Relative Maturity of Cebus and Squirrel Monkeys at Birth and during Infancy MARJORIE F. ELIAS Department o f Nutrition Harvard School o f Public Health Boston, Massachusetts Cebus monkey were less mature at birth than squirrel monkeys in terms of body wieght and brain weight in proportion to adult weight. Postnatally, cebus were slower to develop locomotion, perceptual-motor capacities, and object permanence. The differences in rate of development between the species increased with age. The findings indicate that the cebus have a longer period of infancy before becoming skilled at locomotion and manipulation. In view of the cebus monkey’s recognized skill as a manipulator and problem solver, the long period of infancy suggests that cebus have evolved further in the direction of higher primates.
An evolutionary trend exists among primates for those species which reach higher levels of functioning to prolong the juvenile period of life (Schultz, 1969). Of the 2 species of New World monkey under study here, cebus monkeys are known to attain a high level of manual dexterity and problem solving capacity as adults (see Hill, 1960; Kluver, 1933; Romanes, 1890), markedly higher than that of squirrel monkeys (see Davis, 1974; Moynihan, 1976; Thorington, 1967)). One can hypothesize that, because they reach a higher level of functioning, cebus monkeys have a longer juvenile period than do squirrel monkeys and are therefore less mature at birth and during the 1st months of postnatal life. This paper reports a test of that hypothesis. To compare overall level of maturation across species, one must examine several aspects of physical and behavioral development. The various body systems mature at different rates within an individual and the pattern of maturation of the different systems varies across species (Schultz, 1960). Two aspects of physical development which can be compared at birth are brain growth and body growth, in that birth occurs at different stages of development of the brain (Dobbing, 1974) and the body (Schultz, 1969) in different species. Some aspects of behavioral development which can be assessed during infancy include perceptualmotor, locomotor, and cognitive development. Tests of perceptual-motor and locomotor development in infancy have been devised for rhesus (Mowbray & Cadell, 1962) and adapted for use with squirrel monkeys (King, Fobes, and Fobes, Reprint requests should be sent to Dr. Marjorie F. Elias, Department of Psychiatric Research, Children’s Hospital Medical Center, 300 Longwood Avenue, Boston, Massachusetts 021 15, U.S.A. Received for publication 27 April 1976 Revised for publication 18 November 1976 Developmental Psychobiology, lO(6): 519-528 (1977) @ 1977 by John Wiley (L. Sons, Inc.
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1974; King & King, 1970; Schusteman & Sjoberg, 1969), tamarins (King et al., 1974), greater galagos (Ehrlich, 1974), and slow loris (Ehrlich, 1974). Cognitive development has been assessed in monkeys by tests of problem solving, discrimination learning, and recently by tests based on Piagetian theory (Jolly, 1972). Moreover, one stage of development which has been studied in several species is Piaget’s Stage 4 of sensory-motor development: object permanence, which is ability to find a hidden object (Mathieu, Bouchard, Granger & Herscovitch, 1976; Redshaw & Hughes, 1975; Vaughter, Smotherman, & Ordy, 1972; Wise, Wise, & Zimmermann, 1974). The present study was designed to assess relative maturity of cebus and squirrel monkeys at birth, comparing brain weight and body weight as prjoportions of mature weights, and postnatally, by age of acquisition of mature responses in some items of perceptual-motor, locomotor, and cognitive development. Specifically, I planned to investigate whether cebus and squirrel monkeys differed in maturity at birth and whether any differences found at birth might be diminished or increased during infancy by differences in rate of postnatal behavioral development.
Eight cebus monkeys (Cebus dbifrons), 5 females and 3 males, and 8 squirrel monkeys (Saimiri sciureus from Leticia, Colombia), 3 females and 5 males, were the subjects of the study. They were born in the breeding colony of the laboratory, taken from their mothers at birth, and reared in the laboratory nursery. They were kept for several weeks in incubators (squirrels, 2 weeks; cebus, 3 weeks) and then in cages in the nursery, and fed ad libitum by bottle with a liquid diet of good nutritional quality. Although far from natural, the rearing environment was relatively constant for all animals.
Weight The infants were weighed when they came to the nursery a few hours after birth. Adult body weights were obtained from animals in the breeding colony. The adults were all feral animals who had not been subjected to experimental diets and included the parents of the infants. The weights of the females are non-pregnant weights, each from a single weighing. The weight of each squirrel monkey m d e is a mean of 12 weights obtained monthly for a year, in order to average out the fatted phase of each male (data from K. Rasmussen, personal communication). Although small, the sample of males includes all the breeding males in the colony. No weights were available for cebus males because the breeding males had never been weighed and other adult males had been on experimental diets. Brain weights are wet weights obtained from animals who died or were sacrificed in the laboratory. An autopsy was performed within 12 hr of death. The brain was severed at the occipital-atlas junction, removed, and weighed immediately. Brain weights of newborns were taken from stillbirths and infants who died within
INFANT DEVELOPMENT IN NEW WORLD MONKEYS
521
the 1st week after birth. In order to exclude prematures, only animals whose body weight fell within 2 standard deviations of mean birth weight were included. Brain weights of adults were taken from breeding animals not on experimental diets.
Behavior The behavioral tests were chosen to assess perceptual-motor and locomotor development and the development of object permanence. Test items were selected in which the expected responses were absent at birth but could be elicited consistently after they had been acquired. Therefore, age of acquisition of the expected response was the variable under consideration. The procedures for testing perceptual-motor and locomotor development, except the development of the grasp, were modifications of the tests devised by Mowbray and Cadell (1952) and King and co-workers (1970, 1974). Development of the grasp was measured by a technique used previously by Elias and Samonds (1973, 1974). Object permanence was measured by procedures adapted from the Einstein Scale of Sensory-Motor Development. Seventeen items were scored from 9 procedures, described in order of presentation. The test items were presented in a fured order planned to proceed from less to more disturbing procedures. Testing took place weekly from the 1st week of postnatal life. It was carried out in and near each animal's cage and lasted for about 10 min per animal per session. Each animal was tested when its eyes were open, it appeared to be alert, and had been offered its nursing bottle before testing began. Each item was scored on a S-poht scale (0-4) ranging from no response to the response described below for each item.
Tests Percep tual-Motor Development Orient to sound. The animal turns its head to locate the source of the sound of a snap toy held 15 cm above its head and snapped 5 times at 3-sec intervals. It is lying prone facing away from the tester. Score: 0-no head turn; 2-looks about; 4-locates toy by eye. Visual following. The animal's gaze and head turn follows an object (snap toy) smoothly when it is moved through an arc of 180" around its head at a distance of about 8 cm. Score: 0-does not follow; 2-follows a little but loses, jerky; 4-follows smoothly through arc. Development of grasp. Approach ring. The animal's body comes within 8 cm of ring (plastic baby bottle cap) hung inside door of the cage for 2 min. Score: 0-no approach; 2-move body forward; 4-come within 8 cm. Touch ring. The animal touches ring with finger or nose. Score: 0-no reach; 2-come within 2 cm; 4-touch ring. Grasp ring. The animal grasps the ring with its fingers. Score: 0-no touch; 2-touch, end of fingers; 4-grasp. Swing or pull ring. The animal pulls at ring or makes it swing. Score: 4-swing or pull ring.
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Object Permanence (1 min per presentation) Pick up ring, not hidden. The animal picks up the ring (gold colored metal ring 4.5 cni in dia) placed on the floor of the cage. Score: 0-does not look at ring; 2-approaches to within 5 cm; 4-picks up ring. Find hidden ring. The animal uncovers, looks at, and handles the ring when placed on the floor of the cage and covered by its cage cloth while it watched. Score: 0-does not look where the ring is hidden; 2-looks at the cloth; 4-uncovers the ring.
Locomotor Development ( 1 min per item) orienting up, turn, The animal turns 180" to a head-up position when placed facing down on a plush-covered board (40 x 40 cm) inclined at a 30" slope. Score: 0-no rotation; 2-partid rotation; 4-fuU 180" turn. Get o f t The animal moves off the board. Score: 0-no movement off the board; 2-walk to edge; 4--walk off board. Crawl/walk. Crawl backward. The animal moves backward from the center to an edge of the plush-covered board laid flat, when it has been placed in the center. Score: 0-no movement; 2-move halfway;4-move to an edge. Crawl forward. The animal moves forward on its belly from the center to the edge of the board. Score: same as above but forward. Walk, off belly. The animal walks on 4 legs with its belly off the surface. Score: same as above but off belly. Righting. Right sd$ The animal climbs astride a horizontal cylinder loosely covered with plush ( 5 cm dia x 32 cm for squirrel monkeys; 9 crn x 38 cm for cebus-approximately the diameter of the mother's torso) when placed underneath it with the body oriented along the cylinder in ventral contact with 4 hands clinging to the plush. Score: 0-no righting; 2-partial righting; 4-on top of cylinder. Get off The animal releases its grip and gets down onto a flat surface 6-10 cm below. Score 0-no release of grip. 2-releases 2 hands and placed them on surface; 4-releases all 4 hands, gets down and breaks body contact with cylinder. Climb down. The animal climbs up at least one body length on a vertical wire mesh cylinder (9 x 41 cm for squirrel monkeys; 15 x 54 cm for cebus) when placed on it head-up with hmdquarters one body length from the bottom, releases grip on cylinder, and breaks contact with it. Score: 0--no descent; 2-turn and descend a little; 4-descend to surface and break contact with cylinder. Interobserver reliability for most items was tested by simultaneous observation and independent rating by 2 observers and ranged between .80 and 1.00.
Results Female squirrel monkeys' body weights at birth averaged 16.5% of adult weights, whereas female cebus averaged 11.1% (Table 1). The female squirrel
INFANT DEVELOPMENT IN NEW WORLD MONKEYS
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TABLE 1. Brain Weight and Body Weight ofNewborn and Adult Monkeys. Birth Weight (8)
Adult Weight (g) Birth/Adult Weight
N
Mean
SD
N
104 143
110.0 112.9
13.0 13.8
91 7
Cebus monkey Female Male
61 70
227.7 237.5
19.7 24.5
66
Brain Weight Squirrel monkey Female Male
8 11
14.6 15.5
2.2 2.9
17 35
5 7
32.6 34.4
3.0 2.8
-
Body Weight Squirrel monkey Female Male
Cebus monkey Female Male
-
8
SD
(%I
667.0 989.8
77.0 80.1
16.5 11.4
2060.0 -
220.0
11.1
-
-
23.3 25.3
1.6 2.2
62.7 61.3
6.0
48.8 -
Mean
66.8 -
-
monkeys’ brain wieghts at birth were 62.7% of adult brain weights, whereas cebus females’ brains were 48.8% of adult weight. By these criteria the female squirrel monkeys could be said to be physically slightly more mature than the female cebus at birth. Male squirrel monkeys’ brain and body weights were slightly heavier than females’ at birth. Their bodies were considerably heavier at maturity. For the analyses of the behavioral data the 5-point scale of 0-4 was reduced to a dichotomous rating of < 4:4. The scale was collapsed in this way because 0 and 4 were found to denote consistent forms of behavior whereas the intermediate levels were inconsistent on retest. (An animal was judged to have acquired a response when he obtained a score of 4 during 3 out of 4 consecutive weeks. The 1st of those weeks was identified as the age of acquisition of the response.) The week of age at which the animals reached the criterion of acquisition of each response is presented in Table 2. The Mann-Whitney ti-test was applied t o the data to test for significance of differences between the species. This test was used rather than the Student t-test because the assumption of normal distributions in the population, a necessary assumption for the t-test, could not be met for all variables. For the same reason, the ranges are presented as indicators of the variabihty of the distributions rather than standard deviations. In perceptual-motor development, the squirrel monkeys began to turn their heads t o follow a moving object at 4 weeks, to orient to the sound of a click at 6 weeks, and to approach, touch, and grasp a ring between 5 and 9 weeks. The cebus were 3 weeks later to follow the moving object and 5 weeks later to approach, touch, and grasp. These delays were statistically significant (p’s < .OS). Male-female differences in these very small groups were not significant. In the test of object permanence squirrel monkeys picked up the ring when it was not hidden at 9 weeks and found it when hidden at 12 weeks.
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TABLE 2. Behavioral Development of Squirrel and Cebus Monkeys: Age in Weeks. Squirrel Monkeys Females Behavior Perceptual-Motor Development Orient to sound Visual following Development of grasp Approach ring Touch ring Grasp ring Swing/pull ring
-
Totdl
ra
N
Mean
Range
N
Mean
Range
.96 .97
3 3
6.0 5.7
4-9 2-9
5 5
6.2 4.0
5-8 3-5
8 8
6.1 4.6
4-9 2-9
.97
3 3 2d 2d
5.0 6.7 5.5 7.0
4-6 5-9 5-9
5 5 5 5
5.4 8.4 10.2 10.6
3-7 5-18 5-20 5-20
8 8 7d 7d
5.3 7.8 8.9 9.6
3-7 5-18 5-20 5-20
Object Permanence Ring not hidden Ring hidden Locomotor Development Orienting up Turn Get off Crawl/walk Crawl forward Walk, off belly Righting Get off Climb down
Males
5-6
N Mean Range
3 3
8.7 12.3
6-14 10-15
5 qf
10.2 12.8
7-18 10-15
8 7f
.80 .90
3 3
2.7 3.3
2-4 3-4
5 5
2.8 3.6
2-4 2-5
8 8
2.8 3.5
2-4 2-5
1.00
3 3
1.7 2.3
1-2 2-3
5 5
3.0 3.6g
1-4 3-4
8 8
2.5 3.1
2-4
3 3
2.3 7.3
2-3 2-10
5 4f
3.6g 6.0
3-5 2-1 0
8 7f
3.1 6.6
2-5 2-10
1.00 .98
9.6 6-18 12.6 10-15
1-4
aInterobserver reliability. bAsterisks denote levels of significance of difference tiom mean of squirrel monkeys (both sexes): Mann-Whitney U-test; * p < .05; **p < .01; ***p < .001. 'Only 4 cebus (2 females, and 2 males of the present sample were tested for this response; data from 4 others tested earlier were included. Some animals never acquired this response. %ome animals were not recorded on this response. fOne animal died before acquiring this response. gMales and females were significantly different on this item @ < .05).
a
Cebus were 3 weeks older when they began to pick it up and 6 weeks, older when they found i t hidden. The latter was a statistically significant difference. The sexes showed no difference in finding the hidden ring in either species. In locomotor development, the squirrel monkeys turned to orient themselves upward on a slope at 2 weeks and began to get off the slope the following week. Five of them, 2 females and 3 males, crawled backwards. They began to crawl forward at 2 weeks and then to walk at 3 weeks. The cebus, who all crawled backwards initially, crawled forward at 6 weeks and began to walk at 7 weeks, a statistically significant difference. Five of the 8 squirrel monkeys righted themselves by climbing astride the horizontal cylinder as reported by King et al. (1974). None of the cebus ever did so. Both species got off the horizontal cylinder at 3 weeks of age. The cebus climbed down off the vertical cylinder at 4 weeks, slightly but not significantly earlier than the squirrels. The squirrel females walked and got off the horizontal cylinder a week before the
INFANT DEVELOPMENT IN NEW WORLD MONKEYS
525
TABLE 2. (continued)
Cebus Monkeys Total
Males
Females
N
Mean
Range
6.7
5-8 5-9
N
N
Mean
Range
5 5
8.2 7.2
7-11 5-10
4' 4' 4' 4c
9.8 10.8 11.8 13.8
9-11 10-11 11-14 12-15
11.3 4' 13.5 4' 3C'd 14.7 lCYd 15.0
9-13 9-16 11-18 -
8' 8' 7C'd
2e 4'
10.5 18.5
9-12 15-21
2e ' 4
14.0 19.3
5 5
5 .o 8.8
1-9 5-12
3 3
5 qf
6.2 7.5
5-7 7-9
5 5
4.4 4.8
2-1
1-8
3 3
I .I
8 8
Meanb
Range
7.6 7.4**
5-1 1 5-10
5C'd
10.5*** 12.1*** 13.0* 14.0*
9-13 9-16 11-18 12-15
13-5 18-21
4e 8'
12.3 18.9***
9-15 15-21
3.3 6.7
3-4 5-9
8 8
4.4 8.0***
1-9 5-12
3 3
6.3 1.3
4-9 6-9
8 7f
6.3*** 1.4*+*
4-9 6-9
3 3
2.7 3.7
2-4 0-7
8 8
3.8 4.4
2-1 0-8
males. These were the only significant male-female differences and, being drawn from a set of 28 tests, are scarcely beyond a chance occurrence of findings significant at the .05 level.
Discussion The behavioral findings and birth weights are consistent in showing cebus to be less mature than squirrel monkeys in some aspects of development during the 1st months of postnatal life. The responses acquired latest-swinging or pulling the ring and finding the hidden ring-have the largest gap between the species, 6 and 7 weeks. This result indicates that cebus were not catching up to overcome their relative immaturity at birth but were developing at a generally slower rate postnatally. Squirrel monkeys are known to be large at birth relative to the size of their mothers (Long & Cooper, 1968). The birth weights and mature weights reported here are consistent with those reported previously for squirrel monkeys (Long & Cooper, 1968; Napier & Napier, 1967). 1 had expected, then, that the cebus would be relatively smaller at birth. Adult squirrel monkeys are reported to
526
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have the highest ratio of brain to body weight of any primate (Hill, 11960). This has been explained by their small size relative to most primates in that the ratio of brain to body size varies inversely with absolute body size (Schultz, 1969). Cebus, at more than twice the body weight, have a virtually identical brain t o body ratio (squirrel monkey ratio, 1:29.6; cebus ratio, 1:30.8). T!his finding was not expected. A comparison of findings on behavioral development from field and laboratory studies reveals wide variability within and across species (Hinde, 197 1). Even among studies which have used modifications of the same technique the data are inconsistent (Ehrlich, 1974; Table 1). Studies of acquisition of object permanence also report inconsistent findings. Two rhesus monkeys attained Stage 4 by 10 and 12 weeks (Wise et al., 1974), 2 gorillas both attained it by 18 weeks, and 2 humans attained i t by 34 weeks (Redshaw & Hughes, 1975). The present finding that squirrels attained it by 13 weeks and cebus attained it by 19 weeks is not inconsistent with these findings from other species. But a study which examined squirrel monkeys reports that a 26-week-old animal had not yet attained Stage 4 and a 39-week-old was in transition (Vaughter et al., 1972). That animal was 3 times the age of acquisition of the squirrel monkeys in the present study, a highly inconsistent finding. One is forced to conclude that differences in method of testing or rearing conditions must be producing inconsistencies in findings in both cognitive and motor development. For example, in the righting test, releasing was seen in squirrel monkeys during the first week in Schusterman and Sjoberg’s study (1969), but not until 5 weeks by King et al. (cf. Ehrlich, 1974; Table 1). This difference may have been due to the fact that the animal was lowered until its back made contact with a horizontal surface in the former study, but was held above the surface in the latter study. Comparisons, therefore, are only justified when species are maintained and tested under similar conditions. I could not follow the monkeys in this study long enough to determine the duration of the juvenile period. However, data on dentition are available which document a continued slower rate of development of cebus relative to squirrel monkeys by 3 months and permanent dentition by 21 months (Long & Cooper, 1968). Cebus have completed deciduous dentition by 6 to 8 months and permanent dentition by 36 to 4 0 months (Napier & Napier, 1967). By these criteria, the duration of immaturity is almost twice as long in cebus. The trend of prolongation of immaturity with evolutionary progress identified by Schultz (1969) was referred to at the outset. The duration of juvenile growth ranges from a period of a few months in tree shrews to about 18 mon1.h~in prosimians, 2 to 3 years in monkeys, 8 years in great apes, and up to 14 years in humans. The prolongation of immaturity postpones reproductive capability but it provides juveniles with increased opportunity to learn from adults. The evolutionary advantage t o higher primates of prolonged immaturity must be considerable to outweigh the cost of delayed reproduction. Wilson (1975) has suggested that the advantage is in permitting the animal time to develop skill and experience from the environment in order to allow flexibility in behavioral patterns to fit behavior to short-term changes in the environment. Because learned skills and information cannot be transmitted genetically, evidently the opportunity to acquire them by
INFANT DEVELOPMENT IN NEW WORLD MONKEYS
527
prolonging the juvenile period has been transmitted instead. Although taxonomically close, the 2 species compared here differ strikingly and consistently in maturity at birth and during infancy, in duration of immaturity, and in ultimate level of functioning. The evidence suggests that cebus monkeys have evolved further in the direction of higher primates than have squirrel monkeys.
Notes This investigation was supported in part by Public Health Service Research Grants HD-07032 and HL-10098 and by the Fund for Research and Teaching, Department of Nutrition, Harvard School of Public Health. It was part of a project concerned with the behavioral effects of malnutrition. The author thanks Ms. Sandra Thomas and Professor Joseph C. Speisman for their help in collecting data and Professor D. Mark Hegsted, Principal Investigator of the project, for his cooperation.
References Davis, R. T. (1974). Monkeys as Perceivers. New York: Academic Press. Dobbing, J . (1974). Prenatal development and neurological development. In J. Cravioto, L. Hambraeus, and B. Vahlquist (Eds.), Early Malnutrition and Mental Development. Uppsala, Sweden: Almqvist and Wiksell. Pp. 96-1 10. Ehrlich, A. (1974). Infant development in two prosimian species: Greater galago and slow loris. Dev. Psychobiol., 7: 439-454. Elias, M. F., and Samonds, K. W. (1973). Exploratory behavior of cebus monkeys after having been reared in partial isolation. Child Dev., 44: 218-220. Elias, M. F., and Samonds, K. W. (1974). Exploratory behavior and activity of infant monkeys during nutritional and rearing restrictions. Am. J. Clin. Nutr., 27: 458463. Hill, W . C. 0. (1960). Primates: Comparative Anatomy and Taxonomy. Vol. 4: Cebidae Part A . Edinburgh: Edinburgh University Press. Hinde, R. A. (1971). Development of social behavior. In A. M. Schrier and F. Stollnitz (Eds.), Behavior ofNonhuman Primates. Vol. 3. New York: Academic Press. Pp. 1-68. Jolly, A. (1972). The Evolution ofPrimate Behavior. New York: MacMillan. King, J . E., Fobes, J. T., and Fobes, J. L. (1974). Development of early behaviors in neonatal squirrel monkeys and cotton-top tamarins. Dev. Psychobiol., 7 : 97-109. King, J. E., and King, P. A. (1970). Early behaviors in hand-reared squirrel monkeys. Dev. Psychobiol., 2 : 251-256. Kluver, H. (1933). Behavioral Mechanisms in Monkeys. Chicago: Chicago University Press. Long, J . O., and Cooper, R. W. (1968). Physical growth and dental eruption in captive-bred squirrel monkeys. In L. A. Rosenblum, and R. W. Cooper (Eds.), The Squirrel Monkey. New York: Academic Press. Pp. 193-205. Mathieu, M., Bouchard, M-A., Granger, L., and Herscovitch, J. (1976). Piagetian object-permanence in Cebus capucinus, Lagothrica jlavicauda and Pan troglodytes. Anim Behav., 24: 585-588. Mowbray, J. B., and Cadell, T. E. (1962). Early behavior patterns in rhesus monkeys. J. Comp. Physiol. PSyChOl., 55:350-357. Moynihan, M. (1976). 7he New world Primates. Princeton, N.J.: Princeton University Press. Napier, J . R., and Napier, P. H. (1967). A Handbook ofLivingPrimates. New York: Academic Press. Redshaw, M., and Hughes, J. (1975). Cognitive development in primate infancy. Paper presented at the Annual Meeting of the British Association for the Advancement of Science, Guildford, Surrey, England. Romanes, G. J . (1890). Animal Intelligence. New York: Appleton. Schultz, A. H. (1960). Age changes in primates and their modification in man. In J. M. Tanner (Ed.), Human Growth. London: Pergamon Press. Pp. 1-20.
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Schultz, A. H. (1969). The Life off+zmates; London: Weidenfeld and Nicokon. Schusterman, R. J., and Sjoberg, A. (1969). Early behavior patterns of squirrel monkeys (Saimin sciureus). In C. R. Carpenter (Ed.), Proceedings of the Second International Congress of Primatology. Vol. 1. Behavior. Basel: Karger. Pp. 194-203. Thorington, R. W., Jr. (1967). Feeding and activity of cebus and saimiri in a Colombian forest. In D. Starck, R. Schneider, and H.-J. Kuhn (Eds.), Neue Ergebnisse der Pnmntologie. Stuttgart: Fischer. Pp. 180-184. Vaughter, R. M., Smotherman, W., and Ordy, J. M. (1972). Development of object permanence in the infant squirrel monkey. Dev. Psychol., 7: 34-38. Wilson, E. 0. (1975). Sociobiology. Cambridge: Harvard University Press. Wise, K. L., Wise, L. A., and Zimmermann, R. R. (1974). Piagetian object permanence in the infant rhesus monkey. Dev. Psychol., 10: 429437.
An evolutionary trend exists among primates for those species which reach higher levels of functioning to prolong the juvenile period of life (Schultz, 1969). Of the 2 species of New World monkey under study here, cebus monkeys are known to attain a high level of manual dexterity and problem solving capacity as adults (see Hill, 1960; Kluver, 1933; Romanes, 1890), markedly higher than that of squirrel monkeys (see Davis, 1974; Moynihan, 1976; Thorington, 1967)). One can hypothesize that, because they reach a higher level of functioning, cebus monkeys have a longer juvenile period than do squirrel monkeys and are therefore less mature at birth and during the 1st months of postnatal life. This paper reports a test of that hypothesis. To compare overall level of maturation across species, one must examine several aspects of physical and behavioral development. The various body systems mature at different rates within an individual and the pattern of maturation of the different systems varies across species (Schultz, 1960). Two aspects of physical development which can be compared at birth are brain growth and body growth, in that birth occurs at different stages of development of the brain (Dobbing, 1974) and the body (Schultz, 1969) in different species. Some aspects of behavioral development which can be assessed during infancy include perceptualmotor, locomotor, and cognitive development. Tests of perceptual-motor and locomotor development in infancy have been devised for rhesus (Mowbray & Cadell, 1962) and adapted for use with squirrel monkeys (King, Fobes, and Fobes, Reprint requests should be sent to Dr. Marjorie F. Elias, Department of Psychiatric Research, Children’s Hospital Medical Center, 300 Longwood Avenue, Boston, Massachusetts 021 15, U.S.A. Received for publication 27 April 1976 Revised for publication 18 November 1976 Developmental Psychobiology, lO(6): 519-528 (1977) @ 1977 by John Wiley (L. Sons, Inc.
519
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1974; King & King, 1970; Schusteman & Sjoberg, 1969), tamarins (King et al., 1974), greater galagos (Ehrlich, 1974), and slow loris (Ehrlich, 1974). Cognitive development has been assessed in monkeys by tests of problem solving, discrimination learning, and recently by tests based on Piagetian theory (Jolly, 1972). Moreover, one stage of development which has been studied in several species is Piaget’s Stage 4 of sensory-motor development: object permanence, which is ability to find a hidden object (Mathieu, Bouchard, Granger & Herscovitch, 1976; Redshaw & Hughes, 1975; Vaughter, Smotherman, & Ordy, 1972; Wise, Wise, & Zimmermann, 1974). The present study was designed to assess relative maturity of cebus and squirrel monkeys at birth, comparing brain weight and body weight as prjoportions of mature weights, and postnatally, by age of acquisition of mature responses in some items of perceptual-motor, locomotor, and cognitive development. Specifically, I planned to investigate whether cebus and squirrel monkeys differed in maturity at birth and whether any differences found at birth might be diminished or increased during infancy by differences in rate of postnatal behavioral development.
Eight cebus monkeys (Cebus dbifrons), 5 females and 3 males, and 8 squirrel monkeys (Saimiri sciureus from Leticia, Colombia), 3 females and 5 males, were the subjects of the study. They were born in the breeding colony of the laboratory, taken from their mothers at birth, and reared in the laboratory nursery. They were kept for several weeks in incubators (squirrels, 2 weeks; cebus, 3 weeks) and then in cages in the nursery, and fed ad libitum by bottle with a liquid diet of good nutritional quality. Although far from natural, the rearing environment was relatively constant for all animals.
Weight The infants were weighed when they came to the nursery a few hours after birth. Adult body weights were obtained from animals in the breeding colony. The adults were all feral animals who had not been subjected to experimental diets and included the parents of the infants. The weights of the females are non-pregnant weights, each from a single weighing. The weight of each squirrel monkey m d e is a mean of 12 weights obtained monthly for a year, in order to average out the fatted phase of each male (data from K. Rasmussen, personal communication). Although small, the sample of males includes all the breeding males in the colony. No weights were available for cebus males because the breeding males had never been weighed and other adult males had been on experimental diets. Brain weights are wet weights obtained from animals who died or were sacrificed in the laboratory. An autopsy was performed within 12 hr of death. The brain was severed at the occipital-atlas junction, removed, and weighed immediately. Brain weights of newborns were taken from stillbirths and infants who died within
INFANT DEVELOPMENT IN NEW WORLD MONKEYS
521
the 1st week after birth. In order to exclude prematures, only animals whose body weight fell within 2 standard deviations of mean birth weight were included. Brain weights of adults were taken from breeding animals not on experimental diets.
Behavior The behavioral tests were chosen to assess perceptual-motor and locomotor development and the development of object permanence. Test items were selected in which the expected responses were absent at birth but could be elicited consistently after they had been acquired. Therefore, age of acquisition of the expected response was the variable under consideration. The procedures for testing perceptual-motor and locomotor development, except the development of the grasp, were modifications of the tests devised by Mowbray and Cadell (1952) and King and co-workers (1970, 1974). Development of the grasp was measured by a technique used previously by Elias and Samonds (1973, 1974). Object permanence was measured by procedures adapted from the Einstein Scale of Sensory-Motor Development. Seventeen items were scored from 9 procedures, described in order of presentation. The test items were presented in a fured order planned to proceed from less to more disturbing procedures. Testing took place weekly from the 1st week of postnatal life. It was carried out in and near each animal's cage and lasted for about 10 min per animal per session. Each animal was tested when its eyes were open, it appeared to be alert, and had been offered its nursing bottle before testing began. Each item was scored on a S-poht scale (0-4) ranging from no response to the response described below for each item.
Tests Percep tual-Motor Development Orient to sound. The animal turns its head to locate the source of the sound of a snap toy held 15 cm above its head and snapped 5 times at 3-sec intervals. It is lying prone facing away from the tester. Score: 0-no head turn; 2-looks about; 4-locates toy by eye. Visual following. The animal's gaze and head turn follows an object (snap toy) smoothly when it is moved through an arc of 180" around its head at a distance of about 8 cm. Score: 0-does not follow; 2-follows a little but loses, jerky; 4-follows smoothly through arc. Development of grasp. Approach ring. The animal's body comes within 8 cm of ring (plastic baby bottle cap) hung inside door of the cage for 2 min. Score: 0-no approach; 2-move body forward; 4-come within 8 cm. Touch ring. The animal touches ring with finger or nose. Score: 0-no reach; 2-come within 2 cm; 4-touch ring. Grasp ring. The animal grasps the ring with its fingers. Score: 0-no touch; 2-touch, end of fingers; 4-grasp. Swing or pull ring. The animal pulls at ring or makes it swing. Score: 4-swing or pull ring.
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Object Permanence (1 min per presentation) Pick up ring, not hidden. The animal picks up the ring (gold colored metal ring 4.5 cni in dia) placed on the floor of the cage. Score: 0-does not look at ring; 2-approaches to within 5 cm; 4-picks up ring. Find hidden ring. The animal uncovers, looks at, and handles the ring when placed on the floor of the cage and covered by its cage cloth while it watched. Score: 0-does not look where the ring is hidden; 2-looks at the cloth; 4-uncovers the ring.
Locomotor Development ( 1 min per item) orienting up, turn, The animal turns 180" to a head-up position when placed facing down on a plush-covered board (40 x 40 cm) inclined at a 30" slope. Score: 0-no rotation; 2-partid rotation; 4-fuU 180" turn. Get o f t The animal moves off the board. Score: 0-no movement off the board; 2-walk to edge; 4--walk off board. Crawl/walk. Crawl backward. The animal moves backward from the center to an edge of the plush-covered board laid flat, when it has been placed in the center. Score: 0-no movement; 2-move halfway;4-move to an edge. Crawl forward. The animal moves forward on its belly from the center to the edge of the board. Score: same as above but forward. Walk, off belly. The animal walks on 4 legs with its belly off the surface. Score: same as above but off belly. Righting. Right sd$ The animal climbs astride a horizontal cylinder loosely covered with plush ( 5 cm dia x 32 cm for squirrel monkeys; 9 crn x 38 cm for cebus-approximately the diameter of the mother's torso) when placed underneath it with the body oriented along the cylinder in ventral contact with 4 hands clinging to the plush. Score: 0-no righting; 2-partial righting; 4-on top of cylinder. Get off The animal releases its grip and gets down onto a flat surface 6-10 cm below. Score 0-no release of grip. 2-releases 2 hands and placed them on surface; 4-releases all 4 hands, gets down and breaks body contact with cylinder. Climb down. The animal climbs up at least one body length on a vertical wire mesh cylinder (9 x 41 cm for squirrel monkeys; 15 x 54 cm for cebus) when placed on it head-up with hmdquarters one body length from the bottom, releases grip on cylinder, and breaks contact with it. Score: 0--no descent; 2-turn and descend a little; 4-descend to surface and break contact with cylinder. Interobserver reliability for most items was tested by simultaneous observation and independent rating by 2 observers and ranged between .80 and 1.00.
Results Female squirrel monkeys' body weights at birth averaged 16.5% of adult weights, whereas female cebus averaged 11.1% (Table 1). The female squirrel
INFANT DEVELOPMENT IN NEW WORLD MONKEYS
523
TABLE 1. Brain Weight and Body Weight ofNewborn and Adult Monkeys. Birth Weight (8)
Adult Weight (g) Birth/Adult Weight
N
Mean
SD
N
104 143
110.0 112.9
13.0 13.8
91 7
Cebus monkey Female Male
61 70
227.7 237.5
19.7 24.5
66
Brain Weight Squirrel monkey Female Male
8 11
14.6 15.5
2.2 2.9
17 35
5 7
32.6 34.4
3.0 2.8
-
Body Weight Squirrel monkey Female Male
Cebus monkey Female Male
-
8
SD
(%I
667.0 989.8
77.0 80.1
16.5 11.4
2060.0 -
220.0
11.1
-
-
23.3 25.3
1.6 2.2
62.7 61.3
6.0
48.8 -
Mean
66.8 -
-
monkeys’ brain wieghts at birth were 62.7% of adult brain weights, whereas cebus females’ brains were 48.8% of adult weight. By these criteria the female squirrel monkeys could be said to be physically slightly more mature than the female cebus at birth. Male squirrel monkeys’ brain and body weights were slightly heavier than females’ at birth. Their bodies were considerably heavier at maturity. For the analyses of the behavioral data the 5-point scale of 0-4 was reduced to a dichotomous rating of < 4:4. The scale was collapsed in this way because 0 and 4 were found to denote consistent forms of behavior whereas the intermediate levels were inconsistent on retest. (An animal was judged to have acquired a response when he obtained a score of 4 during 3 out of 4 consecutive weeks. The 1st of those weeks was identified as the age of acquisition of the response.) The week of age at which the animals reached the criterion of acquisition of each response is presented in Table 2. The Mann-Whitney ti-test was applied t o the data to test for significance of differences between the species. This test was used rather than the Student t-test because the assumption of normal distributions in the population, a necessary assumption for the t-test, could not be met for all variables. For the same reason, the ranges are presented as indicators of the variabihty of the distributions rather than standard deviations. In perceptual-motor development, the squirrel monkeys began to turn their heads t o follow a moving object at 4 weeks, to orient to the sound of a click at 6 weeks, and to approach, touch, and grasp a ring between 5 and 9 weeks. The cebus were 3 weeks later to follow the moving object and 5 weeks later to approach, touch, and grasp. These delays were statistically significant (p’s < .OS). Male-female differences in these very small groups were not significant. In the test of object permanence squirrel monkeys picked up the ring when it was not hidden at 9 weeks and found it when hidden at 12 weeks.
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TABLE 2. Behavioral Development of Squirrel and Cebus Monkeys: Age in Weeks. Squirrel Monkeys Females Behavior Perceptual-Motor Development Orient to sound Visual following Development of grasp Approach ring Touch ring Grasp ring Swing/pull ring
-
Totdl
ra
N
Mean
Range
N
Mean
Range
.96 .97
3 3
6.0 5.7
4-9 2-9
5 5
6.2 4.0
5-8 3-5
8 8
6.1 4.6
4-9 2-9
.97
3 3 2d 2d
5.0 6.7 5.5 7.0
4-6 5-9 5-9
5 5 5 5
5.4 8.4 10.2 10.6
3-7 5-18 5-20 5-20
8 8 7d 7d
5.3 7.8 8.9 9.6
3-7 5-18 5-20 5-20
Object Permanence Ring not hidden Ring hidden Locomotor Development Orienting up Turn Get off Crawl/walk Crawl forward Walk, off belly Righting Get off Climb down
Males
5-6
N Mean Range
3 3
8.7 12.3
6-14 10-15
5 qf
10.2 12.8
7-18 10-15
8 7f
.80 .90
3 3
2.7 3.3
2-4 3-4
5 5
2.8 3.6
2-4 2-5
8 8
2.8 3.5
2-4 2-5
1.00
3 3
1.7 2.3
1-2 2-3
5 5
3.0 3.6g
1-4 3-4
8 8
2.5 3.1
2-4
3 3
2.3 7.3
2-3 2-10
5 4f
3.6g 6.0
3-5 2-1 0
8 7f
3.1 6.6
2-5 2-10
1.00 .98
9.6 6-18 12.6 10-15
1-4
aInterobserver reliability. bAsterisks denote levels of significance of difference tiom mean of squirrel monkeys (both sexes): Mann-Whitney U-test; * p < .05; **p < .01; ***p < .001. 'Only 4 cebus (2 females, and 2 males of the present sample were tested for this response; data from 4 others tested earlier were included. Some animals never acquired this response. %ome animals were not recorded on this response. fOne animal died before acquiring this response. gMales and females were significantly different on this item @ < .05).
a
Cebus were 3 weeks older when they began to pick it up and 6 weeks, older when they found i t hidden. The latter was a statistically significant difference. The sexes showed no difference in finding the hidden ring in either species. In locomotor development, the squirrel monkeys turned to orient themselves upward on a slope at 2 weeks and began to get off the slope the following week. Five of them, 2 females and 3 males, crawled backwards. They began to crawl forward at 2 weeks and then to walk at 3 weeks. The cebus, who all crawled backwards initially, crawled forward at 6 weeks and began to walk at 7 weeks, a statistically significant difference. Five of the 8 squirrel monkeys righted themselves by climbing astride the horizontal cylinder as reported by King et al. (1974). None of the cebus ever did so. Both species got off the horizontal cylinder at 3 weeks of age. The cebus climbed down off the vertical cylinder at 4 weeks, slightly but not significantly earlier than the squirrels. The squirrel females walked and got off the horizontal cylinder a week before the
INFANT DEVELOPMENT IN NEW WORLD MONKEYS
525
TABLE 2. (continued)
Cebus Monkeys Total
Males
Females
N
Mean
Range
6.7
5-8 5-9
N
N
Mean
Range
5 5
8.2 7.2
7-11 5-10
4' 4' 4' 4c
9.8 10.8 11.8 13.8
9-11 10-11 11-14 12-15
11.3 4' 13.5 4' 3C'd 14.7 lCYd 15.0
9-13 9-16 11-18 -
8' 8' 7C'd
2e 4'
10.5 18.5
9-12 15-21
2e ' 4
14.0 19.3
5 5
5 .o 8.8
1-9 5-12
3 3
5 qf
6.2 7.5
5-7 7-9
5 5
4.4 4.8
2-1
1-8
3 3
I .I
8 8
Meanb
Range
7.6 7.4**
5-1 1 5-10
5C'd
10.5*** 12.1*** 13.0* 14.0*
9-13 9-16 11-18 12-15
13-5 18-21
4e 8'
12.3 18.9***
9-15 15-21
3.3 6.7
3-4 5-9
8 8
4.4 8.0***
1-9 5-12
3 3
6.3 1.3
4-9 6-9
8 7f
6.3*** 1.4*+*
4-9 6-9
3 3
2.7 3.7
2-4 0-7
8 8
3.8 4.4
2-1 0-8
males. These were the only significant male-female differences and, being drawn from a set of 28 tests, are scarcely beyond a chance occurrence of findings significant at the .05 level.
Discussion The behavioral findings and birth weights are consistent in showing cebus to be less mature than squirrel monkeys in some aspects of development during the 1st months of postnatal life. The responses acquired latest-swinging or pulling the ring and finding the hidden ring-have the largest gap between the species, 6 and 7 weeks. This result indicates that cebus were not catching up to overcome their relative immaturity at birth but were developing at a generally slower rate postnatally. Squirrel monkeys are known to be large at birth relative to the size of their mothers (Long & Cooper, 1968). The birth weights and mature weights reported here are consistent with those reported previously for squirrel monkeys (Long & Cooper, 1968; Napier & Napier, 1967). 1 had expected, then, that the cebus would be relatively smaller at birth. Adult squirrel monkeys are reported to
526
ELIAS
have the highest ratio of brain to body weight of any primate (Hill, 11960). This has been explained by their small size relative to most primates in that the ratio of brain to body size varies inversely with absolute body size (Schultz, 1969). Cebus, at more than twice the body weight, have a virtually identical brain t o body ratio (squirrel monkey ratio, 1:29.6; cebus ratio, 1:30.8). T!his finding was not expected. A comparison of findings on behavioral development from field and laboratory studies reveals wide variability within and across species (Hinde, 197 1). Even among studies which have used modifications of the same technique the data are inconsistent (Ehrlich, 1974; Table 1). Studies of acquisition of object permanence also report inconsistent findings. Two rhesus monkeys attained Stage 4 by 10 and 12 weeks (Wise et al., 1974), 2 gorillas both attained it by 18 weeks, and 2 humans attained i t by 34 weeks (Redshaw & Hughes, 1975). The present finding that squirrels attained it by 13 weeks and cebus attained it by 19 weeks is not inconsistent with these findings from other species. But a study which examined squirrel monkeys reports that a 26-week-old animal had not yet attained Stage 4 and a 39-week-old was in transition (Vaughter et al., 1972). That animal was 3 times the age of acquisition of the squirrel monkeys in the present study, a highly inconsistent finding. One is forced to conclude that differences in method of testing or rearing conditions must be producing inconsistencies in findings in both cognitive and motor development. For example, in the righting test, releasing was seen in squirrel monkeys during the first week in Schusterman and Sjoberg’s study (1969), but not until 5 weeks by King et al. (cf. Ehrlich, 1974; Table 1). This difference may have been due to the fact that the animal was lowered until its back made contact with a horizontal surface in the former study, but was held above the surface in the latter study. Comparisons, therefore, are only justified when species are maintained and tested under similar conditions. I could not follow the monkeys in this study long enough to determine the duration of the juvenile period. However, data on dentition are available which document a continued slower rate of development of cebus relative to squirrel monkeys by 3 months and permanent dentition by 21 months (Long & Cooper, 1968). Cebus have completed deciduous dentition by 6 to 8 months and permanent dentition by 36 to 4 0 months (Napier & Napier, 1967). By these criteria, the duration of immaturity is almost twice as long in cebus. The trend of prolongation of immaturity with evolutionary progress identified by Schultz (1969) was referred to at the outset. The duration of juvenile growth ranges from a period of a few months in tree shrews to about 18 mon1.h~in prosimians, 2 to 3 years in monkeys, 8 years in great apes, and up to 14 years in humans. The prolongation of immaturity postpones reproductive capability but it provides juveniles with increased opportunity to learn from adults. The evolutionary advantage t o higher primates of prolonged immaturity must be considerable to outweigh the cost of delayed reproduction. Wilson (1975) has suggested that the advantage is in permitting the animal time to develop skill and experience from the environment in order to allow flexibility in behavioral patterns to fit behavior to short-term changes in the environment. Because learned skills and information cannot be transmitted genetically, evidently the opportunity to acquire them by
INFANT DEVELOPMENT IN NEW WORLD MONKEYS
527
prolonging the juvenile period has been transmitted instead. Although taxonomically close, the 2 species compared here differ strikingly and consistently in maturity at birth and during infancy, in duration of immaturity, and in ultimate level of functioning. The evidence suggests that cebus monkeys have evolved further in the direction of higher primates than have squirrel monkeys.
Notes This investigation was supported in part by Public Health Service Research Grants HD-07032 and HL-10098 and by the Fund for Research and Teaching, Department of Nutrition, Harvard School of Public Health. It was part of a project concerned with the behavioral effects of malnutrition. The author thanks Ms. Sandra Thomas and Professor Joseph C. Speisman for their help in collecting data and Professor D. Mark Hegsted, Principal Investigator of the project, for his cooperation.
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Schultz, A. H. (1969). The Life off+zmates; London: Weidenfeld and Nicokon. Schusterman, R. J., and Sjoberg, A. (1969). Early behavior patterns of squirrel monkeys (Saimin sciureus). In C. R. Carpenter (Ed.), Proceedings of the Second International Congress of Primatology. Vol. 1. Behavior. Basel: Karger. Pp. 194-203. Thorington, R. W., Jr. (1967). Feeding and activity of cebus and saimiri in a Colombian forest. In D. Starck, R. Schneider, and H.-J. Kuhn (Eds.), Neue Ergebnisse der Pnmntologie. Stuttgart: Fischer. Pp. 180-184. Vaughter, R. M., Smotherman, W., and Ordy, J. M. (1972). Development of object permanence in the infant squirrel monkey. Dev. Psychol., 7: 34-38. Wilson, E. 0. (1975). Sociobiology. Cambridge: Harvard University Press. Wise, K. L., Wise, L. A., and Zimmermann, R. R. (1974). Piagetian object permanence in the infant rhesus monkey. Dev. Psychol., 10: 429437.
