Animal Reproduction Science 82–83 (2004) 361–372
Puberty in South American Bos indicus (Zebu) cattle
G.P. Nogueira∗
UNESP-FOA-Curso de Medicina Veterinária, Laboratório de Endocrinologia,
Rua Clóvis Pestana 793, 16050-680 Araçatuba, SP, Brazil
Abstract
Puberty in Zebu heifers follows a pattern characterized by a decrease in the steroid feedback
mechanism and an increase in LH concentration, which result in the first ovulation followed by
a short estrous cycle and the onset of normal cycles thereafter. These events are similar to those
observed in Bos taurus cattle but occur at a later age. The late onset of puberty is both genetic and
environmental in origin and is reflected by the age at first calving that can be at 40 months of age or
older in these animals. Age at puberty in Zebu heifers has been shown to have a high heritability.
Consequently, selecting precocious heifers may be an effective means of reducing age at puberty in
these animals and this approach is being adopted in commercial practice. Genetic selection is not
the sole solution to the problem because environmental improvements are necessary, particularly
in terms of improved nutrition. South American Zebu cattle are usually subject to sub-optimum
nutritional and management conditions and, hence, exhibit late onset of puberty. Hybrids of Zebu
and Bos taurus cattle exhibit heterosis in respect of the age of puberty with earlier onset than expected
in crossbred animals. Recently, purebred South American Zebu cattle have been shown to have Bos
taurus genes, indicating that there have been previous attempts to improve their productivity using
this approach. It was concluded that the age at first calving in South American Zebu cattle can
be reduced by exposing well-fed, yearling heifers to bulls and selecting, over several generations,
those animals that become pregnant at an early age.
© 2004 Published by Elsevier B.V.
Keywords: Cattle; Bos indicus; Zebu; Puberty; Heifers; South America
1. Introduction
Zebu cattle (Bos indicus) are the predominant humped cattle of the world. Brazil alone
has nearly 170 million bovines of which 80% are Zebu or crossbred Zebu animals. The
extensive systems of management which predominate in South America have continually
exposed these cattle to a tropical climatic and nutritional environment resulting in increased
∗ Tel.: +55-18-3636-3289x204.
E-mail address: [email protected] (G.P. Nogueira).
0378-4320/$ – see front matter © 2004 Published by Elsevier B.V.
doi:10.1016/j.anireprosci.2004.04.007
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tolerance to that environment through selection pressure. This environmental tolerance
means that Zebu cattle can thrive where Bos taurus animals cannot. Resistance to high
temperature and humidity in tropical and sub-tropical regions has been associated with the
fat accumulation at the hump and pronounced dewlap in these cattle (Cartwright, 1980) and
their ability to digest low quality forages (Rajaratne et al., 1983). These features make the
Zebu well adapted to extensive breeding and management systems in a tropical climate.
An unwanted consequence of increased tolerance to environmental pressures has been a
decrease in productivity and precocity. Puberty in South American Zebu occurs at 22–36
months and the age at first calving is around 44–48 months of age (Silva and Pereira, 1986;
Souza et al., 1995; Pereira, 2000). This is a major concern for breeders and research workers,
and they are working to achieve a reduction in the age at puberty and first calving in order
to increase the productivity of Zebu cattle.
The aim of this paper is to review the literature referring to puberty in Zebu cattle, with
special reference to South America; present data from research work in which puberty was
studied; and comment on management and selection approaches that may help to achieve a
decrease in age at puberty in these animals. The Brahman is considered separately because
it is a Bos indicus × Bos taurus admixture.
2. Origin of Bos indicus
Domestication is the deliberate interference by man in the life of cattle that were originally
herded as a source of food and only later subjected to controlled breeding. There are several
theories about the origin of Zebu cattle but according to Naik (1978) the most acceptable is
that they are descended from Bos nomadicus that were wild cattle found in the Indian Pleistocene era. The marked differences in the archeological record and genetic characteristics
between Bos taurus and Zebu cattle confirm their independent origin. There are also several
physiological and behavioral differences related to natural pressures and human selection
resulting in a strong genotype-environment interaction (Buntjer et al., 2002). Compared to
European breeds, Zebu herds show a high degree of social structure and genetic variability
due to their extensive management and a lower degree of human interference and the latter
provides ample scope for genetic improvement.
3. Female Bos indicus
When both genotypes are kept under a tropical or subtropical environment the reproductive performance of the Zebu is superior to that of Bos taurus breeds of cattle (Bó et al.,
2003). Zebu herds are based on matriarchal families interconnected by means of friendship
and relationships between non-kin partners (Reinhardt and Reinhardt, 1981). This herd social structure reflects the closer contact, which is maintained for a longer period, between
Zebu cows and their calves compared to crossbred cattle (Das et al., 2001). Zebu cows are
more sensitive to calf stimulus during milking compared to European breeds, and the physical action of suckling stimulates higher milk yields (Orihuela, 1990). The positive aspect of
this maternal characteristic is that it allows the practice of low cost extensive management
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systems. On the other hand, intensive suckling has a negative effect on reproduction by
decreasing GnRH secretion through a neural mechanism involving prolactin in the cow.
This effect depends on the frequency or the duration of the suckling stimulus within a 24 h
period (McNeilly, 1980). Rodrigues and Segura (1995) showed that restriction of suckling
to 60 min a day from 30 to 60 days after birth increased pregnancy rates. Social interaction
also affects reproduction in the Zebu since the interval to the first postpartum estrus and the
number of days open in cows were reduced by the bull effect (Beloso et al., 1997).
Zebu cattle originate from India where they are kept for milk production and as draught
animals, both of which involve frequent human contact. The converse is true in the extensive
management systems of South America and human interaction is usually associated by
the animals with an unpleasant experience, e.g. vaccination. This results in cattle that are
fearful of, and sometimes aggressive towards, stockmen (Neindre et al., 1996) and may be
one reason for poor reproductive performance, particularly when evaluated by a research
worker unfamiliar to the animals, but intensive handling easily overcomes this aversive
behavior.
Low fertility rate following artificial insemination of Zebu cows may be attributed to the
management, nutrition and genetic characteristics of the animals (Baca et al., 1998; Pereira,
2000). Reduced dietary intake results in failure to ovulate because levels of circulating LH
are insufficient to stimulate maturation of the dominant follicle (Rhodes et al., 1996). The
costs of a selection program based on criteria such as body weight, milk and reproductive
traits in a dual purpose Zebu herd were justified by the consequent high level of genetic
improvement and gain in profit (Lobo et al., 2000).
4. Puberty in Zebu heifers
The onset of puberty is characterized by the first ovulation (Rawlings et al., 2003) which
occurs between 6 and 24 months of age depending on genetic and environmental factors
(Moran et al., 1989). Sexual maturation of heifers involves an increase in ovarian circumference with age that is more pronounced around 13 months old (Lobo et al., 2001). In a recent
experiment, Nellore heifers were examined by ultrasonography from 8 to 16 months of age
and the dominant follicle was observed to increase in diameter as the heifers became older.
The rate of follicle growth remained the same throughout the age range but the growing
phase lasted longer (Fig. 1; de Lucia et al., 2002).
During this experiment (de Lucia et al., 2002) it was observed that 32% of the heifers
became pregnant at 15 months of age and were judged to have exhibited precocious puberty.
These heifers had a larger dominant follicle diameter at 12 and 14 months of age compared
with non-precocious animals. This is in agreement with other observations relating follicle
diameter at 11 months of age to onset of puberty in crossbred Bos indicus heifers (Perry
et al., 1991).
Sexual maturation of Zebu heifers involved an increase in LH secretion while FSH secretion did not change (Fig. 2; Nogueira et al., 2003) and these changes in gonadotrophin
secretion were similar to those reported for Bos taurus cattle (Evans et al., 1994). The progressive decline in the hypothalamic response to estradiol allowed an increase in pituitary
stimulation, which was reflected by higher levels of LH secretion (Day et al., 1987).
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Fig. 1. Growth and regression of the dominant follicle in Nellore heifers at 8 months (n = 20), 10 months (n = 20),
12 months (n = 9), and 14 months (n = 8) of age (de Lucia et al., 2002).
Although precocious heifers had follicles with a larger diameter at 12 and 14 months of
age than non-precocious animals there was no difference in LH secretion suggesting that
precocious heifers respond better to low plasma concentrations of LH (Nogueira et al., 2003).
Factors that determine when estrous cycles will begin in a heifer are age and body
fat content since the hypothalamus is programmed via leptin secretion by the adipocyte
(Foster and Nagatani, 1999; Garcia et al., 2002). In a study of Nellore heifers during sexual
maturation using electrical bioimpedance [the electrodes were placed in pairs 15 cm apart
(center to center) on the neck and rump], we were able to identify an increase in cell number
(conductivity) but there was no increase in fat percentage (resistance) as heifers became
older (Fig. 3; Araújo et al., 2002). This was probably due to the fat distribution particular
to Zebu cattle that allowed mechanisms other than leptin to stimulate the hypothalamus.
The late age at which heifers reach puberty is a major concern in Zebu cattle (Rodrigues
et al., 2002). Although Zebu heifers achieve maturity at an older age and at a higher proportion of mature weight, they have a greater reproductive longevity compared to Bos taurus
Fig. 2. Plasma gonadotrophin concentrations in pre-pubertal Nellore heifers sampled every 4 days (n = 37,
Nogueira et al., 2003).
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Fig. 3. Variations in conductivity and resistance in growing Nelore heifers (n = 37, Araújo et al., 2002).
(Aroeira et al., 1977; Cartwright, 1980). Age at puberty is an important production trait in
heifers that are selected to calve at 2 years old in order to increase their reproductive life
without detrimental effects on longevity or weaning weights compared to those calving at
3 years of age (Tran et al., 1988). The estimated age at puberty (first ovulation or estrus)
for Zebu in the tropics and subtropics ranges from 16 to 40 months. This is attributed to
both genetic and environmental factors including nutrition, disease, temperature, humidity
and season of birth (Mukasa Muguerwa, 1989). It is difficult to determine age at puberty in
extensive management systems but it can be estimated from age at first calving. For beef
cattle in Brazil, age at first calving is over 40 months and is attributed to inadequate nutrition
as well as other factors (Souza et al., 1995; Pereira, 2000) since Zebu cattle are fed on low
quality roughage.
Improvement in post weaning nutrition is an important factor in achieving a decrease
in age at puberty and at first calving (Patterson et al., 1992b). Oyedipe et al. (1982) reported that an increase in protein intake resulted in a decrease in age and increase in weight
at puberty. Greer et al. (1983) demonstrated by mathematical modeling that beef heifers
that were heavier at weaning and had higher levels of post-weaning nutrition reached puberty at an early age and heavier weight. Low nutrition in beef heifers suppresses the LH
pulse generation system located in the hypothalamus (Schillo et al., 1992; Rawlings et al.,
2003) delaying first ovulation. Zebu heifers in the tropics fed according to NRC protein
recommendations can reach puberty at 12.3 and calve at 27 months of age (Fajersson
et al., 1991). Nellore heifers that were selected for precocity and kept under an adequate
nutritional regimen ovulated at 14–15 months old. Progesterone assay showed that the
first estrous cycle was short but the following estrous cycles were regular and similar to
those observed in cows (Fig. 4; Nogueira et al., 2003). In domestic animals there seems
to be a system of “all or none” since after the first ovulation the hypothalamus is mature
enough to support regular, adult-type estrous cycles as demonstrated in horses (Nogueira
et al., 1997). In humans, puberty is characterized by a period of transition between infancy and adulthood. In domestic animals, however, before first ovulation a female is
prepubertal and after that it is adult. What constitutes the pubertal phase in a heifer or
filly?
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Fig. 4. Plasma progesterone concentrations in Nellore heifers after the first ovulation. The short cycle values were
centered on the progesterone surge (n = 32). Thereafter, they were centered on the beginning of progesterone
secretion (second surge, n = 28; third surge, n = 19; fourth surge, n = 9; Nogueira et al., 2003).
There also seems to be a genetic factor involved in precocity since 30% of Nellore heifers
(12 of 37) became pregnant at 16 months of age but with no difference in age or weight
from the group mean at first ovulation. The interval between the first and the second ovulation, however, was longer for precocious (12 days) than for non-precocious (9 days) heifers
suggesting that there was a different degree of maturity in the hypothalamus in the two
types of animal (Nogueira et al., 2003). Nellore heifers that became pregnant after mating
at 17–18 months of age were heavier, older and in better body condition as yearlings with
better visual conformation score, precocity and muscularity than heifers that did not become
pregnant (Semmelmann et al., 2001). In Zebu cattle, the genotype-environment interaction
has a significant effect on post-weaning weight (Ferreira et al., 2001) and, hence, to the
incidence of first ovulation. So, growth is restricted if the heifer is not well fed and this
leads to an increase in age at puberty. Increased productivity can be achieved by introducing
adequate nutritional management to reduce age at puberty in herds that have high calving
rates (Beretta et al., 2001). The experience in our laboratory shows that beef heifers calving first at 2 years of age exhibit a prolonged postpartum interval to resumption of estrous
cycles (Patterson et al., 1992a). In the “1 year system” in which heifers became pregnant
around 1-year-old and first calving occurs at about 2 years of age, the response curve was
quadratic, with maximum production occurring when the calving rate was high. A survey
in Brazil from 1950 to 1964 found that there was no change in age at first calving (around
44 months) suggesting that there had been no selection for decreased age at first calving
or improvement in nutrition during this period (Aroeira et al., 1977). A high heritability
(0.57 ± 0.01) estimate for probability of pregnancy at 14 months was recently reported
for Nellore cattle suggesting that they have not been selected for precocity and, therefore, the genetic variability for this character appears to be higher than normal (Eler et al.,
2002).
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Factors that might predict precocity (exhibited as ovulation or calving at an early age)
have been examined in several studies. The positive relationship observed between scrotal
circumference and earlier puberty in males (Vargas et al., 1998) was not correlated with
ovarian circumference and pelvic area in heifers (Lobo et al., 2001). Although early puberty
was genetically determined, there was no association between mutations of the LHr gene and
this phenotype in Nellore heifers (Milazzotto et al., 2002). A scoring system that considers
several characteristics of the reproductive organs (uterine size and tone, size of the ovaries,
follicular growth and presence of a CL), when used in 2-year-old heifers prior to mating,
was able to identify those animals with a higher probability of ovulating (Ferreira et al.,
1999). In practice, Zebu females need to be around 15–17 months of age before attaining
puberty. For calving to occur at 2 years of age, it is necessary to use a combination of
improved nutrition, selection for early puberty and achievement of a heavy calf weaning
weight (Tran et al., 1988).
Another factor that may be implicated in the time taken to achieve puberty by Zebu heifers
is the tropical climate (Chenoweth, 1994). Even though Zebu heifers are thermally adapted,
changes in follicular dynamics, expressed as reduced follicular growth rate and increased
follicular growth duration, were associated with increased body temperature during summer
(Gama Filho et al., 2002). Cows need to be cooled as efficiently as possible during summer
in order to improve fertility (Wolfenson et al., 2000). High temperatures influence age at
puberty either by affecting circulating LH or prolactin levels and growth rate. Although
cattle are not considered to be seasonal breeders, a study of Bos taurus (Schillo et al., 1983)
demonstrated that season of birth and attainment of puberty influenced age at first ovulation
in heifers. In a subtropical climate, heifers with a large proportion of Zebu genes showed
a direct effect of photoperiod upon the regulation of ovulatory activity but this effect was
absent in Bos taurus cattle (Mezzadra et al., 1993).
Some pharmacological approaches can cause a decrease in age at first conception. Treatment with norgestomet and PMSG can reduce age at first conception in Bos indicus heifers
(Narasimha Rao et al., 1986). Ivermectin treatment also hastened puberty independent of
weight gain in beef heifers (Larson et al., 1995). Monthly bST treatment from 7 to 12
months of age in Nellore heifers altered muscle fiber diameter but did not affect weight gain
or sexual precocity (Moreira et al., 2000).
5. Bos indicus crossbred cattle
Zebu cattle are known to be less fertile and have lower levels of milk production than Bos
taurus breeds, but their better adaptation to the environmental conditions make them more
likely to reproduce successfully in the tropics. Crossbreds incorporate the environmental
adaptation of Zebu cattle and the productivity of Bos taurus (Negussie et al., 1999) and
exhibit a high degree of hybrid vigor. Bos indicus cattle were imported to North America for
crossbreding purposes in order to exploit these characteristics and some of these crossbreds
were “fixed” to produce a new hybrid breed of cattle (Cartwright, 1980). A good example
of the outcome of this process is the Brahman which, although considered to be a Zebu,
is a mixture of the Guzerat, Nellore and Gir breeds with a small genetic contribution from
European breeds that were used in the grading up process (Sanders, 1980). The additive
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effect can be seen in the age at first ovulation which decreases from 22 to 15 months in Zebu
× Bos taurus cattle (Galina and Arthur, 1989). Even in purebred Zebu in South America,
there seems to be a contribution from taurine matrilineages characterized by the presence of
Bos taurus mtDNA (Meirelles et al., 1999) but it is impossible to say when this contribution
was introduced.
Crossbred females that were 1/2 Chianina–Zebu showed earlier precocity and had higher
growth potential than 3/4 Zebu–Chianina animals (Silva and Pereira, 1986). Increasing
the proportion of Bos indicus genes in the mixture was accompanied by a decrease in
productivity (weaning rates) in crossbred heifers kept in a sub-tropical climate (Rocha and
Lobato, 2002). An experiment in Argentina compared purebred with crossbred cattle and
observed earlier puberty in the crossbred animals (Mezzadra et al., 1993). Using crossbred
heifers, Garcia et al. (2002) found that body weight accounted for most of the variation
associated with the onset of puberty followed by the contribution of circulating leptin
concentrations, which increased during a period of 16 weeks before first ovulation.
Early puberty in crossbreds can be attributed to heterosis even where appropriate feed
supplementation is practiced after weaning (Mezzadra et al., 1993; Marson et al., 2001).
Nutrition, however, is a limiting factor because hybrids (5/8 Charolais and 3/8 Zebu) when
fed the same low quality forage, reached puberty at the same age as Zebu cattle (Alencar et
al., 1987).
Some crosses (Red Angus and Simmental × Nellore) have greater production efficiency
at weaning than others (Marchigiana or Guzerat × Nellore) with the higher additive effect
occurring when Bos indicus genes were combined with those from Bos taurus cattle (Perotto
et al., 2001). Restle et al. (1999) showed a heterosis of −12.8 to age and weight at puberty
from hybrid Charolais and Nellore compared to purebreds.
6. Bos indicus males
Puberty in males may be defined as the age at which production of the first ejaculate
with at least 50 × 106 sperm with 10% progressive motility occurs. Under the conditions
experienced in Mexico, Brahman (Bos indicus) males attained puberty between 16 and 17
months of age. Serum testosterone levels prior to puberty seemed to increase in a pattern
similar to Bos taurus but occurred at a later age (Silva-Mena, 1995). Zebu bulls have slower
testicular development and tend to reach puberty later than Bos taurus thus mimicking the
sexual maturity of heifers of this genotype. Heat stress and the quality of available feeds
may contribute to these attributes of males (Galina and Arthur, 1991). Zebu bulls were
heavier and older at puberty and had a lower libido score than Bos taurus animals but
there was no difference in the LH secretion induced by administration of GnRH (Chase
et al., 1997). It seems that the lower reproductive efficiency of Zebu cattle is not only due
to physiological limitations. Nellore bulls that received supplementary food were heavier
with a larger scrotal circumference and higher circulating concentrations of testosterone
and IGF1, demonstrating an interrelationship among reproductive variables and factors that
enhance growth (Costa, 1999).
It is possible to distinguish between postpubertal and prepubertal Nelore bulls at 18
months of age by evaluating circulating testosterone levels. Pinho et al. (1999) showed that
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testosterone concentration was related to scrotal circumference and was higher in bulls with
dense semen than in those that were oligospermic and azoospermic.
7. Conclusions
Puberty in Zebu cattle is a problem that affects their productivity by causing them to
calve first at a late age. Genetic improvement for this characteristic is possible because age
at puberty has a high heritability in these animals. Consequently, heifers selected according
to age at first calving will produce offspring that exhibit puberty at an early age. Another
genetic approach is to crossbreed Zebu with Bos taurus cattle to produce a hybrid that will
have a lower age at puberty. The effect of nutrition is also important and improvements in
this factor, and in other management variables, result in the earlier achievement of puberty.
In summary, genetic selection, crossbreeding and nutrition are all approaches that can be
used to reduce the age at first calving in Zebu heifers.
Acknowledgements
Fundação de Amparo à Pesquisa do Estado de São Paulo (#99/10446-7) and Conselho
Nacional de Desenvolvimento Cientı́fico e Tecnológico (#300211/00-7) are thanked for
financial support.
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