J. Anim. Sci. 2003. 81:2669-2674
© 2003 American Society of Animal Science
The male effect, mounting behavior, and the onset of estrus in farmed muskoxen1
J. E. Rowell2,*,
,
M. C. Sousa*, and
M. P. Shipka*,
* School of Natural Resources and Agricultural Sciences and
and
Institute of Arctic Biology, University of Alaska Fairbanks, Fairbanks 99775-7200 and
and
Center for Reproductive Biology, Washington State University, Pullman
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Abstract
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Muskox farming is an emerging industry in Alaska. For such an endeavor to succeed, it is necessary to develop fundamental husbandry tools specifically for this species. This study examined the role of the bull in the onset of seasonal ovarian activity and the synchrony of estrus and tested the efficacy of a radiotelemetric estrus detection system. Twenty parous female muskoxen, ranging in age from 4 to 15 yr, were divided into three groups (balanced by age and body weight). Groups received early bull exposure (EBE; August 1, n = 7), late bull exposure (LBE; August 22, n = 6), or remained physically isolated from a bull (NBE; n = 7). Just before bull introduction, radiotelemetry transmitters were attached to the rump of muskox cows in the EBE and LBE groups. Plasma samples were collected from all the cows twice weekly and analyzed for progesterone (P4). The mean date of onset of seasonal ovarian activity was earlier in the EBE and LBE groups than in the NBE group (P < 0.001) and was earlier in EBE (P < 0.021) than in LBE. All EBE and LBE cows conceived to the first fertile cycle, giving 100% fertility. The time interval for the onset of ovarian activity between the first and last cow within each group was 7 d in the EBE group, 12 d in the LBE group, and 24 d in the NBE group. Radiotelemetry correctly identified estrus 95% of the time (18 of 19 instances). Mean length of estrus for each cow, calculated from the time of first mount until last mount, was 771 ± 98 min (range = 4 to 1,508 min). Mean number of mounts during estrus was 8.89 ± 1.29 (range = 3 to 25 mounts). Length of estrus at the first short cycle did not differ from the length of the first fertile estrus between, or within, individuals. Estrous behavior was initiated more frequently during the night (2300 to 0500; P < 0.05). Bull introduction can be used as a simple, low-cost management tool for synchronizing estrus in farmed muskoxen. Radiotelemetry was an effective tool for identifying breeding behavior in this species.
Key Words: Breeding Season • Detection • Estrous Cycle • Males • Ovibos moschatus
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Introduction
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Muskoxen are a natural species for farming in Alaska. They evolved in the arctic, adapt well to basic husbandry practices, and produce a luxurious fiber called qiviut (Rowell et al., 2001
). The morphology of the female reproductive tract and the cyclic pattern of steroid and gonadotropin secretion are similar to those in domestic sheep and goats (Rowell et al., 1987; Rowell and Flood, 1988; Rowell et al., 1993). Muskoxen breed from mid-August through September. The onset of the breeding season is characterized by a short (8 to 10 d) cycle, followed immediately by an estrous cycle of normal length, 18 to 21 d (Rowell and Flood, 1988).
Although muskoxen are similar to sheep and goats in many respects, some of their differences have serious impacts on management. The detection of estrus in muskoxen is difficult. Cows rarely exhibit behaviors such as mounting conspecifics or standing to be mounted, and the use of a vasectomized bull met with variable success (Rowell, 1991). A common practice in muskox farming is to maintain cows and bulls separately, except during the breeding season. Harems are formed anywhere from early August to early September and are usually left together for at least six wk (White et al., 1998). During this time, rutting bulls are very aggressive, dangerous to handle, and destructive to property. Thus, bull management and controls over the breeding season are high priorities for successful muskox farming.
The phenomenon of the male effect is well documented in sheep and goats (reviews: Chemineau,1987; Walkden-Brown et al., 1999; Rosa and Bryant, 2002) and recently in reindeer (Shipka et al., 2002), but there is no information about the effect of males on seasonal estrous activity in muskox cows. In this study, we investigated the impact of muskox bull introduction on the timing of seasonal ovarian activity in muskox cows and evaluated the use of a radiotelemetric estrus detection system.
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Materials and Methods
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Twenty parous female muskoxen, ranging in age from 4 to 15 yr, were divided into three groups. One group received early bull exposure (EBE) and the group was placed with a mature bull on August 1. The second group received late bull exposure (LBE) and was placed with a different mature bull on August 22. The last group remained physically isolated from any bull throughout the breeding season (NBE). Groups were balanced for weight and age (Table 1). They were maintained on free choice timothy hay and received a balanced pelleted ration (UAF ration B). Water troughs (approximately 300 L) were cleaned and filled daily. Nineteen of 20 cows had calved the preceding year and were weaned by July 15. The University of Alaska Fairbanks Institutional Animal Care and Use Committee approved all research protocols.
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Table 1. The mean age and body weight of each group of female muskoxen and the date they were introduced to the bull
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Beginning on July 24 and continuing until October 2, female muskoxen were weighed and a jugular blood sample collected twice weekly. On August 1, radiotelemetry transmitters (DDx HeatWatch, Denver, CO) were placed in pocketed patches and glued to a shaved 10- x 10-cm2 area on the rump of each muskox cow in the EBE group. The nylon webbing around the transmitter pocket was trimmed so that approximately 1 cm extended beyond the edge of the pocket. A strand of long guard hair was threaded through the webbing on each side of the pocket and knotted in order to ensure that the transmitter and patch remained in place and would not be lost if the glue failed during mounting. The EBE cows were then placed with a mature, experienced bull. Muskox cows in the LBE group had radiotelemetry transmitters similarly attached just before being placed with a second mature bull on August 22. The objective was to separate the treatments yet ensure that late bull exposure occurred before spontaneous onset of ovulation. Cows were separated from the bull for blood sampling (approximately 45 min twice weekly) but otherwise remained in their respective harems until October 2. The cows in the NBE group remained physically and visually separated from any bull throughout the study. Pregnancy in the EBE and LBE groups was confirmed by transrectal ultrasonography at approximately 60 d after breeding.
The radiotransmitters recorded estrous activity when a cow stood to be mounted. The bull’s mounting activity depressed the transmitter button, interrupting the radio signal from that transmitter. Radiotelemetric data were stored in a buffer and downloaded to a computer at least twice weekly. Individual cow ID, and time and duration of the mount were recorded.
Plasma samples were stored frozen (-20°C) until assayed for progesterone (P4) by RIA using commercial coated tube kits (Diagnostic Products Corporation, Los Angeles, CA) previously validated for muskox plasma (Rowell et al., 1997). Samples were run in four assays. Intraassay CV averaged 9.8%, and interassay CV averaged 3.0, 8.8, and 13.7% for low, medium, and high controls, respectively.
Individual animal P4 profiles were used to define the following variables a) First fertile ovulation was calculated as the date of the last plasma P4 concentration <0.5 ng/mL that preceded a sustained (
3 wk) elevation in P4 concentration (Rowell and Flood, 1988). b) A short cycle was defined as corpus luteum (CL) formation characterized by a brief elevation in P4 concentration (0.5 ng/mL) not exceeding a duration of 14 d. c) Fertility was defined as the percentage of females that successfully conceived to the first fertile ovulation. d) Group synchrony was calculated as the difference (days) between the earliest and the latest onset of ovarian activity within a group.
Individual animal radiotelemetry estrus detection data were used to define the following variables a) Standing estrus was defined as a minimum of two mounts within a 4-h period. b) Estrus refers to standing estrus recorded by radiotelemetry regardless of whether it preceded a short luteal phase or a fertile cycle.
Progesterone profiles were used to assess proximity of estrus to CL formation and ovarian activity.
Data were analyzed with Sigma Stat 2.0 (SPSS Science, SPSS Inc., Chicago, IL). The day of onset of ovarian activity between the three groups was compared using a one-way ANOVA. Time from introduction of the bull to onset of ovarian activity was compared between EBE and LBE using Student’s t-test. Breeding synchrony data were summarized (median, 25th and 90th percentiles). Radiotelemetric data were summarized (range and mean ± SE). Mean length of estrus and mean number of mounts during estrus were compared between the first and second estrus using Student’s t-test. Chi-square was used to detect differences in actual time of onset of estrus compared to the expectation of random time of onset.
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Results
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Mean seasonal ovarian activity began earlier for the EBE and LBE groups compared to NBE (August 21, EBE; August 31, LBE; September 14, NBE; P < 0.001) and was earlier in EBE (P < 0.021) than LBE (Figure 1). Based on P4 profiles and confirmed with ultrasound, all cows in harem conceived to the first fertile cycle, giving 100% fertility for both groups. The time from bull introduction to the onset of ovarian activity was significantly longer in the EBE group compared to the LBE group (18.5 d EBE vs. 8.5 d LBE; Figure 2). Breeding spanned August 16 to 22 in the EBE group, and August 24 to September 4 in the LBE group, whereas the onset of estrous cycles ranged from September 4 to 28 in the NBE group. Short cycles, characterized by a transient progesterone rise (P4 0.5 ng/mL) before the first fertile cycle, were identified in 65 % of the animals (five EBE cows, two LBE cows, and six NBE cows).
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Figure 1. Box and whisker plot for the onset of ovarian activity (first fertile ovulation, calculated from the last progesterone concentration <0.5 ng/mL that preceded a sustained progesterone elevation 3 wk) in three groups of female muskoxen. The centerline represents the median, the box defines the 25 to 75th percentile, the whiskers define the 10 to 90th percentile, and the points represent outliers. In the LBE group, all the data points were on the median with the exception of the two outliers.
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Figure 2. Mean (± SE) progesterone concentrations for three groups of female muskoxen. The arrows indicate the time of bull introduction for both the early bull exposure (EBE) and late bull exposure (LBE) groups. The third group received no bull exposure (NBE).
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All females in the EBE group came into estrus over a 7-d period, those in the LBE group came into estrus over a 12-d period, and those in the NBE group came into estrus over a 24-d period (Figure 1
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Radiotelemetry identified estrus once in seven cows (Figure 3a) and twice in five cows (Figure 3b). When compared to individual P4 profiles of the first full length/fertile cycle of the season, radiotelemetry correctly identified estrus with 95% accuracy (18 of 19 instances). In one cow, the system failed to detect estrus and breeding, although standing behavior was recorded during early pregnancy. Mean length of estrus, calculated from the time of first mount until last mount, was 771 ± 98 min (range = 4 to 1,508 min). Mean number of mounts during estrus was 8.89 ± 1.29 (range = 3 to 25 mounts). Mean number of mounts (range) received during 4 h, 6 h, 12 h, and 24 h after the first mount were 4.39 ± 0.59 (2 to 10), 6.19 ± 0.90 (2 to 15), 7.93 ± 1.20 (2 to 17), and 10.78 ± 1.90 (4 to 21), respectively. Length of estrus before the first short cycle did not differ from the length of estrus at the first fertile estrus among cows (589 ± 181 min vs. 841 ± 114 min) or within individuals (589 ± 181 min vs. 1,056 ± 169 min).
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Figure 3. Progesterone profiles from 12 female muskoxen indicating the radiotelemetric identification of estrus (arrows). Data have been normalized to the first estrus detected by the bull (d 0). (a) In 7 of 12 muskoxen, only one estrous bout was detected, to which all the cows conceived. (b) In the remaining five females, two estrous bouts were detected, the first occurring before a short cycle, which was followed 7 d later by a fertile estrus.
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Estrus was initiated more frequently during the night, 11 of 18 instances (2300 to 0500; 
2 = 14.39; P < 0.05; Figure 4). Darkness in Fairbanks, AK (64° N latitude), during the period of this study, extended approximately from 2300 until 0500.
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Figure 4. The frequency of onset of estrous bouts in 12 muskox cows relative to a 24-h day. Data were analyzed using 2; * indicates difference (P < 0.05) from the expected.
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Discussion
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In this study, muskox bull introduction stimulated seasonal ovarian activity without any reduction in fertility in both the EBE and LBE groups. A brief progesterone rise preceding the first full-length, fertile cycle has been described previously in muskoxen (Rowell and Flood, 1988) and in this study was identified in 65% of the cows. In sheep, first ovulation following ram introduction is invariably "silent" and in 50% of the ewes is followed by a short luteal phase and a second, silent ovulation (Martin and Scaramuzzi, 1983; Knight, 1983; Walkden-Brown et al., 1999). Muskoxen, however, seem to respond more like goats (Walkden-Brown et al., 1999), with a variable number of individuals exhibiting estrus at the first ovulation (followed in the majority of cases by a short cycle) and a second ovulation always accompanied by estrus.
The NBE cows in this study came into estrus throughout September. In a review of muskox breeding season and latitude, September was the estimated time of breeding among captive muskoxen housed continuously with a bull in the Fairbanks area (Flood and Tedesco, 1997). This is consistent with the present study. However, ewes continuously housed with males frequently become refractory to the unchanging male stimulus and exhibit estrous activity similar to isolated ewes (Cushwa et al., 1992). Whether September represents the normal breeding season for muskoxen at this latitude or a delay in the onset of the breeding season cannot be established with the present data.
The relatively poor synchrony within the NBE group suggests that a small group of females does not provide a signal strong enough to produce the synchrony of estrus seen in the EBE and LBE groups. Although the NBE group was both physically and visually separated from any bulls, it is likely that they could smell and hear the bulls. Rutting bulls produced a very strong odor (Flood et al., 1989) that permeated the core area of the facility. They also roared loudly, a sound that could be heard throughout the farm. Although pheromones are important signals in the male effect, it is generally accepted that full physical contact with the male results in the greatest response in both ewes (Rosa and Bryant, 2002) and goats (Chemineau, 1987). In the muskoxen, limited sensory contact was not adequate to either synchronize or stimulate ovarian activity.
Some breeds of sheep, notably Merino, can be stimulated to ovulate within 6 d of ram introduction at almost anytime during anestrus and even postpartum. However, for many breeds of sheep and goats, "depth" of anestrus affects the females’ response to male introduction (Martin et al., 1986; Walkden-Brown et al., 1999; Rosa and Bryant, 2002). In goats, increasing depth of anestrus increases the interval between buck introduction and first ovulation and reduces the proportion of females exhibiting estrus at the first ovulation (Chemineau, 1987). In this study, the EBE group was introduced to the bull 21 d earlier than the LBE group but only initiated ovarian activity 10 d sooner than the LBE cows. This suggests that depth of anestrus may be an important consideration in managing muskox reproduction. Not only was the interval from introduction to the onset of estrus longer in the EBE group, standing estrus before the short luteal cycle was detected only once in the EBE group compared to four instances in the LBE group. Unfortunately, these data are too limited to discriminate between female estrous expression and male libido. The male effect is most potent near the end of anestrus, presumably when the sensitivity of the hypothalamic/pituitary axis is changing (Martin et al., 1986). In the present study, mid-August appears to represent a time when the female muskoxen became responsive to the male.
This study did not evaluate male libido and used only mature, experienced males. Muskox bulls are physiologically capable of breeding at 1.5 yr (Rowell, 1991), but whether a young, subordinate, or inexperienced male could exert a similar influence over the females needs to be investigated. Ideally, employing a crossover design would help separate female estrous expression and male libido.
The radiotelemetric estrus detection system proved an effective technology for identifying estrous standing behavior in muskoxen. Using P4 concentrations to confirm the absence of a functional corpus luteum, radiotelemetry correctly detected breeding activity in 12 of 13 cows. Progesterone concentrations and ultrasound both verified that one muskox was bred and conceived even though the transmitter did not record this breeding activity. We have no explanation as to why the system failed in this cow.
Length of estrus was highly variable among these muskoxen. This has also been reported in cattle where attempts to relate length of estrus to fertility were unsuccessful (Rorie et al., 2002). The expression of standing behavior before the first transient increase in P4 concentration, identified in 5 of 12 muskox cows in this study, has been previously described (Rowell and Flood, 1988). In muskox cows, the length of estrus expressed before the short cycle was the same as the length of estrus at the first fertile ovulation, whether compared within or between individuals. This is in contrast to reports in dairy cattle where radiotelemetry indicated fewer mounts during the first postpartum ovulation compared to subsequent ovulations (Shipka, 2000), or other studies, where the number of mounts have been related to fertility (Rorie et al., 2002).
In these muskoxen, the onset of estrus occurred more often during night than any other period of the day. Maximal estrous activity in dairy cattle also occurs at night (Boyd, 1984). In another study, estrus was initiated more frequently following movement of dairy cattle from a concrete to a dry, dirt lot (Lopez, 2000), suggesting some environmental control over the onset of estrous behavior. Although the increased initiation of estrus during the night in muskoxen may be a photoperiodic response, it could also reflect environmental conditions, such as cooler night temperatures. Night also corresponds with the time of minimal human activity. The preponderance of nighttime breeding may also explain why muskox producers have expressed difficulty observing breeding among their animals. An important point in this study, however, is the high degree of variation in the length of estrus, resulting in some muskoxen continuing to express standing behavior around the clock.
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Implications
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In farmed situations where bull muskox are maintained separately from cows, bull introduction can be used as an effective, low-cost means of inducing and synchronizing estrus. In this study, the females were receptive to bull introduction by mid-August, 2 to 4 wk earlier than cows maintained without a bull. Most females experienced a brief, transient rise in progesterone, followed by a fertile ovulation and full estrous expression. A radiotelemetric estrus detection system worked well and provided detailed information on the timing and duration of mounting behavior in this species.
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Footnotes
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1 Funding was provided by the NRI Competitive Grants Program, USDA grant No. 00-35208-9168 and awarded to the authors through the Institute of Arctic Biology. The authors thank the staff at the R. G. White Large Animal Research Station, Institute of Arctic Biology, for their dedicated care and expert handling of the muskoxen. 
2 Correspondence—phone: 907-474-6009; fax: 907-474-6184; E-mail: j.rowell{at}uaf.edu.
Received for publication April 1, 2003.
Accepted for publication June 17, 2003.
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Literature Cited
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Boyd, H. W. 1984. Aids to estrous detection—a review. Page 61–67 in Dairy Cow Fertility. Proc. Joint Brit. Vet. Assoc. and Brit. Soc. Anim. Prod. Conf., Bristol, U.K.
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Cushwa, W. T., G. E. Bradford, G. H. Stabenfeldt, Y. M. Berger, and M. R. Dally. 1992. Ram influence on ovarian and sexual activity in anestrous ewes: Effects of isolation of ewes from rams before joining and date of ram introduction. J. Anim. Sci. 70:1195–1200.[Abstract]
Flood, P. F., S. R. Abrams, G. D. Muir, and J. E. Rowell. 1989. Odor of the muskox. J. Chem. Ecol. 15:2207–2217.
Flood, P. F., and S. C. Tedesco. 1997. Relationship between conception date and latitude in muskoxen. Rangifer 17:25–30.
Knight, T. W. 1983. Ram induced stimulation of ovarian and estrous activity in anoestrous ewes—a review. NZ Soc. Anim. Prod. 43:7–11.
Lopez, H. 2000. Correlation of estrogen concentrations in milk and plasma in proximity with estrous mounting activity and ovulation in dairy cows. Ph.D. Diss., Utah State Univ., Logan.
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Martin, G. B., and R. J. Scaramuzzi. 1983. The induction of oestrus and ovulation in seasonally anovular ewes by exposure to rams. J. Steriod Biochem. 19:869–875.
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Rowell, J. E., R. G. White, and W. E. Hauer. 1997. Progesterone during the breeding season and pregnancy in female muskoxen on different dietary regimens. Rangifer 17:125–129.
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Abstract
Introduction
