Fecal androgens of bison bulls during the rut
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Hormones and Behavior 46 (2004) 392 – 398
www.elsevier.com/locate/yhbeh
Fecal androgens of bison bulls during the rut
M.S. Mooring, a,* M.L. Patton, b V.A. Lance, b B.M. Hall, a E.W. Schaad, a S.S. Fortin, a
J.E. Jella, a and K.M. McPeak c
a
Department of Biology, Point Loma Nazarene University, San Diego, CA 92106, USA
b
Center for Reproduction of Endangered Species, Zoological Society of San Diego, San Diego, CA 92101, USA
c
Fort Niobrara National Wildlife Refuge, U.S. Fish and Wildlife Service, Valentine, NE 69201, USA
Received 23 January 2004; revised 17 March 2004; accepted 19 March 2004
Available online 20 July 2004
Abstract
The influence of sex hormones is a key proximate factor underlying male reproductive behavior in mammals. Effective conservation
policies for the remaining purebred plains bison (Bison bison bison) herds require knowledge of the physiology underlying bison
reproductive biology. We used fecal steroid analysis to characterize androgen levels in adult bison bulls before, during, and after the rut, and
to examine androgen levels of bulls differing in reproductive status, age, and mating success. Fieldwork was carried out at the Fort Niobrara
National Wildlife Refuge in north-central Nebraska. All adult bison in the herd were individually known by unique brands. Fecal samples
were collected during 2003 from bulls during pre-rut (June), rut (July – August), and post-rut (September), and behavioral observations
focused on reproductive status and mating success during the rut. Matched sample data indicated that androgen levels (ng/g feces) of bulls
peaked during the rut, doubling from pre-rut to rut and then declining by 75% during post-rut. Dominant bulls that tended (guarded) cows
maintained higher androgen levels than bulls that were not tending. There was a positive correlation between bull age (associated with mating
success) and androgens, with higher androgen levels in prime-aged bulls compared with younger bulls. Nonetheless, there was no correlation
between mating success (measured by number of copulations observed) and androgen level. This suggests that while androgens may provide
the proximate motivation to compete for matings, other factors determine the mating success of bison bulls.
D 2004 Elsevier Inc. All rights reserved.
Keywords: Fecal steroid; Testosterone; Androgens; Bison; Pre-rut; Rut; Post-rut; Mating success; Age; Dominance
Introduction reproductive status can be assessed by endocrine measure-
ments (Lasley and Kirkpatrick, 1991). Fecal steroid techni-
The influence of sex hormones is known to be a key ques have recently emerged as a noninvasive and
proximate factor underlying male reproductive behavior in convenient means of determining the reproductive status
mammals. Almost nothing is currently known of the behav- of free-ranging wildlife (Kirkpatrick et al., 1991, 1992,
ioral endocrinology of adult bull bison. Because most 1993; Lasley and Kirkpatrick, 1991). Gonadal steroid hor-
existing bison herds have been polluted with cattle genes mones and their metabolites in feces accurately reflect
through hybridization (Schnabel et al., 2000; Ward et al., endocrine activity, and fecal steroid profiles closely reflect
1999, 2001), the way that the few purebred herds are plasma values (Desaulniers et al., 1989; Lasley and Kirkpa-
managed will be crucial for the preservation of bison genetic trick, 1991). Because hormones and metabolites in feces
diversity in the future. The physiology underlying bison reflect hormone secretion over composite periods of time,
reproductive behavior must be established to understand the they may better represent individual daily hormonal levels
role of individual phenotype on reproductive success and than do blood samples (Pelletier et al., 2003).
genetic structure of bison populations. Because most aspects In many species of artiodactyls, androgens are elevated
of reproduction are mediated through hormonal signals, during the breeding season (Brown et al., 1991; Bubenik et
al., 1987; Hamasaki et al., 2001; Lund-Larsen, 1977;
Mossing and Damber, 1981; Newman et al., 1991; Sanford
* Corresponding author. Department of Biology, Point Loma Nazarene
University, 3900 Lomaland Drive, San Diego, CA 92106. Fax: +1-619-849-
et al., 1977; Schanbacher and Lunstra, 1976; Yamauchi et
2598. al., 1997), whereas in other species, androgens peak during
E-mail address: mikemooring@ptloma.edu (M.S. Mooring). pre-rut (Freudenberger et al., 1993; Pelletier et al., 2003). In
0018-506X/$ - see front matter D 2004 Elsevier Inc. All rights reserved.
doi:10.1016/j.yhbeh.2004.03.008M.S. Mooring et al. / Hormones and Behavior 46 (2004) 392–398 393
either case, the seasonal elevation of androgens is associated frequently challenged by rival bulls surrounding the tending
with morphological, physiological, and behavioral changes pair (‘attending bulls’), and head-to-head fights are com-
in males (Fletcher, 1978; Imwalle et al., 2002; Li et al., mon. A tending bull may guard a cow for anywhere from a
2000, 2001; Lund-Larsen, 1977; Sanford et al., 1977; few minutes to a few days before being displaced by a more
Schanbacher and Lunstra, 1976). Androgen concentrations dominant bull or copulating. A cow may be tended by 10 or
may be positively correlated with aggression, age, or social more different bulls that alternately displace the previous
rank (Ahmad et al., 1992; Ditchkoff et al., 2001; Fletcher, bull (Wolff, 1998; unpublished data). Copulations are quite
1978; Li et al., 2000, 2001; Oba et al., 1988; Patton et al., brief, usually less than 10 s from mount to dismount, and
2001; Pelletier et al., 2003). most cows breed only once in a season (Lott, 1981).
The goal of this study was to use fecal steroid analysis to Immediately following a successful copulation, the cow
characterize androgen levels in adult bull bison before, arches her back, expels a small volume of clear or milky
during, and after the rut, and to examine androgen levels secretions from the vulva (presumably vaginal fluids and
of known bulls differing in reproductive status, age, and semen), and erects her tail (Berger, 1989; Berger and
mating success during the rut. We hypothesized that fecal Cunningham, 1991; Komers et al., 1992b; Lott, 1981;
androgens would increase during the rut and influence Wolff, 1998). So reliable is this behavioral indicator of
rutting behavior in bison. copulation that it can be used to infer copulations not
directly observed (Berger, 1989; Berger and Cunningham,
1991; Wolff, 1998). After copulation with the cow, the bull
Methods may continue to guard her for anywhere from a few minutes
up to 8 h, until he leaves to search for another cow (Wolff,
Study site 1998). Bison bulls and cows are sexually mature starting at
2 years (Meagher, 1986). However, most bulls capable of
The Fort Niobrara National Wildlife Refuge (77 km2) is guarding a cow are >5 years old, with prime breeding age
located along the Niobrara River near the town of Valentine being 7 – 13 years old (Maher and Byers, 1987). Prior
in the Sandhills of north-central Nebraska (N 42j53.65V, W studies have established that the most dominant bulls have
100j28.47V). The topography of the refuge and surrounding the greatest breeding success (Berger and Cunningham,
region is flat or rolling hills of native grassland (mixed and 1994; Lott, 1979; Wolff, 1998).
sandhill prairie), providing excellent visibility for behavioral
observations. Behavioral observations
Established in 1912 as a sanctuary for bison, elk, and
native birds, the refuge supports a population of plains bison We conducted observations during the rut from 15 July
(Bison bison bison) that is currently maintained at 350 heads through 13 August 2003, which bracketed peak rut for this
after the fall roundup, and up to f475 following calving. species (Meagher, 1986). All observations were conducted
During the spring and summer, bison graze over about two- from 4WD vehicles from394 M.S. Mooring et al. / Hormones and Behavior 46 (2004) 392–398
Most cows displayed tail-up only once during the rut (i.e., testosterone (10,000 cpm/0.1 ml, Perkin Elmer, Boston,
they copulated once), although two cows that copulated early MA) was used to compete against standard testosterone
in the rut came into a second estrus 3 weeks later. Tail-ups (7 – 1000 pg, Sigma, St. Louis, MO). Ten microliters of
persisted anywhere from 1 h to 1 week (mean F SD = 29 F ethanolic fecal extract was diluted 1:100 in 0.1 M phos-
42 h). Whenever fecal samples were collected, the current phate-buffered saline pH 7.0 (PBS) and 100 Al of this
reproductive status of the bull (tending, not tending) was diluent was assayed in duplicate. Following an overnight
recorded. The behavioral data reported here pertains only to incubation at 4 jC, the competitive reaction was terminated
bulls from which fecal samples were collected. by the addition of 0.25 ml of charcoal dextran solution (6.25
g charcoal: 0.625 g dextran in 1.0 l PBS) to separate bound
Fecal androgen samples from free hormone. The charcoal-treated samples were held
for 30 min at 4 jC, then centrifuged at 1500 g at 4 jC for
Fecal samples were collected from June to September 15 min. The supernatant was decanted into scintillation vials
2003, from sexually mature bulls during all daylight hours. and scintillation fluid (5 ml, Ultima Gold, Packard Instru-
Samples were collected from bulls z3 years because youn- ment, Meriden, CT) was added and counted for 2 min in a
ger bulls did not participate in the rut, although they may be Beckman liquid scintillation spectrometer (LS 6500).
sexually mature at 2 years (Meagher, 1986). Mean (FSEM)
age of sampled bulls was 8.9 F 0.4 years (range = 3 – 17 High-pressure liquid chromatography
years). We usually collected one sample per bull for each
period (pre-rut, rut, and post-rut). Samples were opportu- Reverse-phase high-performance liquid chromatography
nistically taken from bulls only when defecation was ob- (HPLC) (Ultra Sphere C-18 Column; Beckman, San
served from a known individual. Ramon, CA) was used to characterize the immunoreactive
Fresh fecal material was transferred to a 70-ml polypro- fecal androgen metabolites. Tritiated testosterone (10,500
pylene container with screw cap (Sarstedt, Inc., Newton, cpm) was added to a pooled sample and then analyzed in
NC), with date and bull I.D. written directly on the container an HPLC run. Samples were first evaporated and then
with an industrial super permanent Sharpee. Samples were reconstituted 20:1 in 100% methanol (Fisher; Optima
placed immediately into an ice chest while in the field, and grade). Androgen metabolites were separated using iso-
later transferred to a freezer at 20 jC for storage until cratic methanol and distilled water (30:14) with 0.2 M
shipped overnight on dry ice to San Diego. At the lab, the potassium phosphate buffer, pH 5.35. Fractions were
large samples were lyophilized for 120 h in a Flexi-Dry collected at a rate of 1 ml/min for 40 min, evaporated,
microprocessor manifold lyophilizer (FTS Systems, Inc., and reconstituted in 500 Al PBS buffer. An aliquot (100 Al)
Stone Ridge, NY) to reduce variability in water content. of each was taken and counted in the LS 6500 to assess
Vegetation was removed from the lyophilized samples by the elution profile of the reference 3H testosterone. Cross-
sifting through a mesh screen (2 1.5 mm). A 0.2-g sample reactivity against the androgen antibody was tested in each
of the sifted feces was added to a 16 150 mm borosilicate fraction by RIA.
culture tube, wetted with distilled water (2 ml) and vortexed
(2 min). Five milliliters of diethyl ether anhydrous (Mal- Data analysis and animal welfare
linckrodt, Paris, KY) were added to each tube, vortexed (2
min), and flash frozen in a methanol:dry ice bath. The Data were analyzed using the SPSS 11.5 statistical
supernatant was poured into 12 75 mm culture tubes package for Windows (Norusis, 2002). The level of signif-
and allowed to evaporate in a water bath (37jC). The ether icance was set at 0.05, and all tests were two-tailed.
extract was resolubilized in 1 ml absolute ethanol. Statistical analysis made use of standard parametric tests:
Student’s t tests for independent samples, one-way Analysis
Radioimmunoassays of Variance, and Pearson bivariate correlation. We have
adhered to the guidelines for animal welfare specified in
Androgen content was analyzed in the fecal extracts by National Institutes of Health Guide for the Care and Use of
radioimmunoassay (RIA) using an antibody produced Laboratory Animals (NIH, 1985).
against testosterone 19 carboxymethyl-ether:BSA at a work-
ing dilution of 1:12,000 and a final dilution of 1:84,000.
This antibody was characterized to cross-react 100% with Results
testosterone, 18.75% with 5a-dihydrotestosterone, 3.00%
with 5a-androstane-3a,17h-diol, and 1.00% with 5-andros- Fecal extraction and radioimmunoassay
tene-3h,17h-diol. Other hormones tested were found to
cross-reactM.S. Mooring et al. / Hormones and Behavior 46 (2004) 392–398 395
Accuracy was determined as 95.4 F 6.8 (mean F SD, N =
6) by recovery of six known quantities of standard (7.8 –500
pg) that were equivalent to the standards used in the
standard pool added to a pool of fecal extract. A diluted
fecal sample from a study male was used for this pool,
which contained an immunoreactive content just above the
sensitivity of the assay. Assay sensitivity was 9.079 pg/tube
(calculated as mean pg/tube at 90% B/BO, N = 10). Buffer
blanks were below the assay sensitivity. Inter-assay coef-
ficients of variation (%SD/mean, N = 6) were 19.5% based
on duplicates of a bison fecal pool with an immunoreactive
content that yielded a %B/BO >60% and 10.5% immuno-
reactive content that yielded a %B/BO > 25%. Intra-assay
variation estimates (10 replicates of the same pools in a Fig. 2. Mean (FSEM) androgen levels from fecal steroid analysis (ng/g
feces) for bison bulls at Fort Niobrara NWR, Nebraska, during pre-rut
single assay) were 7.8% for the high pool and 7.7% for the
(samples collected June 6 – 11), rut (July 14 – August 13), and post-rut
low pool. Results are presented as ng/g (equal to ng/g dry (September 15 – 16). Matched samples involved 41 bulls for which fecal
fecal weight). High-pressure liquid chromatography (HPLC) samples were collected from all three periods. Androgens peaked during the
separated fractions of fecal androgen metabolites and an rut, being significantly higher during rut compared with pre-rut or post-rut.
immunoreactive peak at fraction 14 min coeluted with 3H-
testosterone (Fig. 1). This peak (marked I on the figure) was during pre-rut were significantly greater than during post-
followed by 5h-androstan-3-17-dione (the major immuno- rut (matched t test: N = 42, t = 5.2, P = 0.0001). Matched-
reactive peak at II), 5a-dihydroxytestosterone (III), an pair analyses of all bulls for which data were available in
unidentified peak (IV), and 5h-androstan-3a-oI-17h-oI each period showed that androgen levels increased signif-
(V) at fractions 19, 23, 25, and 31, respectively (Fig. 1). icantly from pre-rut to rut (matched t test: N = 84, t = 11.8,
P = 0.0001) and then dramatically declined from rut to
Seasonal levels of androgens post-rut (N = 41, t = 11.3, P = 0.0001). Of the 84 bulls for
which we had fecal samples for pre-rut and rut, only 5
Androgen levels of bulls peaked during the rut (compared (6%) did not show the predicted increase in androgens
with pre-rut and post-rut) for matched samples of 41 bulls for during rut. Of the 41 bulls for which both rut and post-rut
which data were collected in all three periods (one-way data were available, only 2 (5%) failed to show the
ANOVA: F2,120 = 101.0, P = 0.0001; Scheffe multiple predicted decline in androgens following rut.
comparisons, P = 0.0001; Fig. 2). The mean (FSEM) ng
androgens/g dry feces more than doubled from pre-rut (551 F Individual differences in androgens during the rut
34) to rut (1466 F 93), and then sharply declined by more
than 75% during post-rut (311 F 34). Androgen levels During the rut, bulls that were actively tending cows at the
time of fecal collection had higher levels of androgen
compared with bulls that were not tending at that time (t
test: N = 95, t = 3.3, P = 0.001; Fig. 3). Bulls that were
not tending were either attending a tending bull and cow,
or not active in the rut at all. Tending bulls generally
continued to sequentially tend cows throughout the time
they were active in the rut (x̄ = 19 days), while nontending
bulls generally continued to not tend during the rut period
because they were too low-ranking to guard a cow from
rival bulls. Two of the tending bulls in this data set had
very high androgen levels (>4000 ng/g feces); however,
when these outliers were omitted from the data, tending
bulls still had higher androgen levels compared with non-
tending bulls (N = 93, t = 2.8, P = 0.005). During the post-
rut, when reproductive activity was almost over, fecal
Fig. 1. High-pressure liquid chromatography (HPLC) separated fractions of samples taken from three bulls that were still tending cows
fecal androgen metabolites (- - - -, broken line, ‘pg/tube’) and an indicated that the tending bulls had higher levels of
immunoreactive peak at fraction 14 min co-eluted with 3H-testosterone androgen on the day of collection compared with the
(——, solid line, ‘counts/min’). This peak (marked I on the figure) was
followed by 5h-androstan-3-17-dione (the major immunoreactive peak at
nonrutting bulls (t test: N = 41, t = 2.9, P = 0.006; Fig. 3).
II), 5a-dihydroxytestosterone (III), an unidentified peak (IV), and 5h- Pearson correlation analysis indicated no significant
androstan-3a-oI-17h-oI (V) at fractions 19, 23, 25, and 31, respectively. correlation between mating success (number of copulations)396 M.S. Mooring et al. / Hormones and Behavior 46 (2004) 392–398
Fig. 5. Androgen levels from fecal steroid analysis of bison bulls at Fort
Niobrara NWR, Nebraska, according to age. Androgens were log-
transformed for illustrative purposes to compress outlying values. Age of
bull was positively correlated with level of androgen. Bulls z7 years (to
right of dashed line) had significantly higher androgens compared with
bullsM.S. Mooring et al. / Hormones and Behavior 46 (2004) 392–398 397
species, androgen levels may be associated with aggressive 2003). Thus, the positive correlation between fecal andro-
behavior and the attainment of dominance rank, which in gens and age in bison bulls found in this study is consistent
these species is established during pre-rut (Pelletier et al., with previous reports. In our study, older bulls with higher
2003). Although bison bulls engage in dominance interac- androgen levels were more likely to tend cows and enjoyed
tions during pre-rut, the frequency and intensity of male – higher mating success. Surprisingly, however, androgen
male competition reaches a climax during peak rut (Wolff, level was not directly related to mating success as measured
1998). by total observed copulations per season. Similarly, in cattle
During rut and post-rut, bison bulls that were actively bulls, mounting activity was not positively correlated with
tending cows on the day of fecal collection had higher androgen concentration (Imwalle et al., 2002). Indeed, some
androgen levels compared with bulls that were not tending. bison bulls at Fort Niobrara that were completely unsuc-
Nontending bulls were either attending bulls (surrounding a cessful in breeding (according to our observations) had
tending pair), or had retired from rutting behavior altogether. higher levels of androgen than the top-breeding bull in the
Because the level of steroid hormones in feces may repre- herd. This suggests that, while androgens may provide the
sent circulating levels in blood 10 h to 4 days before motivation to compete for matings, other factors (e.g., size,
collection (Morrow et al., 2002; Möstl and Palme, 2002; strength, skill, experience, perseverance, motivation) deter-
Möstl et al., 1999; Palme et al., 1996; Shaw et al., 1995), mine the mating success of particular bulls.
interpretation of these results is not completely straightfor-
ward. Because we had to keep track of up to 40 tending
pairs on a given day, it was impossible to continually Acknowledgments
monitor the reproductive status (tending or not tending) of
all sexually mature bulls before opportunistic fecal collec- We thank the Fort Niobrara National Wildlife Refuge and
tions. However, because the average tending bull was in the the United States Fish and Wildlife Service for permission
rut for 19 days, we are confident that in the majority of cases to study the Fort Niobrara bison herd, and for making
the bulls we sampled had been active in the rut for at least 4 available housing and 4WD vehicles. Special gratitude goes
days prior. Most tending bulls, following copulation, moved to Royce Huber and Bernie Petersen for their support, to
directly to tend another cow. Thus, we believe that the Dana Harty for assisting with fecal collection during post-
rutting status observed at the time of collection was gener- rut, and to all the refuge staff for their assistance. Helpful
ally representative of that bull’s rutting activity at the time comments from two anonymous reviewers improved the
hormones were circulating in the blood. Assuming bull manuscript. This research was supported with funds from
reproductive status at the time of fecal collection was the Research Associates, a PLNU Research and Special Projects
same as that a few days earlier, these results suggest that grant, and a PLNU Provost’s grant.
bulls actively guarding cows from other bulls are operating
under the influence of higher androgen levels. Such an
effect would be consistent with behavioral changes that References
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