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VETERINARSKI ARHIV 89 (2), 233-246, 2019
Determination of reproductive span through morpho-histological
studies on the ovaries of captive brown bears (Ursus arctos)
- a short communication
1*, Agnieszka Sergiel234,
5678,
Tomasz Piasecki8, Doroteja Huber41
1Department of Veterinary Biology, Faculty of Veterinary Medicine, University of Zagreb, Zagreb, Croatia
2Department of Wildlife Conservation, Institute of Nature Conservation of Polish Academy of Sciences,
Krakow, Poland
3
Clinic for Obstetrics and Reproduction
, Faculty of Veterinary Medicine, University of Zagreb, Zagreb, Croatia
4Department of Veterinary Pathology, Faculty of Veterinary Medicine, University of Zagreb, Zagreb, Croatia
5Department of Anatomy, Histology and Embriology, Faculty of Veterinary Medicine, University of Zagreb,
Zagreb, Croatia
6Clinic for Surgery, Orthopaedics and Ophthalmology, Faculty of Veterinary Medicine, University of Zagreb,
Zagreb, Croatia
7Department of Evolutionary Biology and Conservation of Vertebrates, Institute of Environmental Biology,
University of Wroclaw, Wroclaw, Poland
8Department of Epizootiology and Clinic of Birds and Exotic Animals, Faculty of Veterinary Medicine,
Wroclaw University of Environmental and Life Sciences, Wroclaw, Poland
________________________________________________________________________________________
Determination of reproductive span through morpho-histological studies
on the ovaries of captive brown bears (Ursus arctos
The study aimed to determine reproductive span by investigation of the ovarian structures in young
and elderly captive brown bear females (Ursus arctos). The ovaries of two 2-year-old females were obtained
by ovariectomy and during the necropsies of 31 and 36 year old individuals. All the obtained ovaries were
examined macroscopically and histologically. Histological examination of the ovaries of young animals
(2+ years) revealed the presence of primordial, primary, secondary and tertiary follicles within the ovarian
*Corresponding author:
Slaven Reljić, DVM, PhD Candidate, Biology Department, Faculty of Veterinary Medicine, University of Zagreb, Heinzelova
55, 10000 Zagreb, Croatia, Phone: +385 91 584 6114; Fax: +385 1 2390 158; E-mail: sreljic@vef.hr
DOI: 10.24099/vet.arhiv.0471
234 Vet. arhiv 89 (2), 233-246, 2019
S. Reljić et al.: Reproductive span in captive brown bears
cortex. One ovary showed a mature corpus luteum, indicating recent ovulation, what is, to our knowledge,
the rst histological proof of the earliest age of ovulation recorded for captive brown bears. Ovarian atrophy
accompanied by the development of multiple cystic subsurface epithelial structures (SES) in the case of the
old bears in this study indicates that the ovaries of brown bears share similar degenerative and proliferative
patterns with domestic canids. The oldest female had records of successful births at the ages of 26 and 28 years.
Both recorded birth events represent one of the latest conrmed occurrences of ovulation, conception and birth
amongst brown bears.
reproduction; puberty; ovulation; corpus luteum; post-reproductive phase
________________________________________________________________________________________
Introduction
Reproductive span in females, i.e. the age of the earliest and latest reproduction,
is one of the most important parameters inuencing population dynamics in free-living
species (SCHWARTZ et al., 2003a; KNOTT et al., 2014). Opportunities to eectively
investigate reproductive span in free-living brown bears are scarce, and eorts for proper
monitoring need to be well designed and long-lasting. However, some opportunistic
evidence of reproductive span in females has been recorded. TSUBOTA et al. (1989)
described a case of one corpus albicans in a 2-year-old free-living female brown bear
from the Japanese island of Hokkaido. FRKOVIC et al. (2001) presented the earliest
reproduction in one radio-collared 3-year-old female brown bear in Croatia that gave
birth to two cubs. A series of indirect but veried information about two females’ birth
year in an introduced population in Austria and the age of their rst litters, suggested
that free-living female brown bears were able to have a litter at the age of three years
(ZEDROSSER et al., 2004).
Puberty in mammals is the process of acquiring reproductive competence. The onset
of puberty depends upon the ability of specic hypothalamic neurons to produce the
gonadotropin-releasing hormone (GnRH) in sucient quantities to promote and support
gametogenesis. In female animals, the rst direct sign of reproductive activity is the
production of ova (YAMANAKA et al., 2011). Development of hypothalamic GnRH
neurons is inuenced by the development of threshold body size, exposure to a variety of
environmental and social cues, and the genetics of the animal. The age at which puberty
is acquired varies among and within species, but a current hypothesis contends that the
females must develop a certain body size in order to enter puberty (SENGER, 2015).
Several external factors also modulate the timing of puberty, and these vary signicantly
among species. Those factors include the season during which the animal is born (small
and wild ruminants), the presence or absence of the opposite sex during the prepubertal
period (swine and cattle) and the density of the group or herd within the same sex (wild
and domestic swine) (NOAKES, 2009).
Although the mechanism of puberty in bears is still not entirely clear (WHITE et al.,
2005; TSUBOTA et al., 2008), it should follow some of the patterns already described for
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S. Reljić et al.: Reproductive span in captive brown bears
other species of wild mammals. In order to study the mechanism involved, it is crucial to
determine the timing of the rst ovulation and at the same time analyse endogenous and
exogenous stimuli present. In mammals, we can distinguish four developmental stages
of the follicles within the ovarian cortex: primordial, primary, secondary and tertiary
(Gra) follicles (CARNEVALE, 2008). The Gra follicle contains ova that in bears (and
some other species) are released during ovulation induced by coitus, so-called post-coital
ovulation (BOONE et al., 1998; BOONE et al., 2004).
Another important aspect of reproduction is the post-reproductive phase, the period
of life when an animal is incapable of reproduction. In most animal species the post-
reproductive phase of life represents an unproportionally short or even missing segment
of their entire life span (WILLIAMS, 1957; REZNICK et al., 2006; NISHIDA et al.,
2003; PECCEI, 2001). Evolutionary pressure selects towards maximising reproductive
eort and success (CHARNOV, 2004; KIRKWOOD and ROSE, 1991) and minimising
post-reproductive life. Reproductive senescence has been reported in many long-
living species, including humans, non-human primates, horses and other ungulates and
carnivores (BERGA, 2008; CARNEVALE, 2008; KIRBY et al., 2009).
In captivity, individuals of a certain number of animal species may live longer than in
the natural environment and thus prolong both the reproductive and the post-reproductive
phase. The maximum life span recorded for captive brown bears is 50 years (SCHWARTZ
et al., 2003a). In a natural habitat, adult bears live mainly solitarily, and distances between
individuals are considerable, so direct encounters are mostly related to their reproductive
status (STIRLING and DEROCHER, 1990; DAHLE and SWENSON, 2003). In the
areas where food is seasonally abundant (e.g. salmon streams) or concentrated in one
place (e.g. garbage dumps or carcasses), bears may form short-term aggregations and
show tolerance for one another. These situations seem to be restricted to the non-breeding
season when the blood levels of sex hormones aecting aggressive behaviour are low.
However, females with cubs of the current year, facing possible infanticide, generally
avoid salmon stream aggregations (EGBERT and STOKES, 1974; HERRERO, 1983;
BEN-DAVID et al., 2004; TEISBERG et al., 2014). In captivity, bears are often kept in
a combination of conspecics that would rarely or never occur in nature and certainly
would not last as such for an extended period of life (KOENE, 1996).
In order to investigate the earliest and latest signs of ovarian activity in captive brown
bear females and potential successful reproduction, a preliminary morpho-histological
study was performed on ovaries obtained from two young and two senescent individuals.
For a better understanding of the reproductive capacity of captive brown bear females, the
histological ndings from the ovaries were compared to all the available life-history data
concerning housing, life span, mating habits and successful reproductions.
236 Vet. arhiv 89 (2), 233-246, 2019
S. Reljić et al.: Reproductive span in captive brown bears
Materials and methods
Animals, housing and reproductive history. Female No. 1 was captive born in 2007 in
Zagreb Zoo and was housed in the bear sanctuary at Kuterevo (Croatia, 44°49′N 15°08′E)
from the age of 10.5 months in the continuous presence of a male sibling.
Female No. 2 was wild born and orphaned in 2010 when she was moved to the bear
sanctuary at Kuterevo at the age of 8 months (September 2010), and since May 2011, she
has been kept with an unrelated uncastrated male of the same age.
Females No. 1 and 2 were ovariectomized as a routine procedure for sanctuary bears
(RADISIC et al., 2010) at the age of 2 years and 2 months, and 2 years and 4 months,
respectively, and the ovaries were preserved for examination.
Female No. 3 was born captive in 1963 in Frankfurt Zoo in Germany by the parents
genetically originating from Kodiak Island, Alaska, USA. She was kept in Zagreb Zoo
(Croatia, 45°49′N 16°01′E) with a sibling male who died when she was at the age of 21
years. During 21 years of cohabitation, no reproduction was recorded. Female No. 3 was
euthanised ten years later at the age of 31 due to severe arthritis.
Female No. 4 was born captive in 1975 in Łódź Zoo and transferred to Braniewo Zoo
(north-eastern Poland, 54°23′N 19°50′E) as a cub. She cohabitated with an unrelated male
during two reproductive seasons for breeding purposes. She gave birth to a female cub
in 2001, at the age of 26, and to a male cub in 2003, at the age of 28. There is no earlier
history available of her pregnancies. Since 2003 she has been kept with a male ospring
in the same enclosure. Mating attempts were recorded but with no results thereafter.
In February 2011, at the age of 36, the female was euthanised due to her deteriorating
clinical condition without response to therapy.
The examinations of the captive brown bears were performed when the animals
were immobilised for reasons including veterinary monitoring, health intervention or
due to captive animal management reasons, including euthanasia when necessary. All the
methods applied were in accordance with the animal ethics and welfare requirements and
standards.
Macroscopic and histological analysis of the ovaries. The ovaries were macroscopically
photographed (ZEISS AxioCam ERc 5s camera; ZEISS, Göttingen, Germany) and
examined for possible evidence of ovarian activity. For further histopathological
examination, seven ovaries from four females (the exception was female No. 1 with only
one ovary obtained) were submitted to the histopathology lab of the Faculty of Veterinary
Medicine in Zagreb. The ovaries were xed in 10% neutral, buered formalin for 24-48
hours, routinely dehydrated, embedded in paran, cut to a thickness of 5 µm and stained
with hematoxylin and eosin (H&E). In reproductively active females, the presence of
all developmental stages of follicles, as a sign of ovarian activity, and the presence of
any stage of corpora (albicans, luteum, rubra), as proof of ovulation, were histologically
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evaluated. In the older females, senescence-related alterations such as brosis and cysts
were investigated to determine signs of ovarian inactivity.
Results
Histology of ovaries. Only one ovary was examined from female No. 1. We cannot
know the eects of missing ovary status on the present ovary ndings. The ovaries of
both the 2-year-old females had the characteristics of typical ovaries of healthy and
reproductively mature young females.
The cortex showed follicles in all developmental stages: primordial, primary,
secondary and tertiary (Fig. 1A and 2A). One ovary of female No. 2 revealed a mature
corpus luteum (Fig. 2B). Upon comparison of the ndings from the ovaries in females
No. 1 and No. 2, the ovaries of female No. 2 contained more connective tissue in the
cortex, fewer follicles in all developmental stages, and more atretic follicles.
The older females, at the ages of 31 (female No. 3) and 36 years (female No. 4),
both had inactive ovaries. Histology revealed severe brosis of the cortex and medulla
of both females’ ovaries (Fig. 3A). The cortex contained unilateral (female No. 4) and
bilateral (female No. 3), multiple cysts, 9 to 24 mm in diameter, lled with eosinophilic,
proteinaceous uid and lined by at or cubic epithelial cells corresponding to the
subsurface epithelial structure (SES) cysts described in the ovaries of dogs (SCHLAFER
and FOSTER, 2016) (Fig. 1B and 3B).
Fig. 1A. Macroscopic picture of transversal
cuts through the ovaries of the female No. 2,
dehydrated and stained by hematoxylin and
eosin (H&E), measuring 13 × 10 mm and 11
× 6 mm. The cortex contains multiple grossly
visible follicles measuring from 1 to 3 mm in
diameter.
Fig. 1B. Macroscopic photo of a transverse cut
through the left ovary of female No. 4, after 24
hours of xation in formalin, measuring 3.3 ×
2.7 cm. The cortex contains two uid-lled cysts
measuring 10 × 8 mm and 2.6 × 2.4 mm (arrows).
238 Vet. arhiv 89 (2), 233-246, 2019
S. Reljić et al.: Reproductive span in captive brown bears
Discussion
Earliest ovarian activity. The ovaries of both young females in this study represented
typical ovaries of reproductively mature female animals, although they were at the ages of
2 years and 2 or 4 months (in their 3rd year of life). SCHWARTZ et al. (2003b) documented
overall mean ages of primiparity for wild North American brown bear populations, which
averaged 6.3 years for interior and 6.4 years for coastal populations, with the earliest
recorded births at 4.4 years. AUNE et al. (1994) concluded that female grizzly bears
commonly conceive when they are 4 years old and produce a litter at 5 years of age,
with two records of 3-year-old bears breeding in the spring and conceiving to produce
Fig. 2A. Cortex of the ovary from female No.
1, containing multiple follicles. Scale bar = 500
µm. H&E, objective magnication ×10. Inset:
Tertiary follicle in the cortex of the left ovary of
female No. 2. Scale bar: 1000 µm; H&E; ×4.
Fig. 2B. Corpus luteum in the right ovary of
female No. 2 (arrows) measuring 1582 x 980
µm. Scale bar = 1000 µm, H&E, ×4. Inset:
Higher magnication of lutein cells. Scale bar:
200 µm. H&E, ×20.
Fig. 3A. Extensive brosis of the cortex of
the left ovary of female No. 3. Scale bar =
200 µm, H&E, ×20.
Fig. 3B. Cortical area of the right ovary of
female No. 4 containing one cystic subsurface
epithelial structure (SES; arrows) lined by at
epithelial cells. Scale bar = 1000 µm. H&E, ×4.
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S. Reljić et al.: Reproductive span in captive brown bears
a litter at 4 years of age. In Europe, SWENSON et al. (2001) reported that the mean
ages of primiparity in wild brown bears are 4.5 years and 5.4 years in south-central and
northern Sweden, respectively, with a correlation of the beginning of reproduction with
adult female body mass (SWENSON et al., 2007). In our study, the age of the beginning
of reproduction was lower than the reported age in SWENSON et al., 2001, but our
research included only captive bears.
In wild populations of American black bears (Ursus americanus), polar bears
(Ursus maritimus) and American brown bears (Ursus arctos horribilis) the inuence of
the nutritional condition of females has been reported to inuence the age of their rst
birth. Further, it has been proven that the age of primiparity in black bears is nutritionally
inuenced and a weight-dependent parameter (NOYCE and GARSHELIS, 1994), and that
food quality and abundance causes regional variations in the age of primiparity (VITALE,
2015). American black bear females that fed on anthropogenic sources (“panhandler”
bears) had a lower average minimum age of primiparity than that of wild females (3.5
and 4.2, respectively; McLEAN and PELTON, 1990). Captive bears living on a rich diet
develop more rapidly than wild ones (reviewed in ZEDROSSER et al., 2004), which
probably explains the early onset of reproductive changes in the ovaries in the current
study.
There is evidence that in most domestic mammals (NOAKES, 2009), as well as in
humans and rats (FRISCH, 1984), the onset of puberty is closely linked to the attainment
of a critical body mass, as well as a minimum percentage of body fat or metabolic
mass. Namely, the protein leptin, secreted by white fat cells in adipose tissue, serves
as a permissive signal that enables puberty to occur (BARB and KRAELING, 2004).
As circulating leptin concentrations reach a putative stimulatory threshold, it permits
activation of the hypothalamic-pituitary-gonadal axis and the start of ovarian activity
(PRVANOVIĆ BABIĆ et al., 2011). Data on body fat index or leptin concentration were
not available for the bears in our study, but we assumed that the bears had abundant feed,
leading to a higher body mass, attained earlier, and thus the early onset of reproduction.
STØEN et al. (2006) concluded that socially induced reproductive suppression
and delay of primiparity in young, free-living brown bear females was due to resource
competition within female hierarchies. The average age of primiparity was 4.3 years in
females that dispersed outside their mother’s home range, and 5.2 years in philopatric
females. Also, a negative correlation has been found between the age of sexual maturity
in grizzly bears and latitude (STRINGHAM, 1984; AUNE et al., 1994) - the higher the
latitudes, the later the age of sexual maturity. The young female bears in our study lived
at low latitudes, with no contact with other female bears, therefore achieving sexual
maturity at an early age.
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We emphasise the nding of “mature” corpus luteum in the ovary of female No.
2 as clear evidence of ovulation and previous mating. Immediately after ovulation, the
formation of the corpus haemorrhagicum in most species of domestic mammals develops
into a so-called immature corpus luteum in approximately 72 h, which continues to a
mature corpus luteum approximately 150 h after ovulation. The mature corpus luteum
remains with the ovary until luteolysis takes part (NOAKES, 2009). Ovariectomy on
female No. 2 was performed on May 16, 2012 so we may conclude that at least one
coitus with subsequent ovulation took place a minimum of about six days before, which
corresponds to the mating season in free-living brown bears in Croatia (HUBER et al.,
2008) and elsewhere in the world (STEYAERT et al., 2012). To the authors’ knowledge,
this is the earliest recorded and histologically demonstrated ovulation in captive brown
bears. This corresponds to the earliest reported signs of ovulation and successful
reproduction a year later in free-living brown bear females (TSUBOTA et al., 1989;
ZEDROSSER et al., 2004; FRKOVIC et al., 2001).
We assumed certain similarities in food availability between wildlife supplementary
feeding and diet in captive conditions. Hence, we made a short appraisal of the possible
contribution of supplementary feeding on earlier maturity in free-living brown bear
females, and its eect on population dynamics. Free-living brown bears in many countries
have the opportunity to utilise supplemental anthropogenic food sources at feeding sites
(exposed for bears, as well as for other wildlife) to a great extent (KAVČIČ et al., 2015;
ZEDROSSER et al., 2004). The early primiparity in Austrian brown bears occurred in a
population with year-round access to cereals at deer feeding stations (ZEDROSSER et
al., 2004). In mammals, body mass is positively correlated with female survival, juvenile
recruitment and litter size, as well as population dynamics (ZEDROSSER et al., 2013).
Hence, the earlier primiparity that may occur in free-living bears due to supplemental
feeding would have importance for intensied population growth. According to population
matrix modelling (RELJIĆ et al., 2018), females in the third year of life represent about
6.6% of the total number of females in the Croatian brown bear population.
Senescence process and post-reproductive phase. At a certain age, female reproductive
capability decreases due to senescence processes. As explained by CARNEVALE (2008),
an age-associated decrease in fertility and cyclic activity occurs in the second half of the
expected lifespan in women and mares. In senescent female rats, profound alterations in
the neuroendocrine axis were documented by substantially reduced GnRH neurons and LH
surge attenuation (GORE et al., 2000). Female brown bears have a lower rate of fertility,
by 7.5%, after the age of 16 years and it decreases further with age (SCHWARTZ et al.,
2003a). The ndings of ovarian atrophy and multiple SES cysts are frequent in geriatric
female dogs and cats (MacLACHLAN and KENNEDY, 2002). The same alterations
found in this study indicate that the ovaries of brown bears share similar degenerative
and proliferative patterns with domestic canids, and these could be recognised as ageing
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changes in the two old brown bear females from this study as well. However, both the
older females were chronically ill, which could aect the activity of ovaries in these
females, and therefore these results may not reect the actual status of ovarian activity in
healthy old females.
Evolutionary pressure selects towards maximising the reproductive eort and
minimising the post-reproductive phase (NISHIDA et al., 2003; CHARNOV, 2004;
REZNICK et al., 2006). According to a review by STEYAERT et al. (2012) no female
bear older than 29 years has given birth. We reported similarly late litters at 26 and 28
years of age, but also eight years of life after the end of the reproductive activity. This
range of post-reproductive phase in captive conditions may be much wider than in free-
living animals (SCHWARTZ et al., 2003a).
Histological examination of the ovaries of younger animals revealed the presence
of primordial, primary, secondary and tertiary follicles within the ovarian cortex. These
ndings represent typical ovaries of reproductively mature female animals, although they
were at the ages of 2 years and 2 or 4 months (in their 3rd year of life).
The nding of the “mature” corpus luteum in the ovary of female No. 2 indicated
clear evidence of recent ovulation and previous mating. To our knowledge, this is the
rst histological proof of the earliest age of ovulation recorded for captive brown bears.
Ovarian atrophy and severe brosis of the cortex and medulla of both females’
ovaries, accompanied by the development of multiple cystic SES in the case of the older
bears in this study, indicates that the ovaries of brown bears share similar degenerative
and proliferative senescence-related patterns with domestic canids.
The oldest female had records of successful births at the ages of 26 and 28 years.
Both recorded birth events represent one of the latest conrmed occurrences of successful
ovulation, conception and birth amongst brown bears.
_______
Acknowledgements
We thank Piotr Kierzkowski for the high quality macroscopic and microscopic pictures of the ovaries of female
No. 4. We thank the Royal Society for Prevention of Cruelty to Animals (RSPCA) and the city of Braniewo
for funding and help in carrying out the detailed examination and diagnosis of bears kept in Braniewo Zoo,
where the samples from female No. 4 were obtained, and the bear keepers for their valuable support during the
procedures. The authors are thankful to Ivan Pavenka Crnković from Kuterevo Bear Sanctuary for collaboration
during ovariectomy procedures on females No. 1 and 2.
The work was supported by the European Commission under the FP7 “HUNTing for Sustainability” and LIFE+
“LIFE DINALP BEAR” projects. Neither the European Commission nor any person acting on behalf of the
Commission is responsible for the use made of the information. The views expressed in this publication are
the sole responsibility of the authors and do not necessarily reect the views of the European Commission.
Additionally, the work was funded by the Research Council of Norway, grant number ES459363 and
EURONATUR projects.
242 Vet. arhiv 89 (2), 233-246, 2019
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Received: 31 August 2018
Accepted: 21 January 2019
_____________________________________________________________________________________
(Ursus arctos ko
Cilj istraživanja bio je pregledom građe jajnika utvrditi raspon dobi i reproduktivne aktivnosti u mladih
i starih ženki smeđega medvjeda (Ursus arctos) iz zatočeništva. Jajnici su dobiveni ovariektomijom dviju
dvogodišnjih ženki i tijekom razudbe 31-godišnje te 36-godišnje ženke. Svi su jajnici pregledani makroskopski
i histološki. Histološkom pretragom u mladih su životinja u kori jajnika otkriveni primordijalni, primarni,
sekundarni i tercijarni folikuli. U jednom je jajniku dokazano zrelo žuto tijelo (corpus luteum), pokazatelj
nedavne ovulacije što je, prema nama dostupnim podacima, prvi zabilježen histološki dokaz najranije ovulacije
u smeđih medvjeda u zatočeništvu. Atroja jajnika povezana sa starenjem i praćena razvojem multiplih cističnih
supseroznih epitelnih struktura (SES) u starih medvjeda u ovom istraživanju upućuje na to da se u smeđih
medvjeda pojavljuju slične degenerativne i proliferativne promjene kao i u domaćih kanida. Najstarija ženka
imala je zabilježene uspješne porođaje u dobi od 26 i 28 godina. Oba porođaja pripadaju najkasnijim potvrđenim
pojavama uspješne ovulacije, začeća i porođaja u smeđih medvjeda.
reprodukcija; pubertet; ovulacija, žuto tijelo; postreproduktivna faza
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