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Maternal separation alters later consumption of novel liquids in the squirrel monkey
BEHAVIORALAND NEURALBIOLOGY45, 254--260 (1986)
BRIEF REPORT Maternal Separation Alters Later Consumption of Novel Liquids in the Squirrel Monkey MICHAEL B. HENNESSY 1
Department of Psychology, Wright State University, Dayton, Ohio 45435 The consumption of novel, fruit-flavored drinks was measured in juvenile squirrel monkeys that had either had their mother removed from the home cage for 2 h on 80 occasions prior to weaning or had not undergone this separation procedure. Among previously separated animals, males drank more than did females during the first 30 min following presentation, whereas there was no difference in the drinking of nonseparated males and females at this time. Further, the amount of liquid consumed during the 20 h following presentation increased across days of exposure in the nonseparated, but not in the previously separated monkeys. These results show that brief maternal separation can affect the later behavior Of squirrel monkeys, and are consistent with findings in rhesus macaques that maternal separation alters later exploratory behavior. © 1986AcademicPress, Inc.
For many years, there has been concern over the long-term effects of maternal separation on the behavior and neural functioning of children (Bowlby, 1952). Experiments with nonhuman primates have established various lasting, debilitating consequences of early maternal separation, particularly if the separation is permanent and/or combined with other restrictive procedures, such as isolation rearing and severe physical confinement (Mineka & Suomi, 1978; Ruppenthal, Arling, Harlow, Sackett, & Suomi, 1976). The nonhuman primate literature provides less information on the later consequences of temporary separations from the mother that do not involve other significant forms of deprivation. The studies that have been performed have focused almost exclusively on a single species, the rhesus macaque. Separations of 1 or 2 weeks duration have been found to have protracted effects on later mother-infant relations (Hinde,
Leighton-Shapiro, & McGinnis, 1978; McGinnis, 1980) and to produce l This research was supported by Grant HD14591 from NIH. The author thanks Ms. Deborah Mallis, Ms. Kathleen Hagen, and Ms. Carolina Jordan for assistance in rearing the monkeys and collecting data, and Dr. Sally P. Mendoza for carefully evaluating the manuscript. Reprint requests may be sent to the author at the address given. 254 0163-1047/86 $3.00 Copyright© 1986by AcademicPress, Inc. All rights of reproductionin any form reserved.
LATER EFFECTS OF MATERNAL SEPARATION
255
decrements in later object exploration, activity, and play (Hinde & SpencerBooth, 1971) in rhesus monkeys. Exaggerated emotional reactions (e.g., fear grimacing) to unfamiliar conspecifics have been reported in rhesus that had experienced a series of 2-h maternal separations about 1 year earlier (Mitchell, Harlow, Griffin, & Moller, 1967). Suomi, Mineka, and DiLizio (1983) found that rhesus subjected to multiple, 4-day separations exhibited a number of later behavioral anomalies. Most notably, the separated animals appeared to be retarded in their development of independence, showed reduced object exploration, and unlike control monkeys, avoided their mother in later preference tests. When one considers the great variation among species of primates in other early-experience effects (e.g., Sackett, Ruppenthal, Fahrenbruch, Holm, & Greenough, 1981), data concerning the later consequences of temporary maternal separation in monkeys other than the rhesus would be most welcome. Recently, Coe, Glass, Wiener, and Levine (1983) reported that in the squirrel monkey, six 1-h separations from the mother had no lasting effects on various normative behaviors involving motherinfant relations and infant interactions with others. The experiment reported here also investigated the consequences of separation in squirrel monkeys. The dependent variable chosen was a measure of neophobia--the consumption of novel liquids. The consumption of novel substances might be considered an exploratory behavior because it consists of the animal investigating and exposing itself to an unfamiliar feature of the environment. This interpretation is supported by studies with rats in which various early manipulations (prenatal stress, preweaning handling, and postnatal enrichment) were found to increase or decrease the consumption of novel liquids in a manner consistent with the direction of effects on more traditional tests of exploration (Hennessy, Smotherman, & Levine, 1977; Pfister, Golus, & McGee, 1981; Weinberg, Smotherman, & Levine, 1978). The present study demonstrates that repeated, brief, maternal separation that involves no additional restriction, or even exposure to novel surroundings, can modify this measure of later behavior in the squirrel monkey. Six male and six female squirrel monkeys (Saimiri sciureus) of the Bolivian variety served as subjects. Beginning shortly after birth, each subject was housed with its mother in a standard primate cage (74 x 64 × 38 cm) located in a temperature-controlled indoor colony room that contained no animals other than those used in this study. The subjects were visually isolated from all monkeys in other cages. They were maintained on a 12-h light/dark cycle (lights on at 0630 h) and were provided with New World monkey chow and water, which was supplemented with Tang orange-flavored drink. Three male and three female infants were assigned to the separated (S) group, and the other three subjects of each gender were assigned to the nonseparated (N) control group. From 12 through 31 weeks of age,
256
MICHAEL B. HENNESSY
each S monkey had its mother removed from the home cage and taken to a distant room in the building for 2 h/day, 4 days/week (a total of 80 separations). The N monkeys were not subjected to this procedure, but in all other ways were treated as were the S animals. For greater detail concerning the rearing and separation procedures, see Hennessy (in press). At 35 weeks of age, the mother was permanently removed from the cage, and all S and N monkeys lived alone throughout the duration of this study. At Week 43, each animal was weighed. Tests of consumption of novel substances were initiated at about 45 weeks of age. Two novel liquids were used: Hawaiian Punch fruit drink and grape-flavored KoolAid drink which was made without sugar. The novel liquids were presented in a glass bottle with spout that was identical to the animal's water bottle and spout. A small plastic bottle with wide (7 cm in diameter) but tapered mouth was mounted on the inside front wall of the cage directly below the spout of the test bottle in order to collect spillage. The monkey's water bottle was left in place during testing. The test bottle and water bottle were mounted at opposite ends of the front wall of the cage. On the first trial, the bottle with novel liquid was presented at approximately 1500 h, weighed 30 min later, and then returned to the cage. It was weighed again 20 h following initial presentation, but not returned to the cage at this time. An identical trial was begun 4 h later. Each animal was tested for four consecutive trials with one liquid during the first week of novel liquid testing, and for four consecutive trials with the other liquid during the following week. The number of grams drunk at 30 min and at 20 h (corrected for spillage) served as dependent measures. In both the S and N groups, two males and two females were tested with Hawaiian Punch drink the first week and Kool Aid drink the second. The other male and female in each group were exposed to the liquids in the reverse order. Two control trials, during which water consumption was measured, were also administered. The day preceding the first trial with the first novel liquid, the test bottle was filled with water and mounted with the spillage collector on the cage front. The amount of water drunk from this bottle at 30 min and 20 h was measured. This trial was included to detect any differences between groups in tendency to drink, per se, in the unfamiliar situation (i.e., from the second bottle with spillage collector). On the day following the last trial with the second novel liquid, water was presented in both bottles and total water consumption was measured at 30 min and 20 h. This trial provided an estimate of normal total liquid consumption of monkeys in the two groups. A 2 (Rearing Group) x 2 (Gender) analysis of variance (ANOVA) revealed no effect of these variables on body weight at 43 weeks. For tests of consumption of novel liquids, separate 2 (Rearing Group) x 2
L A T E R E F F E C T S OF M A T E R N A L SEPARATION
257
(Gender) x 4 (Day of Exposure) ANOVAs, with the last factor treated as a repeated measure, were used to analyze the number of grams drunk at 30 min and at 20 h. Because the animals drank very little of the grapeflavored drink overall, the data for the two novel liquids were totaled for these analyses. At 30 min, one significant effect was obtained, a Rearing Group x Gender interaction [F(1, 8) = 6.37, p < .05]. Post hoc tests for simple main effects revealed that in the S group, males consumed more of the novel liquids than did females (p < .05). For N monkeys, males and females did not differ in the amount of novel liquids drunk at 30 min (Fig. 1). At 20 h, there was one significant finding, a Rearing Group x Day of Exposure interaction [F(3, 24) = 3.48, p < .05]. Post hoc tests for simple main effects revealed a significant change in the amount of liquid drunk across days for N (p < .05) but not S monkeys. Newman-Keu|s tests showed that the effect for N animals was due to an increase in drinking over days; i.e., more novel liquid was consumed on Day 4 than on either Day 2 or 3 (p < .05, Fig. 2). For the control trials, 2 (Rearing Group) x 2 (Gender) ANOVAs yielded no significant effects for the amount of water drunk from the test bottle at either 30 min or 20 h on the day prior to presentation of the novel liquids, or for the total amount of water drunk (from both bottles) at either 30 min or 20 h on the day following the last day of novel liquid testing. These results show that brief periods of maternal separation can alter later behavior in the squirrel monkey. Two effects were obtained. First, in the 30-min test, previous separation differentially affected males and females. Although there was no difference between those males and females that had not been separated, the S males drank more than did the S females. Young male monkeys are often found to explore and 25 20 15 10 5
S N FIG. 1. Mean number of grams of novel liquids drunk by previously separated (S) and nonseparated (N) males (El]) and females ([]) at 30 rain. The male-female difference was significant for S (p < .05) but not N animals. Vertical bars indicate standard errors of the means.
258
MICHAEL B. HENNESSY
220 2 180
O
E ,~ 140 (5 1O0
Days
FI~. 2. Mean number of grams of novel liquids drunk by previously separated (S; 0 ) and nonseparated (N; O) monkeys on the 4 days of testing. For N monkeys, the value for Day 4 was greater than those for Days 2 and 3 (p < .05).
interact with their environment more than do young females (Baldwin & Baldwin, 1977). The present results suggest that in Saimiri, early maternal separation (and perhaps early exposure to other environmental threats or challenges) may increase the likelihood that such male-female differences will occur. The gender difference obtained here is best characterized as reflecting initial sampling, rather than overall drinking, of novel liquids because it was evident 30 min, but not 20 h, following presentation of the liquids. The second consequence of maternal separation was observed in the 20-h test. N monkeys showed an increase in consumption from Days 2 and 3 to Day 4, whereas S monkeys showed no significant change in consumption across days. Interpretation of this effect is hampered somewhat by the drinking of N monkeys on Day 1 (which was intermediate to that seen on Days 2 and 3 and that on Day 4). Keeping this caveat in mind, it appears that control monkeys increased their consumption of the novel fruit-flavored liquids as these liquids became more familiar with repeated exposure. This was expected based on earlier studies (e.g., Weinberg et al., 1978). However, in S monkeys, previous separation experience appears to have blocked or retarded this effect. The findings observed here do not appear to be due to differences in the size of the animals, since there was no effect of Rearing Group or Gender on body weight at Week 43. Furthermore, the control trials indicate that the monkeys did not differ in their tendency to drink in the unfamiliar setting (i.e., from the second bottle with spillage collector), or in their typical overall intake of liquids. It is suggested here that the most parsimonious interpretation is in terms of exploratory behavior. As noted above, experiments with rodents indicate that measures of consumption of novel substances correlate well with other measures of exploration, and that this behavior is sensitive to various early manipulations.
LATER EFFECTS OF MATERNAL SEPARATION
259
Viewed in this light, the present results are consistent with previous findings that early separation alters later exploratory behavior in rhesus monkeys (Hinde & Spencer-Booth, 1971; Suomi et al., 1983). Finally, it is noteworthy that the effects observed here were the result of separations of only 2 h duration which occurred in the familiar home cage. Further, the separation series was completed more than 13 weeks prior to the beginning of novel substance testing, and, based on the behavior of the infants during separation, this manipulation did not appear to be particularly traumatizing. No significant behavioral (vocalization) response was observed from Separation 14 onward (Hennessy, in press). However, throughout the series of 80 separations, infants evinced pituitaryadrenal activation as shown by elevated plasma cortisol levels at the conclusion of the 2-h separation period. Perhaps this continual neuroendocrine activation contributed in some way to the later effects of separation reported here. REFERENCES Baldwin, J. D., & Baldwin, J. I. (1977). The role of learning phenomena in the ontogeny of exploration and play. In S. Chevalier-Skolnikoff & F. E. Poirer (Eds.), Primate biosocial development: Biological, social, and ecological determinants (pp. 343-406). New York: Garland. Bowlby, J. (1952). Maternal Care and Mental Health. Geneva: World Health Organization. Coe, C. L., Glass, J. C., Wiener, S. G., & Levine, S. (1983). Behavioral, but not physiological, adaptation to repeated separation in mother and infant primates. Psychoneuroendocrinology, 8, 401-409. Hennessy, M. B. (in press). Multiple, brief maternal separations in the squirrel monkey: Changes in hormonal and behavioral responsiveness. Physiology and Behavior. Hennessy, M. B., Smotherman, W. P., & Levine, S. (1977). Early olfactory enrichment enhances later consumption of novel substances. Physiology and Behavior, 19, 481483. Hinde, R. A., Leighton-Shapiro, M. E., & McGinnis, L. (1978). Effects of various types of separation experience on rhesus monkeys 5 months later. Journal of Child Psychology and Psychiatry, 19, 199-211. Hinde, R. A., & Spencer-Booth, Y. (1971). Effects of brief separation from mother on rhesus monkeys. Science, 173, 111-118. McGinnis, L. M. (1980). Maternal separation studies in children and nonhuman primates. In R. W. Bell & W. P. Smotherman (Eds.), Maternal influences and early behavior (pp. 311-335). Jamaica, NY: Spectrum. Mineka, S., & Suomi, S. J. (1978). Social separation in monkeys. Psychological Bulletin, 85, 1376-1400. Mitchell, G. D., Harlow, H. F., Griffin, G. A., &Moller, G. W. (1967). Repeated maternal separation in the monkey. Psychonomic Science, 8, 197-198. Pfister, H. P., Golus, P., & McGee, R. (1981). Prenatal psychological stress effects on taste neophobia. Physiology and Behavior, 27, 133-135. Ruppenthal, G. C., Arling, G. L., Harlow, H. F., Sacken, G. P., & Suomi, S. J. (1976). A 10-year perspective of motherless-mother monkey behavior. Journal of Abnormal Psychology, 85, 341-349. Sackett, G. P., Ruppenthal, G. C., Fahrenbruch, C. E., Holm, R. A. & Greenough,
260
MICHAEL B. HENNESSY
W. T. (1981). Social isolation rearing effects in monkeys vary with genotype. Developmental Psychology, 17, 313-318. Suomi, S. J., Mineka, S., & DiLizio, R. D. (1983). Short- and long-term effects of repetitive mother-infant separations on social development in rhesus monkeys. Developmental Psychology, 19, 770-786. Weinberg, J., Smotherman, W. P., & Levine, S. (1978). Early handling effects on neophobia and conditioned taste aversion. Physiology and Behavior, 20, 589-596.
BRIEF REPORT Maternal Separation Alters Later Consumption of Novel Liquids in the Squirrel Monkey MICHAEL B. HENNESSY 1
Department of Psychology, Wright State University, Dayton, Ohio 45435 The consumption of novel, fruit-flavored drinks was measured in juvenile squirrel monkeys that had either had their mother removed from the home cage for 2 h on 80 occasions prior to weaning or had not undergone this separation procedure. Among previously separated animals, males drank more than did females during the first 30 min following presentation, whereas there was no difference in the drinking of nonseparated males and females at this time. Further, the amount of liquid consumed during the 20 h following presentation increased across days of exposure in the nonseparated, but not in the previously separated monkeys. These results show that brief maternal separation can affect the later behavior Of squirrel monkeys, and are consistent with findings in rhesus macaques that maternal separation alters later exploratory behavior. © 1986AcademicPress, Inc.
For many years, there has been concern over the long-term effects of maternal separation on the behavior and neural functioning of children (Bowlby, 1952). Experiments with nonhuman primates have established various lasting, debilitating consequences of early maternal separation, particularly if the separation is permanent and/or combined with other restrictive procedures, such as isolation rearing and severe physical confinement (Mineka & Suomi, 1978; Ruppenthal, Arling, Harlow, Sackett, & Suomi, 1976). The nonhuman primate literature provides less information on the later consequences of temporary separations from the mother that do not involve other significant forms of deprivation. The studies that have been performed have focused almost exclusively on a single species, the rhesus macaque. Separations of 1 or 2 weeks duration have been found to have protracted effects on later mother-infant relations (Hinde,
Leighton-Shapiro, & McGinnis, 1978; McGinnis, 1980) and to produce l This research was supported by Grant HD14591 from NIH. The author thanks Ms. Deborah Mallis, Ms. Kathleen Hagen, and Ms. Carolina Jordan for assistance in rearing the monkeys and collecting data, and Dr. Sally P. Mendoza for carefully evaluating the manuscript. Reprint requests may be sent to the author at the address given. 254 0163-1047/86 $3.00 Copyright© 1986by AcademicPress, Inc. All rights of reproductionin any form reserved.
LATER EFFECTS OF MATERNAL SEPARATION
255
decrements in later object exploration, activity, and play (Hinde & SpencerBooth, 1971) in rhesus monkeys. Exaggerated emotional reactions (e.g., fear grimacing) to unfamiliar conspecifics have been reported in rhesus that had experienced a series of 2-h maternal separations about 1 year earlier (Mitchell, Harlow, Griffin, & Moller, 1967). Suomi, Mineka, and DiLizio (1983) found that rhesus subjected to multiple, 4-day separations exhibited a number of later behavioral anomalies. Most notably, the separated animals appeared to be retarded in their development of independence, showed reduced object exploration, and unlike control monkeys, avoided their mother in later preference tests. When one considers the great variation among species of primates in other early-experience effects (e.g., Sackett, Ruppenthal, Fahrenbruch, Holm, & Greenough, 1981), data concerning the later consequences of temporary maternal separation in monkeys other than the rhesus would be most welcome. Recently, Coe, Glass, Wiener, and Levine (1983) reported that in the squirrel monkey, six 1-h separations from the mother had no lasting effects on various normative behaviors involving motherinfant relations and infant interactions with others. The experiment reported here also investigated the consequences of separation in squirrel monkeys. The dependent variable chosen was a measure of neophobia--the consumption of novel liquids. The consumption of novel substances might be considered an exploratory behavior because it consists of the animal investigating and exposing itself to an unfamiliar feature of the environment. This interpretation is supported by studies with rats in which various early manipulations (prenatal stress, preweaning handling, and postnatal enrichment) were found to increase or decrease the consumption of novel liquids in a manner consistent with the direction of effects on more traditional tests of exploration (Hennessy, Smotherman, & Levine, 1977; Pfister, Golus, & McGee, 1981; Weinberg, Smotherman, & Levine, 1978). The present study demonstrates that repeated, brief, maternal separation that involves no additional restriction, or even exposure to novel surroundings, can modify this measure of later behavior in the squirrel monkey. Six male and six female squirrel monkeys (Saimiri sciureus) of the Bolivian variety served as subjects. Beginning shortly after birth, each subject was housed with its mother in a standard primate cage (74 x 64 × 38 cm) located in a temperature-controlled indoor colony room that contained no animals other than those used in this study. The subjects were visually isolated from all monkeys in other cages. They were maintained on a 12-h light/dark cycle (lights on at 0630 h) and were provided with New World monkey chow and water, which was supplemented with Tang orange-flavored drink. Three male and three female infants were assigned to the separated (S) group, and the other three subjects of each gender were assigned to the nonseparated (N) control group. From 12 through 31 weeks of age,
256
MICHAEL B. HENNESSY
each S monkey had its mother removed from the home cage and taken to a distant room in the building for 2 h/day, 4 days/week (a total of 80 separations). The N monkeys were not subjected to this procedure, but in all other ways were treated as were the S animals. For greater detail concerning the rearing and separation procedures, see Hennessy (in press). At 35 weeks of age, the mother was permanently removed from the cage, and all S and N monkeys lived alone throughout the duration of this study. At Week 43, each animal was weighed. Tests of consumption of novel substances were initiated at about 45 weeks of age. Two novel liquids were used: Hawaiian Punch fruit drink and grape-flavored KoolAid drink which was made without sugar. The novel liquids were presented in a glass bottle with spout that was identical to the animal's water bottle and spout. A small plastic bottle with wide (7 cm in diameter) but tapered mouth was mounted on the inside front wall of the cage directly below the spout of the test bottle in order to collect spillage. The monkey's water bottle was left in place during testing. The test bottle and water bottle were mounted at opposite ends of the front wall of the cage. On the first trial, the bottle with novel liquid was presented at approximately 1500 h, weighed 30 min later, and then returned to the cage. It was weighed again 20 h following initial presentation, but not returned to the cage at this time. An identical trial was begun 4 h later. Each animal was tested for four consecutive trials with one liquid during the first week of novel liquid testing, and for four consecutive trials with the other liquid during the following week. The number of grams drunk at 30 min and at 20 h (corrected for spillage) served as dependent measures. In both the S and N groups, two males and two females were tested with Hawaiian Punch drink the first week and Kool Aid drink the second. The other male and female in each group were exposed to the liquids in the reverse order. Two control trials, during which water consumption was measured, were also administered. The day preceding the first trial with the first novel liquid, the test bottle was filled with water and mounted with the spillage collector on the cage front. The amount of water drunk from this bottle at 30 min and 20 h was measured. This trial was included to detect any differences between groups in tendency to drink, per se, in the unfamiliar situation (i.e., from the second bottle with spillage collector). On the day following the last trial with the second novel liquid, water was presented in both bottles and total water consumption was measured at 30 min and 20 h. This trial provided an estimate of normal total liquid consumption of monkeys in the two groups. A 2 (Rearing Group) x 2 (Gender) analysis of variance (ANOVA) revealed no effect of these variables on body weight at 43 weeks. For tests of consumption of novel liquids, separate 2 (Rearing Group) x 2
L A T E R E F F E C T S OF M A T E R N A L SEPARATION
257
(Gender) x 4 (Day of Exposure) ANOVAs, with the last factor treated as a repeated measure, were used to analyze the number of grams drunk at 30 min and at 20 h. Because the animals drank very little of the grapeflavored drink overall, the data for the two novel liquids were totaled for these analyses. At 30 min, one significant effect was obtained, a Rearing Group x Gender interaction [F(1, 8) = 6.37, p < .05]. Post hoc tests for simple main effects revealed that in the S group, males consumed more of the novel liquids than did females (p < .05). For N monkeys, males and females did not differ in the amount of novel liquids drunk at 30 min (Fig. 1). At 20 h, there was one significant finding, a Rearing Group x Day of Exposure interaction [F(3, 24) = 3.48, p < .05]. Post hoc tests for simple main effects revealed a significant change in the amount of liquid drunk across days for N (p < .05) but not S monkeys. Newman-Keu|s tests showed that the effect for N animals was due to an increase in drinking over days; i.e., more novel liquid was consumed on Day 4 than on either Day 2 or 3 (p < .05, Fig. 2). For the control trials, 2 (Rearing Group) x 2 (Gender) ANOVAs yielded no significant effects for the amount of water drunk from the test bottle at either 30 min or 20 h on the day prior to presentation of the novel liquids, or for the total amount of water drunk (from both bottles) at either 30 min or 20 h on the day following the last day of novel liquid testing. These results show that brief periods of maternal separation can alter later behavior in the squirrel monkey. Two effects were obtained. First, in the 30-min test, previous separation differentially affected males and females. Although there was no difference between those males and females that had not been separated, the S males drank more than did the S females. Young male monkeys are often found to explore and 25 20 15 10 5
S N FIG. 1. Mean number of grams of novel liquids drunk by previously separated (S) and nonseparated (N) males (El]) and females ([]) at 30 rain. The male-female difference was significant for S (p < .05) but not N animals. Vertical bars indicate standard errors of the means.
258
MICHAEL B. HENNESSY
220 2 180
O
E ,~ 140 (5 1O0
Days
FI~. 2. Mean number of grams of novel liquids drunk by previously separated (S; 0 ) and nonseparated (N; O) monkeys on the 4 days of testing. For N monkeys, the value for Day 4 was greater than those for Days 2 and 3 (p < .05).
interact with their environment more than do young females (Baldwin & Baldwin, 1977). The present results suggest that in Saimiri, early maternal separation (and perhaps early exposure to other environmental threats or challenges) may increase the likelihood that such male-female differences will occur. The gender difference obtained here is best characterized as reflecting initial sampling, rather than overall drinking, of novel liquids because it was evident 30 min, but not 20 h, following presentation of the liquids. The second consequence of maternal separation was observed in the 20-h test. N monkeys showed an increase in consumption from Days 2 and 3 to Day 4, whereas S monkeys showed no significant change in consumption across days. Interpretation of this effect is hampered somewhat by the drinking of N monkeys on Day 1 (which was intermediate to that seen on Days 2 and 3 and that on Day 4). Keeping this caveat in mind, it appears that control monkeys increased their consumption of the novel fruit-flavored liquids as these liquids became more familiar with repeated exposure. This was expected based on earlier studies (e.g., Weinberg et al., 1978). However, in S monkeys, previous separation experience appears to have blocked or retarded this effect. The findings observed here do not appear to be due to differences in the size of the animals, since there was no effect of Rearing Group or Gender on body weight at Week 43. Furthermore, the control trials indicate that the monkeys did not differ in their tendency to drink in the unfamiliar setting (i.e., from the second bottle with spillage collector), or in their typical overall intake of liquids. It is suggested here that the most parsimonious interpretation is in terms of exploratory behavior. As noted above, experiments with rodents indicate that measures of consumption of novel substances correlate well with other measures of exploration, and that this behavior is sensitive to various early manipulations.
LATER EFFECTS OF MATERNAL SEPARATION
259
Viewed in this light, the present results are consistent with previous findings that early separation alters later exploratory behavior in rhesus monkeys (Hinde & Spencer-Booth, 1971; Suomi et al., 1983). Finally, it is noteworthy that the effects observed here were the result of separations of only 2 h duration which occurred in the familiar home cage. Further, the separation series was completed more than 13 weeks prior to the beginning of novel substance testing, and, based on the behavior of the infants during separation, this manipulation did not appear to be particularly traumatizing. No significant behavioral (vocalization) response was observed from Separation 14 onward (Hennessy, in press). However, throughout the series of 80 separations, infants evinced pituitaryadrenal activation as shown by elevated plasma cortisol levels at the conclusion of the 2-h separation period. Perhaps this continual neuroendocrine activation contributed in some way to the later effects of separation reported here. REFERENCES Baldwin, J. D., & Baldwin, J. I. (1977). The role of learning phenomena in the ontogeny of exploration and play. In S. Chevalier-Skolnikoff & F. E. Poirer (Eds.), Primate biosocial development: Biological, social, and ecological determinants (pp. 343-406). New York: Garland. Bowlby, J. (1952). Maternal Care and Mental Health. Geneva: World Health Organization. Coe, C. L., Glass, J. C., Wiener, S. G., & Levine, S. (1983). Behavioral, but not physiological, adaptation to repeated separation in mother and infant primates. Psychoneuroendocrinology, 8, 401-409. Hennessy, M. B. (in press). Multiple, brief maternal separations in the squirrel monkey: Changes in hormonal and behavioral responsiveness. Physiology and Behavior. Hennessy, M. B., Smotherman, W. P., & Levine, S. (1977). Early olfactory enrichment enhances later consumption of novel substances. Physiology and Behavior, 19, 481483. Hinde, R. A., Leighton-Shapiro, M. E., & McGinnis, L. (1978). Effects of various types of separation experience on rhesus monkeys 5 months later. Journal of Child Psychology and Psychiatry, 19, 199-211. Hinde, R. A., & Spencer-Booth, Y. (1971). Effects of brief separation from mother on rhesus monkeys. Science, 173, 111-118. McGinnis, L. M. (1980). Maternal separation studies in children and nonhuman primates. In R. W. Bell & W. P. Smotherman (Eds.), Maternal influences and early behavior (pp. 311-335). Jamaica, NY: Spectrum. Mineka, S., & Suomi, S. J. (1978). Social separation in monkeys. Psychological Bulletin, 85, 1376-1400. Mitchell, G. D., Harlow, H. F., Griffin, G. A., &Moller, G. W. (1967). Repeated maternal separation in the monkey. Psychonomic Science, 8, 197-198. Pfister, H. P., Golus, P., & McGee, R. (1981). Prenatal psychological stress effects on taste neophobia. Physiology and Behavior, 27, 133-135. Ruppenthal, G. C., Arling, G. L., Harlow, H. F., Sacken, G. P., & Suomi, S. J. (1976). A 10-year perspective of motherless-mother monkey behavior. Journal of Abnormal Psychology, 85, 341-349. Sackett, G. P., Ruppenthal, G. C., Fahrenbruch, C. E., Holm, R. A. & Greenough,
260
MICHAEL B. HENNESSY
W. T. (1981). Social isolation rearing effects in monkeys vary with genotype. Developmental Psychology, 17, 313-318. Suomi, S. J., Mineka, S., & DiLizio, R. D. (1983). Short- and long-term effects of repetitive mother-infant separations on social development in rhesus monkeys. Developmental Psychology, 19, 770-786. Weinberg, J., Smotherman, W. P., & Levine, S. (1978). Early handling effects on neophobia and conditioned taste aversion. Physiology and Behavior, 20, 589-596.