Journal of Comparative Psychology 1992, Vol. 106, No. 3,254-261
In the public domain
Affiliative Vocalizations in Infant Rhesus Macaques (Macaca mulatto) Ned H. Kalin and Steven E. Shelton Departments of Psychiatry and Psychology, University of Wisconsin—Madison and Psychiatry Services, William S. Middleton Department of Veterans Affairs Hospital
Charles T. Snowdon University of Wisconsin—Madison In Experiment 1, infant rhesus monkeys (Macaca mulatto) were separated and then reunited with mothers, united with a male, or placed in an empty cage. Infants girned more when with mothers or the male than when alone. Girns declined over time when infants were united with the male. Coo rates were high when the infant was alone or with the male. Shrieks, barks, and fear-related behavior were higher with the male. In Experiment 2 the vocalizations of infants were examined during separation when alone or when mothers or a male were in the same room. Infants cooed more when mothers or a male were present. Cooing increased over time, with a greater increase in the mothers' presence. Girns were given to both mothers and males, but more were given to mothers. Coos and girns are both affiliative vocalizations but are differentially modulated as infants cease cooing when they receive contact comfort.
Nonhuman primates emit a variety of vocalizations that have many functions. For example, vervet monkeys (Cercopithecus aethiops) produce three types of alarm calls that appear specific to their three major predators, eagles, leopards, and snakes. When recorded vocalizations are played back in the absence of a real predator, predator specific responses are elicited, which indicates that to the listener each call represents a specific predator (Seyfarth, Cheney, & Marler, 1980). Vervet monkeys also have four variations of grunt vocalizations that are emitted in the presence of different conspecifics, according to whether the other animal is dominant or subordinate, is moving into an open area, or is a member of another group (Cheney & Seyfarth, 1982). Gouzoules, Gouzoules, and Marler (1984) described five classes of scream vocalizations used by free-ranging juvenile rhesus monkeys (Macaca mulatto) in different agonistic situations. Different variants were used in situations that involved physical contact versus no contact, to related versus unrelated animals, and to higher ranked versus lower ranked monkeys. These calls recruit support from conspecifics in agonistic encounters. Experiments with captive female vervet monkeys showed that they gave more alarm calls to a novel predator when they were with their own infants than when they were with unrelated infants. Male vervets gave more alarm calls to a novel predator when with a female than if another male was present (Cheney & Seyfarth,
1985). Each of these studies indicates that monkeys do not call reflexively but that they adjust their calls according to the type of predator and conspecific present. The responses of infants to separation from their attachment objects has been well studied since Harlow's early work (Harlow & Harlow, 1965). Both behavioral and vocal reactions of separated infants have been examined. The infant vocalization that has received the most study has been the coo or clear call. On the basis of observations that social separation stimulates infant rhesus monkey cooing, these vocalizations have been interpreted as affiliative (Levine, Franklin, & Gonzalez, 1984; Rowell & Hinde, 1962b). Infant rhesus monkeys, in the presence of conspecifics (Levine et al., 1984; Levine, Wiener, Coe, Bayart, & Hayashi, 1987) or humans (Kalin & Shelton, 1989), modulate their rate of cooing. Infant rhesus monkeys out of sight of their mothers give a different form of coo than they do when their mothers are housed in the same room (Bayart, Hayashi, Faull, Barchas, & Levine, 1990). Lillehei and Snowdon (1978) demonstrated that infant stumptail macaques (Macaca arctoides) gave different coos depending on whether they were seeking contact with their mother or with other group members. However, rhesus macaque infants produce a variety of vocalizations in addition to the coo. Rowell and Hinde (1962b) described a variety of structurally different vocalizations emitted by infant rhesus monkeys. For example, when separated from their mothers and confronted with a human staring at them, infants emit barks and shrieks (Kalin, Shelton, & Barksdale, 1988). Infants also scream (Levine et al., 1987). Rowell and Hinde (1962a; 1962b) suggested that barks constitute the vocal component of the threat display for rhesus macaques, and in our experiments with infants, we observed that barking is frequently accompanied by other hostile gestures (Kalin & Shelton, 1989). Infants shriek in situations of extreme fear when they perceive the possibility of imminent physical harm. In experiments that involve brief separations, we noted that infants reunited with their mothers emitted a call that differed
This work was supported by the Medical Research Service, Department of Veterans Affairs, by U.S. Public Health Service Grant MH 46-983 to Ned H. Kalin, and by U.S. Public Health Service Grant MH 29-775 and National Institute of Mental Health Research Scientist Award MH 00-177 to Charles T. Snowdon. All experiments performed were approved by the University of Wisconsin Animal Research Committee. We thank Helen Van Valkenberg, Kathy Renk, Laura Freund, and Dale Johnson for their assistance with this research. Correspondence concerning this article should be addressed to Ned H. Kalin, Department of Psychiatry, Room D6-250, Clinical Sciences Center, University of Wisconsin, Madison, Wisconsin 53792.
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from other vocalizations that occur more commonly during separation (i.e., coos, barks, and shrieks). This call is characterized by a soft, low-frequency, nasal, whimpering sound that is highly variable in duration. The tonal qualities of this sound appear to fit Rowell and Hinde's (1962b) description of girning: Adult rhesus monkeys will sometimes "girn when approaching and joining another animal to huddle together, groom, or sleep" (p. 287). Because these sounds were very soft, Rowell and Hinde could not present spectrograms of girns. A girning vocalization, which seems to have an affiliative or contact function, has also been described for adult Japanese macaques (Blount, 1985; Green, 1975; Masataka, 1989). On the basis of our observations, those of Rowell and Hinde (1962b), and the studies of Japanese macaques, we hypothesized that girning is an affiliative vocalization that an infant may selectively express in the presence of its mother to signal its need for physical contact. The following experiments were performed to test this hypothesis as well as to characterize infant rhesus vocalizations and the situations in which they occur. Finally, we examined whether infant rhesus monkeys modulate the type and frequency of calls they emit in the presence of different conspecifics.
Experiment 1 Is girning a vocalization emitted by infants during reunion with their mothers? We hypothesized that infants would girn while receiving physical comfort from the mother. Vocal and behavioral responses of infants were compared during three different test conditions: (a) reuniting with the mother after a brief separation, (b) uniting with an unfamiliar adult male after a brief maternal separation, and (c) remaining alone for the same period. We predicted that girning would occur during reunion with the mother and would be associated with contact comfort. We did not expect an infant to girn when in the alone condition nor when united with an unfamiliar male who did not physically comfort the infant. Because cooing is thought to be an affiliative vocalization to facilitate maternal retrieval (Harlow & Harlow, 1965; Rowell & Hinde, 1962b), we expected a reduction in cooing when infants were reunited with their mothers. If the infant's need for the mother persisted, as it would in the alone or male condition, then cooing would continue at a high level.
Method The subjects were 9 infant rhesus monkeys (Macaco mulatto; 5 males and 4 females that ranged in age from 4.6 to 7.5 months). Two of the mothers were primiparous and the others, multiparous. The mothers ranged from 5 to 21 years in age. All infants were housed at the Harlow Primate Laboratory and the Wisconsin Regional Primate Center and lived in dyads with their mothers in cages (75 cm wide x 78 cm high x 80 cm deep). A 12:12-hr light-dark cycle (lights on at 0600 hr) was maintained. Mother-infant dyads were housed with visual and auditory contact with other dyads. Tests were conducted at weekly intervals. Between 0830 and 1400 hr infants were removed from their mothers and placed in another cage in a separate room without auditory or visual contact with the mother. After 20 min of separation, infants were transported to another room, placed in a cage (150 cm wide x 78 cm wide x 80 cm deep), and exposed to one
255
of three test conditions: control—the infant was placed in the cage by itself for 10 min; mother reunion—the infant was placed in cage with its mother present for 10 min; and male union—the infant was placed in the cage with an unfamiliar male (5 years old and weighing 8.3 kg) for 10 min. Behavior and vocalizations were recorded by video- and audiotaping. Vocalizations were recorded with a Sennheiser (Wedermark, Germany) ME-80 microphone with a K3U power module onto a Marantz (Chatsworth, CA) PMD 430 cassette tape recorder on Maxell (San Diego, CA) XLII recording tape. Vocalizations were analyzed by a Multigon (New York, NY) Uniscan II real-time sound-spectrum analyzer on a 0- to 10-kHz scale. Cursors provided digital readings of frequency and temporal parameters. Once the calls were characterized spectrographically, the auditory assessment of the observers was compared with the sonograms. The different types of calls were acoustically distinct and observers' auditory ratings were found to be reliable for categorizing call types. Audiotapes were rated independently by two observers with vocal data recorded in three consecutive 3-min epochs throughout each testing session. To compare differences in call structure between coos and girns, a sample of 10 vocalizations of each type was selected from each individual infant. Nine variables were measured: total duration; start-to-peak duration; start, peak, and end frequencies; peak-minus-start frequency; number of energy bands; energy band with the greatest intensity; and number of inflections (changes in direction of slope > 200 Hz). Within-subjects t tests' compared the variables between each call type. To assess whether significant differences existed between test conditions in the number of animals that ever emitted a particular vocalization, the Cochran Q test was performed (Siegel, 1956). Data were normalized by a square root transformation; then a withinsubjects, repeated analysis of variance (ANOVA) was performed for the frequency of occurrence of each vocalization in order to compare test conditions, time course (testing epochs), and the two raters. Analyses of data from both raters revealed no significant differences between them, so averaged data for the raters were used in the principal analysis. When appropriate, Duncan's multiple range tests were performed for post hoc comparisons. Behavior was scored from the videotapes by a trained rater who used a scoring system previously described by Kalin and Shelton (1988). Interactive behaviors were also scored with the infant as the focal animal. The behaviors of interest are defined in Table 1. Repeated measures ANOVAs were performed on behaviors of interest after the data were normalized through a logarithmic transformation.
Results Vocal response. Girns, coos, barks, and shrieks occurred during the test conditions. Measurements of nine vocal parameters indicated significant differences between girns and coos on all variables examined. Girns were shorter, had lower fundamental frequencies, and less peak-minus-start frequency change. Girns had significantly more energy bands and more inflections with the greatest intensity of energy in the second or third band (Table 2). Barks were throaty calls with a flat frequency. Fifty-six barks were measured from the 6 infants that produced them. The duration was 471.0 ± 130.1 ms; the frequency of the first energy band was 1148 ± 245 Hz, and there were 3.6 ± 1.7 distinct energy bands in the call. Fortythree shrieks were recorded from 5 infants. These calls are short (M = 199.7 ± 103.7 ms) and high pitched (start frequency, M = 5.2 ± 1.8 kHz, and peak frequency, M = 6.6 ± 1.9 kHz), with a great frequency range (M =2.1 ± 1.4 kHz). See Figure 1 for spectrographic examples of each call.
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Table 1 Behavioral and Vocal Categories Category
Description Behavior
Freezing
Locomotion Contact cling Hostility
Lipsmacking Rejection Submission
A period of at least 3 s characterized by tense body postures, no vocalizations, and no movement other than slow head turning. Movement of one or more steps at any speed. Includes dropping from ceiling to floor or swinging. Mutual ventral body contact between two animals. Behavioral display involving at least two of the following: piloerection, barks, head bobbing, eyebrow flicking, cage shaking. Rapid, noisy closing and opening of lips. Forceful attempt to terminate contact with another animal. Oriented withdrawal, fear grimacing, cowering, fleeing, or yielding space. Vocalizations
Bark Coo
Short, rasping, low-frequency sound. Long duration call with initial rise then a fall in frequency. Lips are rounded and pursed. Low-frequency, soft, nasal whine. Lips are closed or slightly open. Often given in bouts. Harsh, brief, high-pitched sound with moderate frequency modulation. Lips pulled back.
Girn Shriek
Girns were rarely emitted by infants when they were alone but occurred more frequently when they were united with the male or reunited with the mother. The number of infants that emitted girns differed significantly across the test conditions (Q = 6.0, p < .02). When alone, 3 of the animals girned as compared with 8 that were united with the male and 7 that were reunited with the mother. A repeated measures ANOVA of girning rate demonstrated a main effect of time course; Table 2 Summary of Parameters of Girns and Coos Parameter Duration (ms) Start to peak Duration (ms) Start frequency (Hz) Peak frequency (Hz) End frequency (Hz) Peak minus start Frequency (Hz) No. energy bands Most intense band No. inflections p
In the public domain
Affiliative Vocalizations in Infant Rhesus Macaques (Macaca mulatto) Ned H. Kalin and Steven E. Shelton Departments of Psychiatry and Psychology, University of Wisconsin—Madison and Psychiatry Services, William S. Middleton Department of Veterans Affairs Hospital
Charles T. Snowdon University of Wisconsin—Madison In Experiment 1, infant rhesus monkeys (Macaca mulatto) were separated and then reunited with mothers, united with a male, or placed in an empty cage. Infants girned more when with mothers or the male than when alone. Girns declined over time when infants were united with the male. Coo rates were high when the infant was alone or with the male. Shrieks, barks, and fear-related behavior were higher with the male. In Experiment 2 the vocalizations of infants were examined during separation when alone or when mothers or a male were in the same room. Infants cooed more when mothers or a male were present. Cooing increased over time, with a greater increase in the mothers' presence. Girns were given to both mothers and males, but more were given to mothers. Coos and girns are both affiliative vocalizations but are differentially modulated as infants cease cooing when they receive contact comfort.
Nonhuman primates emit a variety of vocalizations that have many functions. For example, vervet monkeys (Cercopithecus aethiops) produce three types of alarm calls that appear specific to their three major predators, eagles, leopards, and snakes. When recorded vocalizations are played back in the absence of a real predator, predator specific responses are elicited, which indicates that to the listener each call represents a specific predator (Seyfarth, Cheney, & Marler, 1980). Vervet monkeys also have four variations of grunt vocalizations that are emitted in the presence of different conspecifics, according to whether the other animal is dominant or subordinate, is moving into an open area, or is a member of another group (Cheney & Seyfarth, 1982). Gouzoules, Gouzoules, and Marler (1984) described five classes of scream vocalizations used by free-ranging juvenile rhesus monkeys (Macaca mulatto) in different agonistic situations. Different variants were used in situations that involved physical contact versus no contact, to related versus unrelated animals, and to higher ranked versus lower ranked monkeys. These calls recruit support from conspecifics in agonistic encounters. Experiments with captive female vervet monkeys showed that they gave more alarm calls to a novel predator when they were with their own infants than when they were with unrelated infants. Male vervets gave more alarm calls to a novel predator when with a female than if another male was present (Cheney & Seyfarth,
1985). Each of these studies indicates that monkeys do not call reflexively but that they adjust their calls according to the type of predator and conspecific present. The responses of infants to separation from their attachment objects has been well studied since Harlow's early work (Harlow & Harlow, 1965). Both behavioral and vocal reactions of separated infants have been examined. The infant vocalization that has received the most study has been the coo or clear call. On the basis of observations that social separation stimulates infant rhesus monkey cooing, these vocalizations have been interpreted as affiliative (Levine, Franklin, & Gonzalez, 1984; Rowell & Hinde, 1962b). Infant rhesus monkeys, in the presence of conspecifics (Levine et al., 1984; Levine, Wiener, Coe, Bayart, & Hayashi, 1987) or humans (Kalin & Shelton, 1989), modulate their rate of cooing. Infant rhesus monkeys out of sight of their mothers give a different form of coo than they do when their mothers are housed in the same room (Bayart, Hayashi, Faull, Barchas, & Levine, 1990). Lillehei and Snowdon (1978) demonstrated that infant stumptail macaques (Macaca arctoides) gave different coos depending on whether they were seeking contact with their mother or with other group members. However, rhesus macaque infants produce a variety of vocalizations in addition to the coo. Rowell and Hinde (1962b) described a variety of structurally different vocalizations emitted by infant rhesus monkeys. For example, when separated from their mothers and confronted with a human staring at them, infants emit barks and shrieks (Kalin, Shelton, & Barksdale, 1988). Infants also scream (Levine et al., 1987). Rowell and Hinde (1962a; 1962b) suggested that barks constitute the vocal component of the threat display for rhesus macaques, and in our experiments with infants, we observed that barking is frequently accompanied by other hostile gestures (Kalin & Shelton, 1989). Infants shriek in situations of extreme fear when they perceive the possibility of imminent physical harm. In experiments that involve brief separations, we noted that infants reunited with their mothers emitted a call that differed
This work was supported by the Medical Research Service, Department of Veterans Affairs, by U.S. Public Health Service Grant MH 46-983 to Ned H. Kalin, and by U.S. Public Health Service Grant MH 29-775 and National Institute of Mental Health Research Scientist Award MH 00-177 to Charles T. Snowdon. All experiments performed were approved by the University of Wisconsin Animal Research Committee. We thank Helen Van Valkenberg, Kathy Renk, Laura Freund, and Dale Johnson for their assistance with this research. Correspondence concerning this article should be addressed to Ned H. Kalin, Department of Psychiatry, Room D6-250, Clinical Sciences Center, University of Wisconsin, Madison, Wisconsin 53792.
254
INFANT MACAQUE AFFILIATIVE VOCALIZATIONS
from other vocalizations that occur more commonly during separation (i.e., coos, barks, and shrieks). This call is characterized by a soft, low-frequency, nasal, whimpering sound that is highly variable in duration. The tonal qualities of this sound appear to fit Rowell and Hinde's (1962b) description of girning: Adult rhesus monkeys will sometimes "girn when approaching and joining another animal to huddle together, groom, or sleep" (p. 287). Because these sounds were very soft, Rowell and Hinde could not present spectrograms of girns. A girning vocalization, which seems to have an affiliative or contact function, has also been described for adult Japanese macaques (Blount, 1985; Green, 1975; Masataka, 1989). On the basis of our observations, those of Rowell and Hinde (1962b), and the studies of Japanese macaques, we hypothesized that girning is an affiliative vocalization that an infant may selectively express in the presence of its mother to signal its need for physical contact. The following experiments were performed to test this hypothesis as well as to characterize infant rhesus vocalizations and the situations in which they occur. Finally, we examined whether infant rhesus monkeys modulate the type and frequency of calls they emit in the presence of different conspecifics.
Experiment 1 Is girning a vocalization emitted by infants during reunion with their mothers? We hypothesized that infants would girn while receiving physical comfort from the mother. Vocal and behavioral responses of infants were compared during three different test conditions: (a) reuniting with the mother after a brief separation, (b) uniting with an unfamiliar adult male after a brief maternal separation, and (c) remaining alone for the same period. We predicted that girning would occur during reunion with the mother and would be associated with contact comfort. We did not expect an infant to girn when in the alone condition nor when united with an unfamiliar male who did not physically comfort the infant. Because cooing is thought to be an affiliative vocalization to facilitate maternal retrieval (Harlow & Harlow, 1965; Rowell & Hinde, 1962b), we expected a reduction in cooing when infants were reunited with their mothers. If the infant's need for the mother persisted, as it would in the alone or male condition, then cooing would continue at a high level.
Method The subjects were 9 infant rhesus monkeys (Macaco mulatto; 5 males and 4 females that ranged in age from 4.6 to 7.5 months). Two of the mothers were primiparous and the others, multiparous. The mothers ranged from 5 to 21 years in age. All infants were housed at the Harlow Primate Laboratory and the Wisconsin Regional Primate Center and lived in dyads with their mothers in cages (75 cm wide x 78 cm high x 80 cm deep). A 12:12-hr light-dark cycle (lights on at 0600 hr) was maintained. Mother-infant dyads were housed with visual and auditory contact with other dyads. Tests were conducted at weekly intervals. Between 0830 and 1400 hr infants were removed from their mothers and placed in another cage in a separate room without auditory or visual contact with the mother. After 20 min of separation, infants were transported to another room, placed in a cage (150 cm wide x 78 cm wide x 80 cm deep), and exposed to one
255
of three test conditions: control—the infant was placed in the cage by itself for 10 min; mother reunion—the infant was placed in cage with its mother present for 10 min; and male union—the infant was placed in the cage with an unfamiliar male (5 years old and weighing 8.3 kg) for 10 min. Behavior and vocalizations were recorded by video- and audiotaping. Vocalizations were recorded with a Sennheiser (Wedermark, Germany) ME-80 microphone with a K3U power module onto a Marantz (Chatsworth, CA) PMD 430 cassette tape recorder on Maxell (San Diego, CA) XLII recording tape. Vocalizations were analyzed by a Multigon (New York, NY) Uniscan II real-time sound-spectrum analyzer on a 0- to 10-kHz scale. Cursors provided digital readings of frequency and temporal parameters. Once the calls were characterized spectrographically, the auditory assessment of the observers was compared with the sonograms. The different types of calls were acoustically distinct and observers' auditory ratings were found to be reliable for categorizing call types. Audiotapes were rated independently by two observers with vocal data recorded in three consecutive 3-min epochs throughout each testing session. To compare differences in call structure between coos and girns, a sample of 10 vocalizations of each type was selected from each individual infant. Nine variables were measured: total duration; start-to-peak duration; start, peak, and end frequencies; peak-minus-start frequency; number of energy bands; energy band with the greatest intensity; and number of inflections (changes in direction of slope > 200 Hz). Within-subjects t tests' compared the variables between each call type. To assess whether significant differences existed between test conditions in the number of animals that ever emitted a particular vocalization, the Cochran Q test was performed (Siegel, 1956). Data were normalized by a square root transformation; then a withinsubjects, repeated analysis of variance (ANOVA) was performed for the frequency of occurrence of each vocalization in order to compare test conditions, time course (testing epochs), and the two raters. Analyses of data from both raters revealed no significant differences between them, so averaged data for the raters were used in the principal analysis. When appropriate, Duncan's multiple range tests were performed for post hoc comparisons. Behavior was scored from the videotapes by a trained rater who used a scoring system previously described by Kalin and Shelton (1988). Interactive behaviors were also scored with the infant as the focal animal. The behaviors of interest are defined in Table 1. Repeated measures ANOVAs were performed on behaviors of interest after the data were normalized through a logarithmic transformation.
Results Vocal response. Girns, coos, barks, and shrieks occurred during the test conditions. Measurements of nine vocal parameters indicated significant differences between girns and coos on all variables examined. Girns were shorter, had lower fundamental frequencies, and less peak-minus-start frequency change. Girns had significantly more energy bands and more inflections with the greatest intensity of energy in the second or third band (Table 2). Barks were throaty calls with a flat frequency. Fifty-six barks were measured from the 6 infants that produced them. The duration was 471.0 ± 130.1 ms; the frequency of the first energy band was 1148 ± 245 Hz, and there were 3.6 ± 1.7 distinct energy bands in the call. Fortythree shrieks were recorded from 5 infants. These calls are short (M = 199.7 ± 103.7 ms) and high pitched (start frequency, M = 5.2 ± 1.8 kHz, and peak frequency, M = 6.6 ± 1.9 kHz), with a great frequency range (M =2.1 ± 1.4 kHz). See Figure 1 for spectrographic examples of each call.
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N. KALIN, S. SHELTON, AND C. SNOWDON
Table 1 Behavioral and Vocal Categories Category
Description Behavior
Freezing
Locomotion Contact cling Hostility
Lipsmacking Rejection Submission
A period of at least 3 s characterized by tense body postures, no vocalizations, and no movement other than slow head turning. Movement of one or more steps at any speed. Includes dropping from ceiling to floor or swinging. Mutual ventral body contact between two animals. Behavioral display involving at least two of the following: piloerection, barks, head bobbing, eyebrow flicking, cage shaking. Rapid, noisy closing and opening of lips. Forceful attempt to terminate contact with another animal. Oriented withdrawal, fear grimacing, cowering, fleeing, or yielding space. Vocalizations
Bark Coo
Short, rasping, low-frequency sound. Long duration call with initial rise then a fall in frequency. Lips are rounded and pursed. Low-frequency, soft, nasal whine. Lips are closed or slightly open. Often given in bouts. Harsh, brief, high-pitched sound with moderate frequency modulation. Lips pulled back.
Girn Shriek
Girns were rarely emitted by infants when they were alone but occurred more frequently when they were united with the male or reunited with the mother. The number of infants that emitted girns differed significantly across the test conditions (Q = 6.0, p < .02). When alone, 3 of the animals girned as compared with 8 that were united with the male and 7 that were reunited with the mother. A repeated measures ANOVA of girning rate demonstrated a main effect of time course; Table 2 Summary of Parameters of Girns and Coos Parameter Duration (ms) Start to peak Duration (ms) Start frequency (Hz) Peak frequency (Hz) End frequency (Hz) Peak minus start Frequency (Hz) No. energy bands Most intense band No. inflections p
