocity curve was drawn by connecting the pseudo-velocity against intermediate age, for example, (xz+xl)/2. Age at peak velocity, velocity at the peak, and size at peak velocity were estimated from the pseudo-velocity curves. Age at the Peak Height Velocity (PHV-age) was used to align individual growth curves.

RESULTS

ADOLESCENT SPURT IN HEIGHT AND GROWTH OF HEIGHT

The distance and velocity growth curves of height (Figs. 1 & 2) were first observed to deter- mine characteristic points, e.g. age at the beginning of accelerated growth. Velocity curves show a circannual (seasonal) cycle, and several peaks were observed during the study period. Acceleration phases were found at approximately 3, 4, and 5 yr of age in both sexes (Fig. 2). Therefore, the major adolescent spurt (acceleration phase) was decided from these acceleration phases by reference to the time at reproductive maturation. In males, the TV growth curves show that the first and great increase in volume occurred in the period from 4 to 4.5 yr of age, which coincides with a breeding season from autumn to winter. Females were observed to be reproductively mature in the breeding season of the third year of life, that is, at about 3.5 yr of age, and menarche was observed in two individuals at that time.

Age and velocity at the peak velocity is at approximately 3 yr of age in females and at around 4 yr of age in males (Table 1). Average ages at the peak height velocity (PHV) are 3.15 yr (standard deviation, SD-0.134) in females and 4.03 yr (SD=0.107) in males. Average velocities at PHV are as great as 79.43 mm/year (SD=21.392) in females and 122.21 mm/year (SD= 16.990) in males.

442

Table 1. Age, pseudo-velocity, and size at the peak velocity in adolescent Japanese

Male

Y. HAMADA et al.

macaques.

Height Body weight Skinfold-thickness

Subject Age Velocity Size Age Velocity Size Age Velocity Size

Testicular-volume

Age Velocity Size

1412 3.991 129.590 867.560 4.221 4.485 7.169 4.177 14.797 14.085 1428 3.990 101.560 858.440 4.211 3.817 6.938 4.355 21.632 15.171 1439 3.899 108.860 838.280 4.183 2.654 6.550 4.104 11.528 13.765 1459 4.176 143.930 889.010 4.304 7.101 8 . 4 1 1 4.303 24.094 15.004 1470 4.093 127.090 826.790 4.093 3.858 6.156 4.156 22.045 12.591

Average 4.030 122,206 856.016 4,202 4.383 7.045 4.219 18.819 14.123 SD 0.107 16,990 24.477 0,076 1.657 0,856 0,105 5.373 1.043

4.433 63.250 11.144 4.450 72.442 19.634 4.263 41931 5.855 4.498 102.701 17.045 4.351 33.619 5.980

4.399 62.789 11.932 0.093 27.259 6.294

Female

Height Body weight Skinfold-thickness

Subject Age Velocity Size Age Velocity Size Age Velocity Size

1433 3.056 96.405 804.520 3.182 5.180 6.045 3.218 49.747 19.224 1447 3.218 106.210 801.940 3.471 5:217 6.389 3.223 14.353 14.696 1458 3.100 65.930 760.460 3.399 3.457 5.540 3.395 11.528 15.224 1460 3.345 54.680 811.506 3.537 3.762 6.037 3.415 15.207 12.544 1469 3.019 73.930 729.328 3.275 2.503 4.359 3.317 23.298 13.357

Average 3.148 79,431 781,551 3.373 4,024 5.674 3,314 22.827 15.009 SD 0.133 21,391 35,400 0.144 1,169 0.795 0.093 15.672 2.584

D i s t ance g rowth curves o f ind iv idua l s are genera l ly paral lel to each o ther in ma le s (Fig. la) .

T h e pseudo-ve loc i ty cu rve (Fig. 2a) s h o w e d tha t there are acce le ra t ion phases at a round - 1.0,

0, and 1.0 yr of ad jus ted ages in males , and there is wide ind iv idua l var iat ion. No. 1470, for

example , g rew rapidly f rom - 1.0 to - 0 . 7 yr o f age. On the o ther hand, the g rowth cu rve of No.

1459 looks m o r e s t r a igh t fo rward but it was a lways the largest in the five males . The d i f fe rence

in he igh t a m o n g ind iv idua l s r anges f rom 50 to 70 mm.

g

,r,

1050

1000

950

900

850

800

750

700

q.S

' /

,/ , / /

t / ~ I

/ / / / / ' / .~

(a)

1412 1428 1439 1459

..... 1470 ~ A v .

1054

1001

95(

901

,~ gSC

80C

750

700

-1.5

/ ' /

/,

-1 -0.5 0 0.5 1 1.5 2 2.5 3 -1 -0.5 0 0.5 1 1.5

Adjusted age by PHV-age Adjusted age by PHV-agc

/

f . /

/ -

/ J

(b)

- - 1 4 3 3

---1447 -'-1458 --.-1460 .... 1469

, ~ A v . ,

2 2.5 3

Fig. 1. Distance growth curves of height. (a) Males; (b) females. Ages are adjusted by the PHV-ages of individuals.

Adolescent Growth of Japanese Monkeys 443

160

140

120

100 g

"~ 80

6o

40

20

{*

0

-1.5 -1 -0.5 0 0,5 1 1.5

] (a)

- - 1 4 1 2 1 ~ . . . . 14281

14391 ~\ 1459

1470 , - - - ~ , A v . .

2.5

;0

~0

',0

I0

:0

;0

J 0

:~ [ 0

-1.5 -1

(b)

i b I 1433 ;~'~ ~ 1447

I ~ ~ , - - - 1458 . . . . 1460

/ / I x .'~7~ p ----- 1469. I

I - - A v .

i i I [ . . . . .

-0.5 0 0.S 1 1.5 2 2.5 3

Adjusted age by PHV-age Ac[justed age by PHV-age

Fig. 2. Pseudo-velocity curves of height. (a) Males; (b) females. Ages are adjusted by the PHV-ages of individuals.

The peak velocities at 0 yr of adjusted age are the largest among three peak velocities in four subject males (excepting No. 1470). The exceptional male, No. 1439, experienced more rapid growth in the following year. The velocity at the peak ranges from 102 mm/year (No. 1428) to 144 mm/year (No. 1459). 'As described above, the growth in No. 1428 appears curious, and its velocity curve around 0 yr of adjusted age is not sharp but broad, and the period with the velocity larger than 80 mmlyear lasted as along as ten months. Nos. 1470 and 1459 show great velocity at around - 1.0 yr of adjusted age, while the other three do not. No. 1412 has an acceleration at -0 .5 yr of age. All individuals but No. 1439 had peaks of velocity or showed elevated velocity at around the adjusted age of 1.0 yr, but that were smaller in magnitude than those found at 0 yr of adjusted age.

Distance curves in females (Fig. l b) paralleled each other, that is, with alternating accelera- tion and deceleration of comparable amplitude; however, there were considerable individual size differences. Three monkeys, Nos. 1433, 1447, and 1460, grow almost in the same trajec- tory, and were larger than Nos. 1458 and 1469 by approximately 50 and 100 mm respectively.

As shown in Figure 2b, there were three peaks of pseudo-velocity in height of females, and the first at approximately 3 yr of age is the largest. No. 1460 had an additional acceleration in the period from 0.5 to 1.0 yr of adjusted age. All females had a second peak in velocity or a temporal stop in deceleration at around 1.0 yr of adjusted age. After this, pseudo-velocity greatly deceler- ated, with the velocity ranging from 20 to 35 mm per year. After this, only one individual, the smallest, No. 1469, showed a further acceleration while the others kept slow growth.

Sex differences in height growth were examined by the average curves (Fig. 3). The curves were obtained by the application of Loess smoothing function to the data of all individuals aligned by their PHV-age. Then the age was readjusted by the average PHV-age in each sex. At about 3 yr of age, the heights are estimated to be 759 and 778 mm in females and males respec- tively, and the sex difference was not large. Curves of both sexes showed that the difference was maintained until the age of 3.6 yr. In this period, although growth is accelerated in females, velocities of the two sexes are close to each other (Fig. 3b). From about 3.6 yr of age, sex dif- ference in velocity becomes wide, and the distance curve of male showed an acceleration. The difference in velocity was maintained with the result that the sex difference in height became larger, reaching 88 mm at 5 yr of age (Fig. 3a).

444 Y. HAMADA et al.

950

900

850

800

750

2.5

/ /

. . ~

# ,,,~

3.5

~ o~ ~

(a)

,~ M,,, ] I I I "'" Female I

i - - - - 1

i (b)

�9 1.- / r I

i_ Male i 1 I ] "'" Female I

4 4.5 5 5.5 2.5 3 3.5 4 4.5

Age (yr) Age (yr)

5 5.5

Fig. 3. Average growth curves of height. (a) Distance curve; (b) pseudo-velocity curve.

B O D Y W E I G H T

Distance curves of body weight in both sexes (Fig. 4) are similar to the pattern found with height, that is, an annual cycle of acceleration and deceleration of greater amplitude was super- imposed on the linear increase. Pseudo-velocity curve in males (Fig. 5a) clearly reveals the annual cycle, with a pattern of asymmetrical phases of increase (lasting eight months) alternat- ing with decrease (four months) in weight. This is indicated by the shorter period of negative velocity compared with the longer period of positive velocity. The linear growth component is approximately I kg/year.

l l ! I ( a ) I ( b )

9 !" ~12 '2 '

"/t : / " .....

.(/~ .... ~ .............. ~ - - 1 4 3 3 5 5 142~ / ..... ........................ . - - - 1 4 4 7

i - 1 4 3 9 / t 4 5 8 4 . . . . . 1 4 5 9 , : 1460 .

. . . . . . . 1 4 7 b , 1 4 6 9

A v . . - - A v . 3 r r

-1.5 -1 -0.5 0 0.5 1 1.5 2 2.5 3 -1.5 -1 -o,5 o 0.5 1 1.5 2 2.5 3

At[iusted age by PHV-age Adjusted age by PHV-age

F i g . 4 . Distance growth curves o f body weight. (a) Males; (b) females . Ages are adjusted by the PHV-ages o f individuals . I n ( b ) , triangles indicate the date o f parturition.

Adolescent Growth of Japanese Monkeys 445

4

A"

g o

-2

- 6

-L5

i [::

2

~wd

!

!i ,l

i

(a)

\

1412

1428

- - ' - 1439

- ' . -: 1459 1470

, - - A v .

g

f

- - - 1 4 3 3 . . . . 1447

- - - - 1458 - - . . - 1460

. . . . 1469

~ A v .

!

71 '

},/~"

] (b) f

-0.5 0 0,5 1 1.5 2 2.5 3 -1.5 -1 -0.5 0 0.5 1 1,5 2 2.5 3

Adjusted age by PHV-age Adjusted age by PHV.age

Fig. 5. Pseudo-velocity curve of body weight. (a) Males; (b) females. Ages are adjusted by the PHV-ages of individuals. In (b), triangles indicate the date of parturition.

Peak weights occurred at around -0 .5 , 0.5, and 1.5 yr of adjusted age in males, and bottom weights at - 0 .2 and 0.8 yr of adjusted age. At 0 yr of adjusted age, the age at peak height velocity, about 2.5 months have passed since the curve entered the increasing phase. Variation among individuals in males is wide and No. 1459 was always the heaviest, while Nos. 1439 and 1470 were the lightest.

Ages at peak velocity are found at -0 .8 and 0.2 yr of adjusted age in males (Fig. 5a). Velocity at the second peak is not much larger than that at the first peak. Three individuals born in 1992 show a third velocity peak at about 1.3 yr of adjusted age. At the first peak, there is a wide individual variation, and the peaks of Nos. 1428 and 1439 are later than those of other three individuals. Nos. 1459 and 1439 show cycles of the greatest and smallest amplitudes respectively.

Distance growth curve in females (Fig. 4b) shows a pattern similar to that of the males, but reproduction made the pattern complicated. Compared to males, females have a curve with a greater amplitude, especially No. 1433. Although, No. 1469 was lighter than any other individ- ual by more than 1 kg, its curve maintained a clear annual cycle. The first peak weight velocity occurs at about 0.2 yr of adjusted age with smaller variation and the first peak weight was attained at 0.4 yr of adjusted age (Fig. 5b). After the peak, weight entered a decreasing phase, reaching a bottom weight at 0.7 yr of age.

Second peak velocity occurs at about 1.2 yr of adjusted age but with wider variation caused by reproduction. Weight curves in non-pregnant individuals, Nos. 1433, 1460, and 1469 came to the second peak weight at about 1.4 yr of adjusted age, while those in pregnant individuals, Nos. 1447 and 1458, came later, at 1.7 and 1.8 yr of adjusted age respectively. The latter two macaques gave birth during the trough of their velocity curves (Fig. 5b, triangles). It took three months from conception to reach peak weight velocity.

From 2 yr of adjusted age, No. 1447, which did not become pregnant in that season, recov- ered the annual cycle as is shown by its age at the peak weight (2.3 yr of adjusted age). No. 1433, which was pregnant, experienced later peak than the non-pregnant individual; however, significant acceleration in weight gain was not found from conception to parturition in No.

446 Y. HAMADA et al.

26

24

22

20

z 18

.~ 16

14

12

10

8 -1.5

-! ! ~ i~

I ii' gi'

-1 -0.5 0 0.5 1 1.5 2

Adjusted age by pHV-age

I (a)

1412 . . . . . 1428

- - - - - 1439 1459

. . . . . . 1470 Av.

I 2.5 3

,/ ""i/

/',,(. ,, ,

m

i" 't

433 ib) 1447 [458 [460 I469 ~v.

-1.5 -1 -0.5 0 0.5 1 1.5 2 2.5 3

Ac[iusted age by PHV-age

Fig. 6. Age change in skinfold thickness. (a) Males; (b) females. Ages are adjusted by the PHV-ages of individuals. In (b), triangles indicate the date of parturition.

1433. It was noticed that there is a peak velocity before conception, which were observed at 9, 11, and 9 months before parturition in Nos. 1433, 1447, and 1458 respectively.

S K I N F O L D T H I C K N E S S

The distance curve of skinfold thickness looks similar to a sine curve and it does not show a net increase with age (Fig. 6). In males, peak thickness was observed at - 0 . 6 and 0.4 yr of adjusted age and least thickness was at - 0 . 2 and 0.8 yr of age (Fig. 6a), thus thickness changes resemble the cyclical pattern of weight growth. Skinfold is thickest in No. 1459 and its amplitude is strong, and those of Nos. 1428 and 1439 are thinner, with small amplitudes.

Curves of females are not as synchronized as in males (Fig. 6b). Amplitude of the cycle was the greatest in No. 1433. Reproduction affects skinfold thickness in a similar way as it does body weight.

T E S T I C U L A R V O L U M E (TV)

TV starts to increase rapidly at around 0 yr of adjusted years (Fig. 7a), with the peak velocity attained at 0.38 yr of adjusted age (Fig. 7b). The peak TV was attained age at approximately 0.5 yr of adjusted age. The maturity states expressed by TV appear wide in the fourth year of life; TV ranged from 8 cm 3 in No. 1470 to 26 cm 3 in Nos. 1428 and 1459. Alter the peak, velocity decreased quickly to negative values, that is, TV shrank.

Three individuals born in 1992 experienced a second great increase in the filth year of life, which made TV enlarge from 37 to 53 cm 3 in the breeding season, at 1.5 yr of adjusted age. Then TV decreases rapidly again. Within the two males born in 1993, No. 1470 is expected to fully mature in the breeding season of the fifth year of life. It is noteworthy that TV of No. 1459 was 7 cm 3 at - 0 . 5 yr of adjusted age. This individual may be an early-maturer, expressing a partial maturation in the breeding season in the third year of life.

Adolescent Growth of Japanese Monkeys 447

60

50

~" 40

_= 30

20

0

-1.5

, i li i

;", i tL '1 i

j i i : '~ d i,, /!

/ ~ , . / !

-1 -0.5 0 0.5 1 1.5 2

Adjusted age by PHV-age

(a)

i 11412

1421

. . . . 1 4 3 9

. . . . . 1 4 5 9

1 4 7 0

' ! ~ A v .

2.5 3

251

20~

151

~ . 10(

5,

o

c

-5~

-100

-150

-200

I i / )

/ , i l

i J

fl

, i t / [ i ~/ .! // IS t ~ i 1

,I

-1.5 -1 -0,5 0 0.5 1 1.5 2

Adjusted age by P H V - a g e

Fig. 7. Age change in testicular volume. (a) Distance curve; (b) pseudo-velocity curve.

(h)

- - 1 4 1 2

- - - 1421

- - 1 4 3 9

. . . . 1 4 5 9

. . . . . 147(1

- - A v .

,I

2.5 3

TEAT VOLUME (MV)

It was found that the variation in MV was wide between individuals, as is typically shown by No. 1447, which had the largest MV. The age change of MV appears to express the annual cycle and reproductive maturity in female individuals (Fig. 8), but longitudinal observation will be necessary to confirm this. The curves reflected a circannual cycle, and net increase as a whole is slight during the period of study. MV also reflected reproductive states, and peak MV's were found at 0.5 and 1.5 yr of adjusted age. Pregnancy and parturition were reflected by the curve in a similar fashion to body weight growth.

2.5

2

&

= 1.5

[ .

1 - - ~ 1 4 3 3

1447

0.5 " - . . . . 1 4 5 8 , . . . . 1460 . . . . . 1469

- - A v . o

-1.5 -1 -0.5

\,/

i J

f~

i tm, . ~ / / ?~, [ "

i l ' t

0 0.5 1 1.5

Adjusted age by PHV-age

\

2 2.5 3 Fig. 8. Age change in teat volume. Triangles indicate the date of parturition.

448 Y. HAMADA et al.

AGE ORDER IN PEAK VELOCITY AMONG DIMENSIONS

Table 1 also lists parameters for the adolescent growth spurt of other dimensions in Japanese macaques. The age order of peak velocity among somatometrical characters is height, body weight, and TV in males. The age order in females is similar to that in males; height, body weight, and MV.

DISCUSSION

ADOLESCENT GROWTH AND DEVELOPMENT IN JAPANESE MACAQUES

Whether or not non-human primates have an adolescent growth acceleration in linear dimension has long been one of the central issues concerning the evolution of human growth and develop- ment (e.g. WATTS, 1986; TANNER et al., 1990; BOGIN, 1997). Although a variety of anthropoid primate species have an adolescent (pre-adult) growth acceleration in body weight (LEIGH, 1996), it is necessary to demonstrate an adolescent growth spurt in linear (skeletal) dimensions. The adolescent growth spurt is defined for primates as the temporal great acceleration of growth (increase in size) concomitant with the reproductive maturation (puberty). Results on rhesus monkeys and chimpanzees (WATTS & GAVAN, 1982; TANNER et al., 1990) do not necessarily sat- isfy researchers of human auxology (e.g. BOGIN, 1997). Firstly, for a trivial reason, namely that growth of height (stature) has not been studied in non-human primates, so comparisons cannot be made with human auxological studies. The second reason is that the magnitude of growth acceleration in dimensions such as leg or crown-lump lengths is considered to be too small, or the sample size is too small.

The third and fundamentally the most important reason is that growth studies have not neces- sarily been designed specifically for non-human primates. Frequency of measurement is of par- ticular importance, as growth in non-human primates is more rapid, and is of shorter duration than in humans, so measurement must be made more frequently. This has made previous longi- tudinal studies on non-human primates difficult. The further factor concerns the methods of numerical analysis used in previous studies, e.g. exponential function (WATTS & GAVAN, 1982) or visually determined growth phases (SMITH et al., 1975). These do not give comparable growth parameters with those dealt with in the studies on human growth, e.g. age at peak velocity.

The present study was designed to fill some of these shortcomings. The first aim is to describe adolescent growth and development in Japanese macaques, and to examine whether Japanese macaques have an adolescent spurt corresponding to that in humans. Although the sample size is limited, the time interval between consecutive measurements was short, i.e. every two week. The estimate of height (stature), summed length of sitting height, thigh and leg was analyzed using local regression smoothing technique (Loess function of S-Plus 4) for compara- tive purposes. Distance and pseudo-velocity growth curves were o1" considerable value in delin- eating the pattern of growth and development in adolescent Japanese macaques.

Adolescent growth curves of height in Japanese macaques were found to be neither linear nor curved in a simple fashion, i.e. expressed by a simple function. The curves are composed both of circannual cycles of acceleration and deceleration, and of linear increase. The major adoles- cent growth spurt is superimposed to the annual acceleration phase at 3 -3 .5 yr and 4 -4 .5 yr of age in females and males respectively. Pseudo-velocity curves (Fig. 3b) clearly show that the peak velocity at these age periods is the largest among the annual peaks in the periadolescent growth period.

Adolescent Growth of Japanese Monkeys 449

In the period of major adolescent acceleration, which coincides with the season from summer to winter, Japanese macaques become heavier, accumulated body fat and matured reproduc- tively. Female macaques show a swelling of the sexual skin, a pinkish face color, and menarche in the third year of life. Teat volume showed a circannual cycle, the peak of which coincided with the breeding season. Male macaques are evaluated by their TV attaining reproductive maturation in the fourth year of life. The average maximum TV is 18.34 cm 3 (SD=7.457) at 0.552 yr of adjusted age (SD=0.124) on average. TV soon decreased after it reached the maxi- mum (Fig. 8).

The order in ages at peak velocity among physical dimensions in Japanese macaques studied here; height, body weight, and TV in males and MV in females; is comparable to those reported for humans in which the peak velocity of height comes earlier than that of body weight (e.g. MALINA & BOUCHARD, 1991). A similar order was reported for female rhesus monkeys, i.e. lin- ear dimension (leg and crown-rump lengths), body weight, and menarche (TANNER et al., 1990). Peak velocity in Japanese macaques was attained in the summer for height, in the autumn for body weight, and in early winter in TV and MV. HAZAMA (1964) reported that "the weight dur- ing May-June is heavy, and one or two months later, they (wild Japanese monkeys) record the lightest." His conclusion is, however, drawn from adult females, many of which have experi- enced reproductive cycles. Adolescent height growth in humans also accelerates in the summer (MIRWALD & BAILEY, 1997).

The peak height velocities in Japanese macaques are as high as ca 8 cm/year in females and ca 12 cm/year in males. These velocities are comparable to or greater than those in humans (MALINA, 1978). The peak of the pseudo-velocity curve is sharp in Japanese macaques, that is, the duration of higher rate of growth is short. This is due partly to the short time of the whole growth period itself in Japanese macaques, and partly to the seasonal nature of the acceleration period. This led us to question whether the period of adolescent accelerated growth in Japanese macaques was spread over more than one year. The size of the reproductive organs as shown by the TV growth curve (Fig. 8), increases progressively with age, demonstrating that adolescent growth and development in Japanese macaques takes several years. The total gain in body size may be comparable with that in humans with a pattern of one acceleration phase.

As discussed above, Japanese macaques are characterized by punctuated adolescent growth spurts, separated by seasons of slower growth. As these monkeys grow, develop, and reproduce under the strong influence of a seasonal environment, the acceleration in adolescence should be synchronized to the seasonal phase of accelerated growth. As the period for rapid growth is lim- ited by season, they must acquire the total increment destined for the adolescent period in installments during the summer and autumn of two or three consecutive years.

Adolescent growth varies widely among individuals, as reflected by the distribution of ado- lescent growth gain among ages. There was an early-maturing individual (No. 1459) showing partial reproductive maturation and accelerated somatic growth in the third year of life, unlike the late-maturing individuals (Nos. 1439 and 1470 in males and 1469 in females), which exhib- ited a catch-up growth in the next breeding season. Individual variation is also found in the reproductive organs, as shown by a range of maximum TV in the fourth year of life, from 8.28 cm 3 to 25.46 cm 3. Social factors may cause the variation in growth and development in males. The late-maturers, Nos. 1439 and 1470 shared the same cage with Nos. 1412 and 1428, and with No. 1459 respectively, and were the most subordinate in the social order. In females, however, social order was not strong. The possibility of this kind of influence needs to be explored with larger samples.

Human growth is characterized by constraint in childhood and acceleration in adolescence (BOGIN, 1997). However, these are not exclusively human, but are also found in Japanese

450 Y. HAMADA et al.

macaques, as discussed above. Japanese macaques are thus a good primate model for human growth. However, it cannot be expected that all anthropoid species will share these features. Many species of New World monkeys do not show an adolescent growth spurt in body weight (LEIGH, 1996). A cross-sectional study failed to reveal a clear adolescent growth spurt in anterior trunk length in chimpanzees (HAMADA et al., 1996a). The distribution of the adolescent growth spurt among anthropoids and among physical dimensions is the subject for the future study.

GROWTH AND DEVELOPMENT OF ADOLESCENT JAPANESE MACAQUES: ADAPTATION TO A SEASONAL ENVIRONMENT

Japanese macaques live at middle latitudes, inhabiting environments that range from warm temperate to cool with snow in winter. Their morphological characteristics are considered to have evolved under the strong influence of these natural conditions (HAMADA et al., 1996b). It is also to be expected that natural conditions have had a considerable influence on patterns of growth and development in Japanese macaques.

Comparisons of age at the beginning of adolescent growth were made among three macaque species, Macacafuscata, M. mulatta, and M. fascicularis, which are phylogenetically very close to each other (FOODEN, 1980). Age at peak velocity in female rhesus monkeys, ca 24 months of age (TANNER et al., 1990) is earlier by 1 yr than that in female Japanese monkeys (Macacafus- cam). Female crab-eating monkeys do not have a clear body weight growth spurt (LE1GH, 1996), but they reproductively mature at about 2.5 yr of age as shown by the onset of menarche (YoSHIDA, 1994). The three species follow Bergman's rule, that is, the body size order is crab- eating (tropical dwellers), rhesus, and Japanese monkeys (Temperate Zone dwellers). M. fuscata is, therefore, the largest in the three species, and matures later. Age at the start of puberty may scale to body size, which coincides with the hypothesis of SMITH et al. (1994) that the growth period scales to body size. The size of Japanese macaques itself is the product of adaptation to cooler habitats (HAMADA et al., 1996b), thus the late start of adolescent growth is an adaptation to the natural settings in Japanese macaques. This needs to be evaluated through the accumulation of the knowledge of growth patterns in other species of macaques.

Rapid adolescent growth, punctuated by season of slower growth in Japanese macaques is readily explained as an adaptation to natural settings. Although seasonal influence on human growth is reported to be considerable (BoGIN, 1978; MIRWALD &. BAILEY, 1997), seasonal dependency of growth in humans does not appear to be as strong as in Japanese macaques. Body weight shows a seasonal cycle in adolescent Japanese macaques, but it is skinfold thick- ness that reveals clearly a circannual cycle without net increase. The cycle may reflect the annual change in energy balance, as M. fuscam builds up energy reserves from autumn to winter and consumes the energy from winter to spring, when natural food resources are scarce (NAKAGAWA, 1997). The fact that Japanese macaques reared artificially and led regular foods showed a seasonal variation suggests that there is a genetically determined seasonal physiological change that controls the allocation of energy. The annual cycle may also affect growth in linear dimensions.

Age changes in endocrinological features of the monkeys studied here will be reported in detail elsewhere (SUZUKI, in prep.). They clearly demonstrate the mechanism of seasonal varia- tion in the velocity of somatic growth in Japanese monkeys. Data on skeletal maturation also assist in delineating adolescent growth and development in Japanese macaques, as growth in linear dimension relates strongly to skeletal maturation (BOGIN, 1988).

Adolescent Growth of Japanese Monkeys 451

�9 EVOLUTION OF ADOLESCENT GROWTH IN ANTHROPOIDS

The major causes of adaptations in growth and development are suggested to be feeding ecol- ogy and life history (STZARNS, 1992). For example, the risk aversion hypothesis is advocated for slow juvenile growth in primates (JANSON & VAN SCHAIK, 1993). The pattern of growth and development of a given species can not always be determined by reference only to its phyloge- netic position, for primate species may have modified their ancestral patterns in response to environmental demands. We cannot suppose, for example, that chimpanzees (Pan troglodytes) would have an intermediate pattern between Japanese macaques and humans.

The characteristic features of growth and development of Japanese monkeys, punctuated accelerated growth by season, late start of adolescence, and the larger body, are considered to be an adaptation to a strongly seasonal environment, partly through the seasonal variation in food availability (NAKAGAWA, 1997). The adaptation of an adolescent spurt may thus have a different basis in Japanese macaques and humans. Comparing body weight growth between Cebus and Pan, FRAGASZY and BARD (1997) suggested that ecological setting strongly influences growth and development patterns, and a diet of hard objects may delay weaning in Cebus, because the eruption of the permanent dentition is necessary in order to chew foods of this type. Herbivorous anthropoids tend to mature earlier than non-herbivorous anthropoids (Leigh, 1996). Watts (1990) suggested that skeletal development in macaques is a derived feature, and not typical of other taxonomic groups of anthropoid primates. LEIGH (1996) stated that growth spurts have evolved independently in several lineages, and he hypothesized that the presence/absence or the magni- tude of adolescent growth spurts scales to body size. These consideration must be examined in growth studies of a wide range of non-human primate species.

Ackowledgments. The authors would like to express their sincere thanks to all the staff of the Primate Research Institute, Kyoto University, for their help throughout the study. We also thank to Drs. T. YOSHIDA (Tsukuba Primate Center), M. IWAMOTO (Japan Monkey Centre), T. KIMURA (University of Tokyo), and M. OKADA (Tsukuba University) for their suggestions and continued encouragement. We are indebted to Dr. J. CATON who helped to edit the manuscript. This study was partly supported by the fund from the Ministry of Education and Culture (Nos. 06640925 and 08304050).

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- - Received: August 27, 1998; Accepted: March 15, 1999

Authors' Names and Address: YUZURU HAMADA, SEIJ1 HAYAKAWA, JURI SUZUKI, and SArostn, O[IKURA, Primate Research Institute, Kyom University, Inuyama, Aichi 484-8506, Japan. e-mail: hamada@smlp.pri.kyoto-t, ac.jp