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Influence of the male effect on the reproductive performance of female Payoya goats implanted with melatonin at the winter solstice
Animal Reproduction Science 137 (2013) 183–188
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Animal Reproduction Science journal homepage: www.elsevier.com/locate/anireprosci
Influence of the male effect on the reproductive performance of female Payoya goats implanted with melatonin at the winter solstice I. Celi a , M.C. Gatica b , J.L. Guzmán a , L. Gallego-Calvo a , L.A. Zarazaga a,∗ a Departamento de Ciencias Agroforestales, Universidad de Huelva, “Campus de Excelencia Internacional Agroalimentario, ceiA3”, Carretera de Huelva-Palos de la Frontera s/n, 21819 Palos de la Frontera, Huelva, Spain b Universidad Arturo Prat, Avenida Arturo Prat, 2120 Iquique, Chile
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Article history: Received 4 June 2012 Received in revised form 24 January 2013 Accepted 29 January 2013 Available online 8 February 2013 Keywords: Goat Seasonality Melatonin Male effect Fertility
a b s t r a c t This research addressed the effect on reproductive performance of melatonin implants inserted at the winter solstice in Payoya goats. Female goats (n = 100) were divided into two experimental groups, one subjected and the other not subjected to the male effect. Half of each group was implanted with melatonin at the winter solstice; the remaining animals received no such hormone treatment. Oestrous activity, as detected by visual observation, was recorded daily using melatonin implanted bucks. Trans-rectal ultrasonography was used to estimate of time of ovulation. Corpus luteum activity was confirmed by plasma concentrations of progesterone greater than 0.5 ng/mL. Fecundity, fertility, prolificacy and productivity were calculated. Neither the male effect nor melatonin treatment alone influenced reproductive performance. The greater fecundity and fertility: 91.7% (P < 0.05) was obtained with melatonin implantation plus the male effect. Greater productivity occurred when melatonin was used (1.02 ± 0.10 compared with 0.76 ± 0.66 mean number of kids per female for melatonin and non-melatonin treated groups, respectively, P < 0.05). The present results show that the fertility of female Payoya goats implanted with melatonin at the winter solstice can be improved by subjecting females to the male effect. Moreover, productivity of does is enhanced when melatonin implants are used in comparison to productivity of non-treated females. © 2013 Elsevier B.V. All rights reserved.
1. Introduction The seasonal nature of reproduction in goats restricts the opportunities for meat and milk production by goat farmers. In Spain, goats breed in the August–September (end of summer) and February–March (end of winter) time periods (Fálagan et al., 1989; Gómez-Brunet et al.,
∗ Corresponding author at: Departamento de Ciencias Agroforestales, Universidad de Huelva, Carretera de Huelva-Palos de la Frontera s/n, 21819 Palos de la Frontera, Huelva, Spain. Tel.: +34 959 217 523; fax: +34 959 217 304. E-mail address: [email protected] (L.A. Zarazaga). 0378-4320/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.anireprosci.2013.01.015
2003; Zarazaga et al., 2005). The photoperiod appears to be the main environmental cue responsible for this seasonality, with long days inhibiting and short days stimulating ovarian activity (Malpaux et al., 1999; Zarazaga et al., 2011). Photoperiod conveyed by sun light influences melatonin synthesis (Bittman et al., 1983). This secretion is characterised by increased secretion during darkness and decreased secretion during the light hours (Reiter, 1991). Because goats are short-day breeders, attempts have been made to mimic the effect of short days by artificially prolonging the duration of increased concentrations of circulating melatonin. In goats, exogenously administered melatonin from continuous-slow-release implants advances the onset of
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the breeding season (Chemineau et al., 1992), and to induce a breeding period during what would normally be seasonal anoestrous (Zarazaga et al., 2009a). These implants can be used to increase the concentration of melatonin throughout the day, inducing a short-day-like response without suppressing the endogenous secretion of melatonin (O’Callaghan et al., 1991; Malpaux et al., 1997; Zarazaga et al., 2011). The commercial use of exogenous melatonin in goats was authorised in Spain in 2009. In higher latitudes, melatonin implants have traditionally been inserted around the summer solstice to advance the breeding season (Chemineau et al., 1996). However, in commercial Mediterranean flocks implants are usually inserted around the time of the spring equinox (Chemineau et al., 1996; Zarazaga et al., 2009a, 2012a,b). In sheep, the efficacy of implants is enhanced when insertion occurs at the winter solstice (Forcada et al., 2002). However, in goats, little is known about implant efficacy when insertion occurs at times other than the spring equinox. Following melatonin implantation, males and female goats are usually separated for 45 days, providing the conditions necessary to obtain a successful male effect and, therefore, greater synchronisation of time of oestrous. Although melatonin implantation at the spring equinox can induce reproductive activity during seasonal anoestrous in the absence of the male effect (Zarazaga et al., 2009a), however, its effects at other times (such as the winter solstice) are unknown, as is any modifying influence of the male effect. In fact, the male effect is not usually used to induce ovulation during the breeding season (which includes the winter solstice). During this period the hypothalamus–pituitary–ovary axis is active and did not respond with the expected increase in LH secretion as a result of exposure to males. Male exposure to females does not induce ovulation in oestrous cyclic females, but there is evidence that the introduction of novel males stimulates LH secretion in oestrous cyclic females (Hawken et al., 2007, 2009), and alters the distribution of oestrus activity in the herd (Chemineau, 1983; Hawken et al., 2008). The aim of the present research was to determine whether the reproductive performance of Payoya goats achieved with melatonin implants inserted at the winter solstice can be improved by introducing the male effect.
the last 10 months. Goats were assigned to four groups (n = 25, Fig. 1), balanced according to live weight, body condition score (Hervieu et al., 1991) and age: females treated with exogenous melatonin and subjected to the male effect (MEL-ME), females treated with exogenous melatonin but not subjected to the male effect (MEL-NME), females not treated with exogenous melatonin but subjected to the male effect (NMEL-ME), and females subjected to neither exogenous melatonin nor the male effect (NMEL-NME). Over the experimental period, these animals were maintained under intensive management and were fed daily with lucerne hay, barley straw (ad libitum), and commercial concentrate, according to INRA standards for maintaining adult weight and for providing adequate nutrition (Morand-Fehr and Sauvant, 1988). All animals had free access to water. Ovarian corpus luteum function prior to insertion of melatonin implants and buck introduction was determined by plasma concentrations of progesterone in blood samples collected weekly for three consecutive weeks in December and January. Goats were deemed oestrous cyclic if progesterone concentration was >0.5 ng/mL in at least two samples. This pattern of circulating progesterone is indicative of ovulation in Payoya goats (Zarazaga et al., 2005, 2009b).
2. Materials and methods
All males were fitted with a marking harnesses. Oestrous activity was recorded by direct visual observation every day of the marks left by the harnesses (WalkdenBrown et al., 1993).
2.1. Study conditions All procedures were performed by trained personnel in strict accordance with Spanish guidelines for the protection of experimental animals (RD 32/2007), and in agreement with European Union Directive 86/609. The study was conducted at the University of Huelva experimental farm (latitude 37◦ 15 N), which meets the requirements of the European Community Commission for Scientific Procedure Establishments (1986). 2.2. Animals and management The female experimental animals used were 100 adult, non-pregnant Payoya goats, all of which had kids within
2.3. Treatments: melatonin treatment and the male effect On 21 December, melatonin treated females received one implant containing melatonin (18 mg; Melovine® ; CEVA Salud Animal, Barcelona, Spain) at the base of the left ear (Zarazaga et al., 2009a). Also, on 21 December, eight bucks received three subcutaneous melatonin implants at the base of the left ear to increase libido. The females not to be subjected to the male effect were kept in permanent contact with the males (two per group) from the onset of the experiment. The females designated to be subjected to the male effect, however, were not introduced to the males (two per group) until 41 days after melatonin implantation. Bucks remained with the does for approximately 1 month. 2.4. Detection of oestrous behaviour
2.5. Measurements The occurrence of ovulation and ovulation rate were assessed by the presence and number of corpora lutea observed in each female by transrectal ultrasonography conducted 10 ± 2 days after the detection of oestrus (Simoes et al., 2005). Transrectal ultrasonography was performed using an Aloka SSD-500 apparatus connected to a 7.5 MHz linear probe. The presence of corpora lutea was confirmed via the concentrations of plasma progesterone. Weekly blood samples were taken from male introduction until the end of the mating period on February 28. The
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Weekly progesterone samples 3rd
10th
17th December
Weekly progesterone samples 14th 21st 28th January
Melatonin and 41 days of male isolation (MEL-ME, n=25) 41 days of male isolation (NMEL-ME, n=25)
Male effect (breeding period)
21st December Fifty females distributed into two groups
1st February
Weekly progesterone samples
Weekly progesterone samples 14th 21st 28th January
3rd
10th
17th December
Melatonin- for 41 days contact with males (MEL-NME, n=25) For 41 days contact with males (NMEL-NME, n=25)
21st December Fifty females distributed into two groups
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1st February
1st March
Breeding period
1st March
Fig. 1. Diagram showing the different experimental protocols and the number of females involved in each group. NMEL-NME: females subjected to neither exogenous melatonin nor the male effect; MEL-NME: females treated with exogenous melatonin but not subjected to the male effect; NMEL-ME: females not treated with exogenous melatonin but subjected to the male effect; MEL-ME: females treated with exogenous melatonin and subjected to the male effect.
percentage expressing oestrus with or without ovulations or ovulation in the absence of behavioural oestrus was ascertained from plasma concentrations of progesterone. Fecundity (pregnant does/does mounted by the males) was determined via transrectal ultrasonography on Day 45 after exposure to the males (Schrick et al., 1993). Fertility (percentage of goats kidding/does mounted by the males), prolificacy (number of kids born per female kidding) and productivity (number of kids born per female in each mating group) were also determined. 2.6. Blood sampling Blood samples were collected by jugular venipuncture in tubes containing heparin. Plasma was obtained after centrifugation at 3500 × g for 30 min and stored at −20 ◦ C until hormone concentrations were measured. Plasma progesterone was determined in duplicate samples using a commercial enzyme linked immunoassay (ELISA) kit (Ridgeway Science Ltd., Gloucester, UK), in accordance with the manufacturer’s instructions (Madgwick et al., 2005). The mean intra-assay and inter-assay coefficients of variation were 6.6% and 9.9%, respectively. The sensitivity of the assay was 0.1 ng/mL. Females with progesterone concentrations of ≥0.5 ng/mL were considered to have had ovulations (Chemineau et al., 1984; Zarazaga et al., 2009b). 2.7. Statistical analyses During the experiment one female from the MEL-ME and two from the NMEL-ME group died and data were discarded for these animals. The percentage of anovulatory
females at the time of implant insertion and at male introduction, females in each group that entered oestrus, and that showed oestrus and ovulation, fecundity and fertility were compared via the Chi-squared test for multiple group comparisons and Fisher’s exact probability test for two-group comparisons. Prolificacy was compared using the Mann–Whitney U test. Productivity was compared using factorial ANOVA with the experimental treatments as fixed effects. When differences between treatments were observed, a Duncan test was performed. All analyses were performed using the SPSS package (Statistical Package for the Social Sciences, 2008).
3. Results At the time of implant insertion, more females were anovulatory than ovulatory (58.0 compared with 42.0%, respectively, P < 0.05) and at mating period (63.3 compared with 36.7%, respectively, P < 0.01). Pregnancy rate at Day 45 (fecundity) and percent of females kidding (fertility) did not differ by treatment (Table 1). Fertility was greatest when females were implanted with melatonin and also subjected to the male effect (MEL-ME) (P < 0.05 compared to all other groups; Table 1). Similarly, productivity was also improved by melatonin treatment (1.02 ± 0.1 compared with 0.76 ± 0.1 kids born/female for MEL and NMEL groups, respectively, P < 0.05). Productivity was, therefore, also greater in the MEL-ME group compared to the NMELME and NMEL-NME groups (P < 0.05; Table 1). Although exposure to males appeared to have an additive effect (MEL-ME compared with MEL-NME) differences did not reach significance (P > 0.05).
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Table 1 Reproductive results for the four treatment groups: NMEL-NME: females subjected to neither exogenous melatonin nor the male effect; MEL-NME: females treated with exogenous melatonin but not subjected to the male effect; NMEL-ME: females not treated with exogenous melatonin but subjected to the male effect; and MEL-ME: females treated with exogenous melatonin and subjected to the male effect. Groups
NMEL-NME
MEL-NME
NMEL-ME
MEL-ME
n Anovulatory does at implant insertion (%) Anovulatory does at introduction of males (%) Females showing signs of oestrous (%) Females in oestrous and having ovulations (%) Fertility-Fecundity (%) Prolificacy Productivity
25 68.0 ± 0.09a 68.0 ± 0.09a 96.0 ± 0.04a 80.0 ± 0.08ab 64.0 ± 0.09b 1.13 ± 0.09a 0.72 ± 0.12b
25 56.0 ± 0.10a 72.0 ± 0.09a 92.0 ± 0.05a 68.0 ± 0.09b 60.0 ± 0.10b 1.40 ± 0.13a 0.84 ± 0.16ab
25 48.0 ± 0.10a 45.8 ± 0.10a 100 ± 0.00a 87.5 ± 0.07ab 65.2 ± 0.10b 1.27 ± 0.12a 0.79 ± 0.15b
25 60.0 ± 0.10a 66.7 ± 0.09a 100 ± 0.00a 95.8 ± 0.04a 91.7 ± 0.06a 1.32 ± 0.10a 1.21 ± 0.12a
Different letters in the same row reflect differences (P < 0.05).
4. Discussion The results show that melatonin implants inserted at the winter solstice improves the reproductive performance of female Payoya goats when does are subjected to the male effect. The percentage of females in anoestrous at implant insertion contrasts with figure for the same breed and under the same experimental conditions recorded in earlier research (Zarazaga et al., 2005). Although Zarazaga reported 90% of Payoya does having reproductive activity in December, under experimental conditions similar to those of the present study approximately 50% of the does were in anoestrus in the present study. The present results are also inconsistent with those ˜ reported by Gómez-Brunet et al. (2003) for the Malaguena breed. These authors observed 100% of does having corpus luteum activity in December. Differences may be attributed to the year of observation or differences among breeds. The lack of oestrous cyclicity prior to the introduction of the males did not prevent the positive effect of melatonin implants and the male effect (MEL-ME) on reproductive performance. This might be explained by the positive influence of melatonin on reproductive variables in oestrous cycling goats that, at least in part, have an effect at the ovary and uterus. Reduced rates of atresia for medium and large follicles at the beginning of the breeding season (Bister et al., 1999), and an increase in progesterone production by the corpora lutea (Durotoye et al., 1997), have been reported following melatonin treatment. Reproductive performance was similar among does in constant contact with bucks regardless of melatonin treatment indicating melatonin alone at the winter solstice does did not improve reproductive performance. This result is not consistent with previous observations obtained when melatonin was implanted at the spring equinox (Zarazaga et al., 2009a). The reason for this may lie in that, at the spring equinox, all the females were in “deep” anoestrous; no control female showed ovarian or oestrous activity, and contact with sexually active males or other females in oestrus was unable to induce reproductive activity during this period. However, the present experiment was performed at the onset of seasonal anoestrus; social cues, such as the presence of sexually active males and other females in oestrus, may be sufficient to stimulate sexual activity in previously anoestrous females.
The results of fecundity and fertility were the same, indicating that no embryo losses were observed during pregnancy after 45 days of pregnancy diagnosis. Fertility was improved by melatonin implantation (irrespective of the contact with males or the male effect) and productivity when melatonin implantation was in conjunction with the male effect (MEL-ME). This agrees with earlier results obtained using melatonin implants at the spring equinox in conjunction with the male effect (Zarazaga et al., 2012b). The improvement in productivity associated with implantation plus the male effect (MEL-ME) in comparison with females not treated with melotonin was due to the greater fertility of the treated female goats because no differences in prolificacy were observed. This group (MEL-ME) produced 0.42 more kids per female than the NMEL-ME group, and 0.49 more kids per female than the NMEL-NME group. This influence has been previously described in both goats (Zarazaga et al., 2012b) and dairy ewes (Abecia et al., 2007). In dairy animals, it is more important that females give birth than have a greater prolificacy. Reproductive performances, fertility and productivity, were not improved when melatonin treatment was not associated with the male effect. However, Kumar and Purohit (2009) observed a greater pregnancy rate in female goats injected with melatonin in January and not subjected to the male effect. As indicated previously, photoperiod cues can be modulated by social and nutritional factors, time of treatment and breed, which might explain these differences. The effect of melatonin implantation on the ovulation rate and prolificacy may vary widely in both sheep and goats. In sheep, treatment with melatonin improves the number of follicles from which ovulation occurred by reducing the atresia rate of medium and large follicles (Noël et al., 1999). In Rasa Aragonesa ewes, Forcada ˜ et al. (1995) and Zúniga et al. (2002) observed a positive effect of melatonin implants on ovulation rate. However, Zarazaga et al. (2009a), working with Payoya goats, and Santos et al. (2002), working with Florida goats, observed no effect of melatonin implants on ovulation rate and prolificacy, respectively. Additional effects of melatonin at the ovary have also been described, especially the improvement of luteal function and the ability of pineal hormone to increase luteal progesterone secretion in vivo (Wallace et al., 1988; Durotoye et al., 1997; Abecia et al., 2002). Certainly, in goats, melatonin treatment leads to more waves of
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ovarian follicular development, a consequence of the more rapid growth phase of the dominant follicles. Differences in the time for corpora lutea regression with exogenous melatonin have not been reported (Berlinguer et al., 2009). 5. Conclusions Melatonin implants inserted at the winter solstice improve fertility of Payoya goats when associated with the male effect and could be a useful tool to improve milk and meat production in Payoya goats. Conflict of interest None of the authors of this paper has any financial or personal relationship with any other person or organisation that might inappropriately influence or bias the content of the paper. Acknowledgments This research was funded by Grant PETRI 95-0964.OP from the C.I.C.Y.T. (Spain). The authors are grateful to CEVA Salud Animal, Barcelona, Spain, for providing Melovine® implants. We also thank Adrian Burton for revision of the English manuscript. References ˜ Abecia, J.A., Forcada, F., Zúniga, O., 2002. The effect of melatonin on the secretion of progesterone in sheep and on the development of ovine embryos in vitro. Vet. Res. Commun. 26, 151–158. Abecia, J.A., Valares, J.A., Forcada, F., Palacín, I., Martín, S., Martino, A., 2007. The effect of melatonin on the reproductive performance of three sheep breeds in Spain. Small Rumin. Res. 69, 10–16. Berlinguer, F., Leoni, G.G., Succu, S., Spezzigu, A., Madeddu, M., Satta, V., Bebbere, D., Contreras-Solis, I., Gonzalez-Bulnes, A., Naitana, S., 2009. Exogenous melatonin positively influences follicular dynamics, oocyte developmental competence and blastocyst output in a goat model. J. Pineal Res. 46, 383–391. Bister, J.-L., Noël, B., Perrad, B., Mandiki, S.N.M., Mbayahaga, J., Paquay, R., 1999. Control of ovarian follicles activity in the ewe. Domest. Anim. Endocrinol. 17, 315–328. Bittman, E.L., Dempsey, R.J., Karch, F.J., 1983. Pineal melatonin secretion drives the reproductive response to daylength in the ewe. Endocrinology 113, 2276–2283. Chemineau, P., 1983. Effect on oestrus and ovulation of exposing creole goats to the male at three times of the year. J. Reprod. Fertil. 67, 65–72. Chemineau, P., Malpaux, B., Delgadillo, J.A., Guerin, Y., Ravault, J.P., Thimonier, J., Pelletier, J., 1992. Control of sheep and goat reproduction: use of light and melatonin. Anim. Reprod. Sci. 30, 157–184. Chemineau, P., Malpaux, B., Pelletier, J., Leboeuf, B., Delgadillo, J.A., Deletang, F., Pobel, T., Brice, G., 1996. Use of melatonin implants and photoperiodic treatments to control seasonal reproduction in sheep and goats. INRA Prod. Anim. 9, 45–60 (in French, with English abstract). Chemineau, P., Poulin, N., Cognie, Y., 1984. Secrétion de progestérone au cours du cycle induit par l’introduction du mâle chez la chèvre créole en anoestrus: effets de la saison. Reprod. Nutr. Dev. 24, 557–561. Durotoye, L.A., Webley, G.E., Rodway, R.G., 1997. Stimulation of the production of progesterone by the corpus-luteum of the ewe by the perfusion of melatonin in vivo and by the treatment of granulosa cells with melatonin in vitro. Res. Vet. Sci. 62, 87–91. Fálagan, A., González, C., López, A., 1989. Períodos de anoestro de la cabra Murciano-Granadina en la región de Murcia. ITEA 9, 298–300. Forcada, F., Zarazaga, L., Abecia, J.A., 1995. Effect of exogenous melatonin and plane of nutrition after weaning on estrous activity, endocrine status and ovulation rate in Salz ewes lambing in the seasonal anestrus. Theriogenology 43, 1179–1193.
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Animal Reproduction Science journal homepage: www.elsevier.com/locate/anireprosci
Influence of the male effect on the reproductive performance of female Payoya goats implanted with melatonin at the winter solstice I. Celi a , M.C. Gatica b , J.L. Guzmán a , L. Gallego-Calvo a , L.A. Zarazaga a,∗ a Departamento de Ciencias Agroforestales, Universidad de Huelva, “Campus de Excelencia Internacional Agroalimentario, ceiA3”, Carretera de Huelva-Palos de la Frontera s/n, 21819 Palos de la Frontera, Huelva, Spain b Universidad Arturo Prat, Avenida Arturo Prat, 2120 Iquique, Chile
a r t i c l e
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Article history: Received 4 June 2012 Received in revised form 24 January 2013 Accepted 29 January 2013 Available online 8 February 2013 Keywords: Goat Seasonality Melatonin Male effect Fertility
a b s t r a c t This research addressed the effect on reproductive performance of melatonin implants inserted at the winter solstice in Payoya goats. Female goats (n = 100) were divided into two experimental groups, one subjected and the other not subjected to the male effect. Half of each group was implanted with melatonin at the winter solstice; the remaining animals received no such hormone treatment. Oestrous activity, as detected by visual observation, was recorded daily using melatonin implanted bucks. Trans-rectal ultrasonography was used to estimate of time of ovulation. Corpus luteum activity was confirmed by plasma concentrations of progesterone greater than 0.5 ng/mL. Fecundity, fertility, prolificacy and productivity were calculated. Neither the male effect nor melatonin treatment alone influenced reproductive performance. The greater fecundity and fertility: 91.7% (P < 0.05) was obtained with melatonin implantation plus the male effect. Greater productivity occurred when melatonin was used (1.02 ± 0.10 compared with 0.76 ± 0.66 mean number of kids per female for melatonin and non-melatonin treated groups, respectively, P < 0.05). The present results show that the fertility of female Payoya goats implanted with melatonin at the winter solstice can be improved by subjecting females to the male effect. Moreover, productivity of does is enhanced when melatonin implants are used in comparison to productivity of non-treated females. © 2013 Elsevier B.V. All rights reserved.
1. Introduction The seasonal nature of reproduction in goats restricts the opportunities for meat and milk production by goat farmers. In Spain, goats breed in the August–September (end of summer) and February–March (end of winter) time periods (Fálagan et al., 1989; Gómez-Brunet et al.,
∗ Corresponding author at: Departamento de Ciencias Agroforestales, Universidad de Huelva, Carretera de Huelva-Palos de la Frontera s/n, 21819 Palos de la Frontera, Huelva, Spain. Tel.: +34 959 217 523; fax: +34 959 217 304. E-mail address: [email protected] (L.A. Zarazaga). 0378-4320/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.anireprosci.2013.01.015
2003; Zarazaga et al., 2005). The photoperiod appears to be the main environmental cue responsible for this seasonality, with long days inhibiting and short days stimulating ovarian activity (Malpaux et al., 1999; Zarazaga et al., 2011). Photoperiod conveyed by sun light influences melatonin synthesis (Bittman et al., 1983). This secretion is characterised by increased secretion during darkness and decreased secretion during the light hours (Reiter, 1991). Because goats are short-day breeders, attempts have been made to mimic the effect of short days by artificially prolonging the duration of increased concentrations of circulating melatonin. In goats, exogenously administered melatonin from continuous-slow-release implants advances the onset of
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the breeding season (Chemineau et al., 1992), and to induce a breeding period during what would normally be seasonal anoestrous (Zarazaga et al., 2009a). These implants can be used to increase the concentration of melatonin throughout the day, inducing a short-day-like response without suppressing the endogenous secretion of melatonin (O’Callaghan et al., 1991; Malpaux et al., 1997; Zarazaga et al., 2011). The commercial use of exogenous melatonin in goats was authorised in Spain in 2009. In higher latitudes, melatonin implants have traditionally been inserted around the summer solstice to advance the breeding season (Chemineau et al., 1996). However, in commercial Mediterranean flocks implants are usually inserted around the time of the spring equinox (Chemineau et al., 1996; Zarazaga et al., 2009a, 2012a,b). In sheep, the efficacy of implants is enhanced when insertion occurs at the winter solstice (Forcada et al., 2002). However, in goats, little is known about implant efficacy when insertion occurs at times other than the spring equinox. Following melatonin implantation, males and female goats are usually separated for 45 days, providing the conditions necessary to obtain a successful male effect and, therefore, greater synchronisation of time of oestrous. Although melatonin implantation at the spring equinox can induce reproductive activity during seasonal anoestrous in the absence of the male effect (Zarazaga et al., 2009a), however, its effects at other times (such as the winter solstice) are unknown, as is any modifying influence of the male effect. In fact, the male effect is not usually used to induce ovulation during the breeding season (which includes the winter solstice). During this period the hypothalamus–pituitary–ovary axis is active and did not respond with the expected increase in LH secretion as a result of exposure to males. Male exposure to females does not induce ovulation in oestrous cyclic females, but there is evidence that the introduction of novel males stimulates LH secretion in oestrous cyclic females (Hawken et al., 2007, 2009), and alters the distribution of oestrus activity in the herd (Chemineau, 1983; Hawken et al., 2008). The aim of the present research was to determine whether the reproductive performance of Payoya goats achieved with melatonin implants inserted at the winter solstice can be improved by introducing the male effect.
the last 10 months. Goats were assigned to four groups (n = 25, Fig. 1), balanced according to live weight, body condition score (Hervieu et al., 1991) and age: females treated with exogenous melatonin and subjected to the male effect (MEL-ME), females treated with exogenous melatonin but not subjected to the male effect (MEL-NME), females not treated with exogenous melatonin but subjected to the male effect (NMEL-ME), and females subjected to neither exogenous melatonin nor the male effect (NMEL-NME). Over the experimental period, these animals were maintained under intensive management and were fed daily with lucerne hay, barley straw (ad libitum), and commercial concentrate, according to INRA standards for maintaining adult weight and for providing adequate nutrition (Morand-Fehr and Sauvant, 1988). All animals had free access to water. Ovarian corpus luteum function prior to insertion of melatonin implants and buck introduction was determined by plasma concentrations of progesterone in blood samples collected weekly for three consecutive weeks in December and January. Goats were deemed oestrous cyclic if progesterone concentration was >0.5 ng/mL in at least two samples. This pattern of circulating progesterone is indicative of ovulation in Payoya goats (Zarazaga et al., 2005, 2009b).
2. Materials and methods
All males were fitted with a marking harnesses. Oestrous activity was recorded by direct visual observation every day of the marks left by the harnesses (WalkdenBrown et al., 1993).
2.1. Study conditions All procedures were performed by trained personnel in strict accordance with Spanish guidelines for the protection of experimental animals (RD 32/2007), and in agreement with European Union Directive 86/609. The study was conducted at the University of Huelva experimental farm (latitude 37◦ 15 N), which meets the requirements of the European Community Commission for Scientific Procedure Establishments (1986). 2.2. Animals and management The female experimental animals used were 100 adult, non-pregnant Payoya goats, all of which had kids within
2.3. Treatments: melatonin treatment and the male effect On 21 December, melatonin treated females received one implant containing melatonin (18 mg; Melovine® ; CEVA Salud Animal, Barcelona, Spain) at the base of the left ear (Zarazaga et al., 2009a). Also, on 21 December, eight bucks received three subcutaneous melatonin implants at the base of the left ear to increase libido. The females not to be subjected to the male effect were kept in permanent contact with the males (two per group) from the onset of the experiment. The females designated to be subjected to the male effect, however, were not introduced to the males (two per group) until 41 days after melatonin implantation. Bucks remained with the does for approximately 1 month. 2.4. Detection of oestrous behaviour
2.5. Measurements The occurrence of ovulation and ovulation rate were assessed by the presence and number of corpora lutea observed in each female by transrectal ultrasonography conducted 10 ± 2 days after the detection of oestrus (Simoes et al., 2005). Transrectal ultrasonography was performed using an Aloka SSD-500 apparatus connected to a 7.5 MHz linear probe. The presence of corpora lutea was confirmed via the concentrations of plasma progesterone. Weekly blood samples were taken from male introduction until the end of the mating period on February 28. The
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Weekly progesterone samples 3rd
10th
17th December
Weekly progesterone samples 14th 21st 28th January
Melatonin and 41 days of male isolation (MEL-ME, n=25) 41 days of male isolation (NMEL-ME, n=25)
Male effect (breeding period)
21st December Fifty females distributed into two groups
1st February
Weekly progesterone samples
Weekly progesterone samples 14th 21st 28th January
3rd
10th
17th December
Melatonin- for 41 days contact with males (MEL-NME, n=25) For 41 days contact with males (NMEL-NME, n=25)
21st December Fifty females distributed into two groups
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1st February
1st March
Breeding period
1st March
Fig. 1. Diagram showing the different experimental protocols and the number of females involved in each group. NMEL-NME: females subjected to neither exogenous melatonin nor the male effect; MEL-NME: females treated with exogenous melatonin but not subjected to the male effect; NMEL-ME: females not treated with exogenous melatonin but subjected to the male effect; MEL-ME: females treated with exogenous melatonin and subjected to the male effect.
percentage expressing oestrus with or without ovulations or ovulation in the absence of behavioural oestrus was ascertained from plasma concentrations of progesterone. Fecundity (pregnant does/does mounted by the males) was determined via transrectal ultrasonography on Day 45 after exposure to the males (Schrick et al., 1993). Fertility (percentage of goats kidding/does mounted by the males), prolificacy (number of kids born per female kidding) and productivity (number of kids born per female in each mating group) were also determined. 2.6. Blood sampling Blood samples were collected by jugular venipuncture in tubes containing heparin. Plasma was obtained after centrifugation at 3500 × g for 30 min and stored at −20 ◦ C until hormone concentrations were measured. Plasma progesterone was determined in duplicate samples using a commercial enzyme linked immunoassay (ELISA) kit (Ridgeway Science Ltd., Gloucester, UK), in accordance with the manufacturer’s instructions (Madgwick et al., 2005). The mean intra-assay and inter-assay coefficients of variation were 6.6% and 9.9%, respectively. The sensitivity of the assay was 0.1 ng/mL. Females with progesterone concentrations of ≥0.5 ng/mL were considered to have had ovulations (Chemineau et al., 1984; Zarazaga et al., 2009b). 2.7. Statistical analyses During the experiment one female from the MEL-ME and two from the NMEL-ME group died and data were discarded for these animals. The percentage of anovulatory
females at the time of implant insertion and at male introduction, females in each group that entered oestrus, and that showed oestrus and ovulation, fecundity and fertility were compared via the Chi-squared test for multiple group comparisons and Fisher’s exact probability test for two-group comparisons. Prolificacy was compared using the Mann–Whitney U test. Productivity was compared using factorial ANOVA with the experimental treatments as fixed effects. When differences between treatments were observed, a Duncan test was performed. All analyses were performed using the SPSS package (Statistical Package for the Social Sciences, 2008).
3. Results At the time of implant insertion, more females were anovulatory than ovulatory (58.0 compared with 42.0%, respectively, P < 0.05) and at mating period (63.3 compared with 36.7%, respectively, P < 0.01). Pregnancy rate at Day 45 (fecundity) and percent of females kidding (fertility) did not differ by treatment (Table 1). Fertility was greatest when females were implanted with melatonin and also subjected to the male effect (MEL-ME) (P < 0.05 compared to all other groups; Table 1). Similarly, productivity was also improved by melatonin treatment (1.02 ± 0.1 compared with 0.76 ± 0.1 kids born/female for MEL and NMEL groups, respectively, P < 0.05). Productivity was, therefore, also greater in the MEL-ME group compared to the NMELME and NMEL-NME groups (P < 0.05; Table 1). Although exposure to males appeared to have an additive effect (MEL-ME compared with MEL-NME) differences did not reach significance (P > 0.05).
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Table 1 Reproductive results for the four treatment groups: NMEL-NME: females subjected to neither exogenous melatonin nor the male effect; MEL-NME: females treated with exogenous melatonin but not subjected to the male effect; NMEL-ME: females not treated with exogenous melatonin but subjected to the male effect; and MEL-ME: females treated with exogenous melatonin and subjected to the male effect. Groups
NMEL-NME
MEL-NME
NMEL-ME
MEL-ME
n Anovulatory does at implant insertion (%) Anovulatory does at introduction of males (%) Females showing signs of oestrous (%) Females in oestrous and having ovulations (%) Fertility-Fecundity (%) Prolificacy Productivity
25 68.0 ± 0.09a 68.0 ± 0.09a 96.0 ± 0.04a 80.0 ± 0.08ab 64.0 ± 0.09b 1.13 ± 0.09a 0.72 ± 0.12b
25 56.0 ± 0.10a 72.0 ± 0.09a 92.0 ± 0.05a 68.0 ± 0.09b 60.0 ± 0.10b 1.40 ± 0.13a 0.84 ± 0.16ab
25 48.0 ± 0.10a 45.8 ± 0.10a 100 ± 0.00a 87.5 ± 0.07ab 65.2 ± 0.10b 1.27 ± 0.12a 0.79 ± 0.15b
25 60.0 ± 0.10a 66.7 ± 0.09a 100 ± 0.00a 95.8 ± 0.04a 91.7 ± 0.06a 1.32 ± 0.10a 1.21 ± 0.12a
Different letters in the same row reflect differences (P < 0.05).
4. Discussion The results show that melatonin implants inserted at the winter solstice improves the reproductive performance of female Payoya goats when does are subjected to the male effect. The percentage of females in anoestrous at implant insertion contrasts with figure for the same breed and under the same experimental conditions recorded in earlier research (Zarazaga et al., 2005). Although Zarazaga reported 90% of Payoya does having reproductive activity in December, under experimental conditions similar to those of the present study approximately 50% of the does were in anoestrus in the present study. The present results are also inconsistent with those ˜ reported by Gómez-Brunet et al. (2003) for the Malaguena breed. These authors observed 100% of does having corpus luteum activity in December. Differences may be attributed to the year of observation or differences among breeds. The lack of oestrous cyclicity prior to the introduction of the males did not prevent the positive effect of melatonin implants and the male effect (MEL-ME) on reproductive performance. This might be explained by the positive influence of melatonin on reproductive variables in oestrous cycling goats that, at least in part, have an effect at the ovary and uterus. Reduced rates of atresia for medium and large follicles at the beginning of the breeding season (Bister et al., 1999), and an increase in progesterone production by the corpora lutea (Durotoye et al., 1997), have been reported following melatonin treatment. Reproductive performance was similar among does in constant contact with bucks regardless of melatonin treatment indicating melatonin alone at the winter solstice does did not improve reproductive performance. This result is not consistent with previous observations obtained when melatonin was implanted at the spring equinox (Zarazaga et al., 2009a). The reason for this may lie in that, at the spring equinox, all the females were in “deep” anoestrous; no control female showed ovarian or oestrous activity, and contact with sexually active males or other females in oestrus was unable to induce reproductive activity during this period. However, the present experiment was performed at the onset of seasonal anoestrus; social cues, such as the presence of sexually active males and other females in oestrus, may be sufficient to stimulate sexual activity in previously anoestrous females.
The results of fecundity and fertility were the same, indicating that no embryo losses were observed during pregnancy after 45 days of pregnancy diagnosis. Fertility was improved by melatonin implantation (irrespective of the contact with males or the male effect) and productivity when melatonin implantation was in conjunction with the male effect (MEL-ME). This agrees with earlier results obtained using melatonin implants at the spring equinox in conjunction with the male effect (Zarazaga et al., 2012b). The improvement in productivity associated with implantation plus the male effect (MEL-ME) in comparison with females not treated with melotonin was due to the greater fertility of the treated female goats because no differences in prolificacy were observed. This group (MEL-ME) produced 0.42 more kids per female than the NMEL-ME group, and 0.49 more kids per female than the NMEL-NME group. This influence has been previously described in both goats (Zarazaga et al., 2012b) and dairy ewes (Abecia et al., 2007). In dairy animals, it is more important that females give birth than have a greater prolificacy. Reproductive performances, fertility and productivity, were not improved when melatonin treatment was not associated with the male effect. However, Kumar and Purohit (2009) observed a greater pregnancy rate in female goats injected with melatonin in January and not subjected to the male effect. As indicated previously, photoperiod cues can be modulated by social and nutritional factors, time of treatment and breed, which might explain these differences. The effect of melatonin implantation on the ovulation rate and prolificacy may vary widely in both sheep and goats. In sheep, treatment with melatonin improves the number of follicles from which ovulation occurred by reducing the atresia rate of medium and large follicles (Noël et al., 1999). In Rasa Aragonesa ewes, Forcada ˜ et al. (1995) and Zúniga et al. (2002) observed a positive effect of melatonin implants on ovulation rate. However, Zarazaga et al. (2009a), working with Payoya goats, and Santos et al. (2002), working with Florida goats, observed no effect of melatonin implants on ovulation rate and prolificacy, respectively. Additional effects of melatonin at the ovary have also been described, especially the improvement of luteal function and the ability of pineal hormone to increase luteal progesterone secretion in vivo (Wallace et al., 1988; Durotoye et al., 1997; Abecia et al., 2002). Certainly, in goats, melatonin treatment leads to more waves of
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ovarian follicular development, a consequence of the more rapid growth phase of the dominant follicles. Differences in the time for corpora lutea regression with exogenous melatonin have not been reported (Berlinguer et al., 2009). 5. Conclusions Melatonin implants inserted at the winter solstice improve fertility of Payoya goats when associated with the male effect and could be a useful tool to improve milk and meat production in Payoya goats. Conflict of interest None of the authors of this paper has any financial or personal relationship with any other person or organisation that might inappropriately influence or bias the content of the paper. Acknowledgments This research was funded by Grant PETRI 95-0964.OP from the C.I.C.Y.T. (Spain). The authors are grateful to CEVA Salud Animal, Barcelona, Spain, for providing Melovine® implants. We also thank Adrian Burton for revision of the English manuscript. References ˜ Abecia, J.A., Forcada, F., Zúniga, O., 2002. The effect of melatonin on the secretion of progesterone in sheep and on the development of ovine embryos in vitro. Vet. Res. Commun. 26, 151–158. Abecia, J.A., Valares, J.A., Forcada, F., Palacín, I., Martín, S., Martino, A., 2007. The effect of melatonin on the reproductive performance of three sheep breeds in Spain. Small Rumin. Res. 69, 10–16. Berlinguer, F., Leoni, G.G., Succu, S., Spezzigu, A., Madeddu, M., Satta, V., Bebbere, D., Contreras-Solis, I., Gonzalez-Bulnes, A., Naitana, S., 2009. Exogenous melatonin positively influences follicular dynamics, oocyte developmental competence and blastocyst output in a goat model. J. Pineal Res. 46, 383–391. Bister, J.-L., Noël, B., Perrad, B., Mandiki, S.N.M., Mbayahaga, J., Paquay, R., 1999. Control of ovarian follicles activity in the ewe. Domest. Anim. Endocrinol. 17, 315–328. Bittman, E.L., Dempsey, R.J., Karch, F.J., 1983. Pineal melatonin secretion drives the reproductive response to daylength in the ewe. Endocrinology 113, 2276–2283. Chemineau, P., 1983. Effect on oestrus and ovulation of exposing creole goats to the male at three times of the year. J. Reprod. Fertil. 67, 65–72. Chemineau, P., Malpaux, B., Delgadillo, J.A., Guerin, Y., Ravault, J.P., Thimonier, J., Pelletier, J., 1992. Control of sheep and goat reproduction: use of light and melatonin. Anim. Reprod. Sci. 30, 157–184. Chemineau, P., Malpaux, B., Pelletier, J., Leboeuf, B., Delgadillo, J.A., Deletang, F., Pobel, T., Brice, G., 1996. Use of melatonin implants and photoperiodic treatments to control seasonal reproduction in sheep and goats. INRA Prod. Anim. 9, 45–60 (in French, with English abstract). Chemineau, P., Poulin, N., Cognie, Y., 1984. Secrétion de progestérone au cours du cycle induit par l’introduction du mâle chez la chèvre créole en anoestrus: effets de la saison. Reprod. Nutr. Dev. 24, 557–561. Durotoye, L.A., Webley, G.E., Rodway, R.G., 1997. Stimulation of the production of progesterone by the corpus-luteum of the ewe by the perfusion of melatonin in vivo and by the treatment of granulosa cells with melatonin in vitro. Res. Vet. Sci. 62, 87–91. Fálagan, A., González, C., López, A., 1989. Períodos de anoestro de la cabra Murciano-Granadina en la región de Murcia. ITEA 9, 298–300. Forcada, F., Zarazaga, L., Abecia, J.A., 1995. Effect of exogenous melatonin and plane of nutrition after weaning on estrous activity, endocrine status and ovulation rate in Salz ewes lambing in the seasonal anestrus. Theriogenology 43, 1179–1193.
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the males, receive melatonin implants. Reprod. Domest. Anim. 47, 436–442. ˜ O., Forcada, F., Abecia, J.A., 2002. The effect of melatonin implants Zúniga, on the response to the male effect and on the subsequent cyclicity of Rasa Aragonesa ewes implanted in April. Anim. Reprod. Sci. 72, 165–174.