Department of Animal Science, ESALQ, University of So Paulo, Piracicaba, So Paulo, 13418-900, Brazil
Department of Pharmacology, IBB, So Paulo State University (UNESP), Botucatu, So Paulo, 18618-000, Brazil
a r t i c l e
i n f o
Article history:
Available online 21 February 2011
Keywords:
Follicle
Corpus luteum
Hormone
Estrus
Nutrition
Zebu
a b s t r a c t
Several studies using transrectal ovarian ultrasonic scanning in Bos taurus (B. taurus) cattle
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
and more follicular waves during the estrous cycle and ovulate from smaller follicles than
B. taurus. Consequently B. indicus females have smaller corpora lutea and it is assumed circulating concentrations of estradiol and progesterone are also less. However, these ndings
may vary depending on the nutritional status and regimen in which the animals are managed. Moreover, there are signicant differences between B. taurus and B. indicus regarding
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, probably, 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
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 ovarian physiology, there are an increasing number of reports
of studies in B. indicus breeds, such as Brahman and Nellore. Other reviews (Barros and Nogueira, 2001; B 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
245
Fig. 1. Mean (SE) proles 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 development and regression occurs in a wave-like pattern in
cattle. One of the rst 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 occurrence 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 cattle (Fig. 1), with the majority of cows having two (83.3%,
n = 18) and heifers three (64.7%, n = 16) waves of ovarian 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 follicular developer during an estrous cycle, respectively and the
estrous cycle length lasted, on average 20.9 d. In ve Brahman heifers examined over more than 12 estrous cycles,
it was reported that the same follicular wave pattern was
repeated 6087.5% 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 ve 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 (35 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
during the emergence of the rst wave of follicular development. 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 follicular development that were synchronized with the aid of
hormonal treatment (2 mg estradiol benzoate im associated 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 number 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 compared to 25.4 2.5) of small follicles at wave emergence in
Zebu (Nellore and Gir) than European (Angus and Holstein)
breeds. Those signicant differences in ovarian follicle population 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 diameter of the dominant follicle is smaller at about 1012 mm in
Nellore compared with about 1620 mm in Holsteins with
evidence of signicant 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). Similarly, but with a lesser variation, ovulatory follicles ranging
from 10 to 13 mm in diameter have been recorded in
246
Table 1
Ovarian follicular diameter and day of follicle diameter deviation in growth rate of B. indicus cattle.
Reference
Diameter of the
dominant follicle at
deviation (mm)
Day of deviation
(Ovulation = Day 0)
5.7
6.1
5.4
6.2
5.4
5.4
5.3
5.9
2.8
2.4
2.7
2.5
Nellore (Figueiredo et al., 1997; Sartorelli et al., 2005; Carvalho et al., 2008; Machado et al., 2008) and Brahman
(Rhodes et al., 1995) cattle, with the exception of the studies that evaluated the inuence 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 taurus (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 (1.12.0 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 volumes 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
signicant differences regarding size of follicles at deviation 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 8.59.0 mm in diameter and the greatest subordinate has reached 7.58.0 mm (Ginther et al., 1996; Sartori
et al., 2001). In contrast to Holstein cattle, deviation occurs
247
0.78
0.78
0.03
0.58
0.12
0.38
0.51
0.40
12.8 0.4
12.8 0.4 [10.317.0]
9.8 1.2
2469.3 578.2
2.6 0.6
0.62 0.04
407.0 37.2
6.4 1.3
12.5 0.8
12.5 0.8 [12.014.0]
17.2 2.5
2891.6 418.2
3.9 0.5
0.70 0.08
334.9 44.0
4.7 1.5
0.07
<0.01
<0.01
<0.01
0.35
<0.01
<0.01
<0.01
0.50
0.56
0.02
10.7 2.2
8.9 1.9
12.6 0.3
14.0 0.2 [11.217.0]
12.8 0.6
1.2 0.1
5.2 0.3
5198.6 376.0
5.6 0.4
569.8 1.8
14.3 1.8
17.1 2.5
29.8 5.1
10.7 0.3
11.8 0.2 [9.715.5]
14.3 1.5
0.9 0.1
6.9 0.5
4095.9 173.7
5.2 0.6
588.9 23.2
11.8 0.2
Greater intake (n = 9)
Study 2 (Cows)
Lesser intake (n = 9)
Lesser intake (n = 19)
P
Greater intake (n = 20)
Study 1 (Heifers)
Table 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.
248
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250
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