Animal Reproduction Science 124 (2011) 244–250

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Animal Reproduction Science

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Reproductive cycles in Bos indicus cattle夽

R. Sartori a,∗ , C.M. Barros b
a
Department of Animal Science, ESALQ, University of São Paulo, Piracicaba, São Paulo, 13418-900, Brazil
b
Department of Pharmacology, IBB, São Paulo State University (UNESP), Botucatu, São Paulo, 18618-000, Brazil

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

Article history: Several studies using transrectal ovarian ultrasonic scanning in Bos taurus (B. taurus) cattle
Available online 21 February 2011 and more recently in Bos indicus (B. Indicus) females evaluated the reproductive cycles of
heifers and cows under different conditions. In general, B. indicus cattle have more follicles
Keywords: and more follicular waves during the estrous cycle and ovulate from smaller follicles than
Follicle B. taurus. Consequently B. indicus females have smaller corpora lutea and it is assumed cir-
Corpus luteum
culating concentrations of estradiol and progesterone are also less. However, these findings
Hormone
may vary depending on the nutritional status and regimen in which the animals are man-
Estrus
Nutrition aged. Moreover, there are significant differences between B. taurus and B. indicus regarding
Zebu follicle size at the time of deviation of the dominant follicle. These differences in ovarian
function between B. indicus and B. taurus, e.g. greater antral follicle population are, proba-
bly, the main reasons for the great success of in vitro embryo production programs in Zebu
cattle, especially in Brazil.
© 2011 Elsevier B.V. All rights reserved.

1. Introduction pertinent comparisons to other breeds. The reason to focus

An enhanced understanding of reproductive physiology
in cattle, particularly related to ovarian function (Pierson
and Ginther, 1984; Adams et al., 1992; Ginther et al., 1996)
has been achieved in the 20 last years due to the use of
ultrasonography and the development of more accurate
hormonal assays. Although the majority of studies reported
in the literature have used B. taurus cattle to study ovar-
ian physiology, there are an increasing number of reports
of studies in B. indicus breeds, such as Brahman and Nel-
lore. Other reviews (Barros and Nogueira, 2001; Bó et al.,
2003) compared the estrous cycle in Zebu with that in
European breeds of cattle, and the focus is similar with
the present review; however, this article focuses mainly
on data of reproductive cycles in the Nellore breed, with
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 at: Av. Pádua Dias, 11 CP 9, 13418-900, Piraci-
caba, São Paulo, Brazil. Tel.: +55 1934294134.
E-mail address: sartori@pq.cnpq.br (R. Sartori).
on the Nellore breed is because it is the predominant Zebu
(B. indicus) cattle in Brazil; according to the Brazilian asso-
ciation of Nellore breeders, Nellore represents 80% of the
beef cattle in Brazil (above 100 million Nellore animals)
and its use continues to expand in Brazil and other tropical
and subtropical countries (Barros and Nogueira, 2001; Bó
et al., 2003). Moreover, data regarding ovarian function in
Brahman have recently been reviewed (Bó et al., 2003).
2. Estrous cycles in Bos indicus cattle
2.1. Ovarian dynamics
After puberty female cattle enter a period of repro-
ductive cyclicity that continues throughout most of the
productive life, unless pregnancy occurs or a period of
negative energy balance prevails which induces anestrus
(Diskin et al., 2003). These cycles of ovarian function
are indicative of estrous cycles and consist of a series
of events beginning at estrus and ending at the subse-
quent estrus. The cycles are characterized by growth and
regression of follicles and corpora lutea, and last 21 d on

0378-4320/$ – see front matter © 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.anireprosci.2011.02.006
 R. Sartori, C.M. Barros / Animal Reproduction Science 124 (2011) 244–250
Fig. 1. Mean (±SE) profiles of dominant follicles (DF) and corpus luteum diameters for Nellore cows and heifers having estrous cycles with two (n = 20; A)
or three (n = 14; B) waves of follicular development. OF = Follicle from which ovulation occurred. Figure extracted from Figueiredo et al. (1997).
average. Moreover, during the estrous cycle, follicle devel-
opment and regression occurs in a wave-like pattern in
cattle. One of the first studies performed in Nellore cattle
(Figueiredo et al., 1997) reported that estrous cycle length
was on average 20.7 (n = 20) and 22.0 (n = 14) d for “two-”
and “three-wave” animals, respectively. Similar differences
in estrous cycle length between “two-”and “three-wave”
animals were reported in Holstein cattle (Sartori et al.,
2004). Other studies in B. taurus have described the occur-
rence of two to four waves of follicular development during
the estrous cycle, with predominance of two waves, and
very rarely four waves (Sirois and Fortune, 1988; Townson
et al., 2002). The study by Figueiredo et al. (1997) has
observed “two-”and “three-wave” cycles in Nellore cat-
tle (Fig. 1), with the majority of cows having two (83.3%,
n = 18) and heifers three (64.7%, n = 16) waves of ovar-
ian follicular development. These authors also reported
that 70% of Nelore females (n = 10), observed during two
consecutive estrous cycles, repeated the same pattern of
follicular wave development of the previous cycle (i.e.,
“two or three waves”). After evaluating 117 inter-ovulatory
intervals (estrous cycles) from 17 Brahman heifers, Rhodes
et al. (1995) recorded that 26.5%, 66.7%, and 6.8% of estrous
cycles had either two, three, or four waves of ovarian follic-
ular developer during an estrous cycle, respectively and the
estrous cycle length lasted, on average 20.9 d. In five Brah-
man heifers examined over more than 12 estrous cycles,
it was reported that the same follicular wave pattern was
repeated 60–87.5% of the time. Other studies in Nellore
heifers (Sartorelli et al., 2005; Mollo et al., 2007), Gir cows
(Gambini et al., 1998; Viana et al., 2000), and Brahman
cows (Zeitoun et al., 1996) have reported a predominance
of “three-wave” estrous cycles, but also observed animals
with two, four, and even a few with five “waves” per estrous
cycle. To-date, there is only one documented study that
has directly and simultaneously compared reproductive
variables in Nellore and another European breed (Carvalho
et al., 2008).
At the onset of each follicular wave, approximately 24
small (3–5 mm) antral follicles were detected in B. taurus
cattle (Ginther et al., 1996). However, in B. indicus, cattle
a greater numbers of small follicles have been recorded
245
during the emergence of the first wave of follicular devel-
opment. Buratini et al. (2000) recorded approximately 50
small follicles in the ovaries of Nellore heifers. Similarly,
when data were combine from recent studies in 115 Nellore
heifers that had the emergence of 190 waves of follicu-
lar development that were synchronized with the aid of
hormonal treatment (2 mg estradiol benzoate im associ-
ated with an intravaginal progesterone device), the average
number of follicles ≥3 mm at the onset of the wave was
41.5 (R. Sartori, unpublished). By evaluating the ovaries on
Day 17 of the estrous cycle (Day 0 = estrus) from heifers
after slaughter, Segerson et al. (1984) detected a greater
number of small follicles in Brahman than in Angus heifers.
Likewise, Alvarez et al. (2000) also observed a greater num-
ber of follicles at time of follicular wave emergence in
Brahman (39 ± 4) compared to Senepol (33 ± 4), or Angus
(21 ± 4) multiparous lactating cows. Recently, Carvalho
et al. (2008) recorded a greater number (33.4 ± 3.2 com-
pared to 25.4 ± 2.5) of small follicles at wave emergence in
Zebu (Nellore and Gir) than European (Angus and Holstein)
breeds. Those significant differences in ovarian follicle pop-
ulation between B. indicus and B. taurus breeds may be
associated with differences in circulating IGF-I, as reported
by Alvarez et al. (2000) and subsequently discussed in this
review. This greater antral follicle population in B. indicus
cattle is also one of the main reasons for the great success
of in vitro embryo production in Zebu cattle in Brazil (Viana
and Camargo, 2007) because of a greater yield of oocytes
during ovum “pick up” (OPU). Consequently, B. indicus cows
produce more embryos in vitro per OPU session than B.
taurus cows (Gimenes et al., 2010).
Another very distinctive difference between B. indicus
and B. taurus cattle appears to be that the maximum diame-
ter of the dominant follicle is smaller at about 10–12 mm in
Nellore compared with about 16–20 mm in Holsteins with
evidence of significant variability in both types of cattle. For
example, in Holstein cattle, follicles from which ovulation
occurs with diameters of between 12 and 22 mm have been
reported in heifers and cows (Savio et al., 1988; Ginther
et al., 1989; Sartori et al., 2006; Carvalho et al., 2008). Simi-
larly, but with a lesser variation, ovulatory follicles ranging
from 10 to 13 mm in diameter have been recorded in
246 R. Sartori, C.M. Barros / Animal Reproduction Science 124 (2011) 244–250
Table 1
Ovarian follicular diameter and day of follicle diameter deviation in growth rate of B. indicus cattle.
Reference Animal category (n)
Sartorelli et al. (2005) Nellore heifers (7)
Sartorelli et al. (2005) Nellore or Nellore × Gir cows (11)
Castilho et al. (2007) Nellore heifers (7)
Gimenes et al. (2008) Nellore heifers (12)
Nellore (Figueiredo et al., 1997; Sartorelli et al., 2005; Car-
valho et al., 2008; Machado et al., 2008) and Brahman
(Rhodes et al., 1995) cattle, with the exception of the stud-
ies that evaluated the influence of feed intake on ovarian
function (Mollo et al., 2007; Martins et al., 2008), which
observed a greater variation. In another study (Alvarez
et al., 2000), larger follicles from which ovulation occurred
were recorded in B. indicus (Brahman) than in Bos tau-
rus (Angus or Senepol) cows (15.6 ± 0.5, 12.8 ± 0.4, and
13.6 ± 0.4 mm, respectively).
Growth rate of the follicles from which ovulation occurs
and other dominant follicles was less in Nellore cattle
(0.9 mm/d; Figueiredo et al., 1997; Carvalho et al., 2008)
than in European breeds (1.1–2.0 mm/d, Sirois and Fortune,
1988; Knopf et al., 1989; Sartori et al., 2004; Carvalho
et al., 2008). Therefore it would appear that Nellore cattle
have smaller dominant follicles and follicles from which
ovulations occurs than B. taurus breeds because of lesser
follicular growth rate.
Due to the positive correlation between size of
ovulatory follicle and corpora lutea size (Sartori et al.,
2002), it is not surprising that corpus luteum volume in
Nellore cows is also smaller than in European breeds.
While studies report average maximum corpora lutea
volumes of 7303 mm3 (∼24.1 mm diameter) for Holstein
heifers and 11248 mm3 (27.8 mm diameter) for lactating
Holstein cows (Sartori et al., 2004), corpora lutea vol-
umes reported in Nellore cattle range from 1987 mm3
(15.6 mm diameter) to 5199 mm3 (∼21.5 mm diameter;
Figueiredo et al., 1997; Mollo et al., 2007; Machado et al., 2008).
In the study of Carvalho et al. (2008), at about 10 d after
ovulation, corpora lutea in B. indicus cattle were smaller
than in B. taurus heifers (15.3 compared to 18.4 mm in
diameter). In Brahman heifers, the maximum diameter of
the corpus luteum was 18.9 mm (Rhodes et al., 1995).
2.2. Follicle deviation
Follicular deviation has been used to refer to the time at
which differences in the growth rate between the future
dominant and the future subordinate follicles become
apparent (Ginther et al., 1996). The mechanisms involved
in the selection of the dominant follicle are complex and
not fully understood. In B. indicus cattle, although there are
significant differences regarding size of follicles at devia-
tion in comparison to B. taurus breeds, the selection process
seems to be similar. In European breeds, follicular deviation
generally occurs when the greatest developing follicle has
reached 8.5–9.0 mm in diameter and the greatest subordi-
nate has reached 7.5–8.0 mm (Ginther et al., 1996; Sartori
et al., 2001). In contrast to Holstein cattle, deviation occurs
Diameter of the Diameter of the greatest Day of deviation
dominant follicle at subordinate follicle at (Ovulation = Day 0)
deviation (mm) deviation (mm)
5.7 5.4 2.8
6.1 5.4 2.4
5.4 5.3 2.7
6.2 5.9 2.5
in Nellore heifers and cows when the greatest growing
follicle reaches 5–6 mm in diameter (Table 1). After that
stage, the dominant follicle continues to grow and the sub-
ordinate(s) undergo atresia. Because cattle are generally
monovulatory, the presence of a single dominant follicle
is the most common finding at ultrasound examination of
the ovaries. However, co-dominance (two or more domi-
nant follicles) can occur, especially in high producing dairy
cows (Sartori et al., 2002, 2004; Lopez et al., 2005). There
are very few reports of co-dominance observed in Zebu cat-
tle (Sartorelli et al., 2005). This is consistent with twinning
rate being very infrequent in Nellore cows.
All the studies in Nellore cattle cited in Table 1 reported
that follicle diameter deviation occurred 2.3–2.8 d after
ovulation when the greatest growing follicle had reached
a diameter between 5.3 and 6.2 mm. Although follicle size
at deviation differs substantially between genetic groups,
the time of deviation in B. indicus in relation to ovulation
is similar to the ones reported in Holstein cattle (Ginther
et al., 1996; Sartori et al., 2001).
Similar to the study performed in Holstein cows (Sartori
et al., 2001), Gimenes et al. (2008) designed an experi-
ment to determine the size at which the dominant follicle
acquires ovulatory capacity in B. indicus heifers. Heifers
(n = 29) were monitored every 24 h by ultrasonography,
from ovulation until the largest growing follicle reached
diameters between 7.0 and 8.4 mm (n = 9), 8.5 and 10.0 mm
(n = 10), or > 10.0 mm (n = 10). At that time, heifers were
treated im with 25 mg of pLH and monitored by ultrasonog-
raphy every 12 h for a further 48 h. In contrast to Holstein
cows, in which there were only ovulations from follicles
≥10 mm in response to LH, ovulation occurred in 3 of 9, 8 of
10, and 9 of 10 Nellore heifers in the three groups, respec-
tively. This suggests that granulosa cells in the dominant
follicle of Nellore cattle acquire LH receptors at a smaller
diameter when compared to Holstein cattle. In fact, this
was confirmed by Nogueira et al. (2007) and Barros et al.
(2009).
2.3. Reproductive hormones
Near the time of estrus, the preovulatory follicle grows
to a large size and produces large amounts of estradiol.
At some point, circulating estradiol reaches a concentra-
tion and duration sufficient to induce behavioral estrus
and induction of a pre-ovulatory LH surge. This is fol-
lowed by ovulation about 24–32 h later. After ovulation,
the corpus luteum forms from the remaining follicular
cells and there is a progressive increase in circulating con-
centrations of progesterone as the corpus luteum grows.
Concentrations of progesterone remain elevated through-
out the lifespan of the corpus luteum and this is essential for
 R. Sartori, C.M. Barros / Animal Reproduction Science 124 (2011) 244–250
embryo development and maintenance and establishment
of pregnancy. Circulating concentrations of progesterone
also block further preovulatory LH surges and ovulations.
Data in Nellore cattle suggest that circulating concen-
trations of progesterone reach a plateau between Day 8
and 13.4 of the estrous cycle and remain elevated until
luteolysis (Figueiredo et al., 1997; Machado et al., 2008).
The time for regression of the corpus luteum in non-
pregnant cattle is determined by the time of PGF2␣
secretion from the uterus, and occurs between Day 16.0
and 19.0 of the estrous cycle in both Zebu and European
breeds (Figueiredo et al., 1997; Alvarez et al., 2000; Sar-
tori et al., 2004; Machado et al., 2008).
The few studies that have directly compared
serum/plasma steroid hormone concentrations between
B. indicus and B. taurus females have detected significant
differences between genetic groups. For example, Segerson
et al. (1984) detected greater serum concentrations of
estradiol-17␤ and progesterone in Angus than Brahman
females. These findings may be attributable to differences
in size of the pre-ovulatory follicle and corpus luteum
between genetic groups. The study by Alvarez et al.
(2000), however, did not detect differences in maximum
concentration of estradiol-17␤ in plasma among Angus
(9.1 ± 1.4 pg/mL), Brahman (8.9 ± 1.6 pg/mL), and Senepol
(8.7 ± 1.4 pg/mL) cows. Moreover, the authors did not
detect differences in maximum plasma concentration of
progesterone among breeds. That study, however, is the
very few that observed greater follicle and corpus luteum
sizes in B. indicus than B. taurus cattle.
In Nellore cattle, Figueiredo et al. (1997) observed
that overall mean progesterone concentration was less
in heifers (4.9 ± 0.2 ng/mL) than in cows (6.4 ± 0.2 ng/mL),
despite the fact that the maximum corpus luteum diame-
ter was larger in heifers. These results were unexpected
and might be explained by diet. While the heifers were
supplemented with concentrate during the experiment,
the cows were kept on pasture. Studies have described
greater clearance rate, and consequently, lesser circulating
steroid hormone concentrations in animals with greater
feed intake (Sangsritavong et al., 2002; Vasconcelos et al.,
2003). Similarly, when comparing serum concentrations of
progesterone between B. indicus and B. taurus synchronized
heifers during the time in which they were treated with an
intra-vaginal progesterone-releasing device, Carvalho et al.
(2008) detected greater circulating progesterone in Zebu
heifers. In contrast, at about 10 d after ovulation, endoge-
nous circulating concentrations of progesterone were less
(3.8 compared to 4.6 ng/mL) in B. indicus than in B. taurus
heifers, which was associated with smaller corpora lutea in
Zebu heifers.
2.4. Estrous behavior
After luteolysis, serum concentrations of progesterone
decrease and circulating concentrations of estradiol-17␤
produced by the dominant follicle increases. The decrease
in progesterone and increase in estradiol-17␤ are respon-
sible for overt estrous behavior and for the preovulatory
GnRH/LH surge. Estrus, the period of sexual receptivity,
lasts between 30 min and 27 h in B. taurus (Lopez et al.,
247
2004) and between 1 and 20 h in B. indicus (reviewed by Bó
et al., 2003).
The onset of estrus coincides with the preovulatory
surge of LH followed by ovulation, on average, 26–28 h later
(Walker et al., 1996; Pinheiro et al., 1998; Mizuta, 2003).
Studies in Nellore cattle have observed some differences
regarding estrous characteristics in this breed and some of
these are described subsequently in this review.
The interval between the onset of estrus and ovulation
was 27.7 ± 2.4 and 26.1 ± 1.2 h after PGF2␣-induced and
natural estrus, respectively in nulliparous heifers, and in
cows it was 26.8 ± 0.8 and 28.0 ± 0.9 h after PGF2␣-induced
and natural estrus, respectively (Pinheiro et al., 1998).
Additionally, estrous behavior, when detected (<50% of the
cows) was shorter (10.5 ± 1.0 and 13.6 ± 1.0 h after PGF2␣-
induced and natural estrus, respectively) when compared
to European breeds, and there was a greater incidence of
estrus at night.
Combined data of two other studies, in which time
of estrus was synchronized in 90 post-pubertal Nellore
heifers and ovulation was confirmed by ultrasonography,
were analyzed. Although the majority of the heifers (76.7%)
ovulated within 7 d after PGF2␣ treatment, 50.0% were not
observed in standing estrus, even with 24 h a day visual
monitoring along with the aid of estrous mount detec-
tors, such as Kamars (R. Sartori; unpublished). Moreover,
of the 45 heifers not detected in estrus, 25 (55.6%) had
ovulations, and only one (2.2%) heifer detected in estrus
did not have an ovulation. Some of the possible reasons
for the lack of estrous behavior, besides an inherent breed-
effect, were excessive animal handling for daily transrectal
ultrasonic evaluation and blood collection, and/or a rapid
relative decrease in ambient temperature during some of
the nights of these research trials.
To our knowledge, the only study that directly com-
pared estrous behavior in Nellore cows to a European breed
(Angus) was performed by Mizuta (2003). By the aid of
a radiotelemetric estrous detection system (Heat-Watch),
this study verified that average estrous duration in Nel-
lore was shorter than in Angus cows (12.9 ± 2.9 compared
to 16.3 ± 4.8 h). The interval between the onset of estrus
and ovulation, however, did not differ between Nellore
(27.1 ± 3.3 h) and Angus (26.1 ± 6.3 h) cows.
The summation of a greater percentage of Nellore
females displaying no signs of estrus before ovulation,
short estrous duration, and a greater percentage of ani-
mals that start and end standing estrus during the night
makes estrous detection more difficult and, consequently,
provides barriers for development of successful AI regi-
mens in Nellore cattle. This problem can be diminished
if fixed-time AI (FTAI) without estrous detection is per-
formed. Consequently, several hormonal treatments have
been developed to allow FTAI in zebu cattle, including a
protocol for FTAI in embryo donors (Fernandes et al., 2001;
Baruselli et al., 2004; Bó et al., 2007; Barros et al., 2010).
3. Influence of feed intake on ovarian function of
Nellore cattle
A single study in nulliparous pubertal heifers (Mollo
et al., 2007) and another study in non-lactating cows
248 R. Sartori, C.M. Barros / Animal Reproduction Science 124 (2011) 244–250

(Martins et al., 2008) were performed to investigate the

0.78
0.78

0.58
0.12
0.38
0.51
0.03

0.40
influence of feed intake on ovarian function of Zebu cattle.

–
–
P
The first study used pubertal Nellore heifers with greater
(H, n = 20) or less (L, n = 19) feed intake, receiving 1.7
or 0.7 of the maintenance diet, respectively. During the

12.8 ± 0.4 [10.3–17.0]

Greater intake (n = 9)
diet adaptation period, heifers were submitted to estrous
synchronization with cloprostenol and were constantly

2469.3 ± 578.2
Results (mean ± SE) of serum hormone concentrations and size of ovarian structures in Nellore heifers (Study 1; n = 39) or (Study 2; n = 18) with greater (0.7 M) or less (1.7 M) feed intake.

407.0 ± 37.2
observed for estrous behavior 24 h a day until detection

0.62 ± 0.04
12.8 ± 0.4

9.8 ± 1.2

6.4 ± 1.3
2.6 ± 0.6
of ovulation. Ovarian ultrasonography and blood collec-
tion were performed daily from cloprostenol injection until
the end of an estrous cycle and ovulation occurred. These

–
–
procedures aimed to follow up follicular and luteal devel-
opment as well as to quantify serum concentrations of

12.5 ± 0.8 [12.0–14.0]

estradiol-17␤, progesterone, insulin and IGF-I. After clo-

Lesser intake (n = 9)
prostenol administration, heifers from the Group H had a

2891.6 ± 418.2
Study 2 (Cows)
shorter duration of estrus and a less intense estrous behav-

334.9 ± 44.0
0.70 ± 0.08
ior when compared to the Group L heifers (Table 2). At

17.2 ± 2.5
12.5 ± 0.8

4.7 ± 1.5
3.9 ± 0.5
the end of the estrous cycle, the day of luteolysis was
similar (P = 0.74) in both groups (Day 18.0 ± 0.5). Within

–
–
the animals that had a normal estrous cycle, characterized
by ovulation of the growing follicle that was present at
the time of luteolysis, the mean estrous cycle length was
21.4 ± 0.7 and 23.4 ± 1.3 d in the Groups H (n = 18) and L

<0.01
<0.01
<0.01

<0.01
<0.01
<0.01
0.35

0.56
0.07

0.50

0.02
(n = 16), respectively (P = 0.18). Although a previous study

–
P
in B. taurus heifers suggested an effect of feed intake on the
number of waves of ovarian follicular development dur-
ing the estrous cycle (Murphy et al., 1991), in the present

14.0 ± 0.2 [11.2–17.0]

study, with a greater number of heifers, there was no such Greater intake (n = 20)

Serum progesterone concentration: Maximum progesterone in Study 1 and progesterone on Day 7 in Study 2.
effect. The percentage of estrous cycles with two, three,

5198.6 ± 376.0
or four waves of follicular development was 25%, 50% and

Corpus luteum volume: Maximum corpus luteum volume in Study 1 and CL volume on Day 7 in Study 2.
569.8 ± 1.8
14.3 ± 1.8
10.7 ± 2.2

12.6 ± 0.3

12.8 ± 0.6
18%, respectively for Group L and 28%, 56% and 17%, respec-
8.9 ± 1.9

1.2 ± 0.1
5.2 ± 0.3

5.6 ± 0.4
tively for Group H. Moreover, one heifer of the L group had
five waves of follicular development. Although ovulations

–
were from larger follicles in Group H, the groups did not
differ in regard to the amplitude of the estradiol-17␤ surge
prior to ovulation. Growth rate of the follicle from which
11.8 ± 0.2 [9.7–15.5]
Lesser intake (n = 19)

ovulation occurred was greater in Group H heifers and the

number of days between luteolysis and ovulation was less
Study 1 (Heifers)

4095.9 ± 173.7

(Table 2). These results may be associated with the greater

588.9 ± 23.2
17.1 ± 2.5
29.8 ± 5.1

14.3 ± 1.5

11.8 ± 0.2
10.7 ± 0.3

serum insulin concentration observed in this group with

6.9 ± 0.5

5.2 ± 0.6
0.9 ± 0.1

greater feed intake. Unexpectedly, differences in serum

Results of Study 1 include follicles from which ovulation occurred.

concentrations of total IGF-I were not detected between

–

groups during the peri-ovulatory period. Similarly to what

occurred with the follicle from which ovulation occurred,
Adapted from Mollo et al. (2007) and Martins et al. (2008).

the maximum size of the corpus luteum during the estrous

Maximum size of first-wave dominant follicle (mm)

cycle was also greater in Group H heifers. However, there

Maximum size of ovulatory follicle (mm; [range])a
Estradiol-17␤ peak preceding ovulation (pg/mL)

was no difference between groups in serum progesterone

concentrations (Table 2). Based on the results of this study
Days between luteolysis and ovulation (n)

it was concluded that differential feed/energy intake can

Growth rate of ovulatory follicle (mm/d)

affect the reproductive physiology of Nellore heifers, caus-

ing alteration in behavior and estrous cycle patterns.
In the second study, 18 Nellore cows were divided
Corpus luteum volume (mm3 )b
Serum progesterone (ng/mL)c

into two groups, similarly to the first experiment: 1.7

Serum total IGF-I (ng/mL)
Mounts during estrus (n)

(greater feed intake = H) or 0.66 (lesser feed intake = L)

Serum insulin (␮IU/mL)

of the maintenance diet. Within 21 d on the experimen-

Estrous duration (h)

Serum FSH (ng/mL)

tal diets, time of initiation of estrus was synchronized.

Subsequently, ovaries were assessed by trans-rectal ultra-
sonography and blood samples were collected daily until
Day 7 of the cycle (ovulation = Day 1). Cows from Group
Table 2

H gained 1.1 kg/d and from Group L lost 1.5 kg/d of body
a

weight. Although there was no difference between groups

 R. Sartori, C.M. Barros / Animal Reproduction Science 124 (2011) 244–250
Table 3
Comparison of several reproductive variables between B. indicus and B.
taurus female cattle based on a compilation of the literature data pre-
sented in the present manuscript.
B. indicus vs.
B. taurus
Gestation length > Because of the apparent lesser expression of estrous behav-
Estrous cycle length =
Day of luteolysis ≤
Number of waves of follicular development per > regimens without the need of estrous detection (Fernandes
estrous cycle
Number of follicles at time of follicular wave > monal regimens that control follicular development and
emergence
Size of dominant follicle at deviation <
Maximum size of dominant/ovulatory follicle <
Growth rate of dominant/ovulatory follicle ≤ role in the consolidation of IVF industry in Brazil. Addi-
Duration of estrus ≤ tionally, super-stimulatory protocols for ovarian follicular
Luteal tissue volume < development were developed that allow FTAI of embryo
Circulating IGF-I >
regarding maximum diameter of the follicle from ovulation
occurred, a lesser amplitude preovulatory estradiol surge
was observed in Group H cows (Table 2). There was no dif-
ference between groups for luteal tissue volume and serum
progesterone concentration on Day 7 and serum FSH, IGF-
I and insulin concentrations during the peri-ovulatory
period. Experimental diets, therefore, did not alter ovar-
ian function and serum concentrations of reproductive and
metabolic hormones, except for estradiol-17␤, suggest-
ing greater metabolism of this hormone (Sangsritavong
et al., 2002) has occurred in cows with greater feed
intake.
4. Summary and applications
Table 3 summarizes the similarities and differences
between ovarian function of B. indicus and B. taurus cattle,
as reported in the studies covered in the present review.
Although the pattern of ovarian follicular development
is similar in B. indicus and B. taurus cattle, Zebu cattle
have more but smaller antral follicles. The reason for the
large population of small antral follicles in B. indicus is not
well understood, and additional studies are warranted to
determine the importance of IGF-I and other factors in
determining follicle populations, as suggested by others
(Bó et al., 2003). In Nellore heifers (Buratini et al., 2000),
treatment with bovine somatotropin increased plasma IGF-
I concentrations and the number of small follicles (<5 mm),
similarly to what has been reported in B. taurus (Gong
et al., 1991). However, the rate of increase in follicle num-
bers during a wave of follicular development was less than
those reported in B. taurus, suggesting that the ovarian
IGF system may differ between B. taurus and B. indicus.
Brahman cows had greater plasma IGF-I concentrations
(Simpson et al., 1994; Alvarez et al., 2000) and lesser FSH
concentrations than Angus cows (Alvarez et al., 2000). It
has been suggested that greater follicle numbers, despite
the lesser FSH concentrations in Brahman cattle, might be
due to the greater IGF-I concentrations in Brahman cows.
Additionally, it is speculated that IGF-I might enhance fol-
licle responsiveness to FSH in Zebu cattle due to numerous
summary reports in which smaller doses of FSH induced
a superovulatory response that appeared comparable to
249
that in European breeds of cattle using larger doses of
FSH (Barros and Nogueira, 2001). Nevertheless, the greater
antral follicle population in Nellore and crossbred helps
to explain the success of in vitro embryo production in
Brazil. More follicles aspirated per Zebu donor cow result in
more transferable embryos compared to European breeds.
ior in Zebu cattle, it has promoted the development of FTAI
et al., 2001; Baruselli et al., 2004; Bó et al., 2007). Those hor-
synchronize time of ovulation have been widely applied to
embryo recipients (Bó et al., 2002), and have an important
donors, facilitating embryo donor handling (Barros and
Nogueira, 2001; Baruselli et al., 2006). The few studies that
investigated the influence of feed intake on ovarian func-
tion and embryo production of Zebu cattle have detected
major nutritional effects (Santos et al., 2008).
Conflict of interest statement
None of the authors (Roberto Sartori or Ciro Moraes
Barros) has a financial or personal relationship with other
people or organizations that could inappropriately influ-
ence or bias this paper entitled “Reproductive cycles in Bos
indicus cattle”.
Acknowledgements
Data of some studies reported in this article that
have not yet been published elsewhere were part of
dissertations or thesis of the following ex or current
graduate students. Aline Carvalho Martins, Evandro Sar-
torelli e Sartorelli, Marcelo Fábio Gouveia Nogueira, Marcos
Rollemberg Mollo, Michele Ricieri Bastos, Monique Mendes
Guardieiro, Osni Lázaro Pinheiro, Paulo Fernandes, Ricardo
Alamino Figueiredo, and Ronaldo Luiz Ereno. Most of
our studies were financially supported by CAPES, CNPq,
EMBRAPA, FAPDF, and/or FAPESP of Brazil.
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