www.elsevier.comrlocateranireprosci
Influence of bull biostimulation, season and parity
on resumption of ovarian activity of zebu
ž
Bos indicus cattle following parturition
/
P.I. Rekwot
a,), D. Ogwu
b, E.O. Oyedipe
aa
Artificial Insemination Unit, National Animal Production Research Institute, Ahmadu Bello UniÕersity, Zaria, Nigeria
b
Department of Surgery and Medicine, Faculty of Veterinary Medicine, Ahmadu Bello UniÕersity, Zaria, Nigeria
Received 14 June 1999; received in revised form 11 January 2000; accepted 11 April 2000
Abstract
A total of 135 postpartum suckled zebu cows were assigned randomly at calving to two
Ž .
treatments: cows exposed to vasectomised bulls Mature Bull Exposure, MBE and cows not
Ž .
exposed to bulls No Bull Exposure, NBE for a period of 150 days postpartum. This study was conducted to determine the influence of bull biostimulation, season and parity on postpartum reproductive performance of Bos indicus cattle. The trials were conducted in two seasons: cows calving in the dry season and cows calving in the rainy season. Cows with an increase in serum
Ž .
progesterone P4 concentration of )1 ngrml from the weekly blood samples were used to analyse the number of days from calving to the time of resumption of ovarian activity. The introduction of vasectomised bulls shortened the postpartum anoestrus in cattle following calving. Mean interval from calving to resumption of ovarian activity for the MBE cows was 71.7 days, which was significantly earlier following calving than the NBE cows with a duration of 77.8 days. By 60 to 80 days postpartum, the proportion of cows at resumption of postpartum activity for MBE cows was greater than for the NBE cows.
Mean interval from calving to resumption of ovarian activity for cows that calved in the dry season was 71.3 days, which was significantly earlier than for cows that calved in the rainy season
Ž78.6 days . At 60 days postpartum, the proportion of cows at resumption of postpartum ovarin.
activity for cows that calved in the dry season was greater than the cows that calved in the rainy season. Mean interval from parturition to resumption of ovarian activity for cows with three to five calvings was 65.1 days, which was significantly earlier than the value of 71.2 days for cows
)Corresponding author. Tel.:q234-69-551681; fax:q234-69-51272.
Ž .
E-mail address: rekwot@abu.edu.ng P.I. Rekwot .
0378-4320r00r$ - see front matterq2000 Elsevier Science B.V. All rights reserved. Ž .
with one to two calvings. By 60 to 80 days postpartum, the proportion of cows at onset of ovarian activity for cows with three to five calvings was greater than those cows with one to two calvings. Cows that calved in the dry season completed uterine involution by 24.4 days, which was significantly shorter than the duration of 26.5 days for cows that calved in the rainy season. Cows with three to five calvings completed uterine involution earlier than those with one to two calvings. It is concluded that bull–cow biostimulation influences reproductive activity in the cow
Ž .
possibly through olfactory cues pheromones .q2000 Elsevier Science B.V. All rights reserved.
Keywords: Biostimulation; Season; Parity; Postpartum ovarian activity; Zebu cattle
1. Introduction
Reproductive performance is one of the major and most important factors determin-ing the profitability of cattle herds, with the ideal goal to be achieved bedetermin-ing one calf per cow per year. Reduced calving rates and long calving intervals associated with cattle indigenous to tropical Africa have been serious constraints to the cattle industry
ŽOyedipe et al., 1980; Eduvie, 1985 . A calving to conception interval of not more than. Ž
80–85 days is required in order to obtain one calf per cow per year Louca and Legates,
.
1968 . In some countries, this interval is invariably prolonged as a result of prolonged suckling period, nutritional deficiencies, climatic stresses, season, parity, suboptiomal
Ž . Ž .
management and poor husbandry practices Eduvie, 1985 . Eduvie 1985 reported that postpartum ovulation occurred earlier in cows that had calved more than twice compared to cows that calved two or less times. Calving intervals for cows calving in the dry
Ž
season are shorter than for those calving in the rainy season Oliveira, 1974; Oyedipe et
.
al., 1982 .
Biostimulation is the term coined to describe the stimulatory effect of a male on oestrus and ovulation through genital or pheromonal stimulation, or other less
well-de-Ž .
fined external cues Chenoweth, 1983 . Pheromones are air-borne chemical substances orAsignalsB released in the urine or feces of animals or secreted from cutaneous glands that are perceived by the olfactory system and that elicit both behavioural and endocrine
Ž . Ž .
responses in conspecifics Doty, 1976 . The vomeronasal organ VNO is a bilateral blind sac that opens into the incisive duct or nasopalatine canal, and has been implicated as a specialised chemoreceptor involved in the detection of oestrus and in the release,
Ž .
control and coordination of sexual activity Estes, 1972; Wysocki, 1979; Johns, 1980 . In domestic animals, priming pheromones from the male have an influence on the induction of puberty, the termination of seasonal anoestrus and shortening of postpartum
Ž .
anoestrus Izard, 1983 .
Ž .
The duration of postpartum anoestrus in multiparous pluriparous and primiparous
Ž
cows was decreased when cows were exposed to bulls following parturition Zalesky et
.
al., 1984; Gifford et al., 1989 . The influence of a sterile bull on puerperium and fertility in dairy cattle has been reported indicating that the use of a sterile bull could improve
Ž .
fertility Ebert et al., 1972 . The first increase in progesterone, which indicated onset of oestrous cycles occurred at 43 vs. 63 days postpartum in cows exposed and not exposed
Ž .
to bulls, respectively Zalesky et al., 1984 . The same authors reported that a high
Ž .
no exposure groups, respectively. The effect of a sterile bull on ovarian and behavioural activity of suckling beef cows indicated that in the group with the sterile teaser bull present, the proportion of cows in which oestrus and ovulation was detected was higher
Ž .
than in the control group Alberio et al., 1987 . The presence of a male causes more intense stimulation, which decreases the rate of ovulation without expression of
be-Ž .
havioural oestrus Ayalon and Weis, 1970; Ebert et al., 1972; Foote, 1974 .
Ž .
Effects of biostimulation exposure to bulls or testosterone treated cows on various reproductive variables in suckled cows indicated that cows exposed to bulls immediately
Ž
after calving returned to oestrus earlier than cows isolated from bulls Burns and Spitzer,
. Ž .
1992 . Recently, Bolanos et al. 1997 reported that bull and cow biostimulation
effectively enhanced resumption of ovarian activity in 60 anoestrus suckled zebu cows
ŽBos indicus in Costa Rica. The presence of the male stimulates postpartum reproduc-.
tive activity, and that response can be modified effectively by the nutritional condition
Ž
of the postpartum cows Alberio et al., 1987; Zalesky et al., 1984; Gifford et al., 1989;
.
Monje et al., 1982; Stumpf et al., 1992 . Cows pastured with yearling or mature bulls initiated oestrous cycles 12 days earlier than cows isolated from bulls after calving, indicating that biostimulatory effect of bulls on resumption of postpartum ovarian activity of cows is independent of the age of the bulls after they have reached 1 year of
Ž .
age Cupp et al., 1993 . There has been little or no documented information on the biostimulatory influences of bulls on resumption of postpartum ovarian activity in B.
indicus cattle. Therefore, the purpose of the present study was to determine the influence
of bull biostimulation, season and parity on onset of postpartum ovarian function following parturition in B. indicus cattle.
2. Materials and methods
2.1. Location
Ž .
This study was conducted using postpartum cows ns135 at the National Animal
Production Research Institute, Shika, Ahmadu Bello University, Zaria, Nigeria. The
Ž .
study location, Shika, has two distinct seasons: dry season November to April and
Ž .
rainy season May to October . Daily minimum and maximum temperatures range from
10.58C to 23.58C and 26.38C to 37.88C, respectively. Average annual minimum and
maximum temperatures were 17.78C and 31.58C, respectively. During the harmattan
period, daily temperatures range from 10.58C to 23.58C with a relative humidity of
28.8%. Relative humidity during the rainy season was 67.6%. Mean duration of day
Ž
light per day was 11.5 h. Average monthly rainfall for the rainy season May to
.
October was 153.2 mm with a range of 32.4 to 300.8 mm. The dry season was characterised by total lack of rainfall from November to April.
2.2. Experimental cows
A total of 135 postpartum suckling Zebu cows were assigned randomly at calving to
Ž
. Ž .
Bull Exposure, MBE or were not exposed to bulls No Bull Exposure, NBE from the time of calving to 150 days postpartum. Cows were placed with or isolated from bulls within 48 h after calving. The two treatment groups were placed in two different paddocks separated by a distance of 0.8 km.
The trials were conducted out in two seasons; cows calving in the dry season
ŽNovember to April and cows calving in the rainy season May to October for a period. Ž .
of 2 years. In the first trial, a total of 68 postpartum cows consisting of 35 and 33 suckling cows were used for the rainy and dry season experiments, respectively. The rainy season trials consisted of 18 MBE and 17 NBE cows, while the dry season consisted of 16 MBE and 17 NBE cows. In the second trial, a total of 67 postpartum suckling cows consisting of 35 and 32 cows were used for the rainy and dry seasons
Ž .
experiments, respectively. The former rainy seasons experiments consisted of 17 MBE and 18 NBE cows, while the dry season consisted of 16 MBE and 16 NBE cows. Thus, in the rainy season trials, a total of 70 cows consisting of 35 MBE and 35 NBE cows were used, while the dry season trials had a total of 65 cows consisting of 32 MBE and 33 NBE cows, bringing the total number of postpartum cows in the study to 135. The
Ž . Ž
135 cows were comprised of 61 cows three to five calvings; P1 and 74 cows one to
.
two calvings; P . In all the trials, randomization of the experimental cows was2
accomplished by a pair-wise procedure that involved randomly assigning the first cow that calved to either the MBE or NBE treatment groups. The next cow that calved was assigned to the alternate treatment and this procedure was repeated for each successive pair until a total of 67 and 68 postpartum cows for the MBE and NBE treatment groups, respectively, were assigned.
2.3. Management of postpartum cows
The experimental cows in the MBE and NBE treatments were maintained in improved pasture paddocks separated by a distance of 0.8 km to minimize influence of exteroceptive stimuli associated with each other. In addition to grazing improved sown
Ž .
pasture fields Stylosanthes, Brachiaria and Digitaria , the cows were given supplemen-tary concentrates consisting of maize and cotton seedcake of about 1–2 kg per cow per day. Cows were also given baled hay, free access to a salt lick and water ad libitum throughout the experimental period. All cows were ear-tagged with large plastic ear tags
ŽRitchey Europe, Yorkshire, England to enable identification of the cows from a.
distance during observations for detection of oestrus. Before commencement of the study, the cows were screened for blood and helminth parasites and appropriate treatments and vaccination against endemic diseases were performed.
2.4. Body measurements
Cows were weighed and body condition scored within 72 h of calving. Cows were subsequently weighed every 4 weeks until onset of ovarian activity or day 150 postpartum. Cows were body condition scored using a scale of 0 to 5 from the most
Ž .
at the start of the experiments for cows calving in the dry and rainy seasons were 303.1"8.6 and 300.6"7.6 kg, respectively.
2.5. Assessment of the reproductiÕe tract
Postpartum cows were rectally examined for functional reproductive status according
Ž .
to the method of Zemjanis 1970 . Briefly, this involves retraction and subsequent examination and evaluation of the tubular genitalia and ovaries. Following parturition, rectal examination of the genitalia was conducted every 3 days until involution was considered complete and then weekly, until oestrus was detected or 150 days postpar-tum. Involution of the uterus was recorded as being complete when the uterus and its
Ž
contents were easily retractable and palpable within the pelvic cavity Custer et al.,
.
1990 .
2.6. Detection of oestrus and blood sampling
Postpartum detection of oestrus began 10 days after the first cow was assigned to any of the treatments. In both the MBE and NBE groups, cows were observed visually for signs of oestrus twice daily between 0730 and 0830 hours and 1730 and 1830 hours by herdsmen and inseminators. Vasectomised bulls were harnessed with chin-ball mating
Ž .
device containing red paint The Great Outdoor, New Zealand to aid in the detection of oestrus. Blood samples were collected from cows after parturition from the jugular vein once a week during the 150 d experimental period. Blood samples were placed immediately on ice and allowed to clot for 24 h. Serum was separated then by
centrifugation at 3000 rpm for 15 min and stored at y208C until concentrations of
Ž .
progesterone P4 were determined by radioimmunoassay.
Serum P concentrations were determined using a no-extraction,4 ACoat A CountB
Ž .
solid-phase P , RIA kit Bergfeld et al., 1996 . The sensitivity of the assay, defined as4
twice the standard deviation away from the zero standard was 0.075 ngrml. The within
and between assay coefficients of variation was 7.4% and 8.6%, respectively. An
increase in serum P concentration of4 )1 ngrml for two consecutive weekly samples
was taken to indicate the presence of functional luteal tissue, and this was used to
Ž
characterize resumption of postpartum ovarian activity or estrous cycles Oyedipe et al.,
.
1986 .
2.7. Statistical analyses
The number of days from parturition to initiation of cyclic ovarian function was calculated for individual cows by subtracting the date of parturition from the date at which the first rise of P or first onset of ovarian activity was detected. Cows with an4
increase in serum progesterone concentration of )1 ngrml from the weekly blood
samplings were used to statistically analyse the number of days from parturition to the time of resumption of ovarian activity. Presence of bulls, season and parity of postpar-tum cows were the main effects, while interval to completion of uterine involution, interval to resumption of ovarian activities, and liveweight changes as dependent
Ž .
Proportion of postpartum cows that exhibited cyclic ovarian activities after calving were analyzed using the Categorical Data Modelling.
3. Results
Proportion of cows and intervals at completion of uterine involution for MBE and
Ž .
NBE cows were not different P)0.05; Tables 1 and 2 . At 20 and 30 days postpartum,
the proportion of cows having complete uterine involution for cows calving in the dry
Ž .
season was greater than those of the rainy season P-0.05; Table 1 . Cows that calved
in the dry season completed uterine involution by 24.4 days, which was earlier than the
Ž .
duration of 26.5 days for cows that calved in the rainy season P-0.05; Table 2 . It
was observed that for the first 20 days postpartum, the proportion of cows with complete
Ž .
uterine involution for the cows with three to five calvings P1 and cows with one to two
Ž .
calvings P2 groups, were 18.0% and 5.4%, respectively, with a difference in favour of
Ž . Ž .
the former Table 1 . Cows with three to five calvings P1 had completed uterine
involution by 24.1 days, which was earlier than the duration of 26.8 days for cows with
Ž .
one to two calvings P ; P2 -0.05; Table 2 .
At 60 days postpartum, the proportion of cows at resumption of ovarian activity for
Ž
MBE cows was 25.4%, which was greater than the value of 14.7% for NBE cows Table
.
1 . Subsequently, by 80 days postpartum, the proportion of cows resuming of postpar-tum luteal activity for the MBE and NBE group were 53.7% and 35.3%, respectively
ŽTable 1 . Mean interval from parturition to resumption of ovarian activity for MBE.
Ž .
cows was 71.7 days, earlier than the duration of 77.8 days for NBE cows Table 2 . At 60 days postpartum, the proportion of cows resuming postpartum ovarian activity that
Ž .
calved in the dry season 27.7% was greater than cows calving during the rainy season
Table 1
Effect of season of calving, biostimulation and parity on postpartum resumption of cyclic ovarian function
Ž .
Period days postpartum Season of calving Bull biostimulation Parity
Rainy Dry MBE NBE P1 P2
ns70 ns65 ns67 ns68 ns61 ns74
Proportion of cows with uterine inÕolution
a b b a
10–20 4.5 18.5 9.0 13.2 18.0 5.4
b a a b
21–30 55.1 44.9 80.6 77.9 75.4 82.4
b a a b
31–40 11.4 7.7 10.4 8.8 6.6 12.2
Proportion of cows with resumption of oÕarian actiÕity
a b b a b b
40–60 12.9 27.7 25.4 14.7 24.6 16.2
b a b a
61–80 44.3 44.6 53.7 35.3 49.2 40.5
b a a b a b
81–100 37.1 20.0 16.4 41.2 21.3 35.1
101–130 5.7 7.7 4.5 8.8 4.9 8.1
a,b
Data in rows within each treatment group with different letter superscripts are significantly different
Table 2
Intervals from calving to manual detection of uterine involution and resumption of cyclic ovarian activity
Ž .
Treatment No. of cows Interval days from calving to:
Uterine involution Resumption of ovarian activity
Biostimulation
Data within treatment groups with different letter superscripts are significantly different P-0.05 .
Ž12.9%; Table 1 . Mean interval from calving to resumption of ovarian activity for cows.
that calved in the dry season was 71.3 days, which was shorter than for cows that calved
Ž .
in the rainy season 78.6 days; P-0.05; Table 2 .
At 60 and 80 days postpartum, the proportion of cows with resumption of postpartum
Ž .
ovarian activity for cows with three to five calvings P1 were greater than those cows
Ž .
with one to two calvings P ; Table 1 . Mean interval from parturition to resumption of2
ovarian activity for P cows was 65.1 days, which was earlier than the value of 71.21
Ž .
days for P cows P2 -0.05; Table 2 . Interactions between biostimulation and parity;
Ž .
season and parity were significant P-0.05 for uterine involution and resumption of
ovarian activity. Cows that calved in the dry season that were either P or P resumed1 2
ovarian activity earlier than cows that calved in the rainy season. Bull-exposed cows
Table 3
Mean liveweight changes and body condition scores from calving to 150 days postpartum Season of calving n Days postpartum
with three to five calvings resumed ovarian activity earlier than bull-exposed cows with
Ž .
one to two calvings or non-exposed cows that were either P or P1 2 P-0.05 .
Mean liveweight changes and body condition scores from calving to 150 days
Ž .
postpartum are shown Table 3 . In both seasons, all postpartum cows lost liveweight and condition for the first 28 to 56 days postpartum. Cows that calved in the dry season, however, regained body weight and body condition from day 56 to day 84 postpartum, earlier than the cows that calved in the rainy season.
4. Discussion
The results of this study indicate that exposure of postpartum cows to vasectomised
Ž .
bulls biostimulation can shorten the length of postpartum anoestrus. This is in
Ž . Ž .
agreement with the reports of Zalesky et al. 1984 and Naasz and Miller 1987 who have shown that resumption of oestrous cycles was advanced by exposing mature cows to bulls during the early postpartum period. The reported values in favour of the bull-exposed cows in this study appear lower but certainly show a similar trend to the
Ž .
findings of Zalesky et al. 1984 . The latter authors documented that a greater
percent-Ž .
age 89% vs. 18% of cows were in oestrus in the bull-exposed group than the
non-exposed group. Bull–cow interaction can influence reproductive activity through
Ž .
olfactory cues or pheromones Izard, 1983; Izard and Vandenbergh, 1982a,b . Biostimu-lation in this study exerted its stimulatory effects between 50 and 80 days postpartum as
Ž .
previously reported Burns and Spitzer, 1992 .
It is evident that cows that calved in the dry season which were also exposed to vasectomised bulls, completed uterine involution and resumed ovarian activity earlier than the other treatments groups of season and biostimulation; this corroborates the work
Ž .
of Stumpf et al. 1987 . The findings of this study show that intervals from calving to completion of uterine involution, and resumption of ovarian activity were shorter in cows that calved in the dry season than cows that calved in the rainy season, probably because the former regained more body weight than the latter. The above findings are in
Ž .
agreement with the work of Dawuda et al. 1988 , who reported that the mean intervals from calving to first oestrus were 152.8 and 129.9 days for cows that calved during the rainy and dry seasons, respectively. Similarly, the mean interval for cattle calving in the
Ž
wet season was 82 days longer than that of cattle calving in the dry season Oyedipe et
.
al., 1982 . These previous and present observations suggest that cows calving in the dry season usually take advantage of the abundant availability of crop residues during the
Ž .
early dry season November–February and the improved regrowth and abundant lush
Ž .
pasture of the early rains April–May to meet their total requirements for maintenance, growth and reproduction. In the rainy season, these pastures mature and become nutritively poor and are usually heavily contaminated by ticks, helminths and other parasites, thus negatively impeding normal reproductive processes. The high level of feeding after calving can shorten the calving interval. Fertility of grazing cattle is closely related to the liveweight change during the calving to service interval and the animal is only likely to become sexually active after it has regained much of its body weight.
A greater proportion of P cows in the present study completed uterine involution and1
Ž .
lation and parity favoured MBE cows with three to five calvings P , which resumed1
ovarian activity earlier than other treatment groups of biostimulation and parity. These
Ž .
results support the findings of Eduvie 1985 , who reported that first postpartum
ovulation occurred earlier in cows which had more than two calvings or were over 5
Ž . Ž .
years old 50.8 days , than those with one or two calving s or that were 3.5 years old
Ž68.9 days . It was observed that the intervals for uterine involution and resumption of.
ovarian activity were earlier for P cows than those of P cows. This finding is in1 2
Ž .
agreement with the study of Plasse et al. 1972 , who reported that calving interval was
Ž .
longest in primiparous cows and shortest in pluriparous older cows. The present
Ž .
findings also corroborate the study of Gifford et al. 1989 , who reported that primi-parous cows tend to have a longer postpartum anoestrus than multiprimi-parous cows, and that exposure of postpartum cows to bulls immediately after calving reduced anoestrus to a greater extent than for the control group.
A rapid or short pre-oestrus increase of progresterone in postpartum suckled cows has been reported and may act to prime an endocrine system that has been acyclic during
Ž .
gestation and after calving Humphery et al., 1983 . If this is so, then the pre-oestrus progesterone increase associated with bull exposure may shed light on the mechanism of
Ž .
the Abull effectB in postpartum cows Custer et al., 1990 . There is the possibility that the effect of the bull on resumption of cyclic ovarian activity is mediated via the central
Ž
nervous system by stimulating LH release immediately following exposure Custer et
.
al., 1990 . The results of this study indicate that exposure of postpartum cows to
Ž .
vasectomised bulls biostimulation shortens the length of postpartum anoestrus. Re-sumption of ovarian activity was earlier following calving in cows that calved in the dry
season than cows that calved in the rainy season. There was a greater proportion of P1
cows with completion of uterine involution and onset of ovarian activities than P cows2 during early days postpartum. The exact nature of the cues transmitted from the bull and perceived by the cow during the bull–cow interactions are not clearly known. Exterocep-tive cues that likely have a role in male–female interactions include olfactory, visual and
Ž .
auditory stimuli Zalesky et al., 1984 . It is concluded that bull–cow biostimulation does
Ž .
influence reproductive activity in cows possibly through olfactory cues pheromones . However, the role of different levels of nutrition and the interactions with biostimulation would require further investigation.
Acknowledgements
The authors express their sincere gratitude to the International Atomic Energy Agency, Vienna, Austria for the supply of the RIA kits. The assistance of all the inseminators and herdsmen of the Artificial Insemination Unit is acknowledged. We are thankful to the Director, NAPRI for permission to published this work.
References
Alberio, R.H., Schiersmann, G., Carou, N., Mestre, J., 1987. Effect of a teaser bull on ovarian and behavioural activity of suckling beef cows. Anim. Reprod. Sci. 14, 263.
Bergfeld, E.G.M., Kojima, F.N., Cupp, A.S., Wehrman, M.E., Peters, K.E., Mariscal, V., Sanchez, T., Kinder, J.E., 1996. Changing dose of progesterone results in sudden changes in freqency of LH pulses and secretion of 17b-oestradiol in bovine females. Biol. Reprod. 58, 546–551.
Bolanos, T.M., Forsberg, M., Kindahl, H., Rodriguez-Martinez, H., 1997. Biostimulatory effects of estrus
Ž .
cows and bulls on resumption of ovarian activity in postpartum zebu Bos indicus cows in the humid tropics. Anim. Reprod. Sci. 48, 180–195.
Burns, P.D., Spitzer, J.C., 1992. Influence of biostimulation on reproduction in postpartum beef cows. J. Anim. Sci. 70, 358–362.
Chenoweth, P.J., 1983. Reproductive management procedures in control of breeding. Aust. J. Anim. Prod. 15, 28–33.
Cupp, A.S., Roberson, M.S., Stumpf, T.T., Wolfe, M.W., Werth, L.A., Kojima, N., Kittok, R.J., Kinder, 1993. Yearling bulls shortened the duration of postpartum anoestrus in beef cows to the same extent as do mature bulls. J. Anim. Sci. 71, 306–309.
Custer, E.E., Berardinelli, J.G., Short, R.E., Wehrman, M., Adair, R., 1990. Postpartum interval to estrus and patterns of LH and progesterone in first-calf suckled beef cows exposed to mature bulls. J. Anim. Sci. 68, 1370–1377.
Dawuda, P.M., Esievo, K.A.N., Eduvie, L.O., Molokwu, E.C.I., 1988. Interval between calving and first observable oestrus in postpartum Bunaji cows. Br. Vet. J. 144, 258–261.
Doty, R.L., 1976. Mammalian Olfaction, Reproductive Processes and Behaviour. Academic Press, New York. Ebert, J.J., Conteras, P., Saelzer, P., 1972. Influence of a teaser bull on puerperium and fertility in dairy cows. 8th International Congress on Animal Reproduction and Artificial Insemination, Munich 3, 1743–1748. Eduvie, L.O., 1985. Factors affecting postpartum ovarian activity and uterine involution in zebu cattle
indigenous to Nigeria. Anim. Reprod. Sci. 8, 123–128.
Estes, R.D., 1972. The role of the vomeronasal organ in mammalian reproduction. Mammalia 36, 315–318. Foote, R.H., 1974. Estrus detection and oestrus detection aids. J. Dairy Sci. 58, 248–250.
Gifford, D.R., D’Occhio, M.J., Sharpe, P.H., Weatherly, T., Pittar, R.Y., Reeve, D.V., 1989. Return to cyclic ovarian activity following parturition in mature cows and first-calf heifers exposed to bulls. Anim. Reprod. Sci. 19, 209–212.
Humphery, W.D., Kaltenbach, C.C., Dunn, T.G., Koritnik, D.R., Niswender, G.D., 1983. Characterization of hormonal patterns in the beef cow during postpartum anestrus. J. Anim. Sci. 56, 445–448.
Ž .
Izard, M.K., 1983. Pheromones and reproduction in domestic animals. In: Vandenbergh, J.G. Ed. , Pheromones and Reproduction in Mammals. Academic Press, New York, pp. 253–285.
Izard, M.K., Vandenbergh, J.G., 1982a. Priming pheromones from oestrus cows increase synchronization in dairy heifers after PGF alpha injection. J. Reprod. Fertil. 66, 189–192.2
Izard, M.K., Vandenbergh, J.G., 1982b. The effects of bull urine on puberty and calving date on crossbred beef heifers. J. Anim. Sci. 55, 1160–1168.
Johns, M.A., 1980. The role of vomeronasal system in mammalian reproductive physiology. In:
Muller-Ž .
Schwarze, D., Silverstein, R.M. Eds. , Chemical Singals: Vertebrates and Aquatic Invertebrates. Plenum, New York, pp. 341–364.
Louca, A., Legates, J.E., 1968. Production losses in dairy cattle due to days open. J. Dairy Sci. 51, 573–583. Monje, A.R., Alberio, R., Schiersmann, G., Chedrese, P.J., Carou, N., Callejas, S.S., 1982. Male effect on the postpartum sexual activity of cows maintained in two nutritional levels. Anim. Reprod. Sci. 29, 145–156. Naasz, C.D., Miller, H.L., 1987. Effect of bull exposure on postpartum interval and reproductive performance
in beef cows. J. Anim. Sci. 65, 426–428.
Oliveira, F.E.B., 1974. Age at first calving, service period and calving interval in a Nellore herd. Anim. Breed. Abstr. 43, 5799.
Oyedipe, E.O., Buvanendran, V., Eduvie, L.O., 1982. Some factors affecting the reproductive performance of
Ž .
Bunaji cattle. Trop. Agric. Trinidad 59, 231–234.
Oyedipe, E.O., Osori, D.I.K., Jagun, A.G., Tunde, B., Eduvie, L.O., 1980. Postpartum uterine involution and resumption of ovarian activity in Bunaji and Friesian X Bunaji cows as determined by rectal palpation. Niger. J. Anim. Prod. 7, 112–116.
Plasse, D., Pena, N., Verde, O., Koger, M., Linares, T., 1972. Influences ambietales sobre la variancia de intervalos entre partos en Brahman registrado. Mem. - Asoc. Latinoam. Prod. Anim. 7, 47–50.
SAS, 1990. General linear model, S.A.S. User’s Guide. SAS Institute, Cary, NC.
Stumpf, T.T., Wolfe, W.M., Wolfe, P.L., Day, M.L., Kittok, R.J., Kinder, J.E., 1987. Interaction of bull
Ž
exposure and level of nutritional intake on the duration of postpartum anoestrus. J. Anim. Sci. 65 Suppl.
.
1 , 4–8.
Stumpf, T.T., Wolfe, W.M., Wolfe, P.L., Day, M.L., Kittok, R.J., Kinder, J.E., 1992. Weight changes prepartum and presence of bulls postpartum interact to affect duration of postpartum anoestrus in cows. J. Anim. Sci. 70, 3133–3137.
Wysocki, C.J., 1979. Neurobehavioural evidence for the reproduction. Neurosci. Behav. Rev. 3, 301–315. Zalesky, D.D., Day, M.L., Garcia-Winder, M., Imakawa, K., Kittok, R.J., D’Occhio, M.J., Kinder, J.E., 1984.
Influence of exposure to bulls on resumption of estrous cycles following parturition in beef cows. J. Anim.
Ž .
Sci. 59 5 , 1135–1139.
