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Diurnal variations in serum testosterone concentrations of captive adult male chacma baboons (Papio ursinus).

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American Journal of Primatology 1:421-425 (1981)
Diurnal Variations in Serum Testosterone Concentrations
of Captive Adult Male Chacma Baboons (Papio ursinus)
C. BIELERT
Primate Behaviour Research Group and Department o f Psychology, University o f the
Witwatersrand, Johannesburg, South Africa
M. E. HOWARD-TRIPP
Central Animal Unit, University of the Witwatersrand, Johannesburg, South Afnca
L. A. VAN DER WALT
Endocrinology Unit,The South African Institute for Medical Research and Uniuersity o f the
Witwatersrand, Johannesburg South Africa
Captive adult male chacma baboons (Papio ursinus) housed with natural
lighting exposure and blood sampled at 3-hr intervals showed significant
diurnal variations in serum testosterone concentrations. Low mean concentrations were found at 0800 hr approximately 1 hr after sunrise and mean concentrations were their highest at 2000 hr approximately 1 ?A hr after sunset.
Key words: circadian, diurnal variation, serum testosterone, chacma baboon,
Pupio ursinus
INTRODUCTION
Studies on testosterone levels in nonprimate species such as rats, mice [Bartke et al,
19751, and bulls [Sanwal et al, 19741 have failed to demonstrate a clearcut circadian
rhythm. In marked contrast, diurnal rhythms in peripheral testosterone concentrations
have now been reported for a number of primates, including prosimians [Galago crassicuudutus, Van Hornet al, 1976; Lemur catta, Van Hornet al, 19761, catarrhine monkeys
(Cercopithecus sp., Beattie & Bullock, 1978; Macaca muluttu, Goodman et al, 1974;
Michael et al, 1974; Perachio, et al, 1977; Macaca fuscicuhris, Steiner, et al, 19801, and
man [Resko & Eik-Nes, 1966; Lacerda et al, 1973; Judd et al, 19741. Only recently, however, was a study carried out on diurnal variation under conditions more typical of those
found in nature [Rose et al, 19781.
Relatively few data on endocrine parameters of the male baboon are available although
studies have been published on the plasma levels of unconjugated steroids [Aso et al,
19761 and the urinary steroid excretion and conjugation [Setchell et al, 19761 of the
hamadryas or sacred baboon (Papio humdry a s) . In addition there is one study on the
androgen metabolism of the yellow baboon (Pupio cyunocephalus) Bamamoto et al,
19781. As part of an ongoing program examining the relationships between gonadal
hormones and sociosexual behavior in the chacma baboon (Pupio ursinus), it was felt
Received April 24, 1981: accepted June 25. 1981.
Address reprint requests to C. Bielert, Department of Psychology, University of Witwatersrand, 1 Jan Smuts
Avenue, Johannesburg 2001, South Africa.
0275-2565/81/0104-0421$02.00 0 1981 Alan R. Liss, Inc.
422
Bielert, Howard-Tripp, and van der Walt
appropriate to examine the possible diurnal fluctuations which males may show in their
serum testosterone levels.
MATERIALS AND METHODS
Subjects
A total of six adult wild caught male chacma baboons (Nos. 3,6,14,15,532,655)were
subjects in this experiment. They had all been caught in the Waterberg area of the
northern Transvaal near Vaalwater, South Africa. Their adult status was attested to by
full dentition and adult weight. They had all been housed in the colony under the conditions to be described for a minimum of five years.
Housing and Care
The subjects were all individually caged in squeeze cages. Cage dimensions were .91 X
.91 X 1.9 m and each cage was equipped with a sitting shelf approximately 94 cm. above
the cage bottom extending out into the cage about 30 cm. With the removal of the food
and water dishes, the cage could be collapsed into a cube. All animals were fed daily at
1400 hr on a commercially prepared pellet. [Epol (Pty) Ltd., P.O. Box 19096, Pretoria
West, 0117, South Africa.] Their prepared ration was supplemented three times a week
with fresh fruit or vegetables and water was available ad libitum. At no time were the
animals involved in any other experiments. During the experimental period no animal
required any medical care. The males were housed together in a room of dimensions 10 X
9 X 3.5 m. No female baboons were housed in this same room and at no time were any of
the males exposed to females. In addition to the room having glass windows, the animal
house roof has fiberglass panels which ensure natural lighting influences and allow the
animals to adjust to seasonal day length. The animals were not exposed to anything
other than a natural day length except that electric lights were used briefly during nocturnal blood draws.
Blood Collection and Testosterone Assay
On March 10, 1979, at 0200 hr, blood collection was begun. For this procedure the
males' cages were collapsed; the males were then restrained and given an intramuscular
injection (1 mgikg) of phencyclidine (1-[l-phencyclohexyl]piperidine)hydrochloride.
Although the possible effects of this drug on the peripheral testosterone levels of male
baboons are unknown, it has been demonstrated that brief daily periods of sedation with
this drug did not interfere with the menstrual cycle of female rhesus monkeys
(Macaca mulattu) [Ferin et al, 19761. When immobilized, the males were removed from
their cages and, using standard asceptic techniques, 10 ml of blood was drawn off into a
sterile syringe from the femoral vein. The entire collection procedure usually required
about 30 min for completion. The blood was then transferred into a clean glass test tube
and allowed to stand for 30 min for clotting. The blood was then refrigerated for 24 hr,
after which the serum was drawn off and frozen until the time for assay. In order to
minimize any adverse affects of the immobilization, samples were only taken every 4
days for a total period of 29 days in order to obtain blood samples at 3-hr intervals over a
period of 24 hr. Serum testosterone levels were determined by radioimmunoassay as
previously described [van der Walt, et al, 19781. I t should be pointed out that in this
assay dihydrotestosterone shows a cross-reactivity of 78%, whereas that of
androstenedione is negligible (0.5%).
Statistical Analysis
Differences between mean values of testosterone at the 3-hr intervals (refer Table I)
were examined with a single factor analysis of variance for repeated measures [Winer,
Baboon Testosterone Variation
423
TABLE I. Serum Testosterone Concentrations (ngilOaml) at 3-hr Intervals Over
24 hr in Male Papio ursinus
Hour of the day
Male
identification
020P
0500=
0800
1100
1400
1700
200W
2300“
3
6
14
15
532
2436
1033
952
1443
1405
2845
1686
317
1772
1722
1219
2005
1265
1899
1647
134
604
938
728
710
1178
1609
961
154
1240
738
1192
1675
1868
1302
1336
162
1241
1472
1195
1003
2181
2349
1573
228
750
960
1163
1166
1952
2692
1447
299
977
1443
1666
1359
2998
2541
183i
316
1223
1457
1238
1129
2705
1110
1477
251
655
X
k SEM
*Sample collected during darkness
19621. This analysis failed to substantiate any differences across sampling periods ( F =
1.82, df = (47),P = .11).Application of an “Fmax” test [Winer, 19621to the data led to
the rejection of the hypothesis of homogeneity of variance for the subject males ( F max
for data = 5.55; F.,, (df 48,7) = 3.32). The data were therefore subjected to a log” transformation. This procedure eliminated the heterogeneity of variance (F max for data =
1.12; F,9b(df 48,7) = 3.32)but did not affect the evaluation of the hypotheses tested by
the analysis of variance. The comparison between the mean testosterone levels during
the periods of light and dark was carried out with a t test for paired observations
[Snedecor & Cochran, 19671.
RESULTS AND DISCUSSION
The single factor analysis of variance for repeated measures of the log transformed
data substantiated a significant effect of sampling time (f = 2.61, df = (47),P = .03).The
mean k SEM of the nontransformed data are plotted in Figure 1. I t is quite clear that in
our study the testosterone levels are at their lowest at about 0800 hr in the morning and
at their highest at 2000 hr in the evening. During the period of this study the duration of
daylight varied between a total of 11 hr, 51 min and 12 hr, 33 min [List, 19711. Sunrise
varied between 0641 hr and 0704 hr [Hurley, 19781.This means that the nadir for peripheral testosterone levels in this study occurred approximately 1hr after sunrise. The sunset varied between 1830 hr and 1911 hr [Hurley, 19781. This means that the peak peripheral testosterone levels in this study occurred approximately 1%hr after sunset. The
individual means for the periods of light and darkness were examined statistically. The
paired t test revealed ahighly significant difference for these two periods (t = 4.84, df =
(5),P < .005).The mean k SEM for the light period was 1329 181 ngllOO ml serum in
contrast to a level of 1660 f 145 ngilOO ml serum for the dark period. The pattern of
peaks and troughs for the baboon is very similar to that which has been reported for
rhesus monkeys which were exposed to natural lighting influences [Rose et al, 19781.The
pattern is also similar to that which has been reported from other studies of diurnal primates in which animals have been housed indoors and exposed to artificial lighting
regimes [Cercopithecus sp., Beattie & Bullock, 1978; Lemur catta, van Horn et al, 1976;
Macaca mulutta, Goodman et al, 1974; Michael et al, 19741. The baboon’s pattern is
exactly the opposite to that which has been reported for man [Lincoln, et al, 1974;
Nieschlag, 1974; Rowe, et al, 19741. The origin of the reversal in pattern between mian
and the other diurnal primates thus far studied remains obscure. Our study was con-
*
Bielert, Howard-Tripp, and van der Walt
424
2400
2100
E
2
-2E 1800
1500
\
rn
c
5al 1200
4
Q1
-$
C
900
3
600
v)
c“
300
0
0200h 0500h10800h 1lOOh 1400h 1700h 2000h 2300h 0200h
Hour of the Day
Fig. 1. Mean concentrations(bounded by k SEM) of serum testosterone over a 24-hrperiodin malePapio rusinus
(N = 6). Samples were collected at 3-hr intervals every 4 days. Stippled area, period of natural darkness.
ducted during a time of the year when we believe the testosterone levels in our males to
be relatively high, as evidenced by a study of the occurrence of seminal emission [Bielert
et al, 19801. We believe that a similar diurnal pattern would be revealed at other times of
the year, as was shown to be the case for the rhesus [Roseet al, 19781.The question of the
importance of light as a “zeitgeber”for the timing of the diurnal changes in testosterone
level is an important one, and it is hoped that a study of diurnal testosterone changes in
the male baboon may be carried out during a different season of the year some time in
the future.
CONCLUSIONS
1. The male chacma baboon exhibits a diurnal variation in systemic concentration of testosterone which is very similar to that which has been reported for prosimian and
simian primates and is the reverse of that reported for man.
2. With a 3-hr sampling schedule a concentration nadir occurred approximately 1 hr
after sunrise at 0800 hr, and the peak mean concentration level occurred approximately 1%hr after sunset at 2000 hr.
ACKNOWLEDGMENTS
The authors would like to acknowledge the financial support of the University Council
of the University of the Witwatersrand to the Primate Behaviour Research Group. The
staff of the Central Animal Unit of the University of the Witwatersrand and that of the
Steroid Laboratory of the SAIMR are also thanked for their cooperation and assistance.
Appreciation is also expressed to Professor J. A. M. Myburgh for permission to employ
Baboon Testosterone Variation
425
a number of his adult male baboons in our study. Mr. C. Fullager provided statistical
assistance and Mrs. B. Hurwitz is thanked for her conscientious typing.
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