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Novelty, arousal, and nasal marking in the squirrel monkey
BEHAVIORAL AND NEURAL BIOLOGY 28, 116--122 (1980)
BRIEF REPORT
Novelty, Arousal, and Nasal Marking in the Squirrel Monkey GARY G.
SCHWARTZ AND LEONARD A. ROSENBLUM 1
Primate Behavior Laboratotiy, Downstate Medical Center, State University of New York, Brooklyn, New York 11203 The nasal secretions expelled during sneezing in the squirrel monkey (Saimh4 sciureus) were visualized under ultraviolet illumination. The quantity of nasal marking by six squirrel monkey groups in response to novel objects containing clean filter paper showed an ordinal decrement over a 3-day period. When one group was exposed to visually identical objects previously exposed to other groups, nasal marking to the olfactorily novel stimuli was highest on D a y 1 and subsequently decreased over a 3-day exposure. Nasal marking in this species may reflect excitatory state and function in a type of olfactory communication previously undescribed for a primate species.
In recent years, the subject of scent marking in the squirrel monkey
(Saimiri sciureus) has attracted considerable attention among behavioral biologists. Various aspects of olfactory-related behaviors have been investigated in this species, from rump rubbing and urine washing (Hennessy, Coe, Mendoza, Lowe, & Levine, 1978) to the infant's olfactory recognition of mother and the effects of differential rearing odors on filial attachment (Kaplan, Cubicciotti, & Redican, 1979). Despite the corpus of work on olfactory recognition in this species, virtually nothing is known about the nature of the identity cueing odor(s). Moreover, there is no evidence to suggest that such cues may be conferred via back rubbing, rump rubbing, or urine washing, although these behaviors are generally regarded as olfactory related (Hennessy et al., 1978). That other behaviors, whose significance is not yet appreciated, may be involved in such communication in the squirrel monkey is echoed in the conclusion of Marriott and Salzen (1978, p. 15): "In order for humans to fully understand the communicated signal all possible sense modalities must be considered." This research was supported by H E W Grants M H 15965 and MH22640. The authors thank Gayle S. Thompson for her assistance. 116 0163 - 1047/80/010116-07502.00/0 Copyright© 1980by Academic Press, Inc.
All rights of reproductionin any form reserved.
NASAL MARKING AND AROUSAL IN Saimiri
117
Considering the interest in squirrel monkey olfactory behavior, it is surprising that sneezing and its attendant behaviors has received so little attention, despite its ready observation. A deceptive analogy to human sneezing no doubt discouraged the investigation of behaviors with seemingly "obvious" reflexive functions. A taxonomy of sneezing and related behaviors in the squirrel monkey has been presented recently (Rosenblum & Schwartz, in press). Briefly, sneezing consists of rapid side-to-side movements of the head coincident with an audible expulsion of material from the external nares. Other behaviors include the hand-sneeze, in which the monkey places its hand over the circumbuccal region and sneezes onto its palmar surface (see Fig. 1), and the nasal rub, in which the monkey sweeps its circumbuccal region in contact with the perch or wall (see Fig. 2). Sneezing behaviors are primarily observed only in aroused or agitated monkeys. Sneezes caused by respiratory infection or experimentally introduced nasal irritants are occasionally observed. However, these isolated sneezes are not integrated within a matrix of rubbing and apparent marking behaviors as exemplified by the clonic sneeze--a vigorous and protracted episode of rapid and repetitive sneezing and nasal rubbing (Rosenblum & Schwartz, in press). The physical similarity of nasal rubbing to other putative scent marking behaviors (e.g., anogenital rubbing) suggested the possibility of a chemical signal of nasal origin. Sneezing could also provide an excellent mechanism for the aerosolized dispersion of such a substance. The investigation of sneezing behaviors gains added significance from a
FIG. 1. Hand-sneeze in adult squirrel monkey.
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SCHWARTZ AND ROSENBLUM
FIG. 2. Crouchposture of squirrel monkeyperforminga nasal rub. comparative perspective. Thiessen and co-workers, for example, have demonstrated that pheromones present in the nasal secretions of the Mongolian gerbil (Meriones unguiculatus) when released during a facial groom, aid in individual thermoregulation and induce grooming in conspecifics (Thiessen, Graham, Perkins, & Marks, 1974; Thiessen, 1977). In the course of direct observation of numerous sneezing episodes in the squirrel monkey, as well as repeated nasal sampling with sterile swabs, the presence of a nasal secretion could not be readily discerned under normal room illumination. However, following the work of Thiessen (1977), we determined that, although its chemical composition is at present unknown, the nasal secretion expelled during sneezing in the squirrel monkey appears bright blue-green under longwave ultraviolet illumination. As an initial assessment of the relationship of these nasal secretions to low-level arousal, the amount of nasal marking by six groups of squirrel monkeys in response to collection boards placed in their home pens for 3 consecutive days was examined under ultraviolet light. A total of 46 subjects, both laboratory and wildborn (Iquitos, Peru), in six groups of six to eight subjects were exposed to collection boards. Group composition ranged from male and female unisexual groups (Pens 18 and 5, respectively) to groups of two and three males housed with four to six females. All subjects, save for Pen 19 which was composed of three male and six female juveniles between the ages of 14 and 20 months, were young adult or fully adult. Animals were housed in identical pens approximately 1 x 1 x 2.2 mhigh.
119
N A S A L M A R K I N G A N D A R O U S A L IN Saimiri
Collection boards consisted of wooden panels, 58 x 30 x 1.6 cm which contained two 24 x 19 cm stainless-steel 0.32-cm mesh grids. Sheets of coarse-grade filter paper which presented approximately 900 cm z of markable surface were placed behind the protective mesh. The filter paper served as a sampling device to collect nasal secretions directed in the vicinity of the board as a whole. On Day 1 of a test series a clean board with fresh filter paper was placed flush against the back wall of the monkeys' home pens. On the mornings of Days 2 and 3, the boards were briefly removed, the filter paper was changed, and the boards were reinserted without any cleaning of the boards. Pen 9 received three additional series of varied board presentations. These included a series in which Pen 9's board was rinsed with cool water daily and two series in which the boards presented on Day 1 had just been removed, uncleaned, from a 3-day exposure to either of two groups. In all cases, fresh filter paper was provided daily. Filter papers were scored within 1 hr of the boards' removal from the pens. Filter papers were scored by two observers who counted the number of 0.10-cm squares within which material fluoresced under long-wave ultraviolet illumination (Cantron, Model 9100, 315-400 nm). Since other substances (e.g., food, feces) also fluoresce under ultraviolet light, although at different hues, conservative scoring criteria were applied. Any spot containing fluorescent material was discounted if it totaled greater than 2.5 cm 2 (possible urine contamination), and any visible physical contaminants on a fluorescent spot of any size disqualified the entire spot. The results of the board presentations to the six squirrel monkey groups are shown in Table 1. TABLE 1 Nasal Marking in Squirrel Monkey Groups as a Function of Repeated Stimulus Presentations a Days of presentation Group 10 18 5 3 19 9a b c d
1 6.5 15.8 15.2 11.5 152.3 14.2 19.2 12.7 14.0
2 4.5 2.0 10.9 19.4 128.6 7.4 8.4 5.9 7.9
All scores expressed in 0.10 cm 2 units of fluorescent markings.
3 1.6 5.0 7.2 14.3 55.5 3.9 6.3 7.4 5.1
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With one exception, all groups evinced their highest scores on Day 1. The median score of 14.7 on Day 1 dropped to 9.2 on Day 2, and to 6.1 by Day 3. Although there was wide variation in the amount of nasal marking by the different groups, within groups there was a significant ordinal decrement across the 3 days (Friedman two-way analysis of variance, p < .01). The aberrant score for Pen 3 on Day 1 probably reflects a behavioral rather than a statistical variance. Pen 3 seemed unusually frightened of the board on first exposure, and delayed the active investigation of it until the second day. Nevertheless, the decrement in marking from Days 2 to 3 in this group closely paralleled the average decrement in scores for Days 1 and 2 in the remaining groups. The within-group consistency was also evidenced in the four repeated series with Pen 9. In these varied board presentations, indicated in Table 1 as 9a-d, each series resulted in a similar decrement in nasal marking across the 3 days, with the highest scores occurring upon first exposure. Thus, on Day 1, Pen 9's median score was 14.1, on Day 2, 7.9, and by Day 3, the median had dropped to 5.1 (Friedman: p < .05). These preliminary data and our observations of sneezing and apparent nasal marking behaviors in the squirrel monkey are consistent with the hypothesis that sneezing in the squirrel monkey represents a form of olfactory marking previously unrecognized for a primate species. We interpret the decline in nasal marking by the six monkey groups to reflect the decreasing olfactory novelty of the collection boards across the 3-day period. That the decrease in nasal marking was due to changes in olfactory rather than visual novelty is supported by the repeated series with Pen 9. In these series, Pen 9 marked most upon first exposure to visually similar boards that had recently been exposed to other groups. The same decremental pattern was observed when a board previously presented to Pen 9, and thus certainly visually familiar to it, was re-presented after a 3-day exposure to a strange group. These data also point to an intriguing property that we had previously determined for the fluorescent secretion itself; the material is not readily soluble in room temperature water. Thus it is not surprising that the daily rinsing of the board in Pen 9 had no effect on the daily decrement in marking. Although the total secretion may contain a volatile component which has yet gone undetected, the fluorescent material scored in the present study is very enduring. Washing the marked filter paper in cool water and attempting to elute with alcohol and anhydrous ether failed to extract the fluorescent markings. A final point about these data concerns the correlation between arousal and sneezing, already mentioned. Recently, Fragaszy and Mason (1978) have described the increase in behavioral arousal elicited in squirrel
NASAL MARKING AND AROUSAL IN Saimiri
121
monkey groups by the presentation of novel objects. It is possible that the decrease in nasal marking over several days may be mediated by a decrease in arousal resulting from habituation to the olfactory novelty of the collection boards. In this light, the data from Pen 19, containing juvenile monkeys, are of special interest. For this age group, whose threshold for excitation is characteristically low, even its lowest score (55.5) greatly exceeded the highest scores obtained from groups composed of mature animals. These data are in keeping with previous observations which indicated that juvenile squirrel monkeys were the most excited by, and the most active investigators of, novel objects (Fragaszy & Mason, 1978). Several hypotheses can be derived from even these preliminary investigations. The enduring property of the fluorescent substance suggests a possible function in territorial marking. Anatomical evidence indicating the presence of a functional vomeronasal organ in this species (Starck, 1974) gives additional moment to this possibility. The vomeronasal system has recently been implicated in the detection of nonvolatile substances in nonmammalian vertebrates (Kubie & Halpern, 1979). Selfand other-directed nasal marking might function similarly in individual recognitory processes and in the infant's olfactory recognition of mother. A final hypothesis concerns the possibility that nasal secretions in the squirrel monkey may function in individual thermoregulation in a manner analogous to that described for the Mongolian gerbil and other mammals by Thiessen (Thiessen et al., 1974; Thiessen, 1977). The surprisingly low sweating rate in the squirrel monkey (Hales, 1974), raises the question of how an excited and possibly overheated tropical mammal regulates its body temperature. A volatile component in the nasal secretion could serve as an excellent vehicle for temperature reduction through evaporative heat loss. REFERENCES Fragaszy, D. M., & Mason, W. A. (1978). Response to novelty in Saimiri and Callicebus: Influence of social context. Primates, 19, 282-314. Hales, J. R. S. (1974). Physiologicalresponses to heat. In D. Robertshaw (Ed.), Environ-
mental Physiology (MTP International Review of Science, Physiology Series One), Vol. XII, pp. 107-162. Baltimore: Univ. Park Press. Hennessy, M. B., Coe, C. L., Mendoza, S. P., Lowe, E. L., & Levine, S. (1978). Scent-marking and olfactory investigatory behavior in the squirrel monkey (Saimiri sciureus). Behavioral Biology, 24, 57-67. Kaplan, J. N., Cubicciotti, D. D., I I I , & Redican, W. K. (1979). Olfactory and visual differentiation of synthetically scented surrogates by infant squirrel monkeys. Developmental Psychobiology, 12, 1-11. Kubie, J. L., & Halpern, M. (1979). Chemical senses involved in garter snake prey trailing. Journal of Comparative and Physiological Psychology, 93, 648-667. Marriott, B. M., & Salzen, E. A. (1978). Facial expressions in captive squirrel monkeys (Saimiri sciureus). Folia Primatologica, 29, 1-18.
122
SCHWARTZ AND ROSENBLUM
Rosenblum, L. A., & Schwartz, G. G. Nasal marking in the squirrel monkey: Laboratory research and field implications. In J. L. Vogt & D. M. Fragaszy (Eds.), Field and Laboratory Approaches to Social Behavior in New World Primates. Basel: Karger, in press. Starck, D. (1974). The development of the chondrocranium in primates. In W. P. Luckett & F. S. Szalay (Eds.), Phylogeny of the Primates, pp. 127-155. New York: Plenum. Thiessen, D. D., Graham, M., Perkins, J., & Marks, S. (1974). Temperature regulation and social grooming in the Mongolian gerbil (Meriones unguiculatas). Behavioral Biology, 19, 279-288. Thiessen, D. D. (1977). Thermoenergetics and the evolution of pheromone communication. In J. M. Sprague & A. N. Epstein (Eds.), Progress in Psychobiology and Physiological Psychology, Vol. VII, pp. 91-191. New York: Academic Press.
BRIEF REPORT
Novelty, Arousal, and Nasal Marking in the Squirrel Monkey GARY G.
SCHWARTZ AND LEONARD A. ROSENBLUM 1
Primate Behavior Laboratotiy, Downstate Medical Center, State University of New York, Brooklyn, New York 11203 The nasal secretions expelled during sneezing in the squirrel monkey (Saimh4 sciureus) were visualized under ultraviolet illumination. The quantity of nasal marking by six squirrel monkey groups in response to novel objects containing clean filter paper showed an ordinal decrement over a 3-day period. When one group was exposed to visually identical objects previously exposed to other groups, nasal marking to the olfactorily novel stimuli was highest on D a y 1 and subsequently decreased over a 3-day exposure. Nasal marking in this species may reflect excitatory state and function in a type of olfactory communication previously undescribed for a primate species.
In recent years, the subject of scent marking in the squirrel monkey
(Saimiri sciureus) has attracted considerable attention among behavioral biologists. Various aspects of olfactory-related behaviors have been investigated in this species, from rump rubbing and urine washing (Hennessy, Coe, Mendoza, Lowe, & Levine, 1978) to the infant's olfactory recognition of mother and the effects of differential rearing odors on filial attachment (Kaplan, Cubicciotti, & Redican, 1979). Despite the corpus of work on olfactory recognition in this species, virtually nothing is known about the nature of the identity cueing odor(s). Moreover, there is no evidence to suggest that such cues may be conferred via back rubbing, rump rubbing, or urine washing, although these behaviors are generally regarded as olfactory related (Hennessy et al., 1978). That other behaviors, whose significance is not yet appreciated, may be involved in such communication in the squirrel monkey is echoed in the conclusion of Marriott and Salzen (1978, p. 15): "In order for humans to fully understand the communicated signal all possible sense modalities must be considered." This research was supported by H E W Grants M H 15965 and MH22640. The authors thank Gayle S. Thompson for her assistance. 116 0163 - 1047/80/010116-07502.00/0 Copyright© 1980by Academic Press, Inc.
All rights of reproductionin any form reserved.
NASAL MARKING AND AROUSAL IN Saimiri
117
Considering the interest in squirrel monkey olfactory behavior, it is surprising that sneezing and its attendant behaviors has received so little attention, despite its ready observation. A deceptive analogy to human sneezing no doubt discouraged the investigation of behaviors with seemingly "obvious" reflexive functions. A taxonomy of sneezing and related behaviors in the squirrel monkey has been presented recently (Rosenblum & Schwartz, in press). Briefly, sneezing consists of rapid side-to-side movements of the head coincident with an audible expulsion of material from the external nares. Other behaviors include the hand-sneeze, in which the monkey places its hand over the circumbuccal region and sneezes onto its palmar surface (see Fig. 1), and the nasal rub, in which the monkey sweeps its circumbuccal region in contact with the perch or wall (see Fig. 2). Sneezing behaviors are primarily observed only in aroused or agitated monkeys. Sneezes caused by respiratory infection or experimentally introduced nasal irritants are occasionally observed. However, these isolated sneezes are not integrated within a matrix of rubbing and apparent marking behaviors as exemplified by the clonic sneeze--a vigorous and protracted episode of rapid and repetitive sneezing and nasal rubbing (Rosenblum & Schwartz, in press). The physical similarity of nasal rubbing to other putative scent marking behaviors (e.g., anogenital rubbing) suggested the possibility of a chemical signal of nasal origin. Sneezing could also provide an excellent mechanism for the aerosolized dispersion of such a substance. The investigation of sneezing behaviors gains added significance from a
FIG. 1. Hand-sneeze in adult squirrel monkey.
118
SCHWARTZ AND ROSENBLUM
FIG. 2. Crouchposture of squirrel monkeyperforminga nasal rub. comparative perspective. Thiessen and co-workers, for example, have demonstrated that pheromones present in the nasal secretions of the Mongolian gerbil (Meriones unguiculatus) when released during a facial groom, aid in individual thermoregulation and induce grooming in conspecifics (Thiessen, Graham, Perkins, & Marks, 1974; Thiessen, 1977). In the course of direct observation of numerous sneezing episodes in the squirrel monkey, as well as repeated nasal sampling with sterile swabs, the presence of a nasal secretion could not be readily discerned under normal room illumination. However, following the work of Thiessen (1977), we determined that, although its chemical composition is at present unknown, the nasal secretion expelled during sneezing in the squirrel monkey appears bright blue-green under longwave ultraviolet illumination. As an initial assessment of the relationship of these nasal secretions to low-level arousal, the amount of nasal marking by six groups of squirrel monkeys in response to collection boards placed in their home pens for 3 consecutive days was examined under ultraviolet light. A total of 46 subjects, both laboratory and wildborn (Iquitos, Peru), in six groups of six to eight subjects were exposed to collection boards. Group composition ranged from male and female unisexual groups (Pens 18 and 5, respectively) to groups of two and three males housed with four to six females. All subjects, save for Pen 19 which was composed of three male and six female juveniles between the ages of 14 and 20 months, were young adult or fully adult. Animals were housed in identical pens approximately 1 x 1 x 2.2 mhigh.
119
N A S A L M A R K I N G A N D A R O U S A L IN Saimiri
Collection boards consisted of wooden panels, 58 x 30 x 1.6 cm which contained two 24 x 19 cm stainless-steel 0.32-cm mesh grids. Sheets of coarse-grade filter paper which presented approximately 900 cm z of markable surface were placed behind the protective mesh. The filter paper served as a sampling device to collect nasal secretions directed in the vicinity of the board as a whole. On Day 1 of a test series a clean board with fresh filter paper was placed flush against the back wall of the monkeys' home pens. On the mornings of Days 2 and 3, the boards were briefly removed, the filter paper was changed, and the boards were reinserted without any cleaning of the boards. Pen 9 received three additional series of varied board presentations. These included a series in which Pen 9's board was rinsed with cool water daily and two series in which the boards presented on Day 1 had just been removed, uncleaned, from a 3-day exposure to either of two groups. In all cases, fresh filter paper was provided daily. Filter papers were scored within 1 hr of the boards' removal from the pens. Filter papers were scored by two observers who counted the number of 0.10-cm squares within which material fluoresced under long-wave ultraviolet illumination (Cantron, Model 9100, 315-400 nm). Since other substances (e.g., food, feces) also fluoresce under ultraviolet light, although at different hues, conservative scoring criteria were applied. Any spot containing fluorescent material was discounted if it totaled greater than 2.5 cm 2 (possible urine contamination), and any visible physical contaminants on a fluorescent spot of any size disqualified the entire spot. The results of the board presentations to the six squirrel monkey groups are shown in Table 1. TABLE 1 Nasal Marking in Squirrel Monkey Groups as a Function of Repeated Stimulus Presentations a Days of presentation Group 10 18 5 3 19 9a b c d
1 6.5 15.8 15.2 11.5 152.3 14.2 19.2 12.7 14.0
2 4.5 2.0 10.9 19.4 128.6 7.4 8.4 5.9 7.9
All scores expressed in 0.10 cm 2 units of fluorescent markings.
3 1.6 5.0 7.2 14.3 55.5 3.9 6.3 7.4 5.1
120
SCHWARTZ AND ROSENBLUM
With one exception, all groups evinced their highest scores on Day 1. The median score of 14.7 on Day 1 dropped to 9.2 on Day 2, and to 6.1 by Day 3. Although there was wide variation in the amount of nasal marking by the different groups, within groups there was a significant ordinal decrement across the 3 days (Friedman two-way analysis of variance, p < .01). The aberrant score for Pen 3 on Day 1 probably reflects a behavioral rather than a statistical variance. Pen 3 seemed unusually frightened of the board on first exposure, and delayed the active investigation of it until the second day. Nevertheless, the decrement in marking from Days 2 to 3 in this group closely paralleled the average decrement in scores for Days 1 and 2 in the remaining groups. The within-group consistency was also evidenced in the four repeated series with Pen 9. In these varied board presentations, indicated in Table 1 as 9a-d, each series resulted in a similar decrement in nasal marking across the 3 days, with the highest scores occurring upon first exposure. Thus, on Day 1, Pen 9's median score was 14.1, on Day 2, 7.9, and by Day 3, the median had dropped to 5.1 (Friedman: p < .05). These preliminary data and our observations of sneezing and apparent nasal marking behaviors in the squirrel monkey are consistent with the hypothesis that sneezing in the squirrel monkey represents a form of olfactory marking previously unrecognized for a primate species. We interpret the decline in nasal marking by the six monkey groups to reflect the decreasing olfactory novelty of the collection boards across the 3-day period. That the decrease in nasal marking was due to changes in olfactory rather than visual novelty is supported by the repeated series with Pen 9. In these series, Pen 9 marked most upon first exposure to visually similar boards that had recently been exposed to other groups. The same decremental pattern was observed when a board previously presented to Pen 9, and thus certainly visually familiar to it, was re-presented after a 3-day exposure to a strange group. These data also point to an intriguing property that we had previously determined for the fluorescent secretion itself; the material is not readily soluble in room temperature water. Thus it is not surprising that the daily rinsing of the board in Pen 9 had no effect on the daily decrement in marking. Although the total secretion may contain a volatile component which has yet gone undetected, the fluorescent material scored in the present study is very enduring. Washing the marked filter paper in cool water and attempting to elute with alcohol and anhydrous ether failed to extract the fluorescent markings. A final point about these data concerns the correlation between arousal and sneezing, already mentioned. Recently, Fragaszy and Mason (1978) have described the increase in behavioral arousal elicited in squirrel
NASAL MARKING AND AROUSAL IN Saimiri
121
monkey groups by the presentation of novel objects. It is possible that the decrease in nasal marking over several days may be mediated by a decrease in arousal resulting from habituation to the olfactory novelty of the collection boards. In this light, the data from Pen 19, containing juvenile monkeys, are of special interest. For this age group, whose threshold for excitation is characteristically low, even its lowest score (55.5) greatly exceeded the highest scores obtained from groups composed of mature animals. These data are in keeping with previous observations which indicated that juvenile squirrel monkeys were the most excited by, and the most active investigators of, novel objects (Fragaszy & Mason, 1978). Several hypotheses can be derived from even these preliminary investigations. The enduring property of the fluorescent substance suggests a possible function in territorial marking. Anatomical evidence indicating the presence of a functional vomeronasal organ in this species (Starck, 1974) gives additional moment to this possibility. The vomeronasal system has recently been implicated in the detection of nonvolatile substances in nonmammalian vertebrates (Kubie & Halpern, 1979). Selfand other-directed nasal marking might function similarly in individual recognitory processes and in the infant's olfactory recognition of mother. A final hypothesis concerns the possibility that nasal secretions in the squirrel monkey may function in individual thermoregulation in a manner analogous to that described for the Mongolian gerbil and other mammals by Thiessen (Thiessen et al., 1974; Thiessen, 1977). The surprisingly low sweating rate in the squirrel monkey (Hales, 1974), raises the question of how an excited and possibly overheated tropical mammal regulates its body temperature. A volatile component in the nasal secretion could serve as an excellent vehicle for temperature reduction through evaporative heat loss. REFERENCES Fragaszy, D. M., & Mason, W. A. (1978). Response to novelty in Saimiri and Callicebus: Influence of social context. Primates, 19, 282-314. Hales, J. R. S. (1974). Physiologicalresponses to heat. In D. Robertshaw (Ed.), Environ-
mental Physiology (MTP International Review of Science, Physiology Series One), Vol. XII, pp. 107-162. Baltimore: Univ. Park Press. Hennessy, M. B., Coe, C. L., Mendoza, S. P., Lowe, E. L., & Levine, S. (1978). Scent-marking and olfactory investigatory behavior in the squirrel monkey (Saimiri sciureus). Behavioral Biology, 24, 57-67. Kaplan, J. N., Cubicciotti, D. D., I I I , & Redican, W. K. (1979). Olfactory and visual differentiation of synthetically scented surrogates by infant squirrel monkeys. Developmental Psychobiology, 12, 1-11. Kubie, J. L., & Halpern, M. (1979). Chemical senses involved in garter snake prey trailing. Journal of Comparative and Physiological Psychology, 93, 648-667. Marriott, B. M., & Salzen, E. A. (1978). Facial expressions in captive squirrel monkeys (Saimiri sciureus). Folia Primatologica, 29, 1-18.
122
SCHWARTZ AND ROSENBLUM
Rosenblum, L. A., & Schwartz, G. G. Nasal marking in the squirrel monkey: Laboratory research and field implications. In J. L. Vogt & D. M. Fragaszy (Eds.), Field and Laboratory Approaches to Social Behavior in New World Primates. Basel: Karger, in press. Starck, D. (1974). The development of the chondrocranium in primates. In W. P. Luckett & F. S. Szalay (Eds.), Phylogeny of the Primates, pp. 127-155. New York: Plenum. Thiessen, D. D., Graham, M., Perkins, J., & Marks, S. (1974). Temperature regulation and social grooming in the Mongolian gerbil (Meriones unguiculatas). Behavioral Biology, 19, 279-288. Thiessen, D. D. (1977). Thermoenergetics and the evolution of pheromone communication. In J. M. Sprague & A. N. Epstein (Eds.), Progress in Psychobiology and Physiological Psychology, Vol. VII, pp. 91-191. New York: Academic Press.