- Email: [email protected]
Fertility of the early postpartum, lactating domestic rabbit
THERIOGENOLOGY
FERTILITY OF THE EARLY POSTPARTUM, LACTATING DOMESTIC RABBIT
I. C. Lamb,1,3 G. G. Partridge,1 M. F. Fuller' and P. A. Racey2 1Department of Biochemistry Rowett Research Institute Bucksburn, Aberdeen AB2 9SB, United Kingdom *Department of Zoology University of Aberdeen Tillydrone Avenue, Aberdeen AB9 2TN, United Kingdom
Received for publication: July 22, 1987
Accepted:
Apri?,
1,
1988
ABSTRACT
Sixty-four crossbred primiparous lactating does each suckling six pups were allocated at random into four groups and were mated on either Day 1, 2, 3, or 4 post partum (where Day 0 = the day of parturition). They were subsequently killed on Day 10 post coitum (where Day 0 = the day of mating) to assess fertility. There were no significant differences between treatment groups in their mating response (97% overall), ovulation response (77% overall), implantation response (83% overall), implantation rate (8.7 overall), or preimplantation mortality rate (24% overall). Ovulation rate was significantly increased in does mated on Days 3 and 4 (13.3 and 13.1, respectively), compared with those mated on Day 1 (10.2, P
rabbit, lactation, postpartum, fertility
Acknowledgments 3Present address: Poultry Science Department, The Ohio State University, Ohio Agricultural Research and Development Center, Wooster, OH 44691, USA. I.C.Lamb acknowledges receipt of a Science and Engineering Research Council Postgraduate Studentship. The authors wish to thank Miss M. Findlay and Mrs. W.Buchan for their care of the animals.
JULY 1988 VOL. 30 NO. 1
75
THERIOGENOLOGY
and an increase in preimplantation embryo mortality (5) of lactating does following remating soon after parturition. Others (1, 2, 5-9) have reported no such reduction in these components of fertility. The present experiment was therefore undertaken to resolve this contradictory evidence relating to the fertility of the lactating rabbit in the early postpartum period. MATERIALS AND METHODS Animals Primiparous crossbred does, the progeny of New Zealand White (N.Z.W.) male rabbits (bucks) and Californian x N.Z.W. does were housed individually in standard flat deck cages described previously by Spreadbury (10). House temperature was maintained between 18 and 20°C. A cycle of 14 h light and 10 h dark (lights on 0700 h) was used. This photoperiodic regimen has previously been shown (9) to prevent the seasonal depression in reproduction in this species (11). Does had unrestricted access to a supply of water and a pelleted diet based on grassmeal, wheat offal, soybean meal and ground oats, which contained 12 MJ digestible energy/kg dry matter and 154 g digestible crude protein/kg dry matter. Before parturition, does were provided with a nest box as described by Partridge and Allan (12). On the day of parturition (Day 0), 80 does weighing (mean + SEM) 4199 + 22 g and 171 d of age (range 170 to 190 d) were allocated at random to one of four experimental treatments (20 per treatment) to be mated on either Day 1, 2, 3 or 4 post partum and subsequently killed on Day 10 post coitum. All does suckled litters of six pups, the litters being adjusted soon after parturition. Any doe losing pups from her litter was discarded from the experiment. Does and their litters were weighed at birth, on the day of mating, and on Days 7 and 11 post partum. Sexual Behavior Does were tested for mating with ten different mature fertile bucks. On the day of testing, between 0800 and 1000 h, does were randomly placed with a buck for a period of five minutes to obtain a successful mating, This procedure was repeated with other bucks if mating did not occur. A doe was recorded as mating, as described previously (1). Does refusing to mate with all ten bucks on the day of testing were discarded from the experiment in order to remove any conditioning effect due to contact with the bucks. Fertility Two measures of fertility were examined in this experiment: 1) the occurrence of ovulation following mating and 2) the occurrence of implantation following ovulation. Does were killed by cervical dislocation, and the uterus, fallopian tubes and ovaries were removed and dissected free of adipose and mesenteric tissue. Where ovulation had occurred, a count of corpora lutea was made to establish the ovulation rate. The number of antimesometrial swellings in each uterine horn was counted to establish the implantation rate. If implantation had not occurred, the uterine horns were opened and the
76
JULY 1988 VOL. 30 NO. 1
THEFUOGENOLOGY
endometrium examined under a binocular dissecting microscope (x 400 magnification) for sites of decidual reaction. Statistical Analysis Data were analyzed using the Chi-square test (X2) and analysis of variance with any subsequent individual treatment contrasts evaluated using Student's t-test. RESULTS The sexual behavior and fertility of does mated on Days 1 to 4 post partum are shown in Table 1. Of the 80 does starting the experiment, 16 (20%) were removed because of failure to maintain a litter size of six pups. Does removed for this reason were distributed approximately equally across the four experimental treatments, leaving the adjusted starting numbers for each treatment given in Table 1. There was no significant treatment difference (P
JULY 1988 VOL. 30 NO. I
77
22.0
22.0
Preimplantation ova loss (%)d
Preimplantation ova loss (%)e
31.0
17.0
8.121.02 (9)
17 88.0 (15/17) 73.0 (U/15) 82.0 (9/11) 9.6t0.74ce (11)
46.0
28.0
9.450.08 (9)
15 100.0 (15/15) 80.0 (12/15) 75.0 (9/12) 13.3+0.73bd (15)
46.0
29.0
9.6k1.08 (8)
__
N.S.
N.S.
15 _100.0 (15/15) N.S. 73.0 (H/15) N.S. 73.0 (8/11) 13.1+0.62bd (:&0.05) *(cd P
4
Significance level
aMating response - expressed as the percentage of does mating when presented to the male. bOvulation response - expressed as the percentage of does ovulating in response to mating. CImplantation response - expressed as the percentage of does ovulating, having implantation sites. dThe number of ova lost prior to implantation expressed as a percentage of the total corpora lutea observed, excluding those does losing all their preimplantation ova. eThe number of ova lost prior to implantation expressed as a percentage of the total corpora lutea observed, including those does losing all their preimplantation ova. Number of animals shown in parentheses. *Mean values with different superscripts are significantly different at the levels indicated.
7.950.87 (14)
100.~7(17,17) 82.0 (14/17) 100.0 (14/14) 10.2~0.67~~ (14)
Implantation rate (a + SEM)
N Mating response (%)a Ovulation response (%)b Implantation response (%)c Ovulation rate (? + SEM)
1
Day of mating post partum 2 3
Fertility of does mated on Days 1 to 4 post partum
Fertility component
Table 1.
?
!z
8
i
THERIOGENOLOGY
ovulation are operating in these does and are probably similar to those exhibited by the estrous rabbit (17-19). However, the failure of 23% of does to ovulate despite mating normally indicates some dysfunction of the ovulatory mechanism distal to the coital stimulus input, probably involving part or all of the hypothalamic-pituitary-ovarian axis. Breed and Hillard (20) have reported that ovarian function is not affected by lactation or by the stimulus of suckling, and this is supported indirectly by Adams (21) and Foxcroft and Hasnain (l), who showed that ovarian follicular development is increased in the period prior to parturition and early post partum, respectively. This suggests that the hypothalamic pituitary axis may be the site of endocrine abnormalities causing anovulation. Labhsetwar (22) has reported that the luteinizing hormone (LH) content of the pituitary gland is lower in rabbits at parturition than in estrous controls. The precise nature of these endocrine abnormalities remains to be determined. It is unlikely, that progesterone would prevent ovulation (23) since plasma concentrations of this hormone are basal prior to parturition (24). Similarly, estrogens which are present in high concentrations around parturition (and thus probably during the preovulatory period) do not prevent ovulation occurring (25) but are more likely to be beneficial by sensitizing the pituitary gland to gonadotrophin-releasing hormone (23). It has been shown that lactation or the suckling stimulus (1, 6) reduce the ovulation response of does in the early postpartum period and, as in other species (26), this may involve some interaction between prolactin and gonadotrophin release. The ovulation rate of does increased significantly (see Table 1) as the day of mating post partum was delayed. Examination of the data from those does which ovulated and subsequently implanted ova revealed a similar but nonsignificant trend for doe weight at mating. A significant relationship (P
JULY
1988 VOL. 30 NO. 1
79
rHERIOGENOLOGY
findings (1, 2, 5) and suggests that pregnancy is probably being supported by functional corpora lutea (2, 20). For does that exhibited partial ova loss, the implantation rate was related to the ovulation rate and is described overall by the equation: Y = 1.03 + 0.80084 X; 0.12193 SEM, r = 0.76 (where Y = implantation rate; X = ovulation rate). A similar relationship has been reported previously in this species (28). Causes of partial ova loss will include fertilization failure, genetic abnormalities, abnormal ovum/embryo development, or transport and implantation dysfunction. From this experiment, it was not possible to define to what extent each was responsible for ova loss. The total loss of ova before implantation observed in some does probably resulted from genetic abnormalities, abnormal ovum/embryo development or transport,or corpus luteum regression, because examination of uteri from these does revealed no evidence of decidual reaction; therefore, failure of implantation does not appear to be responsible for ova loss. Furthermore, examination of service records revealed no differences in fertility between males, suggesting that failure of the male was not responsible for ova loss, and fertilization probably occurred to some extent in all does, as found by Foxcroft and Hasnain (5). Assuming that abnormal ovum/embryo development or transport and corpus lutewn regression were mainly responsible for ova loss, it is probable that they were caused by endocrine abnormalities (28). REFERENCES 1.
Foxcroft, G.R. and Hasnain, H. Effects of suckling and time to mating after parturition on reproduction in the domestic rabbit. J. Reprod. Fertil. 3:367-377 (1973).
2.
Torres, S., Gerard, M. and Thibault, C. Fertility factors in lactating rabbits mated 24 hours and 25 days after parturition. Ann. Biol. Anim. Bioch. Biophys. 1;2:63-69 (1977).
3.
Prud'hon, R., Rouvier, R., Cael, J. and Bel, L. Action of the birth-mating interval on the fertility and prolificacy of rabbits. Annls. Zootech. u:317-329 (1969).
4.
Surdeau, P., Perrier, G., Sartorio, J.M. and Valentin, D. Comparison of two reproductive rhythms in the meat rabbit. results. Annls. Zootech. a:136 abstr. (1979).
First
5.
Foxcroft, G.R. and Hasnain, H. Embryonic mortality in the postparturient domestic rabbit. J. Reprod. Fertil. =:315-318 (1973).
6.
Harned, M.A. and Casida, L.E. Some postpartum reproductive phenomena in the domestic rabbit. J. Anim. Sci. =:785-788 (1969).
7.
Foxcroft, G.R. Reproductive Physiology of the Post-parturient Domestic Rabbit. Ph.D. Thesis. University of Nottingham, U.K., 1972.
JULY 1988 VOL. 30 NO. 1
THERIOGENOLOGY
8.
Prud'hon, M. and Bel, L. Early weaning of young rabbits and reproduction of does. Annls. Zootech. =:23-30 (1968).
9.
Partridge, G.G., Allan, S.J., Findlay, M. and Corrigall, W. The effects of reducing the remating interval after parturition on the reproductive performance of the commercial doe rabbit. Anim. Prod. %:465-472 (1984).
10.
Spreadbury, D. Nutrient Requirements of the Growing Rabbit. Ph.D. Thesis. University of Aberdeen, U.K., 1975.
11.
Bradbury, J.T. Seasonal incidence of anestrus in the postpartum rabbit. Anat. Rec. a:424 abstr. (1944).
12.
Partridge, G.G. and Allan, S.J. The effects of different intakes of crude protein on nitrogen utilization in the pregnant and lactating rabbit. Anim. Prod. 35:145-155.
13.
Partridge, G.G., Foley, S. and Corrigall, W. Reproductive performance in purebred and crossbred commercial rabbits. Anim. Prod. 2:325-331 (1981).
14.
Beyer, C. and Rivaud, N. Sexual behaviour in pregnant and lactating domestic rabbits. Physiol. Behav. 4:753-757 (1969).
15.
Challis, J.R.G., Davies, 1.3. and Ryan, K.J. The concentration of progesterone, estrone and estradiol-178 in the plasma of pregnant rabbits. Endocrinology %:971-976 (1973).
16.
Beyer, C. and McDonald, P. Hormonal control of sexual behaviour in the female rabbit. a: Bishop, M.W.H. (ed.). Advances in Reproductive Physiology. Vol. 6. Elek Science, London, 1973, pp. 185-219.
17.
Tsou, R.C., Daily, R.A., McLanahan, C.S., Parent, A.D., Tindall, G.T. and Neill, J.D. Luteinizing hormone releasing hormone (LHRH) levels in pituitary stalk plasma during the preovulatory gonadotrophin surge of rabbits. Endocrinology m:534-539 (1977).
18.
Osteen, K.G. and Mills, T.M. Serum LH and FSH levels in the pregnant rabbit. Proc. Expt. Biol. Med. m:454-457 (1979).
19.
Chung, H.Wu, Blasco, L., Flickinger, G.L. and Mikhail, G. Ovarian function in the preovulatory rabbit. Biol. Reprod. x:304-308 (1977).
20.
Breed, W.G. and Hilliard, J. Effect of lactation on ovarian function in the rabbit. J. Reprod. Fertil. =:73-78 (1970).
21.
Adams, C.E. Ovarian response to human chorionic gonadotrophin and egg transport in the pregnant and post-parturient rabbit. J. Endocr. 40:101-105 (1968).
JULY 1988 VOL. 30 NO. 1
81
I’HERIOGENOLOGY
22.
Labhsetwar, A.P. Pituitary luteinizing hormone content of unmated, pseudopregnant, pregnant and progesterone treated rabbits. J. Reprod. Fertil. B:415-418 (1972).
23.
Carlson, J.C. and Perrin, D.G. The effect of LH-RH administration on LH release in the female rabbit. J. Reprod. Fertil. 2:175-180 (1979).
24.
Harrington, F.E. and Rothermel, J.D. Daily changes in peripheral plasma progesterone concentrations in pregnant and pseudopregnant rabbits. Life Sci. a:1333-1340 (1977).
25.
LeMaire, W.J., Janson, P.O., Kallfelt, B.J., Holmes, P.V., Cajander, S., Bjersing, L. and Ah&n, K.E.B. The preovulatory decline in follicular oestradiol is not required for ovulation in the rabbit. Acta Endocr. m:452-457 (1982).
26.
McNeilly, A.S. Prolactin and the control of gonadotrophin secretion in the female. J. Reprod. Fertil. =:537-549 (1980).
27.
Gregory, P.W. The potential and actual fecundity of some breeds of rabbits. J. Exp. 2001. m:271-285 (1932).
28.
Adams, C.E. Studies on prenatal mortality in the rabbit: the amount and distribution of loss before and after implantation. J. Endocr. =:325-344 (1960).
82
JULY 1988 VOL. 30 NO. 1
FERTILITY OF THE EARLY POSTPARTUM, LACTATING DOMESTIC RABBIT
I. C. Lamb,1,3 G. G. Partridge,1 M. F. Fuller' and P. A. Racey2 1Department of Biochemistry Rowett Research Institute Bucksburn, Aberdeen AB2 9SB, United Kingdom *Department of Zoology University of Aberdeen Tillydrone Avenue, Aberdeen AB9 2TN, United Kingdom
Received for publication: July 22, 1987
Accepted:
Apri?,
1,
1988
ABSTRACT
Sixty-four crossbred primiparous lactating does each suckling six pups were allocated at random into four groups and were mated on either Day 1, 2, 3, or 4 post partum (where Day 0 = the day of parturition). They were subsequently killed on Day 10 post coitum (where Day 0 = the day of mating) to assess fertility. There were no significant differences between treatment groups in their mating response (97% overall), ovulation response (77% overall), implantation response (83% overall), implantation rate (8.7 overall), or preimplantation mortality rate (24% overall). Ovulation rate was significantly increased in does mated on Days 3 and 4 (13.3 and 13.1, respectively), compared with those mated on Day 1 (10.2, P
rabbit, lactation, postpartum, fertility
Acknowledgments 3Present address: Poultry Science Department, The Ohio State University, Ohio Agricultural Research and Development Center, Wooster, OH 44691, USA. I.C.Lamb acknowledges receipt of a Science and Engineering Research Council Postgraduate Studentship. The authors wish to thank Miss M. Findlay and Mrs. W.Buchan for their care of the animals.
JULY 1988 VOL. 30 NO. 1
75
THERIOGENOLOGY
and an increase in preimplantation embryo mortality (5) of lactating does following remating soon after parturition. Others (1, 2, 5-9) have reported no such reduction in these components of fertility. The present experiment was therefore undertaken to resolve this contradictory evidence relating to the fertility of the lactating rabbit in the early postpartum period. MATERIALS AND METHODS Animals Primiparous crossbred does, the progeny of New Zealand White (N.Z.W.) male rabbits (bucks) and Californian x N.Z.W. does were housed individually in standard flat deck cages described previously by Spreadbury (10). House temperature was maintained between 18 and 20°C. A cycle of 14 h light and 10 h dark (lights on 0700 h) was used. This photoperiodic regimen has previously been shown (9) to prevent the seasonal depression in reproduction in this species (11). Does had unrestricted access to a supply of water and a pelleted diet based on grassmeal, wheat offal, soybean meal and ground oats, which contained 12 MJ digestible energy/kg dry matter and 154 g digestible crude protein/kg dry matter. Before parturition, does were provided with a nest box as described by Partridge and Allan (12). On the day of parturition (Day 0), 80 does weighing (mean + SEM) 4199 + 22 g and 171 d of age (range 170 to 190 d) were allocated at random to one of four experimental treatments (20 per treatment) to be mated on either Day 1, 2, 3 or 4 post partum and subsequently killed on Day 10 post coitum. All does suckled litters of six pups, the litters being adjusted soon after parturition. Any doe losing pups from her litter was discarded from the experiment. Does and their litters were weighed at birth, on the day of mating, and on Days 7 and 11 post partum. Sexual Behavior Does were tested for mating with ten different mature fertile bucks. On the day of testing, between 0800 and 1000 h, does were randomly placed with a buck for a period of five minutes to obtain a successful mating, This procedure was repeated with other bucks if mating did not occur. A doe was recorded as mating, as described previously (1). Does refusing to mate with all ten bucks on the day of testing were discarded from the experiment in order to remove any conditioning effect due to contact with the bucks. Fertility Two measures of fertility were examined in this experiment: 1) the occurrence of ovulation following mating and 2) the occurrence of implantation following ovulation. Does were killed by cervical dislocation, and the uterus, fallopian tubes and ovaries were removed and dissected free of adipose and mesenteric tissue. Where ovulation had occurred, a count of corpora lutea was made to establish the ovulation rate. The number of antimesometrial swellings in each uterine horn was counted to establish the implantation rate. If implantation had not occurred, the uterine horns were opened and the
76
JULY 1988 VOL. 30 NO. 1
THEFUOGENOLOGY
endometrium examined under a binocular dissecting microscope (x 400 magnification) for sites of decidual reaction. Statistical Analysis Data were analyzed using the Chi-square test (X2) and analysis of variance with any subsequent individual treatment contrasts evaluated using Student's t-test. RESULTS The sexual behavior and fertility of does mated on Days 1 to 4 post partum are shown in Table 1. Of the 80 does starting the experiment, 16 (20%) were removed because of failure to maintain a litter size of six pups. Does removed for this reason were distributed approximately equally across the four experimental treatments, leaving the adjusted starting numbers for each treatment given in Table 1. There was no significant treatment difference (P
JULY 1988 VOL. 30 NO. I
77
22.0
22.0
Preimplantation ova loss (%)d
Preimplantation ova loss (%)e
31.0
17.0
8.121.02 (9)
17 88.0 (15/17) 73.0 (U/15) 82.0 (9/11) 9.6t0.74ce (11)
46.0
28.0
9.450.08 (9)
15 100.0 (15/15) 80.0 (12/15) 75.0 (9/12) 13.3+0.73bd (15)
46.0
29.0
9.6k1.08 (8)
__
N.S.
N.S.
15 _100.0 (15/15) N.S. 73.0 (H/15) N.S. 73.0 (8/11) 13.1+0.62bd (:&0.05) *(cd P
4
Significance level
aMating response - expressed as the percentage of does mating when presented to the male. bOvulation response - expressed as the percentage of does ovulating in response to mating. CImplantation response - expressed as the percentage of does ovulating, having implantation sites. dThe number of ova lost prior to implantation expressed as a percentage of the total corpora lutea observed, excluding those does losing all their preimplantation ova. eThe number of ova lost prior to implantation expressed as a percentage of the total corpora lutea observed, including those does losing all their preimplantation ova. Number of animals shown in parentheses. *Mean values with different superscripts are significantly different at the levels indicated.
7.950.87 (14)
100.~7(17,17) 82.0 (14/17) 100.0 (14/14) 10.2~0.67~~ (14)
Implantation rate (a + SEM)
N Mating response (%)a Ovulation response (%)b Implantation response (%)c Ovulation rate (? + SEM)
1
Day of mating post partum 2 3
Fertility of does mated on Days 1 to 4 post partum
Fertility component
Table 1.
?
!z
8
i
THERIOGENOLOGY
ovulation are operating in these does and are probably similar to those exhibited by the estrous rabbit (17-19). However, the failure of 23% of does to ovulate despite mating normally indicates some dysfunction of the ovulatory mechanism distal to the coital stimulus input, probably involving part or all of the hypothalamic-pituitary-ovarian axis. Breed and Hillard (20) have reported that ovarian function is not affected by lactation or by the stimulus of suckling, and this is supported indirectly by Adams (21) and Foxcroft and Hasnain (l), who showed that ovarian follicular development is increased in the period prior to parturition and early post partum, respectively. This suggests that the hypothalamic pituitary axis may be the site of endocrine abnormalities causing anovulation. Labhsetwar (22) has reported that the luteinizing hormone (LH) content of the pituitary gland is lower in rabbits at parturition than in estrous controls. The precise nature of these endocrine abnormalities remains to be determined. It is unlikely, that progesterone would prevent ovulation (23) since plasma concentrations of this hormone are basal prior to parturition (24). Similarly, estrogens which are present in high concentrations around parturition (and thus probably during the preovulatory period) do not prevent ovulation occurring (25) but are more likely to be beneficial by sensitizing the pituitary gland to gonadotrophin-releasing hormone (23). It has been shown that lactation or the suckling stimulus (1, 6) reduce the ovulation response of does in the early postpartum period and, as in other species (26), this may involve some interaction between prolactin and gonadotrophin release. The ovulation rate of does increased significantly (see Table 1) as the day of mating post partum was delayed. Examination of the data from those does which ovulated and subsequently implanted ova revealed a similar but nonsignificant trend for doe weight at mating. A significant relationship (P
JULY
1988 VOL. 30 NO. 1
79
rHERIOGENOLOGY
findings (1, 2, 5) and suggests that pregnancy is probably being supported by functional corpora lutea (2, 20). For does that exhibited partial ova loss, the implantation rate was related to the ovulation rate and is described overall by the equation: Y = 1.03 + 0.80084 X; 0.12193 SEM, r = 0.76 (where Y = implantation rate; X = ovulation rate). A similar relationship has been reported previously in this species (28). Causes of partial ova loss will include fertilization failure, genetic abnormalities, abnormal ovum/embryo development, or transport and implantation dysfunction. From this experiment, it was not possible to define to what extent each was responsible for ova loss. The total loss of ova before implantation observed in some does probably resulted from genetic abnormalities, abnormal ovum/embryo development or transport,or corpus luteum regression, because examination of uteri from these does revealed no evidence of decidual reaction; therefore, failure of implantation does not appear to be responsible for ova loss. Furthermore, examination of service records revealed no differences in fertility between males, suggesting that failure of the male was not responsible for ova loss, and fertilization probably occurred to some extent in all does, as found by Foxcroft and Hasnain (5). Assuming that abnormal ovum/embryo development or transport and corpus lutewn regression were mainly responsible for ova loss, it is probable that they were caused by endocrine abnormalities (28). REFERENCES 1.
Foxcroft, G.R. and Hasnain, H. Effects of suckling and time to mating after parturition on reproduction in the domestic rabbit. J. Reprod. Fertil. 3:367-377 (1973).
2.
Torres, S., Gerard, M. and Thibault, C. Fertility factors in lactating rabbits mated 24 hours and 25 days after parturition. Ann. Biol. Anim. Bioch. Biophys. 1;2:63-69 (1977).
3.
Prud'hon, R., Rouvier, R., Cael, J. and Bel, L. Action of the birth-mating interval on the fertility and prolificacy of rabbits. Annls. Zootech. u:317-329 (1969).
4.
Surdeau, P., Perrier, G., Sartorio, J.M. and Valentin, D. Comparison of two reproductive rhythms in the meat rabbit. results. Annls. Zootech. a:136 abstr. (1979).
First
5.
Foxcroft, G.R. and Hasnain, H. Embryonic mortality in the postparturient domestic rabbit. J. Reprod. Fertil. =:315-318 (1973).
6.
Harned, M.A. and Casida, L.E. Some postpartum reproductive phenomena in the domestic rabbit. J. Anim. Sci. =:785-788 (1969).
7.
Foxcroft, G.R. Reproductive Physiology of the Post-parturient Domestic Rabbit. Ph.D. Thesis. University of Nottingham, U.K., 1972.
JULY 1988 VOL. 30 NO. 1
THERIOGENOLOGY
8.
Prud'hon, M. and Bel, L. Early weaning of young rabbits and reproduction of does. Annls. Zootech. =:23-30 (1968).
9.
Partridge, G.G., Allan, S.J., Findlay, M. and Corrigall, W. The effects of reducing the remating interval after parturition on the reproductive performance of the commercial doe rabbit. Anim. Prod. %:465-472 (1984).
10.
Spreadbury, D. Nutrient Requirements of the Growing Rabbit. Ph.D. Thesis. University of Aberdeen, U.K., 1975.
11.
Bradbury, J.T. Seasonal incidence of anestrus in the postpartum rabbit. Anat. Rec. a:424 abstr. (1944).
12.
Partridge, G.G. and Allan, S.J. The effects of different intakes of crude protein on nitrogen utilization in the pregnant and lactating rabbit. Anim. Prod. 35:145-155.
13.
Partridge, G.G., Foley, S. and Corrigall, W. Reproductive performance in purebred and crossbred commercial rabbits. Anim. Prod. 2:325-331 (1981).
14.
Beyer, C. and Rivaud, N. Sexual behaviour in pregnant and lactating domestic rabbits. Physiol. Behav. 4:753-757 (1969).
15.
Challis, J.R.G., Davies, 1.3. and Ryan, K.J. The concentration of progesterone, estrone and estradiol-178 in the plasma of pregnant rabbits. Endocrinology %:971-976 (1973).
16.
Beyer, C. and McDonald, P. Hormonal control of sexual behaviour in the female rabbit. a: Bishop, M.W.H. (ed.). Advances in Reproductive Physiology. Vol. 6. Elek Science, London, 1973, pp. 185-219.
17.
Tsou, R.C., Daily, R.A., McLanahan, C.S., Parent, A.D., Tindall, G.T. and Neill, J.D. Luteinizing hormone releasing hormone (LHRH) levels in pituitary stalk plasma during the preovulatory gonadotrophin surge of rabbits. Endocrinology m:534-539 (1977).
18.
Osteen, K.G. and Mills, T.M. Serum LH and FSH levels in the pregnant rabbit. Proc. Expt. Biol. Med. m:454-457 (1979).
19.
Chung, H.Wu, Blasco, L., Flickinger, G.L. and Mikhail, G. Ovarian function in the preovulatory rabbit. Biol. Reprod. x:304-308 (1977).
20.
Breed, W.G. and Hilliard, J. Effect of lactation on ovarian function in the rabbit. J. Reprod. Fertil. =:73-78 (1970).
21.
Adams, C.E. Ovarian response to human chorionic gonadotrophin and egg transport in the pregnant and post-parturient rabbit. J. Endocr. 40:101-105 (1968).
JULY 1988 VOL. 30 NO. 1
81
I’HERIOGENOLOGY
22.
Labhsetwar, A.P. Pituitary luteinizing hormone content of unmated, pseudopregnant, pregnant and progesterone treated rabbits. J. Reprod. Fertil. B:415-418 (1972).
23.
Carlson, J.C. and Perrin, D.G. The effect of LH-RH administration on LH release in the female rabbit. J. Reprod. Fertil. 2:175-180 (1979).
24.
Harrington, F.E. and Rothermel, J.D. Daily changes in peripheral plasma progesterone concentrations in pregnant and pseudopregnant rabbits. Life Sci. a:1333-1340 (1977).
25.
LeMaire, W.J., Janson, P.O., Kallfelt, B.J., Holmes, P.V., Cajander, S., Bjersing, L. and Ah&n, K.E.B. The preovulatory decline in follicular oestradiol is not required for ovulation in the rabbit. Acta Endocr. m:452-457 (1982).
26.
McNeilly, A.S. Prolactin and the control of gonadotrophin secretion in the female. J. Reprod. Fertil. =:537-549 (1980).
27.
Gregory, P.W. The potential and actual fecundity of some breeds of rabbits. J. Exp. 2001. m:271-285 (1932).
28.
Adams, C.E. Studies on prenatal mortality in the rabbit: the amount and distribution of loss before and after implantation. J. Endocr. =:325-344 (1960).
82
JULY 1988 VOL. 30 NO. 1