The squirrel monkey (Saimiri boliviensis boliviensis) has a well-defined breeding season during which adult ... A significant sea- sonal variation was noted in ...
American Journal of Primatology 14:285-291(1988)
Seasonal Changes in Serum Dehydroepiandrosterone, Androstenedione, and Testosterone Levels in the Squirrel Monkey (Saimiri boliviensis boliviensis) R. HERBERT WIEBE', LAWRENCE E. WILLIAMS', CHRISTIAN R. ABEE2, RICHARD R. YEOMAN', AND EDWARD J. DIAMOND' 'Department of Obstetrics and Gynecology, 2Department of Comparative Medicine, University of South Alabama, College of Medicine, Mobile
The squirrel monkey (Saimiri boliviensis boliviensis) has a well-defined breeding season during which adult males undergo androgen-dependent morphological changes, with acquisition of active spermatogenesis. To assess the hormonal events of this annual cycle, blood samples were obtained weeklyfromtenadult males,andserumwasassayedfortestosterone(T),androstenedione (AA), and dehydroepiandrosterone (DHEA). A significant seasonal variation was noted in mean serum T (P < 0.02), AA (P < 0.02), and DHEA (P < 0.001) concentrations. Mean AA concentrations increased from a nonbreeding season nadir of 91.4 f 12.9 ng/ml (mean f standard error) to a prebreeding concentration of 139 f 10.5 ng/ml and breeding season peak of 167.5 f 15.4 ng/ml (P < 0.05). Mean DHEA concentrations increased from a nonbreeding season nadir of 8.3 & 0.8 to a breeding season peak of 14.3 k 1.2 (P < 0.001). Mean T levels in the nonbreeding (52.2 & 11.6 ng/ ml) and prebreeding season (48.6 f 7.4) were similar. However, T significantly increased during the breeding season to 103.5 k 12.8 ng/ml 8 < 0.05). Progressive changes in body weight and morphology paralleled the rise in serum AA levels. The pattern of peripheral serum androgen concentrations throughout the year would suggest annual activation of the hypothalamic-pituitary-adrenal and/or hypothalamic-pituitary-gonadal axes. Key words: seasonality, androgens, testosterone, androstenedione, DHEA
INTRODUCTION The squirrel monkey has a well-defined annual breeding season during which adult males undergo morphological ("fatting") and behavioral changes thought to be androgen-dependent [Nadler & Rosenblum, 1972; Mendoza et al., 1978; Chen et al., 19811. Although earlier studies failed to demonstrate a definitive annual change in serum testosterone (T) concentrations [Wilson et al., 19781, recent studies have shown a seasonal variation in plasma T concentrations, which peak during the
Received February 13,1987; revision accepted September 20,1987. Address reprint requests to R. Herbert Wiebe, M.D., University of South Alabama College of Medicine, Department of ObstetricdGynecology, Mobile, AL 36688.
0 1988 Alan R. Liss, Inc.
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breeding season [Mendoza et al., 1978; Chen et al., 19811. These studies have described morphological changes in the male squirrel monkey before any appreciable rise in daytime T concentrations [Mendoza et al., 1978; Coe & Rosenblum, 19781. It has been suggested that T may potentiate the “fatting” process and that other androgenic steroids with appreciable anabolic effects, possibly of adrenal origin, may be responsible for the initiation and maintenance of this process [Mendoza et al., 1978; Coe & Rosenblum, 19781. Wiebe et al. [1984] have previously shown that androstenedione (AA),an androgen predominantly of adrenal origin in humans and rhesus monkeys, is quantitatively the major androgen in the male squirrel monkey during the breeding season. In contrast, plasma concentrations of dehydroepiandrosterone (DHEA),another predominant adrenal androgen in humans and rhesus monkeys, are relatively low in squirrel monkeys during the breeding season when compared to peripheral concentrations of T and AA. To elucidate further the phenomenon of seasonality, the temporal association of peripheral T, AA, and DHEA concentrations along with body weight and morphological changes were assessed over a period of one year in male squirrel monkeys.
METHODS Ten sexually mature male squirrel monkeys (Saimiri boliuiensis boliuiensis), all proven breeders, were studied. Each male was housed in 1.5 x 2 x 4.5-meter cages with eight to ten sexually mature females and one to two juvenile males. Each animal was exposed to the same light/dark interval (i.e., 15 h of light and 9 h of dark). The study began in September and extended to the following August, encompassing the prebreeding (mid-September-mid-December),breeding (mid-Decembermid-March), postbreeding (mid-March-mid-June),and nonbreeding (mid-June-midSeptember) seasons. The breeding season was determined retrospectively by counting back 147 days (average gestation) from the delivery of the first and last full-term fetuses. All males were observed weekly for morphological (“fatting”) and behavioral changes [Mendoza, 1978; Williams, 19861, and weekly weights were recorded. Blood samples, obtained every one to two weeks for one year, were drawn randomly at 0900 h from all animals studied. Samples were obtained from the femoral vein without anesthesia within three min of capture. Samples were separated, and serum was stored at -20°C until assayed by radioimmunoassay (RIA) for T, AA, and DHEA [Wiebe et al., 19841. Before assay, serum was extracted and purifed by celite column chromatography. Respective eluates were then assayed for T, AA, and DHEA by radioimmunoassay, using antitestosterone 11-BSA serum (#250)(gift of Dr. Gordon D. Niswender), antiandrostenedione 3-oxime-HSA (OP/O9), and anti-DHEA-3-Hemi-succinate-HSA (OPI10)(purchased from Optimox, Palos Verdes, California), respectively. Plasma T, AA, and DHEA concentrations and body weights were grouped into biweekly sampling periods and subjected to the Duncan multiple range test for analysis of variance. For an additional analysis of variance, the hormonal data were grouped into four sampling periods (seasons): prebreeding (mid-September-midDecember), breeding (mid-December-mid-March), postbreeding (mid-March-midJune), and nonbreeding (mid-June-mid-September).Pearson correlation coefficients were calculated between T, AA, DHEA, and body weight.
RESULTS The breeding season in the colony at the time of the study extended from midDecember, 1982, to mid-March, 1983. A significant seasonal variation was noted in body weights (P < 0.001). As shown in Figure 1, an increase in mean body weight
Androgens in Squirrel Monkey I 287 I
1100 -
-6
T
1050 -
v
5 1000950 300 -
200 -
. E
0
100 -
Sept.
OCt.
Nov.
Dec.
Jan.
Feb.
Mar.
Apr.
May
June
July
Aug.
Sept.
Fig. 1. Biweekly mean serum T (+SE)and A (+SE)concentrations and mean body weights k S E ) in ten sexually mature male squirrel monkeys. A significant variation was noted in mean body weight (P < 0.0001) and mean serum T (P < 0.02)and AA (P < 0.02) concentrations.
commenced in late October and peaked in late December, with a subsequent decline by early March t o a mean body weight similar to that observed in early October. Serum androgen concentrations fluctuated widely in each monkey throughout the year. This is best illustrated by the ranges of peripheral androgen concentrations during the breeding season as depicted in Table I. Despite this extensive individual variation in serum androgen concentrations, a significant seasonal variation was noted in mean serum T (F24,215= 1.76,P < 0.02),AA (F24,215= 1.75,P < 0.02), and DHEA (F24,215 = 5.46,P < 0.0001)concentrations. All three androgens attained peak mean concentrations in January, during the early portion of the breeding season. The pattern of steroid concentrations is shown in Figure 1. Mean serum T concentrations began increasing by early December, attained significantly higher concentrations by early January (F24,215 = 1.76,P < 0.021, and declined to prebreeding season concentrations by March. Serum AA, however, followed a somewhat different trend. A trend towerd increasing AA concentrations began in early October, before a discernible rise in serum T concentrations. Serum AA concentrations peaked during the breeding season (F24,215 = 1.75,P < 0.02) and declined gradually thereafter, attaining early prebreeding season concentrations by early May. Throughout the entire year, serum AA concentrations were quantitatively higher than serum T concentrations. DHEA concentrations,although
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TABLE I. Range of Peripheral Androgen Concentrationsin Ten Male Squirrel Monkeys During the Breeding Season Monkey #30 #32 #38 #697 #751 #798 #856 #888
#921 #922
Testosterone (nglml)
Androstenedione
DHEA
(ng/ml)
(ng/ml)
5.3-171 8.3-356 27-151 2-245 9-218 21-239 5-151 3-37 3-298 2.8-240
25-311 61-577 53-263 12-275 24-388 47-293 33-500 22-176 73-312 20-276
8-26 8.3-47 8.1-24 2-35 2-23 2-22 6.4-24 2-14 2.4-13 2.5-31
125 100
*
I
T
a,
= :z -. g2
75
1
50 I-
25
Non breeding
Pre Breeding breeding Seasons
Post breeding
Fig. 2. Mean serum T (5SE)concentrations in ten sexually mature squirrel monkeys according to season, i.e., nonbreeding season (mid-June-midSeptember), prebreeding season (mid-September-mid-December), breeding season (mid-December-mid-March),and postbreeding season (mid-March-mid-June). Mean serum T concentrations were similar in the nonbreeding, prebreeding, and postbreeding seasons. A significant increase in mean serum T concentrations was noted in the breeding season. *, P < 0.05).
following a trend similar to that of AA, attained significantly higher concentrations in the early portion of the breeding season (F24, 215 = 5.46, P < 0.001), with a gradual decline thereafter. Peripheral concentrations of all three androgens correlated throughout the year. The correlations during the nonbreeding season were high (T and AA, r = 0.94, P < 0.0001; T and DHEA, r = 0.89, P < 0.001; AA and DHEA, r = 0.91, P < 0.001). Correlations decreased during the prebreeding season (T and AA, r = 0.58, P < 0.001; T and DHEA, r = 0.51, P < 0.001; DHEA and AA, r = 0.57, P < 0.001) and breeding season (T and AA, r = 0.69, P < 0.0001;T and DHEA, r = 0.53, P < 0.001; AA and DHEA, r = 0.53, P < 0.001). AA correlated with body weight (r = 0.44, P < 0.001) during the prebreeding season only. No correlation between body weight and T (i.e., prebreeding season, r = 0.21; breeding season, r = 0.11)was evident in
Androgens in Squirrel Monkey I 289
*
15
a$5
10
f3c
5
Nan breeding
Pre Breeding breeding Seasons
Post breeding
Fig. 3. Mean serum DHEA (+SE) concentrations according to season: A significant increase in mean DHEA concentrations was noted in the breeding season as compared to Concentrations in other seasons. * P < 0.001.
6
2oo 150
t
r
Non breeding
Pre Breeding breeding Seasons
Post breeding
Fig. 4. Mean serum AA (&SE)concentrations according to season. The mean serum AA concentration was higher in the breeding season than in the nonbreeding and postbreeding season. The mean serum AA concentrations in the breeding and prebreeding seasons did not differ significantly. P < 0.05.
any season. Correlation coefficients for body weight and DHEA in the prebreeding and breeding seasons were 0.29 (P < 0.01) and 0.3 (P < 0.01),respectively. With the hormonal data divided according to season (Fig. 2), the mean serum T concentration during the breeding season was significantly higher than concentrations during the prebreeding, postbreeding, and nonbreeding seasons (F3,27 = 3.51, P
