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Effects of exposure to an estrual female on the attainment of puberty in gilts
ELSEVIER
EFFECTS OF EXPOSURE TO AN ESTRUAL FEMALE ON THE ATTAINMENT PUBERTY IN GILTS
OF
J. A. Sterle and W. R. Lamberson’ Department of Animal Sciences University of Missouri, Columbia, MO 65211 Received for publication: Accepted:
May 10, I.995 October
2,
2995
ABSTRACT A total of 304 prepubertal gilts were randomly allocated to 4 treatment groups across 10 replications for a 50 d treatment period beginning at 170 d of age. The 4 treatment groups consisted of 1) Gilts that were continuously exposed to one of a group of older, ovariectomized females that had been treated with 2 mg/ml estradiol benzoate to stimulate estrus (SE); 2) Gilts that were continuously exposed to an older, anestrous, ovariectomized female (OVX); 3) Gilts that were exposed to a mature boar for 15 mm/d (BE); 4) Gilts that were isolated from any direct physical contact with other pigs (C). A gilt was considered to have attained puberty when she exhibited a standing reflex when mounted by the boar (BE group only) or to pressure applied manually to the back or had plasma progesterone concentrations > 2 ng/ml for 2 consecutive Data were analyzed as a randomized complete block design with treatment and weeks. replication in the model. A higher percentage of gilts attained puberty in the BE group than in the 3 other groups (52 vs 26, 30 and 32%, BE vs SE, OVX and C, respectively; P = 0.002). Gilts exposed to an estrual female or a mature boar attained puberty sooner after treatment was initiated than gilts in other treatment groups (12.6 and 17.8 vs 26.7 and 24.1 d, SE and BE vs OVX and C, respectively; P = 0.0003). Of the gilts attaining puberty during the experimental period, the highest percentage of gilts exhibited estrus within 10 d of treatment in the SE group (55.0 vs 26.1, 37.8 and 16.7%, BE vs SE, OVX and C, respectively; P = 0.05). Age at puberty was also lower SE or BE than OVX or C groups (176.3 and 181 .O vs 189.4 and 188.1 d, respectively; P = 0.0001). Weight at puberty was unaffected by treatment. These results suggest that exposure to an estrual female was effective in stimulating peripubertal females to express estrus, thus reducing the age at puberty. Boar exposure had a stimulatory effect not only at the initiation of exposure but throughout the experimental period,resulting in a higher percentage of gilts attaining puberty. Key words: puberty, sow exposure, gilts Acknowledgments ‘To whom correspondence should be addressed. This is a contribution from the Missouri Agricultural Experiment Station Journal Series No. 12,410. The authors thank August Reike, Tom Cantley, Betty Nichols and Miroslav Kaps for their assistance. Theriogenology 45:733-744, 1996 0 1996 by Elsevier Science Inc. 655 Avenue of the Americas, New York, NY 10010
0093-691X/96/$15.00 PII SOO93-691X(96)00003-1
Theriogenology INTRODUCTION Producers are constantly stiving to decrease the costs of production and increase profitability. Decreasing the age of attainment of puberty in gilts has been identified as a major opportunity for decreasing the costs of production by decreasing the number of nonproductive days as well as the variable feed and nonfeed costs (15). A major factor contributing to the number of nonproductive days (any day in an animal’s life when it is not achieving a high growth rate or contributing reproductively to the herd) in a gilt’s lifetime is the age at which she becomes sexually mature and begins to ovulate (puberty). Due to a reported increase in litter size when gilts are bred at the second estrus instead of the pubertal estrus, most producers currently wait until the second standing heat to breed their gilts (14). The earlier a gilts reaches puberty, the younger she is when bred at second estrus and the fewer days the producer needs to feed and maintain an animal before she becomes productive. The attainment of early puberty does not appear to have negative aspects on the future reproductive ability of the female (1). Reproductive productivity was not decreased across 5 parities in a line of gilts selected for decreased age at puberty (7). Eliasson (5) reported that early puberty did not influence the duration of estrus in gilts. Ovulation rate at second estrus, conception rate or embryonic survival rate during the first 20 d of gestation were not affected by weight or age at puberty (8). The attainment of puberty can be influenced by manipulating many environmental factors (3, 9). Daily exposure to a mature boar has yielded the most consistent results for stimulating precocious puberty, although this practice is time-consuming and labor intensive. Other factors affecting the average age at puberty include the genetic base of the herd and current selection practices, moving and mixing the gilts, and plane of nutrition. The season of the year, photoperiod, geographic location and ambient temperature during the maturing phase may also play a role, as well as type of housing (confinement vs open lots), and the degree of social interaction (mainly restricted by group size). Exposure to an estrual female hastens the return to estrus in weaned sows (11). An experiment was developed to determine if a similar effect was present when prepubertal gilts were exposed to a mature intact female (13). Although age at puberty was not different between gilts exposed to an intact mature female or an ovariectomized mature female, a greater proportion of gilts exposed to an intact female reached puberty before 225 d of age than gilts exposed to an ovariectomized female (7 of 19 vs 0 of 19, respectively). Pearce (12) also reported a synchrony of the onset of puberty in gilts exposed to 4 penmates hormonally induced into standing estrus at 5-d intervals. The same researcher reported that gilts exposed to an estrual ovariectomized sow attained puberty earlier than gilts exposed to an anestrual ovariectomized sow or control gilts. To further investigate these interactions and their effects, the following study was developed to determine the effect of an estrual female on the attainment of puberty in gilts.
Theriogenology
735 MATERIALS AND METHODS
Animals and Experimental Design Three hundred and four crossbred (Yorkshire&&race X Duroc) prepubertal gilts were The gilts were randomly allocated to 1 of 4 used in the experiment across 10 replications. treatment groups: 1) Gilts were continuously exposed to an older, ovariectomized female that had been treated with 2 mg/ml estradiol benzoate to stimulate estrus (SE); estradiol treatment caused this female to exhibit physical signs of estrus for 3 d. To provide continuous exposure, this gilt was rotated with other treated gilts every third day. 2) Gilts were continuously exposed to an older, untreated, ovariectomized female (OVX). This female was anestrous and was also rotated every third day to equalize the effect of introducing a new, older (range: 250 d of age to > 400 d of age) pig into the group. 3) Gilts were exposed to a mature boar for 15 min/d (BE). Since a consistent response has previously been observed with this treatment, boar exposure was used as a positive control. 4) Gilts were isolated from any direct physical contact with other pigs (C). All the gilts were maintained in 4 adjacent pens in a modified open-front confinement building with gutter flush waste system and natural ventilation or in 0.5 ha pasture lots (Table 1). The confinement building had partially slatted floors and a space allotment of 1.0 to 1.3 m2 for each gilt. Treatment groups were randomly allotted to pens for each replication to prevent the same treatments from being adjacent to each other for each replication. The number of pigs per pen was held constant at 7 to 8 gilts. Exposure began when the oldest gilt in a replication was 170 d of age (range 156 to 170 d, with the exception of Replication 5). Gilts were checked daily for estrus. The gilts not being exposed to a boar were scored according to degree of swelling of the vulva, and observations were recorded daily for behavioral and physical signs of estrus. Gilts in the BE group were exposed daily to a mature boar. The gilts and boar were transferred to a nearby neutral pen and were allowed direct physical contact for 15 mm/d. This boar was rotated daily with the other available boars. A total of 8 boars were used at various times throughout the duration of the experiment. Age of the boars ranged from 11 mo to 2.5 yr. Gilts were weighed at the beginning of each replication and once weekly throughout the trial period. Weight at puberty was determined by calculating average daily gain between weekly weighings and adding the appropriate gain onto the last weight available before puberty. Gilts were fed a limited (5 to 6 lbs/gilt/day) diet of corn-soybean meal balanced to meet current NRC requirements. The gilts were allowed access to water ad libitum. Blood Sampling and Hormone Assay Blood samples were obtained once weekly via jugular venipuncture and stored on ice during the blood collection period. Samples were also taken at the beginning of each replication, and any gilt having a plasma progesterone concentration of > 2 nglml was considered to be postpubertal and was excluded from the experiment. It has been reported that the stress caused by normal methods of restraint and blood collection similar to those used here is not sufficiently
50 50 50 50 70 50 50 50 50 50
Length of
160 1 32 MOFe 170 2 32 MOF 170 3 32 MOF 170 4 28 MOF 150 5 30 Pasture 170 6 32 MOF 170 7 32 MOF 170 8 28 Pasture 170 9 32 MOF 10 170 26 MOF %E = Exposure to an estrual female. bOVX = Exposure to an ovariectomized female. ‘BE = Boar exposure for 15 minutes per day. dC = No direct physical contact with other pigs. eMOF = Modified open front confinement building.
Age at 9127193-l l/17/93 12/l/93-1/20/94 212194 - 3124194 4/l 3194 - 612194 6/19/94-8128194 6/22/94-8ilOl94 8131l94- 1O/20/94 813l/94- 1O/20/94 11/2/94- 12122194 l/10/94 - 312195
N-r of giltserty SEaOVXb--JE?----&_ 0 0 2 4 3 2 1 0 2 0 6 5 2 3 3 3 2 1 3 2
0 5 4 3 1 5 5 5 4 4
0 3 2 2 1 6 1 4 1 4
Table 1. Variables of number of animals, housing, age at initiation of treatment, length of exposure, dates of . . exment Wer of g&s reachw nubertv foreach renhcatlon.
737
Theriogenology
high to induce puberty in gilts and therefore should not affect the attainment of puberty (4). Samples were assayed for progesterone according to the procedures of Flowers et al. (6) for nonextracted porcine plasma. A gilt was considered to have attained puberty when she stood to be mounted by the boar (BE group only); exhibited lordosis to pressure applied manually to her back (back pressure test); or had 2 consecutive weekly plasma progesterone concentrations of >2 ng/ml. If a gilt was not detected in standing estrus but had 2 consecutive weekly progesterone concentrations greater than 2 ng/ml, the age at puberty was determined by subtracting 21 d from the date of the subsequent standing es&us. Once a gilt reached puberty, she was allowed to remain with her pen-mates in order to keep the number of pigs per pen constant and to not disrupt the social structure within a pen. Gilts were taken off trial after 50 d of exposure, with the exception of Replication 5. The gilts in Replication 5 were accidentally initiated on treatment at 150 d of age. These gilts remained on trial for 70 d to maintain a consistent age when taken off trial. Statistical Analyses Dependent variables of age at puberty, weight at puberty and interval from initiation of treatment to first estrus were fitted to a randomized, complete block design model containing replication and treatment. Although the original model also included litter within replication, this effect was removed (F-value < 1). Variation due to treatment-by-replication interaction was included in the error term to give a conservative test of significance. Only data from gilts attaining puberty during the experimental period were included in these analyses. Categorical observations of pigs attaining puberty within 10 d of treatment as well as those reaching puberty throughout the trial period were each fitted to a log-likelihood analysis containing treatment in the model. RESULTS During the trial period, a greater percentage of gilts exposed to mature boars attained puberty (P = 0.002) than those exposed to an estrual or anestrual female or those isolated from direct contact with other pigs (52 vs 26,30 and 32%, BE vs SE, OVX and C, respectively; Figure 1). Gilts exposed to either an estrual female or a mature boar reached puberty at a younger age (P = 0.0003) than gilts in the other treatment groups (176.3 + 3.0 and 181.0 + 2.1 d of age vs 189.4 + 2.7 and 188.1 + 2.7 d of age, SE and BE vs OVX and C, respectively; Figure 2). Although gilts exposed to an estrual female attained puberty at a numerically younger age than those exposed to a boar, this difference was not significant (P = 0.12). The interval from the initiation of treatment to first estrus was also shorter (P = 0.0001 j when gilts were exposed to either an estrual female or a boar (12.6 + 3.0 and 17.8 + 2.1 d vs 26.7 2 2.7 and 24.1 + 2.6 d, SE and BE vs OVX and C, respectively, Figure 3). Once again, there was a numeric difference but no statistical difference between the SE and BE groups (P = 0.14). Of the gilts that reached puberty during the experimental period, a greater percentage of gilts exposed to an estrual female reached puberty within 10 d of treatment (P = 0.05; Figure 4) than the other 3 groups (55 vs 26, 38 and 17 % of the gilts that attained puberty, SE vs OVX, BE and C, respectively). Treatment
Theriogenology
738 60
1
40 1
20
10
0 L
Treatment
Figure 1.
Effect of treatment on the percentage of gilts attaining puberty during the experimental period. Boar exposure (BE) vs exposure to an estrual female (SE), exposure to an ovariectomized female (OVX) or to controls (C; P = 0.0017)
Theriogenology
739
I SE
Figure 2.
ovx
Effect of treatment on age at which reached puberty. Exposure to an estrual female (SE) and boar exposure (BE) vs exposure to an ovariectomized female (OVX) and to controls (C; P = 0.0003).
740
Theriogenology
30
1 25
20
G$ z
15
g 9
10
5
0
ovx Treatment
Figure 3.
Average interval from initiation of treatment to first estrus in gilts. Exposure to an estrual female (SE) and boar exposure (BE) vs exposure to an ovariectomized female (OVX) and to controls (C; P = 0.0001).
Theriogenology
741
742
Theriogenology
did not affect weight at puberty (107.5 + 2.36, 107.5 + 2.13, 110.0 + 1.68 and 114.1 + 2.09 kg, respectively; P = 0.09). DISCUSSION Data from the present study suggest that while exposure to an estrual female was as effective as exposure to a boar in inducing puberty in some gilts, a higher percentage of gilts reached puberty when exposed to a mature boar. The female-induced stimulation may be caused by a combination of stress and pheromones; however, the exact mechanism is not known. Similar percentages (40.4%) of gilts receiving various types of boar exposure attained puberty by 210 d of age using this same herd in a previous experiment (2). Age at puberty as well as the interval from initiation of treatment to first estrus was lower when the gilts were exposed to an estrual female or a mature boar compared with gilts exposed to an anestrual, ovariectomized female or isolated from contact with other pigs. Decreasing the age at puberty was expected to decrease the weight at puberty, since gilts are younger and have had fewer days on feed; however, there was no effect of treatment on weight at puberty. Exposure to an estrual female hastens the return to estrus in weaned sows (11). Vandenbergh (16) found similar results in mice. Although prepubertal female mice exposed to a mature female reached puberty at a later age than those exposed to a mature male (P < O.OOS),the mice in that treatment group were significantly younger at puberty than the mice not receiving any exposure (P < 0.005). These results suggest that, although not as effective as male exposure, interaction with a mature female stimulates early puberty in mice. Exposure of prepubertal heifers to mature cows resulted in a decrease in the age at puberty (P < 0.01; interaction of treatment-by-sire breed effect during the first year of a study with heifers sired by Hereford, Charolais and Tarentaise bulls, but these effects were not observed during the second year with heifers sired by Hereford, Charolais, Jersey, Shorthorn, Tarentaise, Brahman and Longhorn bulls (10). It is not clear why there was a difference between the 2 yr, although the authors suggested that there may have been a difference in physiology and sensitivity to the stimuli. Pnmier and Mounier (13) have reported the results of an experiment designed to determine whether exposing prepubertal gilts to a mature, sexually intact female stimulated puberty. Forty gilts were allotted to 1 of 2 treatments: introduction of either a mature intact female or an ovariectomized female at 155 d of age. Although age at puberty was similar between the 2 treatment groups (23 1 + 24 d and 243 + 12 d, exposure to an intact female and exposure to an ovariectomized female, respectively), a higher proportion of gilts exposed to an intact female reached puberty before 225 d of age than those exposed to an ovariectomized female (7 of 19 vs 0 of 19, respectively; 1 prepubertal gilt in each treatment group was removed from the experiment early). However, the duration and frequency of estrus in the intact mature females was not reported, and thus it is difficult to determine the exact mechanism involved. Nevertheless, our results support the above findings. A similar set of experiments was conducted to determine the effect of contact with a female in estrus on the attainment of puberty in gilts (12). Experiment 1 compared boar exposure vs no boar exposure along with either removing gilts from the pen as soon as they were
Theriogenology
743
discovered to be in estrus or leaving estrual females with their pen-mates. Boar exposure stimulated puberty in these gilts compared with no boar exposure (P < 0.05). Although the mean age at puberty was similar, the degree of synchronization was better when estrual gilts were allowed to remain with their pen-mates (P < 0.001). Another experiment in Pearce’s study (12) involved exposing prepubertal gilts to anestrual or estrual ovariectomized sows. Sixty-four gilts were allotted to the following treatment groups: 1) gilts received no exposure (controls), 2) gilts were exposed to an ovariectomized anestrual sow, 3) gilts were exposed to an estrual ovariectomized sow, and 4) gilts were exposed to a mature boar. All 3 exposure treatments lasted 20 mm/d. Gilts exposed to an estrual sow or a mature boar were younger (P < 0.05) at puberty than the control gilts. There was no significant difference in the age at puberty or interval to puberty between the gilts exposed to an anestrual sow or to control gilts. There was also no significant difference in age at puberty or interval to puberty between gilts exposed to a boar or those exposed to an estrual sow. The results of Pearce (12) closely agree with those presented here. The interaction between gilts is intensified when one or more gilts are in standing heat. Stress caused by frequent mounting attempts and increased vocalization and activity in the estrual female may be an adequate stimulus for inducing precocious puberty in gilts. The higher percentage of gilts reaching puberty that were exposed to a mature boar during the trial period suggests that the additional exposure to pheromones present in the submaxillary gland of the boar had the greater effect on stimulating puberty in these gilts. Female to female interaction appears to play an important role in the onset of puberty in gilts. Although this treatment does not appear to be as effective as exposure to a mature boar, it is less time-consuming, less dangerous and easy to apply to a variety of production systems. For example, a producer could take a newly-weaned sow expected to return to estrus within 5 to 10 d, and introduce her into a pen of prepubertal females. This practice has an advantage over boar exposure treatment since the producer would be able to leave the sow in the pen unsupervised until she is to be reintroduced into the breeding herd. The short interval from initiation of treatment to estrus suggests that this treatment is most effective soon after it is begun. Although the age at puberty was numerically decreased with exposure to an estrual female compared with exposure to a mature boar in our present experiment, the means were not statistically different. Producers strive to increase productivity and to decrease the costs of production. One way to accomplish this is to decrease the age at puberty in gilts in order to decrease the total number of nonproductive days. Although exposure to a mature boar has been most effective in stimulating the onset of puberty in gilts, this practice is both time and labor-consuming and is potentially dangerous. Exposure to a mature estrual female, by contrast, could yield similar results without some of the drawbacks of boar exposure. REFERENCES 1. Brooks PH, Smith DA.. Ovulation rate and embryonic mortality in gilts reaching puberty at young ages. Anim Prod 1976;22:139 abstr. 2. Caton JS, Jesse GW, Day BN, Ellersieck MR. The effect of duration of boar exposure on the frequency of gilts reaching first estrus. J Anim Sci 1986;62:1210-1214.
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3. Christenson RK. Swine management to increase gilt reproductive efficiency. J Anim Sci 1986;63:1280-1287. 4. Diekman MA, Hoagland TA. Influence of supplemental lighting during periods of increasing or decreasing day length on the onset of puberty in gilts. J Anim Sci 1983;57:1235-1242. 5. El&son L. A study on puberty and estrus in gilts. J Vet Med 1989;36:46-54. 6. Flowers B, Cantley TC, Martin MJ, Day BN. Effect of elevated ambient temperatures on puberty in gilts. J Anim Sci 1989;67:779-784. 7. Holder RB, Lamberson WR, Bates RO, Sal&ski TJ. Lifetime productivity in gilts selected for decreased age at puberty. Anim Sci 1995;61: 115- 12 1. 8. Hughes PE, Cole DJA. Reproduction in the gilt. I. The influence of age and weight at puberty on ovulation rate and embryo survival in the gilt. Anim Prod 1975;21: 183-l 89. 9. Hughes PE. Factors affecting the natural attainment of puberty in the gilt. In: Control of Pig Reproduction. Butterworths Press, 1982. 10. Nelsen TC, Short RE, Phelps DA, Staigmiller RB. Nonpuberal estrus and mature cow influences on growth and puberty in heifers. J Anim Sci 1985;61:470-473. 11. Pearce GP, Pearce AN. Contact with a sow in oestrus or a mature boar stimulates the onset of oestrus in weaned sows. Vet Ret 1992;130:5-9. 12. Pearce GP. Contact with oestrus female pigs stimulates puberty in gilts. Vet Ret 1992;130:318-323. 13. Prunier A, Mounier AM. Influence of the presence of a mature female on puberty attainment in gilts. Theriogenology 1991;36:537-542. 14. Schukken YH, Buurman J, Huirne RBM, Willemse AH, Vernooy JCM, van den Broek J, Verheijden JHN. Evaluation of optimal age at first conception in gilts from data collected in commercial swine herds. J Anim Sci 1994;72:1387-1392. 15. Tess MW, Bennett GL, Dickerson GE. Simulation of genetic changes in life cycle efficiency of pork production. II. Effects of components on efficiency. J Anim Sci 1983;56:354-368. 16. Vandenbergh JG. Effect of the presence of a male on the sexual maturation of female mice. Endocrinology 1967;81:345-349.
EFFECTS OF EXPOSURE TO AN ESTRUAL FEMALE ON THE ATTAINMENT PUBERTY IN GILTS
OF
J. A. Sterle and W. R. Lamberson’ Department of Animal Sciences University of Missouri, Columbia, MO 65211 Received for publication: Accepted:
May 10, I.995 October
2,
2995
ABSTRACT A total of 304 prepubertal gilts were randomly allocated to 4 treatment groups across 10 replications for a 50 d treatment period beginning at 170 d of age. The 4 treatment groups consisted of 1) Gilts that were continuously exposed to one of a group of older, ovariectomized females that had been treated with 2 mg/ml estradiol benzoate to stimulate estrus (SE); 2) Gilts that were continuously exposed to an older, anestrous, ovariectomized female (OVX); 3) Gilts that were exposed to a mature boar for 15 mm/d (BE); 4) Gilts that were isolated from any direct physical contact with other pigs (C). A gilt was considered to have attained puberty when she exhibited a standing reflex when mounted by the boar (BE group only) or to pressure applied manually to the back or had plasma progesterone concentrations > 2 ng/ml for 2 consecutive Data were analyzed as a randomized complete block design with treatment and weeks. replication in the model. A higher percentage of gilts attained puberty in the BE group than in the 3 other groups (52 vs 26, 30 and 32%, BE vs SE, OVX and C, respectively; P = 0.002). Gilts exposed to an estrual female or a mature boar attained puberty sooner after treatment was initiated than gilts in other treatment groups (12.6 and 17.8 vs 26.7 and 24.1 d, SE and BE vs OVX and C, respectively; P = 0.0003). Of the gilts attaining puberty during the experimental period, the highest percentage of gilts exhibited estrus within 10 d of treatment in the SE group (55.0 vs 26.1, 37.8 and 16.7%, BE vs SE, OVX and C, respectively; P = 0.05). Age at puberty was also lower SE or BE than OVX or C groups (176.3 and 181 .O vs 189.4 and 188.1 d, respectively; P = 0.0001). Weight at puberty was unaffected by treatment. These results suggest that exposure to an estrual female was effective in stimulating peripubertal females to express estrus, thus reducing the age at puberty. Boar exposure had a stimulatory effect not only at the initiation of exposure but throughout the experimental period,resulting in a higher percentage of gilts attaining puberty. Key words: puberty, sow exposure, gilts Acknowledgments ‘To whom correspondence should be addressed. This is a contribution from the Missouri Agricultural Experiment Station Journal Series No. 12,410. The authors thank August Reike, Tom Cantley, Betty Nichols and Miroslav Kaps for their assistance. Theriogenology 45:733-744, 1996 0 1996 by Elsevier Science Inc. 655 Avenue of the Americas, New York, NY 10010
0093-691X/96/$15.00 PII SOO93-691X(96)00003-1
Theriogenology INTRODUCTION Producers are constantly stiving to decrease the costs of production and increase profitability. Decreasing the age of attainment of puberty in gilts has been identified as a major opportunity for decreasing the costs of production by decreasing the number of nonproductive days as well as the variable feed and nonfeed costs (15). A major factor contributing to the number of nonproductive days (any day in an animal’s life when it is not achieving a high growth rate or contributing reproductively to the herd) in a gilt’s lifetime is the age at which she becomes sexually mature and begins to ovulate (puberty). Due to a reported increase in litter size when gilts are bred at the second estrus instead of the pubertal estrus, most producers currently wait until the second standing heat to breed their gilts (14). The earlier a gilts reaches puberty, the younger she is when bred at second estrus and the fewer days the producer needs to feed and maintain an animal before she becomes productive. The attainment of early puberty does not appear to have negative aspects on the future reproductive ability of the female (1). Reproductive productivity was not decreased across 5 parities in a line of gilts selected for decreased age at puberty (7). Eliasson (5) reported that early puberty did not influence the duration of estrus in gilts. Ovulation rate at second estrus, conception rate or embryonic survival rate during the first 20 d of gestation were not affected by weight or age at puberty (8). The attainment of puberty can be influenced by manipulating many environmental factors (3, 9). Daily exposure to a mature boar has yielded the most consistent results for stimulating precocious puberty, although this practice is time-consuming and labor intensive. Other factors affecting the average age at puberty include the genetic base of the herd and current selection practices, moving and mixing the gilts, and plane of nutrition. The season of the year, photoperiod, geographic location and ambient temperature during the maturing phase may also play a role, as well as type of housing (confinement vs open lots), and the degree of social interaction (mainly restricted by group size). Exposure to an estrual female hastens the return to estrus in weaned sows (11). An experiment was developed to determine if a similar effect was present when prepubertal gilts were exposed to a mature intact female (13). Although age at puberty was not different between gilts exposed to an intact mature female or an ovariectomized mature female, a greater proportion of gilts exposed to an intact female reached puberty before 225 d of age than gilts exposed to an ovariectomized female (7 of 19 vs 0 of 19, respectively). Pearce (12) also reported a synchrony of the onset of puberty in gilts exposed to 4 penmates hormonally induced into standing estrus at 5-d intervals. The same researcher reported that gilts exposed to an estrual ovariectomized sow attained puberty earlier than gilts exposed to an anestrual ovariectomized sow or control gilts. To further investigate these interactions and their effects, the following study was developed to determine the effect of an estrual female on the attainment of puberty in gilts.
Theriogenology
735 MATERIALS AND METHODS
Animals and Experimental Design Three hundred and four crossbred (Yorkshire&&race X Duroc) prepubertal gilts were The gilts were randomly allocated to 1 of 4 used in the experiment across 10 replications. treatment groups: 1) Gilts were continuously exposed to an older, ovariectomized female that had been treated with 2 mg/ml estradiol benzoate to stimulate estrus (SE); estradiol treatment caused this female to exhibit physical signs of estrus for 3 d. To provide continuous exposure, this gilt was rotated with other treated gilts every third day. 2) Gilts were continuously exposed to an older, untreated, ovariectomized female (OVX). This female was anestrous and was also rotated every third day to equalize the effect of introducing a new, older (range: 250 d of age to > 400 d of age) pig into the group. 3) Gilts were exposed to a mature boar for 15 min/d (BE). Since a consistent response has previously been observed with this treatment, boar exposure was used as a positive control. 4) Gilts were isolated from any direct physical contact with other pigs (C). All the gilts were maintained in 4 adjacent pens in a modified open-front confinement building with gutter flush waste system and natural ventilation or in 0.5 ha pasture lots (Table 1). The confinement building had partially slatted floors and a space allotment of 1.0 to 1.3 m2 for each gilt. Treatment groups were randomly allotted to pens for each replication to prevent the same treatments from being adjacent to each other for each replication. The number of pigs per pen was held constant at 7 to 8 gilts. Exposure began when the oldest gilt in a replication was 170 d of age (range 156 to 170 d, with the exception of Replication 5). Gilts were checked daily for estrus. The gilts not being exposed to a boar were scored according to degree of swelling of the vulva, and observations were recorded daily for behavioral and physical signs of estrus. Gilts in the BE group were exposed daily to a mature boar. The gilts and boar were transferred to a nearby neutral pen and were allowed direct physical contact for 15 mm/d. This boar was rotated daily with the other available boars. A total of 8 boars were used at various times throughout the duration of the experiment. Age of the boars ranged from 11 mo to 2.5 yr. Gilts were weighed at the beginning of each replication and once weekly throughout the trial period. Weight at puberty was determined by calculating average daily gain between weekly weighings and adding the appropriate gain onto the last weight available before puberty. Gilts were fed a limited (5 to 6 lbs/gilt/day) diet of corn-soybean meal balanced to meet current NRC requirements. The gilts were allowed access to water ad libitum. Blood Sampling and Hormone Assay Blood samples were obtained once weekly via jugular venipuncture and stored on ice during the blood collection period. Samples were also taken at the beginning of each replication, and any gilt having a plasma progesterone concentration of > 2 nglml was considered to be postpubertal and was excluded from the experiment. It has been reported that the stress caused by normal methods of restraint and blood collection similar to those used here is not sufficiently
50 50 50 50 70 50 50 50 50 50
Length of
160 1 32 MOFe 170 2 32 MOF 170 3 32 MOF 170 4 28 MOF 150 5 30 Pasture 170 6 32 MOF 170 7 32 MOF 170 8 28 Pasture 170 9 32 MOF 10 170 26 MOF %E = Exposure to an estrual female. bOVX = Exposure to an ovariectomized female. ‘BE = Boar exposure for 15 minutes per day. dC = No direct physical contact with other pigs. eMOF = Modified open front confinement building.
Age at 9127193-l l/17/93 12/l/93-1/20/94 212194 - 3124194 4/l 3194 - 612194 6/19/94-8128194 6/22/94-8ilOl94 8131l94- 1O/20/94 813l/94- 1O/20/94 11/2/94- 12122194 l/10/94 - 312195
N-r of giltserty SEaOVXb--JE?----&_ 0 0 2 4 3 2 1 0 2 0 6 5 2 3 3 3 2 1 3 2
0 5 4 3 1 5 5 5 4 4
0 3 2 2 1 6 1 4 1 4
Table 1. Variables of number of animals, housing, age at initiation of treatment, length of exposure, dates of . . exment Wer of g&s reachw nubertv foreach renhcatlon.
737
Theriogenology
high to induce puberty in gilts and therefore should not affect the attainment of puberty (4). Samples were assayed for progesterone according to the procedures of Flowers et al. (6) for nonextracted porcine plasma. A gilt was considered to have attained puberty when she stood to be mounted by the boar (BE group only); exhibited lordosis to pressure applied manually to her back (back pressure test); or had 2 consecutive weekly plasma progesterone concentrations of >2 ng/ml. If a gilt was not detected in standing estrus but had 2 consecutive weekly progesterone concentrations greater than 2 ng/ml, the age at puberty was determined by subtracting 21 d from the date of the subsequent standing es&us. Once a gilt reached puberty, she was allowed to remain with her pen-mates in order to keep the number of pigs per pen constant and to not disrupt the social structure within a pen. Gilts were taken off trial after 50 d of exposure, with the exception of Replication 5. The gilts in Replication 5 were accidentally initiated on treatment at 150 d of age. These gilts remained on trial for 70 d to maintain a consistent age when taken off trial. Statistical Analyses Dependent variables of age at puberty, weight at puberty and interval from initiation of treatment to first estrus were fitted to a randomized, complete block design model containing replication and treatment. Although the original model also included litter within replication, this effect was removed (F-value < 1). Variation due to treatment-by-replication interaction was included in the error term to give a conservative test of significance. Only data from gilts attaining puberty during the experimental period were included in these analyses. Categorical observations of pigs attaining puberty within 10 d of treatment as well as those reaching puberty throughout the trial period were each fitted to a log-likelihood analysis containing treatment in the model. RESULTS During the trial period, a greater percentage of gilts exposed to mature boars attained puberty (P = 0.002) than those exposed to an estrual or anestrual female or those isolated from direct contact with other pigs (52 vs 26,30 and 32%, BE vs SE, OVX and C, respectively; Figure 1). Gilts exposed to either an estrual female or a mature boar reached puberty at a younger age (P = 0.0003) than gilts in the other treatment groups (176.3 + 3.0 and 181.0 + 2.1 d of age vs 189.4 + 2.7 and 188.1 + 2.7 d of age, SE and BE vs OVX and C, respectively; Figure 2). Although gilts exposed to an estrual female attained puberty at a numerically younger age than those exposed to a boar, this difference was not significant (P = 0.12). The interval from the initiation of treatment to first estrus was also shorter (P = 0.0001 j when gilts were exposed to either an estrual female or a boar (12.6 + 3.0 and 17.8 + 2.1 d vs 26.7 2 2.7 and 24.1 + 2.6 d, SE and BE vs OVX and C, respectively, Figure 3). Once again, there was a numeric difference but no statistical difference between the SE and BE groups (P = 0.14). Of the gilts that reached puberty during the experimental period, a greater percentage of gilts exposed to an estrual female reached puberty within 10 d of treatment (P = 0.05; Figure 4) than the other 3 groups (55 vs 26, 38 and 17 % of the gilts that attained puberty, SE vs OVX, BE and C, respectively). Treatment
Theriogenology
738 60
1
40 1
20
10
0 L
Treatment
Figure 1.
Effect of treatment on the percentage of gilts attaining puberty during the experimental period. Boar exposure (BE) vs exposure to an estrual female (SE), exposure to an ovariectomized female (OVX) or to controls (C; P = 0.0017)
Theriogenology
739
I SE
Figure 2.
ovx
Effect of treatment on age at which reached puberty. Exposure to an estrual female (SE) and boar exposure (BE) vs exposure to an ovariectomized female (OVX) and to controls (C; P = 0.0003).
740
Theriogenology
30
1 25
20
G$ z
15
g 9
10
5
0
ovx Treatment
Figure 3.
Average interval from initiation of treatment to first estrus in gilts. Exposure to an estrual female (SE) and boar exposure (BE) vs exposure to an ovariectomized female (OVX) and to controls (C; P = 0.0001).
Theriogenology
741
742
Theriogenology
did not affect weight at puberty (107.5 + 2.36, 107.5 + 2.13, 110.0 + 1.68 and 114.1 + 2.09 kg, respectively; P = 0.09). DISCUSSION Data from the present study suggest that while exposure to an estrual female was as effective as exposure to a boar in inducing puberty in some gilts, a higher percentage of gilts reached puberty when exposed to a mature boar. The female-induced stimulation may be caused by a combination of stress and pheromones; however, the exact mechanism is not known. Similar percentages (40.4%) of gilts receiving various types of boar exposure attained puberty by 210 d of age using this same herd in a previous experiment (2). Age at puberty as well as the interval from initiation of treatment to first estrus was lower when the gilts were exposed to an estrual female or a mature boar compared with gilts exposed to an anestrual, ovariectomized female or isolated from contact with other pigs. Decreasing the age at puberty was expected to decrease the weight at puberty, since gilts are younger and have had fewer days on feed; however, there was no effect of treatment on weight at puberty. Exposure to an estrual female hastens the return to estrus in weaned sows (11). Vandenbergh (16) found similar results in mice. Although prepubertal female mice exposed to a mature female reached puberty at a later age than those exposed to a mature male (P < O.OOS),the mice in that treatment group were significantly younger at puberty than the mice not receiving any exposure (P < 0.005). These results suggest that, although not as effective as male exposure, interaction with a mature female stimulates early puberty in mice. Exposure of prepubertal heifers to mature cows resulted in a decrease in the age at puberty (P < 0.01; interaction of treatment-by-sire breed effect during the first year of a study with heifers sired by Hereford, Charolais and Tarentaise bulls, but these effects were not observed during the second year with heifers sired by Hereford, Charolais, Jersey, Shorthorn, Tarentaise, Brahman and Longhorn bulls (10). It is not clear why there was a difference between the 2 yr, although the authors suggested that there may have been a difference in physiology and sensitivity to the stimuli. Pnmier and Mounier (13) have reported the results of an experiment designed to determine whether exposing prepubertal gilts to a mature, sexually intact female stimulated puberty. Forty gilts were allotted to 1 of 2 treatments: introduction of either a mature intact female or an ovariectomized female at 155 d of age. Although age at puberty was similar between the 2 treatment groups (23 1 + 24 d and 243 + 12 d, exposure to an intact female and exposure to an ovariectomized female, respectively), a higher proportion of gilts exposed to an intact female reached puberty before 225 d of age than those exposed to an ovariectomized female (7 of 19 vs 0 of 19, respectively; 1 prepubertal gilt in each treatment group was removed from the experiment early). However, the duration and frequency of estrus in the intact mature females was not reported, and thus it is difficult to determine the exact mechanism involved. Nevertheless, our results support the above findings. A similar set of experiments was conducted to determine the effect of contact with a female in estrus on the attainment of puberty in gilts (12). Experiment 1 compared boar exposure vs no boar exposure along with either removing gilts from the pen as soon as they were
Theriogenology
743
discovered to be in estrus or leaving estrual females with their pen-mates. Boar exposure stimulated puberty in these gilts compared with no boar exposure (P < 0.05). Although the mean age at puberty was similar, the degree of synchronization was better when estrual gilts were allowed to remain with their pen-mates (P < 0.001). Another experiment in Pearce’s study (12) involved exposing prepubertal gilts to anestrual or estrual ovariectomized sows. Sixty-four gilts were allotted to the following treatment groups: 1) gilts received no exposure (controls), 2) gilts were exposed to an ovariectomized anestrual sow, 3) gilts were exposed to an estrual ovariectomized sow, and 4) gilts were exposed to a mature boar. All 3 exposure treatments lasted 20 mm/d. Gilts exposed to an estrual sow or a mature boar were younger (P < 0.05) at puberty than the control gilts. There was no significant difference in the age at puberty or interval to puberty between the gilts exposed to an anestrual sow or to control gilts. There was also no significant difference in age at puberty or interval to puberty between gilts exposed to a boar or those exposed to an estrual sow. The results of Pearce (12) closely agree with those presented here. The interaction between gilts is intensified when one or more gilts are in standing heat. Stress caused by frequent mounting attempts and increased vocalization and activity in the estrual female may be an adequate stimulus for inducing precocious puberty in gilts. The higher percentage of gilts reaching puberty that were exposed to a mature boar during the trial period suggests that the additional exposure to pheromones present in the submaxillary gland of the boar had the greater effect on stimulating puberty in these gilts. Female to female interaction appears to play an important role in the onset of puberty in gilts. Although this treatment does not appear to be as effective as exposure to a mature boar, it is less time-consuming, less dangerous and easy to apply to a variety of production systems. For example, a producer could take a newly-weaned sow expected to return to estrus within 5 to 10 d, and introduce her into a pen of prepubertal females. This practice has an advantage over boar exposure treatment since the producer would be able to leave the sow in the pen unsupervised until she is to be reintroduced into the breeding herd. The short interval from initiation of treatment to estrus suggests that this treatment is most effective soon after it is begun. Although the age at puberty was numerically decreased with exposure to an estrual female compared with exposure to a mature boar in our present experiment, the means were not statistically different. Producers strive to increase productivity and to decrease the costs of production. One way to accomplish this is to decrease the age at puberty in gilts in order to decrease the total number of nonproductive days. Although exposure to a mature boar has been most effective in stimulating the onset of puberty in gilts, this practice is both time and labor-consuming and is potentially dangerous. Exposure to a mature estrual female, by contrast, could yield similar results without some of the drawbacks of boar exposure. REFERENCES 1. Brooks PH, Smith DA.. Ovulation rate and embryonic mortality in gilts reaching puberty at young ages. Anim Prod 1976;22:139 abstr. 2. Caton JS, Jesse GW, Day BN, Ellersieck MR. The effect of duration of boar exposure on the frequency of gilts reaching first estrus. J Anim Sci 1986;62:1210-1214.
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3. Christenson RK. Swine management to increase gilt reproductive efficiency. J Anim Sci 1986;63:1280-1287. 4. Diekman MA, Hoagland TA. Influence of supplemental lighting during periods of increasing or decreasing day length on the onset of puberty in gilts. J Anim Sci 1983;57:1235-1242. 5. El&son L. A study on puberty and estrus in gilts. J Vet Med 1989;36:46-54. 6. Flowers B, Cantley TC, Martin MJ, Day BN. Effect of elevated ambient temperatures on puberty in gilts. J Anim Sci 1989;67:779-784. 7. Holder RB, Lamberson WR, Bates RO, Sal&ski TJ. Lifetime productivity in gilts selected for decreased age at puberty. Anim Sci 1995;61: 115- 12 1. 8. Hughes PE, Cole DJA. Reproduction in the gilt. I. The influence of age and weight at puberty on ovulation rate and embryo survival in the gilt. Anim Prod 1975;21: 183-l 89. 9. Hughes PE. Factors affecting the natural attainment of puberty in the gilt. In: Control of Pig Reproduction. Butterworths Press, 1982. 10. Nelsen TC, Short RE, Phelps DA, Staigmiller RB. Nonpuberal estrus and mature cow influences on growth and puberty in heifers. J Anim Sci 1985;61:470-473. 11. Pearce GP, Pearce AN. Contact with a sow in oestrus or a mature boar stimulates the onset of oestrus in weaned sows. Vet Ret 1992;130:5-9. 12. Pearce GP. Contact with oestrus female pigs stimulates puberty in gilts. Vet Ret 1992;130:318-323. 13. Prunier A, Mounier AM. Influence of the presence of a mature female on puberty attainment in gilts. Theriogenology 1991;36:537-542. 14. Schukken YH, Buurman J, Huirne RBM, Willemse AH, Vernooy JCM, van den Broek J, Verheijden JHN. Evaluation of optimal age at first conception in gilts from data collected in commercial swine herds. J Anim Sci 1994;72:1387-1392. 15. Tess MW, Bennett GL, Dickerson GE. Simulation of genetic changes in life cycle efficiency of pork production. II. Effects of components on efficiency. J Anim Sci 1983;56:354-368. 16. Vandenbergh JG. Effect of the presence of a male on the sexual maturation of female mice. Endocrinology 1967;81:345-349.