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American Journal of Primatology 19:l-13 (1989)
RESEARCH ARTICLES
Free-Ranging Cay0 Santiago Rhesus Monkeys (Macaca mulatta): 1. Body Size, Proportion, and Allometry
JEAN E. TURNQUIST1,2,3 AND MATTHEW J. KESSLER' 'Department of Anatomy, University of Puerto Rico, School of Medicine, San Juan, Puerto Rico 'Caribbean Primate Research Center, University of Puerto Rico, Medical Sciences Campus, Sabana Seca, Puerto Rico 3Department of Anatomy and Embryology, Hadassah Medical School, Hebrew University, Jerusalem, Israel
Key words: development, growth, body proportions, morphometrics, quetelet index, body weight, allometry
This paper presents comprehensive baseline data on body size and propor- tion of 661 (315 male, 346 female) free-ranging Cay0 Santiago rhesus monkeys (Macaca muZatta) ranging in age from 24 hours to 25 years. All animals were born and raised in the free-ranging colony on Cay0 Santiago, and exact ages were known for all. Tabular data from this cross-sectional study are provided to enable comparisons with data from laboratory, wild, and other captive populations of rhesus monkeys, as well as with other species. Despite the extensive literature on rhesus monkey behavior and biology, to date published accounts of its morphometrics have been limited to only a few measurements from animals of unknown age, small sample sizes, or caged colonies. Results of this study showed a distinct intraspe- cific pattern for body proportions throughout the life cycle. Relative linear increases in overall body proportions of maturing animals appeared to be from greatest to least in the trunk, hindlimb, and forelimb, respectively. Within the limbs, allometric scaling appeared to be fastest in the proximal segment and slowest in the distal segment. Males and females differed in the duration of growth, and gender dimorphism was associated primarily with differences in size rather than proportion. Although the primary purpose of this paper is to present numerical data on the Cay0 Santiago colony, the results are compared with previous studies of both laboratory and free-ranging rhesus monkeys.
INTRODUCTION Rhesus monkeys (Macaca mulatta) are used extensively for both behavioral
and biomedical research, yet morphometric data on the rhesus is very limited [Bourne, 1975; Napier & Napier, 19671. Theoretical arguments derived from field studies [Crook, 1972; Washburn et al., 19681 may depend on accurate assessments of age, but little data are available to use as a reference. Some field primatologists,
Received for publication January 9, 1989; revision accepted June 19, 1989.
Address reprint requests to Dr. Jean E. Turnquist, Department of Anatomy, University of Puerto Rico School of Medicine, GPO Box 5067, San Juan, Puerto Rico 00936 USA.
0 1989 Alan R. Liss. Inc.
2 / Turnquist and Kessler
such as Altmann [1962], have attempted to create their own scale based on mor- phometrics, but these lacked a standard with which to compare their results. Gavan and Hutchinson [ 19731 encountered similar difficulties in assessing the age of captive animals, as only estimated ages of free-ranging animals were available for comparison. Although growth in humans and nonhuman primates [e.g., Tan- ner, 1962; Watts, 1985; Coelho, 19851 show many similarities, further data on a large sample of known aged nonhuman primates are needed to establish their suitability as substitutes for humans in experimental research [Watts, 19851 and to verify evolutionary theories [Schultz, 19681.
Longitudinal studies, like those in humans [Krogman, 1949; Tanner, 19621, have recently been begun in nonhuman primates to analyze age-related morpho- metric changes [Glassman et al., 19841. Until such time as these data are available for the entire life span of the animals (+25 yrs), large cross-sectional studies utilizing the entire age spectrum of a primate population can be used to infer longitudinal changes in morphometry [Coelho et al., 1984; Coelho, 19851 in addi- tion to providing data on the range of variability within a species.
Early descriptions of postnatal growth in rhesus monkeys are available from Schultz and colleagues [Schultz, 1933, 1956; Lumer & Schultz, 19411 based on a limited number of specimens. Data on body size, adolescent growth spurts, and the development of gender dimorphism in rhesus monkeys [Gavan & Hutchinson, 1973; Watts & Gavan, 1982; Watts, 1982, 1985; van Wagenen & Catchpole, 19561 have been derived from small captive colonies. Other studies include detailed data for only part of the growth period [Clark & New, 1969; Lotz et al., 19861. None of these studies address natural variation between individuals nor present profiles of an entire population.
Recently some morphometrics (body weights, crown-rump lengths and modi- fied Quetelet ponderal indices) of Cay0 Santiago monkeys of known age have been published [Rawlins et al., 19841, but there has been no comprehensive report on the body proportions of known-age, free-ranging Macaca mulatta. Obtaining this in- formation on feral populations is extremely difficult due to problems inherent in identifying and trapping animals of known age in the field. The Cay0 Santiago rhesus monkeys (Macaca mulatta) thus represent a unique population in which to study morphometic data on a large sample of free-ranging animals of known age and gender. This cross-sectional study reports the body size and proportions for 661 free-ranging Cay0 Santiago macaques representing the entire life span (birth to 25 years) of these animals. Although from a provisioned colony, data from these monkeys provide information for comparison with both feral and captive popula- tions of rhesus macaques.
METHODS Cay0 Santiago is a 15.2-hectare island located 1 km off the southeast coast of
Puerto Rico, which since 1938 [Carpenter, 19421 has been inhabited by a colony of free-ranging rhesus monkeys to which no new stock has been added except through births. The history, management, demography, and genetics of this colony since its establishment by Carpenter 50 years ago was recently described elsewhere [Raw- lins et al., 1984; Rawlins & Kessler, 1986; Duggleby et al., 19861. Identity, date of birth, gender, and maternity were known for all animals. Animals were provi- sioned with commercial high-protein (24-26%) monkey chow (Agway, Inc., Syra- cuse, NY; Allied Mills Inc., Chicago, IL; Ralston Purina Co., St. Louis, MO) a t 0.25 kg per individual per day. This diet was supplemented by ad lib consumption of natural semitropical vegetation and soil [Sultana & Marriott, 1982; Marriott et al.,
Rhesus Body Size and Allometry I 3
Fig. 1. digit 3; e, lower limb length; f, thigh, g, leg; h , foot at digit 3; i, crown-rump length.
Method of measuring linear variables: a, upper limb length; b, brachium,; c, antebrachium; d, hand at
19861. Stored rainwater was distributed at fountains located throughout the is- land.
All measurements in this cross-sectional study were made during the annual capture of the population for health surveillance, tattooing, and genetic studies (January-February 1983, 1984, and 1985). A total of 661 (315 male and 346 fe- male) different monkeys from four social groups in the population were measured. In rare instances, not all measurements were made on an individual; thus, the total number sampled differs slightly for some variables. Ages ranged from 24 hours to 25 years. A field scale accurate to 0.1 kg was used to weigh animals larger than 750 g. Infants were weighed on a platform scale accurate to 1.0 g. Animals over 3 months of age were chemically restrained with ketamine hydrochloride (Vetalar, Parke-Davis, Morris Plains, NJ) administered intramuscularly a t a dose of approximately 12 mg per kg body weight. Measurements on infants (5 5 weeks) were made without chemical restraint while a field assistant helped position the infants who, in most cases, continued to nurse on their chemically restrained mothers.
All measurements were made on the right side with the animal in left lateral recumbency. Body and body-segment lengths were measured with sliding calipers accurate to 1.0 mm. Circumferences were measured with a tape measure to the nearest 1.0 mm. All measurements were made between easily palpable bony land- marks [Turnquist, 19841.
As illustrated in Figure 1, measurements included: crown-rump length (vertex to caudal tip ischial tuberosities), upper-limb length (greater tuberosity humerus to tip digit 3 with limb fully extended at 90" angle to body), brachium (greater
4 / Turnquist and Kessler
tuberosity to distal tip lateral epicondyle humerus), antebrachium (olecranon pro- cess to tip styloid process ulna), hand (on dorsum, proximal surface lunate to tip digit 3 with hand at 90" angle to antebrachium and elbow flexed), lower-limb length (greater trochanter femur to tip digit 3 with limb fully extended a t 90" angle to body), thigh (greater trochanter to distal tip lateral condyle femur with knee a t 90" angle), leg (proximal border of lateral condyle tibia to lateral malleolus fibula), foot (on plantar surface, posterior calcaneous to tip digit 3 with foot at 90O-angle to leg and knee flexed), circumference midbrachium, and circumference midthigh. Midbrachium and midthigh circumferences were measured on only 379 (174 male and 205 female) animals. Most of these measurements were either described by Schultz [19291 or modified by the authors because of difficulty in consistently locating a particular landmark in living animals (e.g., the proximal border of the head of the radius) or to facilitate comparison with motion pictures of the animals. Because measurements of living animals include the overlying soft tissue, the measurements are of body segments rather than of bones per se. The Quetelet Index ((body weight in kg)/((crown-rump length in cm) -2)) x 1,000, is a ponderal index used to estimate body fat in primates [Walker et al., 19841. All measure- ments were taken by the senior author under similar conditions.
Data were statistically analyzed using Statistical Package for the Social Sci- ences (SPSS) [Nie et al., 19751 on a DEC 2020 (Digital Equipment Corporation) computer. Significance for statistical comparisons was set at P 5 0.01.
RESULTS Age, gender, and reproductive state of the monkeys from whom morphometric
data were obtained are presented in Table I. The infants (0 years) were from 24 hours to 5 weeks old, yearlings (1 year) ranged from 6 to 13 months of age, 2- year-olds from 18 to 25 months of age, etc. The 7-month age range for each age category demonstrates the fact that monkeys born the previous birth season be- come (for recordkeeping purposes) 1 year older on January 1 of the following calendar year. The distribution of births during the birth season and the timing of the measurements is such that the average age of monkeys in each age category approximates the stated age of a given cohort.
Table I1 presents data on the measurements for each age and gender category of animals. The mean value 2 1 standard deviation is given for each group. These data are included in detail for use in comparisons by other researchers. To facili- tate statistical analyses, adults are grouped into age categories that approximate phases of the life cycle and do not include significant yearly variations. Six through 9 years of age are the years immediately following complete eruption of permanent dentition [Cheverud, 19811; 10 through 14 years of age represent animals in their prime; and 15 years of age and over are aged animals [Schultz, 1956; Rawlins et al., 19841.
There were large standard deviations for some measurements of 15- to 19- year-old males as the result of inclusion of one animal (age 19) with extreme kyphosis of the spine and an inability to extend his upper limb fully. Because body and limb lengths were measured linearly between the two endpoints, measure- ments for crown-rump length, upper limb length, and Quetelet Index of this ani- mal were extremely small when compared with age cohorts, but he was not elim- inated from the sample because his individual limb segments were typical for his age group, and both kyphosis and restriction of limb mobility are typical age- related changes in this population [DeRousseau, 1982; DeRousseau et al., 1981, 1983, 1986; Turnquist, 1986; Turnquist & Kessler, this issue].
Results of analysis of variance (ANOVA) showed that linear dimensions (e.g.,
Rhesus Body Size and Allometry I 5
TABLE I. Cayo Santiago Sample Size by Age, Sex, Reproductive State ~
Females by reproductive state Age Total Total in years males females Pregnant Lactating Nonpregnant Lact + N-P
0 19 22 1 52 44 2 48 48 3 40 35 1 4 29 43 22 5 21 28 9 6 21 18 9 7 12 17 9 8 13 19 9 9 9 11 7
10 11 11 3 11 7 8 3 12 3 9 4 13 7 6 1 14 7 6 1 15 2 3 1 16 3 2 1 11 2 2 18 1 3 1 19 1 3 2 20 1 4 2 21 2 1 1 22 2 23 2 1 24 1 25 1
Totals 315 346 86
11 10 6 5 8 2 6 5 3 4 5 2 1 1
1 1
22 44 48 34 10 9 3 3 2 2 2
2 1
1 2
1
22 44 48 34 21 19 9 8
10 4 8 5 5 5 5 2 1 2 2 1 2
1 1 1 1 1 1
71 189 260
crown-rump length, upper limb length, etc.) do not vary significantly between groups of females in different reproductive states. Weight-related variables (e.g., weight, brachial and thigh circumferences, and the Quetelet Index) do, however, differ significantly, depending on the female’s reproductive state (Rawlins et al., 1984).
Plotting representative data (Fig. 2) illustrated that most body dimensions in females do not appear to change significantly after the age of 5 years, whereas in males most body dimensions continue to change significantly through the age of 6 years.
Analysis of differences in body dimensions between males and females of the same age showed that, although younger animals occasionally showed significant differences for some variables, beginning at the age of 4 years males were signif- icantly larger than females for all variables not affected by pregnancy. Variables affected by pregnancy are body weight, midbrachium and midthigh circumfer- ences, and Quetelet Index.
Allometric scaling and the relationship between the apparent growth of var- ious body dimensions were estimated using linear regressions [Huxley, 1932; Jungers & Fleagle, 19801. These analyses showed that in the Cayo Santiago rhesus monkey population there is a marked linear relationship between various body dimensions regardless of size. All regressions of pairs of linear body dimensions for the population had correlation coefficients r 20.95, indicating great homogeneity
6 / Turnquist and Kessler
200
5 400
g 350 a
E u
- - B I 1
600 _ _ 5 5 0 -.
E 500..
5 400 - -
I4
450 E u
g 350 ._ 9: 9 2 300 .. U
2 5 0 ~
1 ; I I 1 I
0 1 2 3 4 5 6-9 10-14 15-19 2 O+ b A Q N Y Z A E
Fig. 2. length; c: Antebrachium length; d Lower limb length. Females = open squares, males = closed squares.
Body dimensions versus age in free-ranging rhesus monkeys. a: Crown-rump length; b Upper limb
despite considerable diversity in actual body size. Regressions with correlations 0.90 5 r 5 0.95 included either a circumference measurement (or weight) as one of the variables. The only correlations of body dimensions with r 5 0.90 included body weight (or its derivative Quetelet Index) as one of the variables. Segregating data by gender did not significantly change the correlations (k 0.03).
Rhesus Body Size and Allometry I 7
I 2 160 u ’ 140 B 2 120
3 g 100
80
W
0
R
0 W W
W
0 0 0 en
H
0
6 0 1 ’ ~ : :
I I
0 1 2 3 4 5 6-9 10 -14 15-1) 20+ C A(;c I19 YPULS
500 5 5 0 i
H
a
h 8 H W rn
0 0 0 0
200 . fl t I I
1
0 2 o+ 10-14 15-19 1 2 3 4 5 6-9 I,:
d m z xn Y=
DISCUSSION The entire Cay0 Santiago colony was derived from an original stock of 409
animals which, in 1938, were shipped from India and released on Cay0 Santiago by Dr. Clarence Carpenter [Rawlins & Kessler, 19861. Long-term blood genetics stud- ies on the population [Duggleby et al., 19861 show that none of the monitored genetic alleles have been lost in the ensuing years, and that the Cay0 Santiago population shows genetic allele diversity similar to that found in feral populations of rhesus monkeys. Thus, the consistency of body proportions in this colony appear to reflect a species-specific pattern rather than a phenomenon of genetic isolation.
TA
BL
E 1
1. M
orph
omet
ric
Dat
a o
n F
ree-
Ran
ging
Cay
0 S
anti
ago
Rhe
sus
Mon
keys
*
01
02
03
04
05
06-0
9
10-1
4
15-1
9
20 i
Sex
N W
eigh
t C
r-R
ump
Bra
ch
Ant
ebr
M
19
F 22
M
52
F
44
M
48
F 48
M
40
F
35
M
29
F
43
M
21
F 28
M
55
F
65
M
35
F 40
M
9
F 13
M
7
F8
0.6 i 0
.2
0.5 t 0
.1
2.1 i 0
.3
1.9
? 0
.3
3.3 t 0
.4
3.1 i 0
.3
4.4 i 0
.6
4.2 i 0
.5
6.0 t 0
.8
6.2 t 0
.8
7.8 t 1
.0
7.41
I 1.4
10.5
t 1
.6
8.8 f 1
.7
11.9
t 1
.7
9.6 i 1
.3
10.9
t 1
.1
9.7 i 1
.7
9.4 t 1
.3
8.6 i 0
.9
211 t 1
9 20
6 i 1
4 33
5 t 1
5 32
7 i 1
7 40
1 I 18
395 I 13
44
7 i 1
7 44
3 t 1
8 49
8 t 1
8 48
0 i 1
6 53
5 i 1
5 50
4 t 1
8 57
3 t 2
0 52
2 i 2
4 58
8 i 2
2 53
6 f 1
9 54
3 I 76
526
t- 2
6 54
8 t 2
5 52
2 t- 3
4
163
2 1
5 16
0 I 11
240 i 1
0 23
4 t 1
3 28
3 i 1
1 28
0 i 1
1 31
9 t 1
4 31
5 ? 1
2 35
7 t 1
4 33
8 t 1
1 38
7 i 1
3 35
3 t-
15
405 i 1
3 35
8 t 1
5 40
0 t 1
3 35
8 i 1
3 38
3 i 6
8 35
7 f 1
2 39
9 i 1
6 35
5 i 1
5
59 i 6
57
t 4
93
t 5
91
f 6
11
2 i 5
11
0 i 5
12
7 t 6
12
6 i 5
14
2 t-
6 13
8 t 6
15
5 i 7
14
2 i 7
16
7 i 7
14
8 i 6
16
7 t 8
14
9 t 6
17
1 i 5
14
9 I 6
168 t 9
14
7 t 1
2
69 i 7
67
i 5
10
5 t 5
10
3 i 5
12
7 t 6
12
5 t 5
14
3 2 6
14
1 t 6
16
1 i 7
15
4 t-
6 17
2 t 7
15
9 t 6
18
3 i 7
16
2 2 7
18
4 i 7
16
1 f 6
18
8 t 5
16
3 i 8
18
5 t 7
16
3 t 4
Han
d3
59 2
5
58 i 3
78
2 4
76
i 4
89
t 4
88
t 4
99
? 5
98
t 4
11
0 i 5
10
0 i 6
11
4 i 5
10
4 t 3
11
8 t 5
10
5 ? 5
11
8 t 5
10
5 i 4
11
9 t 5
10
4 i 4
11
4 t 4
10
7 t 4
Low
er
Thi
gh
198
21
9
70 i 6
19
4 t 1
2 68
i4
30
5 i 1
3 1
15
i 6
298i
; 14
11
3 t 6
36
3 i 1
3 13
9 i; 7
35
8 t 1
3 13
8 i
6
407 i 1
7 16
0 2
9
404
t- 14
15
9 t 8
45
5 f 1
9 18
3 i 1
0 43
6 t 1
2 17
5 i 6
49
2 i 2
0 19
8 t 1
2 45
1 i 1
7 18
1 t 1
2 51
6 2 1
9 21
4 t 1
2 45
1 2 2
1 18
5 i 1
3 52
0 t 1
9 21
8 ? 1
4 45
3 I 16
18
5 i 1
0 51
6 f 1
6 21
8 I 10
45
4 t 2
1 19
1 i 1
7 51
1 i- 23
21
2 2 1
9 45
0 i 1
3 19
3 t 1
3
Cir
cba
Circ
t"
QI"
63 t 5
62
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10
1 t 5
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9 i 8
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7 i 7
15
5 t 7
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9 f 5
16
7 t 1
0 15
3 i 6
17
5 t- 8
15
4 t-
8 17
6 t 9
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3 f 6
17
6 i 8
15
4 I 8
179 t 9
15
0 i 6
84 i 7
81
t 6
11
6 i 5
11
3 +
5 13
5 i 5
13
2 i 5
14
9 t 6
14
5 i 6
16
3 5 6
15
0 f 5
16
9 t 5
15
4 t 6
17
4 t 5
15
4 i 6
17
2 i 5
15
4 t-
6 17
1 f 3
15
5 i 5
17
2 I 7
154 i 7
69 i 9
68
t 8
98
i 8
95
t 1
1
115 i 1
0 12
7 I 12
115 i 8
126 i 8
15
1 2
13
15
0 i 1
2 15
8 t 1
3 15
3 t-
12
179 t 1
6 16
5 t 1
1 19
5 f 1
4 17
4 ? 1
2 19
0 2
7
162 t 1
1 17
9 i 2
1 17
1 i 1
78 i 1
4 80
t 1
2 13
3 i 1
2 13
1 -C
20
159 * 1
2 15
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6 18
1 i 2
2 18
5 t 2
0 20
9 t 2
5 21
2 ~
t 23
216 i 2
2 21
2 t 2
1 24
2 t 2
5 23
1 t 2
2 25
3 i 2
1 23
7 i 1
9 24
2 i 4
1 21
7 t 2
7 21
5 i 3
4 22
8 i 1
1.18
t 0
.35
1.25
2 0
.15
1.84
t 0
.24
1.76
i 0
.24
2.02
t 0
.17
1.95
i 0
.15
2.19
t- 0
.20
2.11
f 0
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2.42
i 0
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2.71
i 0
.27
2.70
i 0
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2.90
t 0
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3.17
i 0
.37
3.21
i 0
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3.44
i 0
.32
3.33
t 0
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4.00
t 1
.64
3.48
20.
42
3.12
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.19
3.19
t 0
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*'A
ge is
in y
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. M in
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umbe
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1,
000.
Rhesus Body Size and Allometry I 9
The observation that even with marked gender dimorphism in size, body propor- tions remain almost constant further supports Huxley’s [ 19321 hypothesis of a species-specific pattern for body proportions regardless of body size.
Body weights and crown-rump lengths reported in our study provide a refer- ence for assessing the accuracy of earlier studies, which used estimated age in this colony [Altmann, 1962; Gavan & Hutchinson, 19731. Differences among studies may reflect the change from regular to high-protein monkey diet in 1969, errors inherent in using estimated ages versus known ages, or secular growth trends in the population.
This study supported findings of Lumer and Schultz [1941] that in macaques the postnatal growth rate of the trunk exceeded that of the limbs; juvenile M . mulatta so described correspond to 2-year-old animals on Cay0 Santiago. Adult females in the two groups appeared to be similar in size but adult males in the free-ranging colony were larger than those of Lumer and Schultz [ 19411. Compar- isons of crown-rump length (sitting height) and body weight between Cay0 Santiago macaques and the “basic” macaque group of Gavan and Hutchinson [ 19731 showed that, although the animals started out similar a t birth, growth in the two groups differed. Initially the crown-rump length of the Cay0 Santiago animals increased more slowly so that by the age of 5 years the Cay0 Santiago animals were almost 1 year behind the Gavan and Hutchinson animals. In subsequent years, however, the Cay0 Santiago monkeys continued to increase in size so that the mean crown- rump length of 6- to 9-year-old Cay0 Santiago males was equal to the largest mean value reported by Gavan and Hutchinson. The 10- to 14-year-old Cay0 Santiago males were larger than any animals in the Gavan and Hutchinson colony. Among females, the crown-rump length in the two groups were similar before the 4th year. By the age of 4 years, however, the Cay0 Santiago females passed the Gavan and Hutchinson animals of the same age and from 5 years on the free-ranging animals were larger than any female in the Gavan and Hutchinson colony.
Comparisons between males and females of the same age in the Cay0 Santiago population showed that, although the genders were very similar in size a t birth, juvenile females were generally smaller than males of the same age. The gender dimorphism seen in adults was evident by the 4th year, which marks the begin- ning of the adolescent growth spurt in rhesus males [Watts & Gavan, 1982; Watts, 19851. The present findings on the development of gender dimorphism agree with those of Watts’ [1982] longitudinal study of 16 rhesus monkeys. This pattern is also very similar to that recently reported by Coelho [19851 for baboons (Papio cyno- cephalus anubis).
As an animal approaches maturity, the growth rate of various body segments and proportions slows down. The data presented here indicate that in both genders the extremities reach adult size before either crown-rump length or body weight and that midbrachial circumference closely parallels body weight. In general, the cessation of growth in body and segmental lengths precedes that in body weight or segment circumferences.
Both adult males and females showed significant differences for some vari- ables when animals were grouped into young adults (6-9 years) versus middle- aged adults (10-14 years), age groupings which in this population correspond to locomotor behavioral and physiological differences [ Kessler et al., 1983; Rawlins, undated]. Yearly differences, however, between adjacent age cohorts of males over 7 years and females over 6 years of age were not significant. Once maturity is reached, the only significiant age-related changes in body dimensions are weight, crown-rump length, and midbrachial circumference.
Further comparisons between our data and that of van Wagenen and Catchpole
10 / Turnquist and Kessler
[19561 show that young animals in both groups were similar in size. As the animals matured, the crown-rump length of the Cay0 Santiago animals exceeded that of age-matched animals (by age 5 years for females and 6 years for males) from the van Wagenen and Catchpole sample. Body weights of adult males on Cay0 Santiago, however, were less than those of the van Wagenen and Catchpole colony. Most Cay0 Santiago females 2 4 years were either pregnant or less than 5 weeks postpartum at the time of the study; thus, their weights could not be compared with the van Wagenen and Catchpole group. By the age of 4 years, both groups showed evidence of gender dimorphism, which continued to increase to the age of 6 years.
Data on the longitudinal growth of 60 rhesus monkeys by Lotz et al. [19861 indicated that they had body dimensions and rates of growth similar to those in the Cay0 Santiago population. Exact comparisons, however, were difficult because the data were presented in graphic, not tabular, form, and animals left the study a t the age of 4.5 years, which was prior to full maturity in the free-ranging colony.
Comparison of body weights and various body dimensions of 20 animals ex- amined by Schultz [19331 and the Cay0 Santiago colony showed that, although similar a t birth, the free-ranging animals of all other ages were consistently larger than the Schultz animals. Many of Schultz’s [1956] indices of relative body pro- portions in macaques utilize trunk height, which was not measured here; thus, exact comparisons between our results and those of Schultz were not always pos- sible. Relative changes in proportions with age were the same in both studies. As a monkey passes from infancy to adulthood, the relative proportion of limb length to body length decreases, as does the relative proportion of upper limb to lower limb lengths and handifoot length to body length.
This pattern of relative growth of individual segments is similar to that de- scribed by Grand [19771 for maturational changes in the relative weights of body segments of Macaca mulatta. His findings that as body weight increases the rela- tive weight of the hand and foot decreases parallels the findings in this study; i.e., as body length increases, the relative length of the hand and foot decreases. Grand [19771 found that relative weight gain in the limb is greatest in the proximal segment (brachiumithigh), followed next by the gain in the middle segment (an- tebrachiumileg), and finally the least weight gain is in the distal segment (hand/ foot). The linear data from Cay0 Santiago shows the same pattern, with the great- est relative increase in the proximal segment, followed by the middle segment, and finally the distal segment. The present results parallel Grand’s 119811 findings that during postnatal development the relative increases of the limbs of M. mulatta progress along the limb from distal to proximal. A similar pattern has been re- ported by Gavan [19531 for chimpanzees. Reports on Cebus apella and Cebus albi- frons [Jungers & Fleagle, 19801 as well as on Cebus capucinus and Ateles geoffroyi LLumer & Schultz, 19471 differ from these findings. In New World monkeys, fore- armileg scalings were found to be faster than brachiumlthigh; handifoot scaling was the slowest. Current findings thus support the idea expressed by Jungers and Fleagle [ 19801 that there may be allometric distinctions between catarrhines and platyrrhines.
Although comparisons of linear dimensions and weight of individual body segments show similar tendencies in terms of relative growth, comparisons be- tween overall body proportions do not. Grand [1977] found the order of greatest to least relative weight increase is the hindlimb, the forelimb, and the trunk, respec- tively. This study showed the greatest to least relative linear increase is the trunk, the hindlimb, and the forelimb, respectively. The newborn thus has relatively long, yet light, extremities, whereas the adult has relatively short, heavy extremities.
Linear regressions of body dimensions showed that gender differences were
Rhesus Body Size and Allometry / 11
primarily the result of differences in size rather than proportion. Thus, the gender dimorphism seen in adults appears to be mainly the result of slightly different growth rates and earlier cessation of growth in females rather than different growth patterns for the two genders. Body segment lengths show little change once maturity is reached and, although older animals generally weighed less than an- imals in their prime, these differences were not significant. Just as human stature decreases in the elderly [Trotter & Glaser, 19511, crown-rump length in monkeys appears to decrease as mature animals become aged (215 years) [Kessler et al., 1983, 19861, and intervertebral discsivertebral bodies collapse and spinal curva- ture increases. In free-ranging macaques, as in human beings [Lasker, 19531, this decrease appears to occur earlier in males than in females.
Pregnancy and lactation significantly altered both body weight and midbra- chial and midthigh circumferences in adult females. Thus, the weight gain asso- ciated with pregnancy and early lactation included a general overall body gain affecting the extremities as well as the torso. The nonpregnantinonlactating adult females in the colony did not differ significantly in any linear body dimensions from either the pregnant or lactating females.
In summary, this study of 661 members of the free-ranging rhesus macaque colony on Cay0 Santiago, Puerto Rico, documents the growth and development of the postcranial morphology of rhesus monkeys under seminatural conditions and characterizes their distinct specific pattern for changes in body proportions throughout the life cycle.
CONCLUSIONS
1. This study documents the postcranial growth and development of provi- sioned free-ranging rhesus macaques maintained on Cay0 Santiago under semi- natural conditions.
2. Changes in rhesus body proportions throughout the life cycle are charac- terized by a distinct intraspecific pattern.
3. Allometric scaling within the limbs of maturing animals appears to be relatively faster in the proximal segment than in the middle segment and slowest in the distal segment.
4. Relative linear increases in overall proportions appear to be from greatest to least in the trunk, the hindlimb, and the forelimb, respectively.
5. The duration of growth differs for males and females. 6. Gender dimorphism, evident by 4 years of age, is associated primarily with
differences in size rather than proportion.
ACKNOWLEDGMENTS The Cay0 Santiago colony of the Caribbean Primate Research Center is sup-
ported by USPHS Grant RR-03640 and the University of Puerto Rico Medical Sciences Campus. The authors thank Mr. Sammy Martinez, Ms. Janice Gonzales, and the other workers a t the CPRC for their excellent assistance in handling the animals. Thanks also to Ms. Eleni Kapsalis and the other “scribes” who helped in collection of this data. Finally, thanks to Mr. Ivan Martinez, without whose com- puter expertise these data could not have been analyzed.
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