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Differentiall behavioral and adrenocortical responses to stress among three macaque species.

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American Journal of Primatology 14:37-52 (1988)
Differential Behavioral and Adrenocortical Responses to
Stress Among Three Macaque Species
A. SUSAN CLARKE, WILLIAM A. MASON, AND GARY P. MOBERG
California Primate Research Center, university of California,Davis, California 95616
Behavioral and adrenocortical responses of rhesus (Macaca mulatta),bonnet
(M.radiata), and crabeating (M. fascicularis) macaques were compared in
their home cages, during exposure to novelty and during physical restraint.
Both behavioral and adrenocortical responses differentiated species in each
condition. In all conditions, post-test corticosteroid levels were highest for
crabeaters and lowest for rhesus. Rhesus were the most active behaviorally,
and bonnets were the most passive, while crabeaters exhibited the greatest
signs of behavioral disturbance. Relationships between adrenocortical and
behavioral responses varied between groups. Both adrenocortical and behavioral profiles were in accord with the behavior of these three species
under more natural conditions. The role of psychophysiological responses in
general behavioral dispositions toward the environment is discussed. It is
concluded that behavioral dispositions, inclusive of psychophysiological responses, may vary qualitatively even among closely related primate species.
Key words: corticosteroids, behavioral dispositions, psychophysiological responses, Mucacu mulatta, M. rudiata,M. fasciculuria, rhesus monkey, bonnet monkey,
crabeating monkey
INTRODUCTION
Primates show considerable interspecific variability both in social organization
(eg, group size, modal grouping tendencies, intragroup relationships, and frequency
of specific behavior patterns) and in nonsocial aspects of their general life history
patterns (eg, activity levels, diet, foraging behavior, use of space and substrates,
etc.). Interspecific differences in social organizations and life modes may contrast
markedly even between closely related species. These contrasts appear to be based,
at least in part, on fundamental differences between species in characteristic modes
of responding to environmental events [Fragaszy & Mason, 1983; Mason, 1978;
Mendoza & Mason, 1986, in press].
Received March 27,1987;revision accepted June 23,1987.
Address reprint requests to: Dr. William A. Mason, California Primate Research Center, University of
California, Davis, CA 95616.
0 1988 Alan R. Liss, Inc.
38 / Clarkeet al.
Such differences are manifest over a broad range of situations and contexts. An
obvious example is the response to social stimuli. Many studies have noted interspecific differences in behavioral responses to conspecifics [eg, Anzenberger et al, 1986;
Davis et al, 1968; Mason, 1975; Mendoza, 1983; Rosenblum & Alpert, 19771. These
differences are congruent with interspecific differences in social organization and
life history patterns [Box, 1984; Davis et al, 1968; Mason and Epple, 1969; Mendoza,
1983; Rosenblum & Alpert, 19771. Interspecific differences are also likely to be
evident in responses to objects or events in the nonsocial environment [Davis et al,
1968; Fragaszy & Mason, 1978; Glickman & Sroges, 1966; Parker, 19741.
To the extent that such contrasts are based on fundamental differences in
behavioral dispositions or response tendencies, one might expect them also t o be
reflected in patterns of physiological responsiveness. The most compelling evidence
in support of this possibility is provided by the results of a series of comparisons of
two New World species, squirrel (Saimiri sciureus), and titi monkeys (Callicebus
moloch). The two species differ distinctly in social organization and interaction
patterns [Baldwin & Baldwin, 1972; DuMond, 1968; Kinzey, 1981; Mason, 1966;
Terborgh, 1983; Thorington, 19681, and in other aspects of their behavior, such as
use of space, activity levels and feeding patterns [Andrews, 1984; Fragaszy, 1980;
Fragaszy & Mason, 1978, 19831. They also show large and consistent differences in
the responsiveness of the adrenocortical and cardiovascular systems to a variety of
situations, such as novelty, physical restraint, and exposure to unfamiliar conspecifics [Anzenberger et al, 1986; Cubicciotti et al, 1986; Mendoza & Mason, 1984, in
press; Mendoza & Moberg, 19851. Such findings clearly suggest that the comparative
study of interrelationships between behavioral dispositions and physiological responsiveness can provide important new information on the proximal mechanisms
contributing to interspecies differences in social organization and life modes in
natural habitats. Furthermore, knowledge of species differences in behavioral and
physiological responsiveness can contribute to more effective management and husbandry of primates under captive conditions (eg, methods of group formation, housing, etc.).
The present study was designed to extend the assessment of psychophysiological
differences to three closely related species of macaques. Behavioral and adrenocortical responses to stress were compared among rhesus (Macaca mulatta), bonnets
(Macaca radiata), and crabeaters (Macaca fascicularis). These three species show
several similarities in general features of their life history patterns. All three live
in large multimale groups, are polygynous, breed seasonally, have dominance hierarchies, and are omnivorous. The species differ, however, in their patterns of intragroup interaction.
As compared to the other two species, the social interactions of bonnet monkeys
are characterized by high levels of interindividual tolerance, contact and grooming
[Caine et al, 1981; Hawkes, 1970; Coe & Rosenblum, 1984; Rahaman & Parthasarathy, 1968; Small, 19821. This is also reflected in high levels of maternal permissiveness [Rosenblum & Kaufman, 19671 and male tolerance of infants [Brandt et al,
19701, low frequencies of agonistic encounters [Coe & Rosenblum, 1984; Hawkes,
1970; Jensen et al, 1980; Rahaman & Parthasarathy, 1969; Simonds, 19741, labile
hierarchies [Silk et al, 1981; Shively et al, 19821and interactions that are relatively
independent of rank and kin relationships [Caine, 1980; Caine & Mitchell, 1979,
1980; Glick, 1978, 1980; Raney et al, 1981; Silk, 1982; Simonds, 1965; Sugiyama,
19711.
The social organizations of rhesus and crabeaters are qualitatively similar. Both
are characterized by linear hierarchies [Angst, 1975; Bernstein & Sharpe, 1966;
Gabow, 19731; relatively low levels of interindividual tolerance, grooming, and
Responses to Stress Among Macaques I 39
paternal behavior [Brandt et al, 1970; Caine, 1980; Caine & Mitchell, 1980; Drickamer, 1976; Hawkes, 1970; Poirer & Smith, 19741; high levels of agonism [Angst,
1975; Bernstein & Ehardt, 1985a; Hawkes, 1970; Shively et al, 1981, 1982; Thierry,
1985a,b]; and interactions that are constrained by rank and kin relationships [Angst,
1975; Bernstein & Ehardt, 1985b; Caine & Mitchell, 19801. Some quantitative
differences between these two groups have been reported, however. Rhesus spend
more time in nonaggressive physical contact than do crabeaters [Hawkes, 19701.
However, they also show more frequent and severe aggression toward conspecifics
[Caine et al, 1981; Hawkes, 1970; Thierry, 1985a; Zumpe & Michael, 19831, and
dominance appears to be a more important determinant of their access to resources
than it is for crabeaters [Shively & Smith, 19831. Field experiments indicate that
crabeaters are more tolerant of strange conspecifics than are rhesus [Angst, 1973;
Southwick et al, 19741.
The available data from a recent study of adult males of these three species,
maintained outdoors under comparable conditions in large social groups suggest
that the species also differ in some hormonal measures and in relationships between
behavioral and hormonal variables [Clarke et al, 1981; Shively et al, 1981, 19821.
Cortisol values were highest for crabeater males and lowest for rhesus males.
Testosterone values were also highest for crabeaters but were lowest for bonnets.
For rhesus males, dominance rank was positively related to plasma testosterone and
sexual behavior and negatively related to plasma cortisol levels [see also Bernstein
et al, 1974; Chamove & Bowman, 1978; Golub et al, 1979; Rose et al, 1972, 19751.
For crabeater males, rank was only modestly correlated with testosterone and
cortisol values but was highly related to sexual behavior. For bonnet males rank
was highly but negatively related to sexual behavior and cortisol but had little
relation to testosterone. This evidence suggests that males of the three species differ
in their characteristic modes of relating to the social environment, as reflected in
patterns of hormonal and behavioral response to subordination [Clarke et al, 1981;
Shively et al, 1981, 19821.
These observations led us to question the generality of such differences. Specifically, we asked if interspecific differences in behavioral dispositions and physiological responsiveness could also be discerned in adolescent females housed and tested
individually and whether any obtained differences might be generally congruent
with results for group-living adults. Accordingly, behavioral and adrenocortical
responses to environmentally induced stress were compared across three conditions:
1)in the living cage 2) during exposure to novelty, and 3) during physical restraint.
GENERAL METHODS
Subjects
The subjects were 21 adolescent female macaques, seven from each of three
species: rhesus (Macaca mulatta), bonnets (Macaca radiata), and crabeaters or cynomolgus (Macaca fascicularis). Their ages ranged from 25 to 38 months. All but one
rhesus participated in three experiments. She was removed from the study prior to
experiment 3, after being diagnosed as having Simian Acquired Immunodeficiency
Syndrome (SAIDS). Blood samples collected from this subject in experiments 1and
2 were discarded without assay, Therefore, sample sizes were unequal for hormonal
data in experiments 1and 2 and for all measures in experiment 3. All subjects were
captive-born and had been raised in multi-animal social groups. Approximately 4
months before the first experiment they were transferred to individual Harford
squeeze cages (.3 x .6 x 1.4 m) in rooms containing approximately 30 other monkeys. During the period preceding the first experiment, they were observed in the
40 I Clarke et al.
home cage on a regular basis and trained to enter a transport cage. Daily cleaning
occurred at 0800-0900 hours and feeding at 1500-1700 hours.
General Procedures
All three experiments followed the same general procedure. Testing was immediately preceded by collecting a blood sample from the subject in its home cage. This
was followed by handcatching the monkey and fitting it with a lightweight fabric
chest harness equipped with two electrodes and a battery-pack transmitter. [This
equipment was used to record heart rate telemetrically; these results are reported
in Clarke, 1985, 1986al. Following these procedures, the subject was either carried
a short distance and then returned to its living cage (experiment 1)or transported
to the testing area. Testing began within 3 minutes after completion of pretest
procedures. Each test session lasted 1 hour. Behavioral data were recorded by two
methods: During six 5-minute trials, each separated by 5 minutes, data were recorded via one-zero sampIing [Altmann, 19741 using 15-secondintervals; during the
six 5-minute intervening trials, absolute frequencies and durations of three t o four
behavior categories (varying according to condition) were recorded using a cumulative event recorder. Thus, data were collected by each method €or 30 minutes over
the test hour. A second blood sample was collected from the subject immediately
following testing. Two subjects were tested per day, between 1100 and 1400 hours.
Order of testing of monkeys from different species was balanced over testing times
and days; order within species was randomly assigned.
Blood Sample Collection and Assay
Blood samples (0.5 ml) were collected by either anticubital or saphenous venipuncture using 1-ml heparinized syringes. Blood samples were collected within 3
minutes of entry into the testing rooms (pretest samples) or within 3 minutes of test
completion (post-test samples). Samples were processed by centrifugation (8 minutes
at 2,800 rpm), followed by removal of plasma. Plasma was frozen at -20°C until
assay. Plasma samples were assayed in triplicate for total corticosteroid concentrations, using a competitive protein binding technique [Bassett & Hinks, 19691. Assay
coefficients of variation were 8.8%(intraassay) and 9.5%(interassay).
Data Analysis
For each condition, behaviors that occurred with sufficient frequency for analysis in all three groups were compared between groups by the Kruskal-Wallis test.
Where appropriate, post hoc comparisons were made using the Kruskal-Wallis
multiple comparisons method [Conover, 19801. Behaviors occurring with sufficient
frequency for analysis in only two groups were compared by Mann-Whitney test.
For those behaviors measured by one-zero frequency and by absolute frequency and
duration, only the absolute measures are reported. For each condition, temporal
changes were evaluated by grouping behavioral data into three blocks (each comprising two 5-minute trials) and comparing across blocks using Friedman’s one-way
analysis of variance. Behavioral comparisons between conditions were made by
Wilcoxon tests.
Corticosteroid data within conditions were analyzed by a mixed-design analysis
of variance using a n unweighted means analysis [Winer, 19711. Pre- and post-test
data were also analyzed separately within each condition and across conditions by
one-way analysis of variance. Kendall’s coefficient of concordance (Kendall’s W) was
used to assess the stability of individual post-test corticosteroid values across conditions. Correlations between corticosteroid concentrations and behavioral measures
were based on the Spearman’s rho statistic.
Responses to Stress Among Macaques I 41
ORHE
5
. 80 EXP. 1
WBON
EXP. 2
$ 70
v
rn
CRA
CEXP. 3
3
PRE
POST
T
6o
50
w 40
I-
30
0
20
8
10
+
0
0
PRE
POST
PRE
POST
REC
CONDITIONS
Fig. 1.Mean (+SE)plasma corticosteroid levels for M. mulatta, M. radiata, and M. fascicularis compared
across home cage, novel environment, and restraint conditions.
Experiment 1: Home Cage Test (disturbance control). The purpose of this
experiment was to gather data from the monkeys in their home cages in response
to the pretest procedures (blood-sampling,hand-catching, harnessing, confinement,
and transport in the carrying cage) and wearing the harness. Data from this
condition therefore do not constitute baseline (undisturbed) measures; they do,
however, allow the effects of procedures incidental to testing in the (presumptively)
more stressful conditions of experiments 2 and 3 to be assessed.
Procedure. Following completion of the pretest procedures (described above),
the subject was transferred to a carrying cage and carried half the distance to the
Novelty and Restraint testing area and back again, then returned to its home cage.
This required approximately 5 minutes. Behavioral recording started as soon as
the animal was returned to the home cage. Behavioral data were recorded by an
observer seated approximately 1 m from the front of the cage. Of the behaviors
recorded by one-zero sampling, only harness manipulation is reported here (ie,
responses to the observer are not reported). Behaviors recorded by absolute frequency and duration were screecWalarm call (scored together), coo, locomotion, and
depressed posture (huddling over or lying down). Immediately following the testing
hour, a second blood sample was collected.
Results. Corticosteroid data from pre- and post-test samples are presented in
the left panel of Figure 1.All three groups exhibited significantly higher corticosteroid values at the post-test sample (F = 68.5; df = 1,17; P < .001), indicating that
the pretest procedures and wearing the harness over the hour were stressful.
Although the main effect of species was not significant, the crabeater group showed
a greater mean increase from pretest levels than either the rhesus or bonnet groups,
yielding a significant interaction effect (F = 3.7; df = 2,17; P < .05). Separate
analyses indicated that the difference between species in post-test corticosteroid values was significant (F = 3.5; df = 2,17; p = .05), whereas the difference
in pretest values was not.
Pronounced interspecific differences were found for several behavioral measures. As shown in Figure 2, mean duration of locomotion was much longer (more
than seven times) for rhesus than for crabeaters (P < .05) and both groups locomoted significantly more than bonnets (P < .05). The occurrence of screechialarm
42 I Clarke et al.
180 r
44 r
f
160
140
38
g
120
32
2
100
a,
0
16
60
Ga
40
0
20
3
24
80
8
0
0
BON
RHE
CRA
Fig. 2. Mean locomotion duration per 30 minutes for M. mulatta, M. radiata, and M. fascicularis in home
cage and novel environment conditions.
35
h
30
m
C
0
0EXP. 1
EXP. 2
v)
25
0
(1,
v)
v
20
Z
0
15
Ga
10
3
n
5
0
RHE
CRA
Fig. 3. Mean duration of screech and/or alarm call vocalizations per 30 minutes for M. mulatta and M.
fascicularis i n home cage and novel environment conditions (M. radiata did not emit these vocalizations).
call was at least three times more frequent for crabeaters than for rhesus, as shown
in Figure 3 (bonnets did not emit these vocalizations). This difference was significant for both duration and frequency (P < .05); only duration data are shown.
Although not significant, levels of harness manipulation, cooing and depressed
posture were greatest for rhesus. Crabeaters were similar to bonnets in frequency
of harness manipulation and showed very low levels of cooing. Bonnets fell between
rhesus and crabeaters in levels of depressed postures, although these differences
were not significant.
Comparisons over time were made for absolute frequencies and durations of
locomotion, depressed posture, coo (rhesus only), and screechialarm call (crabeaters
only), and for one-zero frequency scores for harness manipulation. The majority of
these behaviors decreased over time (none was observed to increase), but no difference reached statistical significance.
Spearman’s rho correlations were calculated between behavioral measures
(harness manipulation, depressed posture, coo, screechialarm call, and locomotion)
and post-test corticosteroid values for each species. For bonnets, all correlations
Responses to Stress Among Macaques I 43
between behavioral measures and corticosteroid values were modest and nonsignificant (range = -.26 to -29). In the crabeater group, locomotion duration was
highly and negatively correlated with post-test corticosteroid response (rho = - .86,
P < .05). Harness manipulation, depressed posture, and screecldalarm call showed
moderate (nonsignificant)correlations with post-test corticosteroid response (range
= -54 to .66). For rhesus, depressed posture was positively related to post-test
corticosteroid concentrations (duration and frequency rho = .43),whereas all other
correlations were negative (range = -.03 t o -.44).None of these correlations was
significant.
Experiment 2: exposure to novelty. In this experiment, subjects were placed
individually in an unfamiliar room, much larger than the living cage, in which
they were able to locomote freely and to explore the environment, and thus had the
opportunity to display a variety of behavioral responses.
Apparatus and procedure. The novel room measured 6 x 8 m and was equipped
with several climbing structures and sitting platforms. The floor was marked to
form a grid of numbered 1-m squares, such that the subject’s location or change of
location could be recorded.
After completion of the pretest procedures, the subject was transported to the
testing area and released. Behavioral data were recorded by an observer seated
behind a one-way window. Behaviors recorded by one-zero frequency included
environmental exploration, harness manipulation, and location change (moving
from one square completely into another, or from the floor to an elevated structure
or vice versa). Behaviors measured by absolute frequency and duration included
locomotion, depressed posture, coo, and screecWalarm call. At the end of the test
session, the subject was hand-captured and restrained while a second blood sample
was drawn. The subject was then returned to the living cage.
Results. Corticosteroid concentrations from pre- and post-test samples are presented in the center panel of Figure 1. As can be seen from the figure, the results
generally parallel those from experiment 1.-Mean pre- and post-test corticosteroid
values were highest for crabeaters and lowest for rhesus, resulting in a significant
species effect (F = 11.6;df = 2,16;P = .001).Separate one-way analyses also yielded
a significant species effect for pretest (F = 6.4; df = 2,17;P = .OOS) and post-test (F
= 9.7; df = 2,17; P = .002)corticosteroid values. All three groups showed substantially higher mean values after exposure to novelty CF = 31.9; df = 1,17;P < .001),
demonstrating that the test condition was clearly stressful by this measure.
The rhesus group exhibited the highest levels of gross motor activity in the
novel environment by all measures (one-zero frequency of harness manipulation
and location change, absolute frequency and duration of locomotion). The differences for two of these measures (locomotionduration and location change; see Figs.
2 and 4)were greatest between rhesus and crabeaters, and were significant (P <
.05). Bonnets fell between the rhesus and crabeater groups in measures of harness
manipulation, locomotion, and location change. One of these differences was significant: bonnets changed location more frequently than crabeaters (P< .05;Fig. 4).
Crabeaters scored highest on measures of depressed postures and rhesus scored
lowest, but these differenceswere not statistically reliable. Both rhesus and crabeaters occasionally emitted screeches andor alarm calls, but no vocalizations were
heard from bonnets in the novel environment.
The species differed in patterns of behavioral change over the hour. For rhesus,
all measures of motor activity and vocalization (screecldalarm call) decreased over
the hour, whereas depressed postures increased. For bonnets, all behaviors decreased except environmental exploration (observed only in bonnets) and harness
manipulation, both of which increased slightly over the hour. Decreases in locomo-
44 / Clarke et al.
20
-
n
RHE
BON
CRA
Fig. 4. Mean frequency of location change per 30 minutes for M. rnulutta, M.radiuta, and M.fasciculuris
in the novel environment.
5
4
62
W
3
3
sa
L
2
1
0
1
2
3
TIME BLOCKS
Fig. 5. Mean frequency of harness manipulation for M. muluttu, M. radiuta, and M. fuscicularis by 10minute blocks distributed over one hour in the novel environment.
tion, location change, depressed postures, and vocalizations were observed for crabeaters, whereas harness manipulation increased for this group. The increase in
harness manipulation for crabeaters was the only change that was statistically
significant (P < .05) and is illustrated (with comparative data for rhesus and
bonnets) in Figure 5 .
Spearman’s rho correlation coefficients between post-test corticosteroid concentrations and behavioral measures were calculated for each species. Post-test corticosteroid values showed no significant relationship with any behavioral measure
for either bonnets or rhesus (range = .09 to .69).For crabeaters, post-test corticosteroid values were positively correlated with frequency of depressed postures (rho =
.85,P < .05). Consistent with this result, a significant negative relationship was
found between post-test corticosteroid values and location change (rho = - 3 6 , P <
.05). No other correlations between corticosteroid values and behavioral measures
were significant for crabeaters (range = .25 to .27).
Responses to Stress Among Macaques I 45
60
0EXP.
1
EXP. 2
50
6
40
z
W
3, 30
sa
L
20
10
bL
BON
0
RHE
CRA
Fig. 6. Mean frequency of harness manipulation per 30 minutes for M. mulattu, M. radiatu, and
M.fmcicularis in home cage and novel environment.
Four behaviors (harness manipulation, locomotion, depressed posture, and
screechlalarm call) that were observed in both the home cage test and the novel
environment were compared between the two experimental conditions. Patterns of
behavioral change across conditions differed between the three species. For only
one behavior, harness manipulation, was the change in the same direction for all
three groups, and this was a significant decrease (P < .05, Fig. 6).This finding may
have reflected habituation to the harness but was probably also the result of the
subjects’ attention being focused away from the harness and toward their novel
surroundings. All other behaviors decreased between conditions for rhesus, but not
significantly. For the bonnet group, duration of locomotion increased significantly
in the novel environment (P < .05; see Fig. 21, and depressed postures increased
slightly. No vocalizations were heard from bonnets in either condition. In the
crabeaters, duration of locomotion increased slightly in the novel environment,
depressed posture increased significantly (P < .05 for duration and frequency, only
duration data are shown; Fig. 7), and vocalizations (screechialarm call) decreased
significantly (P < .05 for duration and frequency; only duration data are shown;
see Fig. 3). Changes in frequency of locomotion were not significant for any group.
Experiment 3: Physical Restraint. This experiment, in which the subject was
immobilized throughout the test period, presumably presented the most stressful
condition of the three experiments. The test situation was selected to contrast
sharply with the conditions of experiments 1 and 2 by providing minimal opportunity for overt behavioral responses.
Apparatus and procedure. Following the pretest procedures, the subject was
carried to the novel room used in experiment 2, hand-caught from the carrying
cage, and secured in a supine position to a padded surgical cross using Velcro straps
and Vetrap. The restrained subject was then placed on a table in the middle of the
room. Behaviors measured by one-zero sampling were coo and “passive-eyes open”.
Absolute frequencies and durations were recorded for screechialarm call, “passiveeyes closed,” and struggling (forceful movements against the restraining materials). At the end of the test hour, a post-test blood sample was drawn. The subject
was then removed from the surgical cross, placed in the transport cage, and returned to the home cage. One hour later, a third (post-recovery)blood sample was
collected from the subject in the home cage.
46 I Clarke et at.
1200
h
1000
v)
U
0EXP.
1
EXP. 2
r
800
Q)
v)
v
600
9
a
400
3
200
0
RHE
BON
CRA
Fig. 7. Mean duration of depressedposture per 30 minutes for M. mulatto, M. radiata, and M. fascicularis
in home cage and novel environment.
Results. Corticosteroid values from pretest, post-test, and post-recovery samples
are shown in the right panel of Figure 1. As in both previous experiments, corticosteroid values in all three sampling conditions were highest for crabeaters and
lowest for rhesus, with bonnets falling between these two groups. This result was
reflected in a significant main effect for species in the multifactorial analysis (F =
10.4; df = 2,17; P = .001), and i n one-way analyses of pretest (F = 7.7; df = 2,17; P
= .004) and post-test (F = 22.8; df = 2,17; P < .001) corticosteroid values. Corticosteroid concentrations differed between all three sampling times for all but the
rhesus, yielding a reliable effect of conditions (F = 2.3; df = 2,34; P < .001). For
rhesus, mean post-recovery corticosteroid level was virtually unchanged from the
mean value a t post-test, resulting in an interaction that approached statistical
significance (F = 2.3; df = 4,34; P = .07). These results suggest that, although the
adrenocortical response of the rhesus was less vigorous than that of the other
species, it was more persistent, showing little or no change during the hour following termination of restraint.
Consistent with their greater motor activity in the previous experiments, the
rhesus group struggled more than the other two groups but also showed the greatest
duration of being passive with eyes closed (a behavior presumably indicative of
behavioral depression). Levels of struggling and “passive-eyes closed” were lowest
for bonnets, although interspecies differences in these measures were not significant. Levels of “passive-eyes open”were similar for the three groups. Vocalizations
were absent during restraint in rhesus and bonnets, and emitted by only one
crabeater subject, who occasionally alarm-called. None of the observed behaviors
changed significantly over the restraint period for any of the groups. As might be
expected, compared to the previous experiments, interspecific behavioral differences were diminished under conditions of severe behavioral restriction.
In agreement with both prior experiments, correlations between corticosteroid
concentrations and behavioral measures were not significant for rhesus (range =
-.14 to .43) or bonnets (range = -.04 to -.46).For crabeaters, struggle frequency
was significantly correlated with post-recovery corticosteroid level (rho = .78, P <
.05), but no other coefficients were significant for this group (range = - .61 to .32).
As expected, the subjects showed a progressive increase in post-test corticosteroid values across experiments, in keeping with the presumed increase in stress
Responses to Stress Among Macaques I 47
imposed by each experimental condition. Analysis of variance for the combined
groups resulted in a significant conditions effect (F = 7.5; df = 2,36; P = -002) for
post-test corticosteroid values from the home cage, novel environment, and restraint samples. Moreover, individual differences in post-test corticosteroid responses (including post-restraint recovery) for the combined groups were consistent
across conditions (Kendall’s W = 594; x2 = 42.77; P < .001). The average pretest
corticosteroid value for the combined groups decreased across conditions, and this
result was reflected in a significant effect in the one-way analysis (F = 4.08; df =
2,38; P = .02). As shown in Figure 1, however, the decline in pretest values across
conditions occurred only in rhesus and bonnets. Mean pretest values for crabeaters
were similar across conditions, suggesting that this group habituated more slowly
than the others to the change in their living arrangements and to the experimental
regime.
DISCUSSION
The results of the three experiments demonstrate distinct and consistent differences among adolescent female rhesus, bonnet, and crabeating macaques in their
adrenocortical responses to each experimental condition. In each situation, the
crabeater group exhibited the largest adrenocortical response, and the rhesus exhibited the smallest.
Several explanations might account for these differences. One possibility is that
basic differences exist between these species in the organization of the adrenocortical
system at the physiological level, as has been shown for squirrel and titi monkeys
[Mendoza & Moberg, 19851. This possibility is not supported by data from other
comparative studies [Chrousos et al, 1982, 1986; Pugeat et al, 19841, showing that
rhesus and crabeaters do not differ from each other or from baboons, chimpanzees,
and humans in any of a number of measures of adrenocortical function. These Old
World species did differ, however, in all comparisons made with three New World
taxa (Saimiri, Callithrix, and Aotus). Although there are significant species differences in pretest corticosteroid values in the last two of the three experiments
reported here, we believe that these reflect differences in habituation to environmental change between the crabeaters and the other two species. In contrast to rhesus
and bonnets, mean pre-test corticosteroid values did not decline across conditions for
crabeaters, suggesting that this group habituated more slowly than the other two to
indoor caging and experimental participation. In a previous experiment [Clarke,
1985,19871,it was found that this group did not differ from the other two in baseline
values but showed a significantly higher adrenocortical response to brief confinement in a transport cage both before and after systematichabituation t o confinement.
We favor the hypothesis that the interspecific differences we have obtained in
adrenocortical response are primarily mediated by psychological processes, as suggested by J. W. Mason [1971; 19751. This interpretation is supported by the additional finding that crabeaters showed the highest heart rate, and rhesus the lowest,
in the same three experimental conditions [Clarke, 1985; 1986al.
Psychological mediation of the observed differences in physiological responsiveness is further supported by the result that interspecific contrasts in behavior were
also pronounced and consistent. The rhesus group was characterized in all conditions
by higher levels of motor activity (locomotion,harness manipulation, and struggling)
than the other species and showed only moderate frequencies of disturbance vocalizations and behaviors indicative of depression. They also struggled more vigorously
during blood sampling than the other species and behaved more aggressively toward
the investigators [Clarke, 1986bl. Overall, the characteristic tendency of this group
was toward active coping with environmental events. The crabeaters appeared to be
48 I Clarkeet al.
the most behaviorally distressed of the three groups; they showed high levels of
disturbance vocalizations, moderate to high levels of depressed postures, and moderate levels of motor activity. These observations suggest that, from a behavioral
standpoint, the crabeaters were the most “aroused,” “fearful,” or “emotional” of the
three species in these experiments.
In general, the bonnets were less behaviorally responsive than the other two
species. They emitted few or no disturbance vocalizations, showed low levels of
harness manipulation, and exhibited low levels of struggling during restraint. They
presented the least resistance during blood sampling, and were never observed to
respond aggressively toward the investigators. Moreover, this was the only group to
engage in any environmental exploration or self-groomingin the novel environment.
In spite of a corticosteroid response that was intermediate between that of the rhesus
and crabeater groups, the bonnets appeared to be the least behaviorally disturbed
and to be the most passive in their mode of coping with environmental events.
Additional data for the same subjects are congruent with those reported here.
Rhesus were the first species to achieve criterional performance when trained to
enter a transport cage, and they showed the lowest corticosteroid response to cage
confinement in a post-training test. Although the crabeaters were intermediate
between the rhesus and the bonnets in achieving the training criterion,they showed
the highest levels of behavioral disturbance during training and the greatest corticosteroid response to cage confinement [Clarke, 19851. Rhesus were the most aggressive and crabeaters were the most fearful in their responses to a passive observer,
whereas bonnets showed little fearful or aggressive behavior and gave indications
of affiliative attraction to the observers [Clarke, 1986bl.
Examination of the pattern of results for each species suggests that they differed
qualitatively in their responses to the experimental situations. This is most evident
in the relationships between measures of adrenal corticosteroids and behavior. No
significant correlations were found between these measures for rhesus and bonnets.
For crabeaters, four behaviors were significantly related to adrenocortical response:
locomotion duration in the home cage (negatively), frequency of depressed posture
in the novel environment (positively), frequency of location change in the novel
environment (negatively),and frequency of struggling during restraint (positively).
Interspecific contrasts in changes in the relative incidence of behaviors across time
or experimental situations provide further indications of qualitative differences.For
example, in the home cage, the bonnets showed the lowest level of locomotion of the
three species, whereas they showed the highest level in the novel room; the rhesus
showed a modest reduction in locomotion between the home cage and the novel room
but remained substantially above the crabeaters, who showed a modest increase
between the two situations. Similarly, changes in harness manipulation over time
in the novel room showed a sizable increase for crabeaters, a slight increase for
bonnets, and a decrease for rhesus. These findings add to the growing evidence that
the stress response is not a unitary phenomenon [Moberg, 19851. Species may differ
widely in their characteristic modes of responding to stressful situations, as shown
by the present results and by findings for other species [Anzenberger et al, 1986;
Cubicciotti & Mason, 1975; Cubicciotti et al, 1986; Mendoza & Moberg, 19851. The
particular measures that will differentiate species most clearly on any given occasion, however, are likely to depend on the specific features of the situation [Anzenberger et al, 1986; Mendoza & Mason, 19861.
Although these data are based on individually housed adolescent females and
were obtained in highly constrained experimental situations, they are consistent
with results obtained €or other age-sex classes and in less restrictive settings.
Interspecific differences in corticosteroid values reported here are in the same
Responses to Stress Among Macaques I 49
direction a s those found for males of the three species in large outdoor groups [Clarke
et al, 1981; Shively et al, 19811. The behavioral differences reported here are also in
agreement with other findings. Others [Kling & Orbach, 1963; Zumpe & Michael,
19833 have observed that crabeaters are fearful of their handlers, whereas rhesus
are highly aggressive. Rhesus are reported to be more aggressive toward conspecifics
in captive groups than either crabeaters [Thierry, 1985a, 1986; Zumpe & Michael,
19831or bonnets [Hawkes, 1970,19711.The tolerance and passivity that we observed
in the bonnets is congruent with the low levels of agonism and high levels of contact
and grooming reported for wild and captive social groups [Caine et al, 1981; Hawkes,
1970, 1971; Rahaman & Parthasarathy, 1968; Simonds, 19741 . Together, these
findings suggest that each of the three species is disposed toward a distinctive and
characteristic mode of response to social and nonsocial stimuli in the environment,
which is reflected in behavioral as well as physiological measures.
In summary, the consistent interspecies differences reported here support the
notion that species display behavioral dispositions and patterns of physiological
responsiveness that are characteristic of their reactions to a broad range of environmental events. Although relationships between behavioral and physiological responses varied among the three species, it seems reasonable to regard both kinds of
measures as components of highly general, species-typical coping patterns.
CONCLUSIONS
1. Rhesus, bonnet, and crabeating macaques showed distinct and consistent
differences in behavioral and adrenocortical responses to induced stress.
2. Data from the present experiment and others in this series are in accord with
previous reports of differences among these species in behavioral and physiological
responses displayed under less restrictive conditions.
3. These findings suggest that each of the three species may be characterized by
a generaliztd and distinctive mode of coping with environmental events that is
reflected both behaviorally and physiologically.
ACKNOWLEDGMENTS
The research was supported in part by a Regent’s Fellowship and a Dissertation
Research Award from the University of California (to A S . Clarke), and National
Institutes of Health grants HD06367 and RR00169. Preparation of the manuscript
was supported in part by NIMH Training grant MH171073. We thank K. Morgan,
J. Harrah, M. Seifart, and A. Ho for assistance in data collection, and S.P. Mendoza and L. Berenstain for comments on the manuscript.
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