Animal Reproduction Science 124 (2011) 176–183

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Animal Reproduction Science

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Reproductive cycle of the elephant夽

Thomas B. Hildebrandt ∗ , Imke Lueders, Robert Hermes, Frank Goeritz, Joseph Saragusty
Department of Reproduction Management, Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowlke-Strasse 17, D-10315 Berlin, Germany

a r t i c l e i n f o a b s t r a c t

Article history: The combination of a few factors, including poor captive reproduction, secession of
Available online 20 November 2010 importation from the wild and advances in hormone detection and ultrasonography, has
contributed to the current knowledge on the elephant reproductive cycle. Several repro-
Keywords: ductive features in elephants differ markedly from other mammals. These include the
Female elephant urogenital tract anatomy, length and structure of the reproductive cycle, the formation
Estrous cycle
of multiple corpora lutea and the type and secretion pattern of reproductive hormones.
Hormonal pattern
Being 13–18 weeks in length, the elephant estrous cycle is the longest amongst all studied
Follicular development
Accessory corpora lutea non-seasonal mammals to date. Progesterone increases 1–3 days after ovulation, indicating
the start of the luteal phase, which lasts 6–12 weeks. This is followed by a 4- to 6-week
follicular phase that is concluded by two, precisely spaced and timed, LH surges. In gen-
eral, the first, anovulatory LH surge occurs exactly 19–21 days before the second, ovulatory
surge. Normally, a single follicle is ovulated. However, beside a corpus luteum (CL) form-
ing on the site of ovulation, multiple accessory CLs can be found on the ovaries. Unlike
many other species, the predominant progestagen secreted by luteal tissues is not pro-
gesterone, but rather its 5-alpha-reduced metabolites. The currently known aspects of the
unique estrous cycle in Asian and African elephants, covering estrous behavior, circulating
hormones, ultrasonography and anatomy of the reproductive organs as well as hormonal
manipulation treatment possibilities, will be reviewed here.
© 2010 Elsevier B.V. All rights reserved.

1. Introduction as the onset of puberty, ovarian cycle activity and repro-

In the past, few zoological institutions were successful
in breeding elephants. Unable to sustain captive popu-
lations due to cessation of imports from the wild and
insufficient captive offspring production and the decline of
elephant numbers in their natural habitats, have prompted
research on the reproductive physiology of these magnifi-
cent creatures. These efforts were coupled by advances in
hormone detection techniques in serum, urine and fecal
samples and the utilization of ultrasonography as a non-
invasive tool to help understand reproductive events such
夽 This paper is part of the special issue entitled: Reproductive Cycles of
Animals, Guest Edited by Michael G Diskin and Alexander Evans.
∗ Corresponding author. Tel.: +49 30 5168 220; fax: +49 30 5126 104.
E-mail address: hilderbrand@izw-berlin.de (T.B. Hildebrandt).
ductive senescence in elephants.
The order proboscidea contains only one family of living
animals – the elephantidae, which includes the genera Lox-
odonta with two species and Elephas with a single species.
This separate taxon position makes the comparison of the
elephant reproduction physiology with models of related
animals difficult. Thus, research on these animals, primarily
in their natural habitat, provides us with knowledge of new,
and apparently successful, reproductive strategies within
the animal kingdom (Rasmussen et al., 1982; Hildebrandt
et al., 2006). The reproduction of elephants, as our largest
and most charismatic land mammal, has interested many
researchers. During the large culls in African from the 1950s
to the 1980s the understanding of reproductive physi-
ology increased due to post mortem investigations (e.g.
Perry, 1953; Short, 1966; Hanks and Short, 1972). Advances
in the use of ultrasonography and radio- and enzyme-

0378-4320/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.anireprosci.2010.08.027
 T.B. Hildebrandt et al. / Animal Reproduction Science 124 (2011) 176–183
immunoassays in wildlife medicine played a decisive role
in the progression of reproductive understanding and man-
agement in both elephant genera.
In general, the reproductive processes within the fam-
ily elephantidae are believed to be similar (Hodges, 1998),
however, when compared, slight differences in the hor-
mone profiles, especially during pregnancy, are apparent
(Brown et al., 2004; Meyer et al., 2004). The growing
database on reproduction biology of elephants has led
to the development of assisted reproduction technolo-
gies (Hildebrandt and Schnorrenberg, 1996; Hildebrandt
and Göritz, 1998) and enhanced birth rates in captivity
(Saragusty et al., 2009). However, there are still some gaps
in knowledge.
2. Anatomy of the reproductive tract
Formerly, most of the knowledge on the reproductive
organs in elephants is derived from culls of African ele-
phants (e.g. Perry, 1953) and single specimens of Asian
elephants (e.g. Balke et al., 1988a). Thus, historically, basic
information has mostly relied on findings in African savan-
nah elephants and from them applied to the other species.
These pioneers provided the groundwork for understand-
ing of elephant reproduction. Possibly the most striking
characteristic of the female elephant reproductive tract is
its size. Being about 3 m in total length, it is the longest
amongst all land mammals (Balke et al., 1988a,b). The
vestibule (canalis urogenitalis) has an average length of
1.3 m and it opens at the vulva between the hind legs. This
tube-like structure runs caudo-vertical from between the
hind legs towards the tail, where it curves cranially around
the pelvic bone to form a 20- to 40-cm long horizontal
sac. At its cranial end, the hymeneal membrane is found,
leaving only a tiny opening of about 4 mm × 2 mm to the
vagina. This vaginal os is guarded left and right by two
blind pouches of similar size. The hymen will rupture dur-
ing the first delivery and not during copulation, as is the
case in other species. The vagina extends to a length of up
to 50 cm and its internal surface is folded into longitudinal
folds. The lumen of the vagina is filled with mucous which
increases markedly during the transition from the luteal
to the follicular phase. The mucous gradually dissolves
between the first and second LH surges and is excreted
during urination. The mixture of urine and mucous con-
tain specific pheromones that act to attract the breeding
bulls to the female in estrus (Rasmussen et al., 2008). The
folded cervix is about 15 cm long with a prominent cone-
shaped portio cervicalis. The bi-corneal uterus includes a
corpus uteri (about 15 cm long) that splits into two long
uterine horns. The endometrium lining the uterine body
and horns show longitudinal rugae. Each pregnancy leaves
permanent damage on the endometrium that is repaired by
scar tissue so that the number of pregnancies can be deter-
mined during autopsy by counting these scars (Laws, 1967).
The comparably small ovaries, averaging 55–65 mm (Short,
1966; Kidson et al., 1995), of adult females are completely
enveloped in a serosal pouch which forms the oviductal
infundibulum and is incorporated into the two ovarian bur-
sae (Amoroso and Perry, 1964). Physiologically, the ovaries
always contain functional structures such as small follicles
177
during the follicular phase, in addition to a preovulatory
follicle at estrus, and multiple corpora lutea at all times,
however the progestagen concentration remains at base-
line during the follicular phase (Smith and Buss, 1975;
Hermes et al., 2000). Between 6 and 42 corpora lutea have
been recorded on both ovaries (Laws, 1969), with larger
number recorded in younger, pregnant cows (Hanks and
Short, 1972).
3. Ovarian cycle
Elephants are considered to be non-seasonal, polye-
strous breeders although the issue of seasonality has been
challenged (see section on sociosexual behavior). In the
wild, females reach maturity at an age of 10–12 years
(Perry, 1953; Sukumar, 1994), whereas in captivity preg-
nancy was reported to occur at an age as young as 3.5 and 7
years for Asian and African elephants, respectively. The ele-
phant exhibits the longest spontaneous estrous cycle of any
mammal studied to date: 13–18 weeks in duration, with a
6- to 12-week luteal phase and 4- to 6-week follicular phase
(First reports, Asian: Hess et al., 1983; African: Plotka et al.,
1988). This suggests that females may express only three to
four fertile cycles per year. Free-ranging animals, however,
are either pregnant or in lactational anestrus, thus mul-
tiple non-conceptional cycles seem to be rare in the wild
(Hildebrandt et al., 2006).
Elephants are monovular species, however multiple CL
are present in every reproductive cycle. The origin of the
accessory CL stayed unresolved for a long time, leaving
room for speculations. The fact that elephants are pri-
marily uniparous (twins occur in approximately 1% of the
births, Niemuller et al., 1998) and the finding of only one
recent ovulation in an African elephant female shot shortly
after copulation (Short, 1966), led to the assumption that
elephants must be monovulatory. It was not until the
introduction of ultrasonic technologies for reproduction
monitoring (Hildebrandt et al., 1996, 2000; Hermes et al.,
2000) that it was possible to prove this theory to be correct.
Changes throughout the cycle were studied in African
elephants by Hermes et al. (2000). The study demonstrated
two ovarian follicular waves within the inter-luteal phase.
Only the second wave bore a dominant follicle that ovu-
lated. For an animal of such a body size, the ovulatory
follicle ruptures at a comparatively small diameter of about
21 ± 0.5 mm, 12–24 h after the ovulatory LH peak. The max-
imum follicular diameter around the first, anovulatory LH
surge, for comparison, is 13.7 ± 0.7 mm. Even before estrus,
luteinization of non-ovulatory follicles can be regularly
seen after the first LH peak. The ovulatory CL reaches a
diameter of 22.5 ± 0.8 mm shortly after ovulation, and it
can no longer be distinguished from the other CLs after
that. No follicular growth takes place throughout the luteal
phase (Hermes et al., 2000). Follicles start forming as soon
as concentrations of progesterone have reached baseline
(unpublished data).
The endocrine status has distinctive influence on the
uterine texture. Under estrogen dominance, during the
late follicular phase, the cross-section of the endometrium
becomes enlarged (35.4 ± 0.2 mm) and the horns become
more convoluted than during the luteal phase (Hildebrandt
178 T.B. Hildebrandt et al. / Animal Reproduction Science 124 (2011) 176–183
and Göritz, 1998; Hermes et al., 2000). Towards the end
of the luteal phase, the endometrial diameter decreases
(23.7 ± 0.2 mm) and reaches the smallest measured thick-
ness (17 ± 1.5 mm) during the early follicular phase. The
anovulatory LH peak in the mid-follicular phase has little
to no effect on the thickness of the endometrium.
4. Sociosexual behavior
Under good conditions, elephants breed throughout
the year, with some evidence of distinct seasonality or
estrous synchrony. In wild African elephants, concep-
tion rates and births were reported to mainly occur in
the rainy season, when feed resources and water are
abundant (Craig, 1984). Similar trends may exist in cap-
tive breeding herds, where irregular reproductive cycles
may occur during winter time, when time spent outdoor
and daylight duration are short (Schulte, 2000). In cap-
tive Asian elephants, living under their natural climatic
conditions, seasonal differences in the length of the fol-
licular and luteal phases were also reported (Thitaram
et al., 2008). Occasionally, females in one facility may
synchronize their estrous cycle, possibly to be consis-
tent with the timing of that of the dominant female
(Bechert et al., 1999; Weissenböck et al., 2009). The phys-
iological function of such synchronization is not clear
and might be the result of captive conditions because
elephants in the wild are usually either pregnant or in
lactational anestrous. Under natural and wild conditions,
series of non-conceiving estrous cycles, which are fre-
quently observed in captive elephants, most likely do not
occur.
Based on behavioral studies, estrus lasts about 4–5 days
(Jainudeen et al., 1971; Vidya and Sukumar, 2005). In cap-
tivity, a receptive period of 2–3 days was recorded and
multiple copulations are usually observed for up to three
consecutive days (Hildebrandt et al., 2006). As a polygy-
nous mammal, mating with more than one male during a
single estrus does occur (Short, 1966; Poole, 1989a). How-
ever, mating with multiple males is a rare event due to the
presence of the dominant breeding bull. Estrous behavior
in the female include walking away from its herd in an
arc-shaped trail with its head tilted to the side to entice
males or communicate its state (“estrous walk”), produce
deep roaring sounds and flick its tail against the vulva and
then lift and hold it in the air for a while. When chased, it
may first run away but eventually will back up towards the
bull and accept his mounting (Vidya and Sukumar, 2005).
Other indications of estrus include mucus droppings and
the reddening of the clitoris, which may appear through the
vestibular opening when the female is urinating or simply
relaxed.
Estrus is also signaled though infrasonic sounds and
olfactory chemicals, which can be transmitted over greater
distances (Asian: Payne et al., 1986; African: Poole et al.,
1988; Poole, 1989b). This method of communication seem
to be less affected by reflection, refraction and absorption
(Sukumar, 1994) and might help in attracting bulls over
longs distances (African savannah elephant) or in dense for-
est areas (African forest and Asian elephants). Pheromones
in the urine seem to play an important role in signal-
ing an approaching estrus, inducing flehmen response in
bulls, using their vomeronasal organ (Rasmussen et al.,
1982; Rasmussen and Schulte, 1998). The pheromone,
(Z)-7-dodecenyl acetate (Z7-12:Ac) is excreted in the pre-
ovulatory urine (Dehnhard et al., 2001). It increases during
the follicular phase and was reported to induce sexual
behavior.
When a bull approaches a herd of females, it will
inspect the anal and vestibular region and taste out the
urine of its members, showing great interest in females
in estrus (Jainudeen et al., 1971). If the male engages in
wrestling with intertwined trunks, reaching over and chin
resting, driving, neck biting and attempt to mount, it can
be assumed that the female is in estrus (Eisenberg et al.,
1971; Jainudeen et al., 1971). The bull is dependent on
the female’s cooperation when breeding, as she needs to
stand perfectly still to allow intromission of the S-shaped
penis into the vulva, which is positioned ventrally, between
her hind legs. In the wild, large males, over 35 years of
age and in breeding excitement (Hildebrandt et al., 2006)
are preferred partners for mating by mid-estrous females
and are frequently observed to guard them (Poole, 1989b).
Since most signs of estrus relate to social interactions, they
might be difficult to discern in captive situations, where
the matriarchal social group structure is not preserved
(Brannian et al., 1988).
5. Endocrinology of the cycle
A schematic representation of changes in reproductive
hormones during the estrous cycle in elephants is pre-
sented in Fig. 1. Important reviews and summaries of the
reproductive endocrinology of the elephant include those
by Hodges (1998), Niemuller et al. (1998), Brown (2000)
and Brown et al. (2004). Routine endocrine monitoring of
the estrous cycle has been achieved through sampling of
faeces, blood and urine by many elephant keeping facilities.
It is an indispensable tool for the successful management
of elephant breeding groups. In the following text, a brief
overview of major circulating hormones is presented.
5.1. Progestagens
Until the early 1980s it was believed that the Asian
elephant has an estrous cycle length of about 3 weeks
(Jainudeen et al., 1971; Ramsay et al., 1981). This assump-
tion was due to the difficulties in measuring progesterone
at that time. In early attempts, no progesterone could
be measured in serum samples (Hanks and Short, 1972).
Plotka et al. (1975) demonstrated for the first time differ-
ences in serum concentrations of progesterone between
immature, cyclic and pregnant African elephants, but
no correlation with the stage of the ovarian cycle was
detected. It was Hess et al. (1983), who succeeded in
measuring transient elevation in concentrations of proges-
terone in six non-pregnant Asian elephants in a typical
biphasic cycle fashion. They reported that the mean
concentrations of progesterone increased from 30 to
70 pg/mL during the follicular phase to a peak of 400 to
700 pg/mL during the luteal phase. Based these fluctua-
tions in 15 ovarian cycles, they determined the length
 T.B. Hildebrandt et al. / Animal Reproduction Science 124 (2011) 176–183 179

Fig. 1. A general model of the reproduction-associated hormones fluctuations and associated follicular waves during the estrous cycle in elephants. The
dashed vertical line marks the time of ovulation (adapted from Bechert et al., 1999; Brown, 2000).

of the cycle to be 16.3 ± 0.4 weeks (mean ± SEM). The
luteal phase was 10.5 ± 0.3 weeks, with 5.1 ± 0.4 weeks
separating subsequent luteal periods. This was later con-
firmed by other scientists and was found to be true
for African elephants as well. More than a decade later
it was shown that it was not progesterone, but rather
its 5-alpha-reduced metabolites (5-alpha-Pregnan-3,20-
dion and 5-alpha-Pregane-3-ol-20-one) that are secreted
by the CLs into peripheral circulation, with 5-alpha-
Pregnan-3,20-dion predominating (Hodges et al., 1997;
Schwarzenberger et al., 1997). Previous differences in the
results on progesterone were therefore most probably
related to cross-reactivity of the alpha-reduced pregnanes
with the antibodies originally used to detect proges-
terone. In Asian elephants 17-alpha-hydroxyprogesterone
is another metabolite present in significant quantities in
serum (Niemuller et al., 1997). This is strikingly different
from other mammals, where circulating progesterone is
quantitatively the major progestagen.
5.2. Estrogens
Early attempts to measure the fluctuations of the estro-
gens during the estrous cycle in the elephant failed to
show a clear pattern (e.g. Hess et al., 1983). Later stud-
ies showed that serum estrone and 17␤-estradiol seem
to be mostly conjugated in the elephant serum so the
remaining, unconjugated, estrone is basal – less than
20–50 pg/mL (Taya et al., 1991; Czekala et al., 1992). The
assumption in the early days, based on measurements of
both serum and urine estrogen contents, was that estro-
gen fluctuations occurred at 18–21 days intervals and
reflected waves of follicular growth. Through the use of a
more sensitive radioimmunoassay (RIA), Taya et al. (1991)
found baseline estradiol values during luteal phase and
elevations in the follicular phase, with only one distinct
peak (Asian elephant), whereas other scientists later found
slight, but significant estrogen elevations in serum sam-
ples prior to each of the two LH surges in African elephants
180 T.B. Hildebrandt et al. / Animal Reproduction Science 124 (2011) 176–183
(Kapustin et al., 1996). This was confirmed for the Asian
species through urinary estradiol, where 17␤-estradiol
start increasing 5 days prior to and reaching its peak a day
prior to each LH peak (Czekala et al., 2003). This estradiol
pattern supports the suggestion regarding the occurrence
of two follicular waves.
5.3. Inhibin
It is generally accepted, that inhibins are secreted from
the granulosa cells of ovarian follicles in females and,
through suppression of FSH secretion, play a key role in
dominant follicle selection and in the determination of
species-specific ovulation rates. As in many other mam-
mals, in elephants, concentrations of FSH and inhibin are
negatively correlated during the estrous cycle (reviewed
in Brown, 2000). Serum concentrations of inhibin remain
basal during early inter-luteal phase, begin increasing in
the late part of this phase and the early luteal phase
and reach maximum values during the mid-luteal phase.
Concentrations then gradually decrease to reach nadir
in the early follicular phase. Concentrations of inhibin
are, therefore, phase-shifted and positively correlated
with concentrations of progesterone. This, together with
immunohistochemical staining on luteal cells indicates
that in elephants the CLs, in addition to the granulosa cells
of ovarian follicles, secretes bioactive inhibins (Taya, 2007).
In the Asian elephant, the bioactivity and immunoreactiv-
ity of inhibin in the follicular fluid has been demonstrated
with inhibin ␣, ␤A and ␤B localized to the granulosa cells
of the antral follicles. In African elephants, the immunore-
activity of the ␣ subunits of inhibin was found in the lutein
cells, indicating its secretion from the CLs during the luteal
phase (Taya, 2007).
5.4. Luteinizing hormone
Luteinizing hormone (LH) is secreted by the anterior
pituitary gland and is maximal shortly before ovulation in
most mammals. This preovulatory LH surge induces matu-
ration and ovulation of the dominant follicle and initiation
of granulosa cells’ luteinization to finally form the corpus
luteum. In elephants, however, it was noted that the LH
activity is different. Hess et al. (1983) already observed
that “Peaks of immunoreactive LH were observed, although
more than 50% of such ‘surges’ were unrelated to incre-
ments in progesterone (P4) secretion, and no evidence of
bioactivity was observed in any serum sample.” More than
a decade later it was determined that not one but two dis-
tinct LH peaks occur in an estrous cycle (African: Kapustin
et al., 1996; Asian: Brown et al., 1999). These peaks occur
consistently 19–21 days apart. No qualitative or quantita-
tive differences between the two surges or between the
two genera of elephants are detectable. Only the second LH
peak induces ovulation and the subsequent increase in pro-
gesterone. The time, however, from the commencement of
the follicular phase to the first LH peak may vary according
to season, being significantly longer during the rainy sea-
son (33.4 ± 1.8 days) than during the summer (18.9 ± 2.6
days) or winter (22.2 ± 4.5 days) in semi-captive elephants
in Thailand (Thitaram et al., 2008). Several explanations
were proposed for the function of the first, anovulatory
LH peak. One theory suggests that it may be part of the
elephants mating strategy (Czekala et al., 2003). Chemical
signals in urine sampled near the first and second LH surges
are similar. It was, therefore, hypothesized that the first
LH peak produces the necessary chemical signal required
to attract the usually solitary-roaming bulls early enough
prior to ovulation. Another hypothesis suggests that the
function of the first LH peak is to serve as a filter for follicu-
lar development so as to avoid multiple ovulations, which
could lead to fatal twin conceptions occurrence (Hermes
et al., 2000; Hildebrandt et al., 2006). And still another
explanation for anovulatory LH peak may be to prepare the
uterus for ovulation and conception. After the long luteal
phase, the first LH peak may have some sort of organizing
function on the endometrium, and it was suggested to be a
short estrous cycle within the longer cycle (Kapustin et al.,
1996). It can also be suggested that the purpose of the first
LH surge is to reset the system so that proper and synchro-
nized endocrine and follicular development will take place
towards the second LH surge and the eventual ovulation.
Based on correlations between ultrasonic and endocrine
measurements, we think that the most probable explana-
tion is that the first LH peak has the function to luteinize
larger follicles from the first follicular wave which are the
source of the accessory CLs (Hermes et al., 2000).
5.5. Follicle stimulating hormone (FSH)
During the inter-luteal phase of the bovine estrous
cycle, each follicular wave is preceded by an elevation in
FSH secretion. Circulating concentrations of FSH decline
after the selection of dominant follicles in each wave and
the resulting secretion of inhibin and/or estradiol (Kaneko
et al., 1995). Yet, for the elephant, FSH secretion seems to
follow a different pattern. Its concentrations reach their
maximum at the beginning of the non-luteal phase and
then declined steadily to a minimum within 4 days of
the ovulatory LH surge. Concentrations remain basal until
after the ovulatory LH surge and then increase during the
early luteal phase followed by a relatively long period of
increased concentrations lasting at least 7–8 weeks that
covers the late luteal and early follicular phases (Brown
et al., 1999; Brown et al., 2004). Because FSH serves as
the key hormone for follicle recruitment and growth (Taya,
2007), these findings imply a single, prolonged, stimulation
for follicular development of the two waves over most of
the inter-luteal period. During the luteal phase no follic-
ular activity was recorded (Hermes et al., 2000). However,
there is one study, in which two peaks of bioactive FSH were
detected within the 5- to 6-week follicular phase when
daily urine samples of an Asian elephant were analyzed
(Dahl et al., 1989).
5.6. Prolactin
The species differences between Asian and African ele-
phant reproduction are most apparent in the secretion of
prolactin (PRL). Whereas in the African elephant, the con-
centration of PRL is greatest in the follicular phase, in Asian
elephants with no clear pattern of PRL during the estrous
 T.B. Hildebrandt et al. / Animal Reproduction Science 124 (2011) 176–183
cycle (Brown and Lehnhardt, 1997; Brown et al., 2004).
Elevated PRL to pathological concentrations (hyperpro-
lactinemia) in African elephants were linked to anestrous
(Brown and Lehnhardt, 1997). In the pregnant elephant,
PRL increases after 4 months of gestation in both species
(Hodges et al., 1987; Brown and Lehnhardt, 1995). PRL can
have luteotropic, luteolytic or luteostatic effects depending
on the species and reproductive status. It may, therefore,
have a role in the control of the CL lifespan and function at
least during the pregnancy (Bechert et al., 1999).
6. Hormonal manipulation of the estrous cycle
6.1. Luteal regression
Knowledge on hormonal manipulation in the normal
estrous cycle remains very limited. Prostaglandin F2-alpha
(PGF2 ␣), which is used in domestic animals to interrupt the
luteal phase and induce the initiation of another estrous
cycle, failed to achieve a similar effect in elephants. In a
study on two cycling African elephants, PGF2 ␣ was injected
i.m. at a dose of 80–125 mg per elephant on Days 25, 30, 45
and 60 post-estrus. However, only in one female treated on
Day 60, did serum concentrations of progestagens decrease
4 days after the injection (Gross et al., 1991), which, how-
ever, is also the natural timing of the end of the luteal phase.
In an anecdotal report, the administration of PGF2 ␣ to a
young, 5-month pregnant Asian elephant, on three con-
secutive days failed to induce abortion. Although urinary
progesterone metabolites concentrations dropped to base-
line during treatment, concentrations returned to those
normal for pregnancy 10 days after the last injection. A
healthy calf was delivered by this dam (Stephanie Sander-
son, Chester Zoo, UK, personal communication). Based on
this report it can be suggested that PGF2 ␣ is capable of
inhibiting progesterone secretion from the CLs but not to
induce lyses of luteal cells. Further studies on the role of
prostaglandins as luteolytic agents are warranted.
6.2. Ovulation induction
When applying an assisted reproductive technology
such as artificial insemination (AI), appropriate timing of
insemination is determined by detecting of the anovula-
tory LH peak and then timing the AI 19–21 days later.
To ensure ovulation at the time of AI, human chorionic
gonadotropin (hCG) has been used (unpublished data). A
dosage of 5000 IU, injected at the time of the last AI, induced
rupture of the follicle in six cases. However, coincidental
occurrence of the natural second LH peak cannot be dis-
counted in these observations. Furthermore, in one case
of an Asian elephant female, hCG failed to induce rupture
of the dominant follicle. The follicle, which had a diam-
eter of 18.9 mm 19 days after the anovulatory LH surge,
eventually ovulated naturally. A regular ovulatory LH peak
and subsequent ovulation were detected 2 days later (21
days after the first LH peak) when the follicular size was
21.0 mm. Nevertheless, this female became pregnant. This
case indicates that the follicle needs to reach a certain
size or stage of maturation to be receptive for ovulation
induction. In another personal observation on an African
181
elephant female, hCG injection led to follicular stimula-
tion. The ovaries showed more than 15 follicles each, with
diameters ranging between 7.0 and 16.0 mm.
Although detailed effects of GnRH on the pituitary-
gonadal function in elephants is still unknown, several
studies suggest that administration of GnRH can induce
release of LH at concentrations less than normal LH surges
(e.g. Brown, 2000). A study in Thailand provided more
promising results for LH-peak induction (Thitaram et al.,
2009). A GnRH-agonist (Buserelin-Acetate), given 13–43
days after progesterone had reached baseline concentra-
tions (but not earlier), at a dose of 80 ␮g, resulted in an
immediate anovulatory LH surge. This was followed by an
ovulatory LH surge 15–22 days later. One female was bred
and became pregnant following this protocol. Induction of
the first LH peak in proximity to the time it would natu-
rally occur, as shown in this study, could help determine
the right time for an AI.
6.3. Suppression of ovarian activity/contraception
In particular situations, it can be desirable to stop cycli-
cal estrous activity. An example, is when pathologies of
the reproductive tract occur or to avoid inbreeding in cap-
tive settings or if overpopulation in certain African regions
needs to be prevented. Stopping of estrous cycles can be
accomplished by immunocontraceptives such as porcine
zona pellucida (PZP) or Gonadotropin-releasing hormone
(GnRH) or GnRH analogues vaccine. PZP stimulates anti-
bodies against the zona pellucida and therefore can block
the fertilization of the ovum. This treatment has been
successfully applied to African elephants in South Africa,
however, long-term effects are not yet known (Fayrer-
Hosken et al., 2000). Synthetic GnRH analogues (agonists
or antagonists), when given at the proper doses, suppress
the secretion of LH through negative feedback or desensi-
tization. In a controlled study, such a treatment was used
to avoid musth and aggressive behavior in captivity and
to induce infertility in free ranging African bulls (Brown
et al., 1993). Inhibition of LH and FSH secretion stops fol-
licular growth and avert ovulation. This in turn abolishes
estrogen stimulation and thus might have a therapeutic
use to reverse or prevent the growth of uterine leiomy-
omas, a commonly found pathology in non-reproductive
elephants.
7. Conclusion
The enhanced scientific interest in the reproduction
biology of African and Asian elephants resulted in the accu-
mulation of a vast database of information. However, many
voids in knowledge on estrous cycles still prevail and await
elucidation. These include, for example, questions such as
why elephants express two LH peaks, why estrous cycle
needs to be, on average, 16 weeks long, what roles do the
accessory CLs have, and what is the mechanism of luteoly-
sis?
Elephants are certainly difficult to study. Due to their
endangered status and restrictions imposed by interna-
tional laws, sample collection is not without problems and
mostly limited to populations in zoological facilities or
182 T.B. Hildebrandt et al. / Animal Reproduction Science 124 (2011) 176–183
occasionally from dead individuals in the wild. The dif-
ferent physiology and, at times, use of different hormonal
metabolites makes many commercially available measure-
ment kits lacking in sensativity or not suitable for use in
elephants. The study of comparative reproductive phys-
iology is also difficult. The elephant closest relatives are
the sirenia and the hyracoidea. The reproduction aspects of
both orders are not studied well enough to allow evolu-
tionary related conclusions. Nevertheless, the information
accumulated thus far has already helped to better manage
captive elephant populations.
Conflict of interest statement
The authors have no conflict of interest in publishing
this review.
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