Theriogenology 61 (2004) 1163–1169

Evidence that bears are induced ovulators

William R. Boonea,*, Becky B. Keckb,1, Jeffery C. Catlinc,
Kevin J. Caseyd, Edna T. Boonee, Penny S. Dyef,
Randy J. Schuettg, Toshio Tsubotah,2, Janice C. Bahrh
a
Reproductive Endocrinology & Infertility, Greenville Hospital System,
890 W. Faris Road, Suite 470, Greenville, SC 29605, USA
b
Clemson University, Department of Animal and Veterinary Sciences, Clemson, SC 29634, USA
c
Cook OB/GYN, Inc., 1100 W. Morgan Street, Spencer, IN 47460, USA
d
Bear Country USA, HCR 33, Box 1110, Rapid City, SD 57701, USA
e
107 Cardinal Court, Simpsonville, SC 29681, USA
f
Dakota Hills Veterinary Clinic, 1571 E. Highway 44, Rapid City, SD 57701, USA
g
Pewaukee Veterinary Service, SC, W240 N3425, Pewaukee Road (Highway J),
Pewaukee, WI 53072, USA
h
Department of Animal Science, University of Illinois, Room 328, 1207 W. Gregory Drive,
Urbana, IL 61801-3838, USA
Received 12 November 2002; accepted 4 July 2003

Abstract

The objective of this study was to determine if black bears are induced ovulators. We conducted a
single experiment with two replicates; each replicate was divided into two arms: females exposed to
male bears and females without male exposure. We used laparoscopy to examine ovaries for corpora
lutea and measured serum progesterone concentrations. Six of the seven isolated females failed to
ovulate, while seven of the eight females exposed to males produced one to four corpora lutea.
Furthermore, isolated females had significantly lower progesterone concentrations than females
exposed to males. Thus, our data suggest that the American black bear is an induced ovulator. These
results may aid biologists in their efforts to reproduce ursids in controlled environments.
# 2003 Elsevier Inc. All rights reserved.

Keywords: Induced ovulation; Black bear; Reproduction; Corpora lutea; Progesterone

*
Corresponding author. Tel.: þ1-864-455-5979; fax: þ1-864-455-8492.
E-mail address: bboone@ghs.org (W.R. Boone).
1
Present address: Horry-Georgetown Technical College, P.O. Box 261966, Conway, SC 29528-6066, USA.
2
Present address: Laboratory of Zoo and Wildlife Medicine, Devision of Veterinary Medicine, Faculty of
Agriculture, Gifu University, Gifu 501-1193, Japan.

0093-691X/$ – see front matter # 2003 Elsevier Inc. All rights reserved.
doi:10.1016/j.theriogenology.2003.07.016
1164 W.R. Boone et al. / Theriogenology 61 (2004) 1163–1169

1. Introduction

Ovulation, the production of oocytes, can occur spontaneously, or can be induced

through physical stimulus. Most mammalian species are spontaneous ovulators. Spon-
taneous ovulation is a process in which ovulation occurs as a result of a hormonal
sequence of events at a specific time in the reproductive cycle and is independent of
mating [1].
In induced ovulation, the act of copulation initiates a series of neural events that
pass to the brain and lead to the release of one or more oocytes. Several species
are known to be induced ovulators, including the short-tailed shrew (Blarina brevi-
cauda), 13-lined ground squirrel (Citellus tridecemlineatus), short-tailed field vole
(Microtus agrestis), domestic cat (Felis catus), rabbit (Oryctolagus cuniculus), ferret
(Mustela putorius), mink (Mustela vison), raccoon (Procyon lotor), and llama (Lama
glama) [2].
Whether animals should be classified as induced versus spontaneous ovulators is not
always clear. Although bears are assumed to be induced ovulators, factual evidence has not
been established [3]. Wimsatt proposed that this question of induced ovulation ‘‘. . . could
easily be resolved in captive bears; one need only to isolate females during the period when
ovulation normally occurs and examine the ovaries thereafter for the presence of large
follicles or corpora lutea. It would be essential to the experiment not only that sexually
mature females be used, but that they had not born cubs the preceding winter or they had
been deprived of their cubs in early spring’’ [3].
The objective of this study was to confirm preliminary data concerning induced
ovulation among bears [4]. In this report, we related mating behavior to ovulatory events
in American black bears (Ursus americanus).

2. Materials and methods

Bear Country USA, is a drive-through park in Rapid City, SD, USA. Inside this park are
approximately 80 female and 110 male American black bears that are housed in an area of
approximately 30 hectares.
We performed two replicates in this study. In the first replicate, eight female bears were
randomly selected and placed in one of two protocols. Four females were allowed to roam
with the 80 female and 110 male bears in the 30-hectare pen, while four females
were isolated from male contact in a 220 m2 pen approximately 100 m from the edge
of the 30-hectare pen.
Between replicates, a 4-year respite gave all bears time to re-equilibrate to the 30-hectare
pen. We repeated the replicate with the use of seven, randomly-assigned, female bears;
four from the previous replicate and three new bears. The same protocol was used for the
second replicate with the exception that three females were isolated and four were allowed
to mate.
Because of limited resources, we used the females in a nonsurgical embryo transfer
study in conjunction with this induced ovulation study. If the females had reproductive
tracts that we could not palpate per rectum because of their small size, the females were
 W.R. Boone et al. / Theriogenology 61 (2004) 1163–1169 1165

eliminated from the study. Because four of the eight females were replaced and because
there were four years in between these replicates, the animals were simply re-randomized
into one of the two arms of the study.
The females (n ¼ 11) selected for this study were mature (4 year of age) and weighed
116:2  5:6 kg (mean  S:E:M:). (Female bears with compromised body weight and
reproductive status fail to complete the reproductive cycle and lose cubs before birth
[5,6].) Only bears that previously produced cub(s) were eligible for this study. To insure
that the bears had the opportunity to ovulate, caretakers removed all cubs from their
mothers in March. Furthermore, to confirm that the bears selected were actively breeding,
visual detection of estrus, similar to that reported for cattle, was used [7]. In addition,
mounting was a prerequisite for acceptance into the study.
Estrus detection started in mid-May with the first mating and ended in late June or early
July after approximately 1 week of no observed matings. All bears in the study that were
housed with the males in the 30-hectare pen were aroused daily at 10:00 h and observed for
signs of estrus (sexual receptivity), which included mating. The arousal was performed by
driving a park vehicle near the female bears. We continued to observe the bears until
20:00 h, with intermittent observations, as is customary when observing cattle for detection
of estrus. Because the female American black bear is polygamous and because estrus is

Table 1
Body weight and reproductive end points in nonmated and mated American black bears

Replicate Bear Weight Number of Estrus Interval from last Number Serum
identification (kg) matings duration observed mating of CL progesterone
(within (days) to observation of (ng/ml)a
30–60 min) CL (days)

1 A 129 N/Ab N/R Not mated 0 1.50

1 B 111 N/A N/R Not mated 0 0.95
1 C 107 N/A N/R Not mated 0 0.75
1 D 132 N/A N/R Not mated 0 0.95
1 E 111 2c N/R 9 1 0.70
1 F 91 4c N/R 20 2 1.75
1 G 102 4c N/R 30 1 2.50
1 H 123 3c N/R 35 4 2.70
2 B 106 N/Rd N/A Not mated 2 0.88
2 D 149 N/R N/A Not mated 0 0.32
2 F 115 N/R N/A Not mated 0 0.37
2 C 90 N/R 11e 27 N/Vf 2.27
2 I 80 N/R 10e 27 2 1.39
2 J 148 N/R 1e 63 3 1.90
2 K 149 N/R 2e 37 2 1.82
a
Mated females had higher progesterone concentration than nonmated females (P ¼ 0:029).
b
Not applicable.
c
Number of matings within 30–60 min of observations.
d
Not recorded.
e
Number of days in which matings occurred, as determined from opportunistic observations.
f
Ovaries were not visible.
1166 W.R. Boone et al. / Theriogenology 61 (2004) 1163–1169

several days in duration (Table 1), we were confident that we could detect estrus during the
day-light hours and so we did not perform night-time observations. Similar regimens are
used for estrus detection in cattle. Females were considered to be in estrus if they remained
still when mounted. The females that were isolated from males were not aroused for estrus
detection.
Breeding behavior in the American black bear has been described in detail elsewhere [8].
In brief, bears undergo a breeding pattern similar to many other mammalian species (e.g.
cattle, sheep, cats), which can be divided into three standard segments: courtship, mating,
and refractory period. Courtship begins with an obvious movement by the male toward the
female and ends when the male mounts the female. Courtship includes posturing by the
male, urogenital sniffing of the female, as well as auditory emissions to the female. If the
female is responsive, she will undergo lordosis, and is subsequently mounted by the male.
Mating includes mounting and pelvic thrusts that are often followed by a flutter. The
refractory period begins with a dismount by the male or a ‘‘roll-out’’ by the female to break
the union. During the refractory period, the male is no longer interested in the female and
the female is less receptive to a male.
Estrus in the American black bear has many aspects. Prior to an intensive study designed
to study this topic, we attempted to gather preliminary data. The first year, our objective
was to determine if the female mated more than once and, if so, was she monogamous or
polygamous (Table 1). Having determined that American black bears mate more than once
and with more than one male, we did not pursue these data any further during the first year.
During the second year of this study, we turned our attention to the length of the estrus cycle
for individual females (Table 1).
In July, we moved the bears from their respected pens to the laboratory where we
performed phlebotomy and laparoscopy. To restrain the bears, we sedated them with either
ketamine hydrochloride (4 mg/kg, i.m.; Ketaset1, Fort Dodge Laboratories, Fort Dodge,
IA, USA) and xylazine (1 mg/kg, i.m.; Rompun1, Miles, Inc., Shawnee Mission, KS,
USA) or tiletamine/zolazepam HCL (8 mg/kg, i.m.; Telazol1, Fort Dodge Laboratories)
and xylazine. (We selected the drug regimes based upon cost and availability.) Bears were
transported, via stretcher, to the on-site laboratory. In the laboratory, bears were intubated
and placed on isoflurane (1–5% Forane1, Ohmeda, Guayama, Puerto Rico). Heart rate and
respiration were monitored every 5 min.
The laparoscopic procedure in the American black bear has been described in detail
elsewhere [9]. Briefly, after surgically preparing the abdomen, we placed a pneumoper-
itoneum needle through the umbilicus and filled the abdominal cavity with CO2. A trocar
and sleeve were placed through the umbilicus. The trocar was removed and a laparoscope
was passed through the sleeve. In addition to the laparoscope, a retractor and a grasper were
inserted similarly into the lower abdominal quadrants to retract bowel and facilitate a better
view of the ovaries.
Blood was drawn from an intravenous catheter with serum being separated and frozen at
20 8C and shipped (with dry ice), to the laboratory for radioimmunoassay of progesterone
as previously described [10,11]. Intra- and inter-assay coefficients of variation were 4.1 and
10.4%, respectively.
The difference in mean progesterone concentrations between mated and nonmated bears
was assessed with Analysis of Covariance (covariate ¼ bear).
 W.R. Boone et al. / Theriogenology 61 (2004) 1163–1169 1167

Fig. 1. Corpora luteum (CL) on an ovary of an American black bear. The ovary and oviduct (OV) are encased in
a bursa (2).

3. Results

Laparoscopy revealed six of seven isolated bears failed to ovulate (Table 1). Bear B did
not ovulate in the first trial, but, while isolated in the second trial, produced two corpora
luteum (CL). In contrast, seven of eight females allowed to mate with males in the open pen
had one to four CL per animal (Fig. 1).
Progesterone concentrations for isolated bears were 0:82  0:15 ng/ml (mean  S:E:M:)
compared to 1:82  0:30 ng/ml for bears allowed to mate (P ¼ 0:029).

4. Discussion

Using laparoscopy and radioimmunoassay, we demonstrated that most American black

bears are induced ovulators. A few bears appear to release ova without neurological
response provided by the mating process, but the proportion of the bears that do so is
unknown. Similar results are reported for felids, which are classified as induced ovulators
[12–14].
It would appear that most bears, like most cats, require vaginal touch to induce ovulation.
While the isolated females did not come in direct contact with males, the short distance
(approximately 100 m) between these two groups of bears would allow for olfactory and
auditory cognition. Because bears are known to have a keen sense of smell [15], we
speculated that the isolated females were aware of males in the area.
Progesterone concentration remained near baseline among nonmated females (0.32–
1.50 ng/ml). Others report similar baseline results for serum progesterone concentrations
from pre-bred, estrus, and lactating adult black bears (<1.0 ng/ml [6,9]), for brown bears
that were 210–300 days pre-parturition (0.4–1.1 ng/ml [16]), and for nonpregnant polar
1168 W.R. Boone et al. / Theriogenology 61 (2004) 1163–1169

bears (<1.0 ng/ml [10]). In our study, as post-mating interval increased, progesterone
concentrations increased among mated females (0.70–2.70 ng/ml). Similarly, elevated
progesterone concentrations appear among pregnant bears, regardless of the species
[5,6,10,16–18]. Furthermore, our findings were confirmed by observing the number of
CL. In isolated bears, seven of eight bears had no detectable CL, whereas in mated females,
at least one CL was present in each bear when ovaries were observable.
By observing reproductive tracts from feral animals killed between late May to mid-
December, Wimsatt speculated that bears were induced ovulators. However, Wimsatt’s
observations were based upon indirect evidence. Using factors directly associated with
ovulation, i.e. progesterone concentrations and number of CL, our report is the first to
verify that mating is required to initiate ovulation. While not directly observing CL, Sato
et al. have confirmed in Japanese black bears (Ursus thibetanus japonicus) similar
differences in progesterone concentrations between isolated and mated bears [18].
On the basis of current results, two future studies need to be performed. One, a study to
determine what proportion of the bears are spontaneous ovulators should be conducted.
Two, even though we repeated this study to reduce potential year-to-year variation, the
number of bears used was small. We would encourage others to repeat our study, possibly
with different bear species, to verify or to disprove our results.
Our preliminary data indicated that the estrus cycle in the American black bear has many
aspects that need to be explored. While it appears that the black bear has a single estrus
period that occurs in late spring, this may not be the case. Furthermore, the estrus cycle may
last for more than 1 week. During this time, the female is receptive to more than one male
and will mate multiple times during a day. What is not known is the number of copulations
that are necessary to induce ovulation, if multiple partners will produce offspring from
different sires, or if the estrus characteristics that we have observed are altered depending
upon the male population present. The factors that determine the length of the estrus, the
numbers of matings per day, and the males with which the female is willing to breed are
unknown. Further studies are needed to address these questions.
In conclusion, we confirmed that the majority of nonmated bears failed to ovulate,
whereas most mated bears ovulated and produce corpora lutea. Thus, the American black
bear can be considered an induced ovulator.

Acknowledgements

Bear Country USA, Rapid City, SD provided animals and facilities for this research.
United States Surgical Corporation, Norwalk, CT, provided laparoscopic equipment.
Greenville Hospital System, Greenville, SC, provided a supportive environment in which
to conduct this research.

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