Actividad Reproductiva Pelibuey y Sufolk arroyo 2007 PDF

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Reproducción, Ovinos, Pelo...

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Animal Reproduction Science 102 (2007) 24–30

Reproductive activity of Pelibuey and Suffolk ewes at 19◦ north latitude L.J. Arroyo a,b, J. Gallegos-S´ anchez c , A. Villa-Godoy a , J.M. Berruecos a , G. Perera a , J. Valencia a,∗ a

c

Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Aut´onoma de M´exico, M´exico 04510, D.F., M´exico b Universidad del Mar, Campus Puerto Escondido, Km. 3.5 Carr. Puerto Escondido-Sola de Vega, San Pedro Mixtepex-Juquila, 71980 Oaxaca, M´exico Especialidad de Postgrado en Ganader´ıa, Colegio de Posgraduados, Km. 36.5 Carr. M´exico-Texcoco, 56230 Texcoco, M´exico Received 3 April 2006; accepted 21 September 2006 Available online 20 October 2006

Abstract Under photoperiod regulated conditions, some Pelibuey ewes appear to express estrous cycles continuously throughout the year. Ovulatory activity of Suffolk ewes has not being determined at 19◦ N. The aim of the present study was to describe the annual reproductive cycle of Pelibuey and Suffolk ewes under natural conditions at 19◦ N. Ten adult ewes of each breed were maintained under natural environmental conditions, on a constant plane of nutrition and isolated from rams. The ovulatory activity of both breeds was monitored over 2 years (2003 and 2004) by quantifying progesterone concentrations in blood samples taken twice a week. For both breeds, the proportion of ovulating ewes per month and year was analyzed by χ2 . The duration of anestrus was compared between breeds and years by analysis of variance. Correlation of ambient temperature and weight changes with the ovulatory activity was evaluated by regression procedure. Ovulatory activity was different (P < 0.05) between breeds from February to July. Pelibuey sheep (60%, 6 of 10) ovulated continuously during the entire study; one animal was eliminated in the second year, due to ovarian follicular cysts and three ewes had anestrous periods from 65 ± 46 to 70 ± 36 days. Suffolk ewes displayed reproductive seasonality similar to that observed in sheep of the same breed in latitudes greater than 35◦ . Within breed, reproductive behavior of sheep was similar between years, with the only difference (P < 0.05) observed in February for Pelibuey and in July for Suffolk relative to other months. Ambient temperature was not correlated with ovulatory activity. The body weight of Pelibuey ewes was constant during the entire study and was not correlated with ovulatory activity. There was, however, an increase on the body weight of Suffolk ewes, but this variation was not related to ovulatory activity. These findings lead to the conclusion that at

∗

Corresponding author. Tel.: +52 56 22 58 60; fax: +52 56 16 71 10. E-mail address: [email protected] (J. Valencia).

0378-4320/$ – see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.anireprosci.2006.09.025

L.J. Arroyo et al. / Animal Reproduction Science 102 (2007) 24–30

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19◦ N, a high proportion of Pelibuey ewes is capable of ovulating throughout the year, whereas Suffolk ewes undergo seasonal anestrous periods similar to those observed in individuals of the same breed at latitudes greater than 35◦ . Identification of continuous ovulatory Pelibuey ewes may be the first step for developing a selection program against seasonality to increase lambing frequency. © 2006 Elsevier B.V. All rights reserved. Keywords: Ewe-breeding seasonality; Ovulatory activity; Seasonal anestrus; Photoperiod; Pelibuey; Suffolk

1. Introduction Seasonality of reproduction is a common feature in sheep breeds of temperate latitudes (Malpaux et al., 1997). Ovulatory activity of ewes is generally inhibited for several consecutive months of the year, referred to as the anestrous season, which occurs in Spring (Pelletier et al., 2000). The pineal hormone, melatonin, through its nocturnal mode of secretion, has been shown to be the primary transducer of photoperiodic information to the neuroendocrine reproductive axis (Malpaux et al., 1999, 2002). Seasonal ovulatory activity is clearly expressed in European breeds (in latitudes >35◦ ), such as Suffolk ewes (Hafez, 1952; Legan and Karsch, 1979; Karsch et al., 1984; Robinson and Karsch, 1984; Robinson et al., 1985; Malpaux et al., 1987). In contrast, seasonal anestrus in tropical hair sheep, once thought to be absent (Castillo et al., 1972, 1974; Valencia et al., 1975; Gonz´ alez-Reyna et al., 1991; Gonz´alez et al., 1992; Cruz et al., 1994), has been demonstrated in Pelibuey sheep of Mexico (Heredia et al., 1991; Valencia et al., 1981). In all these studies, males were used for estrous detection and this as well as factors other than photoperiod such as amount of nutritional intake, variations in environmental temperature or relative humidity could be responsible for the seasonal reproductive changes. Because of the conflicting results derived from studies under natural photoperiod conditions, the effects of artificial photoperiod in absence of males on Pelibuey sheep were examined. The first study showed that ewes are capable of responding to extreme variations in the day length by inhibiting (16L:8D) or stimulating (8L:16D) their ovulatory activity (Porras, 1999). Artificially simulated photoperiod typical of 19◦ north latitude, induced short anovulatory intervals from January to July (Cerna et al., 2000), thus even when the photoperiod gradient is short, Pelibuey ewes display anestrus when the day length increases. Porras (1999) and Cerna et al. (2000), respectively, observed two and three ewes expressing estrous cycles throughout the year, despite some of these ewes being under an inhibitory photoperiod. Later, Valencia et al. (2003), under natural photoperiod conditions (19◦ ) and in absence of males, identified Pelibuey ewes with ovulatory activity during the seasonal anestrous period (February–May). However, these findings were obtained in experiments that lasted between one season and 1 year. The impact that constant ovulating ewes would have on productivity, justifies a study designed for demonstrating that this trait is repeatable. Even though when Suffolk ewes are at 42◦ north latitude, the reproductive seasonality in Suffolk ewes is clearly expressed (Robinson and Karsch, 1984; Karsch et al., 1984; Robinson et al., 1985), it has been documented that European ewes (>35◦ north latitude) that inhabit or are transferred to equatorial regions tend to express estrous cycles at irregular intervals or show an undefined ovulatory season (Yeates, 1949; Hafez, 1952; Jansen and Jackson, 1993); nevertheless, a single study conducted at 19◦ N in which estrus was detected with the assistance of penis deviated rams, indicated that Suffolk ewes appear to have a defined anestrous season (De Lucas-Tron et al., 1997). The objective of this study was to characterize the ovulatory activity of Pelibuey and Suffolk ewes at 19◦ N, in absence of males and under controlled feeding.

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2. Materials and methods The study was conducted in an experimental farm located at 19◦ 13′ N. Adult Pelibuey native born ewes (n = 10), 3–5 years of age with a live weight of 54.97 ± 1.5 kg (mean ± S.D.) were used. Additionally, we included 10 adult Suffolk ewes that were descendent from a flock imported to Mexico at least 15 years ago, that had a previous reproductive season but remained nulliparous, and were 1.5 years old with a live weight of 89.2 ± 6.7 kg (mean ± S.D.). The animals were isolated from males throughout the study, and were maintained on a constant plane of nutrition using oat hay, alfalfa hay, corn silage and concentrate. Heparinized blood samples were obtained from all the ewes twice a week during 2 years (2003 and 2004). The samples were immediately centrifuged; plasma was collected and kept frozen at −20◦ C until assayed for progesterone (P4 ). P4 was quantified by a solid-phase radioimmunoassay (Pulido et al., 1991). Sensitivity of the assay was 0.02 ng/mL; intra- and inter-assay variation coefficients were 2.5% and 6.6%, respectively. Females were considered to be anestrus when progesterone remained below 1 ng/mL in eight or more consecutive samples (Porras, 1999), or to be having regular ovulatory activity when no more than two consecutive samples were below this concentration (Yuthasastrakosol et al., 1975; Walton et al., 1977; Bartlewski et al., 1998). Throughout the study, the body weight of all females was recorded every 2 weeks and the daily environmental temperature (mean, maximum and minimum) in the experimental farm were recorded. Proportion of ovulating and anestrous females within breeds in each month were compared between years by χ2 -test (Infante and Z´ arate, 1990). Although it was not the objective of the present study, we simultaneously evaluated the proportion of ovulating and anestrous ewes between breeds over months and years. Mean, maximal and minimal monthly values of ambient temperature were calculated from daily measurements; the association of these independent variarate, 1990). ables and ovulatory activity were estimated by correlation analysis (Infante and Z´ Duration of anestrus was compared between breeds and years by analysis of variance using PROC GLM (SAS, 1989). To verify diet impacts on body weight change for each breed, monthly variations in weight were regressed on proportion of ovulating females and correlation coefficients between these variables were determined by using PROC REG (SAS, 1989). 3. Results During the 2 years of study, ovulatory activity was different (P < 0.05) between breeds from February to June in 2003 and from February to July in 2004 (Table 1). From August to January, the reproductive behavior of both breeds was similar (Table 1). Ewes (60%, 6 of 10) had continuously occurring ovulations during the entire study (Fig. 1). One ewe was eliminated from the experiment during the second year due to ovarian follicular cysts and three had seasonal anestrous periods from 65 ± 46 to 70 ± 36 days (mean ± S.D.), which were shorter (P < 0.05) than in the Suffolk ewes (166 ± 43 to 198 ± 26 days; Table 2) and the interval of seasonal anestrus was similar among years within each breed (Table 2). In contrast, a greater proportion of Suffolk ewes showed anestrus in January and 100% had seasonal anestrus in February and March in 2003 and between March and June in 2004 (Table 1 and Fig. 1). There was no correlation between ambient temperature and ovulatory activity of sheep for either breed (data not shown). The body weight of Pelibuey ewes did not significantly vary during the study and was not correlated with ovulatory activity (data not shown). There was an increase on the body weight of Suffolk ewes, however, between 2003 and 2004 (83.7 ± 5 and 94.6 ± 2 kg, mean ± S.D., respectively), but this variation was not correlated to ovulatory activity of females (data not shown).

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Table 1 Monthly ovulatory activity (%) of Pelibuey and Suffolk ewes under natural environmental conditions (19◦ N), controlled feeding and absence of males Month

Breed Pelibuey

January February March April May June July August September October November December

Suffolk

Year 2003 (n = 10)

Year 2004 (n = 9)

Year 2003 (n = 10)

Year 2004 (n = 10)

100 a 100 a 100 a 100 a 100 a 100 a 90 a 90 a 80 a 90 a 100 a 80 a

77.7 a 66.6 b 77.7 a 100 a 100 a 100 a 100 a 100 a 100 a 100 a 100 a 100 a

70 a 0c 0b 10 b 10 b 20 b 80 a 80 a 90 a 100 a 100 a 100 a

50 a 10 c 0b 0b 0b 0b 10 b 80 a 100 a 100 a 100 a 100 a

Different letters (a, b, c) in the same row indicate differences (P < 0.05).

4. Discussion The results of this study showed that in the Mexican highland (19◦ N), there are Pelibuey ewes that are capable of having ovulation throughout the year. This finding is relevant because it opens the possibility to select ewes with this trait, a breeding scheme developed in the Merino D’Arles,

Fig. 1. Annual ovulatory activity in Pelibuey (gray bars) and Suffolk (black bars) ewes under natural environmental conditions (19◦ N), controlled feeding and in absence of males. Air temperature (- - -) and light hours (—).

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Table 2 Duration of the seasonal anestrus in Pelibuey and Suffolk ewes under natural environmental conditions (19◦ N), controlled feeding and absence of males Breed

Pelibuey Suffolk

n

3 10

Days of anestrus (mean ± S.D.) Year 2003

Year 2004

65 ± 46 a 166 ± 43 b

70 ± 36 a 198 ± 26 b

Values in a row or column with different letters (a, b) indicate differences (P < 0.05).

in which it has been determined that heritability as well as repeatability are high enough (20% and 30%, respectively) to establish genetic programs to control seasonality (Malpaux et al., 2002). A high proportion of these sheep were continuously ovulating throughout the year for two consecutive years, regardless of natural changes in photoperiod. Thus, according to data from the present study and those reported by Porras (1999), there might exist three different types of Pelibuey ewes. One type is the approximately 40% of the animals having a low threshold for sensitivity to the subtle changes of tropical photoperiod thus those with a regular anestrous season from 1 year to the next. A second group is the proportion of ewes that can be as great as 60% with a significant threshold for sensitivity to variations of day length, thus these ewes are insensible to the light shifts typical of 19◦ N, and continue to have estrous cycles throughout the year under these conditions. The third group of ewes (approximately 20%; Porras, 1999), with an extremely high threshold to being insensitive to photoperiodic changes, continue to have estrous cycles throughout the year even under annual photoperiodic changes typical of higher latitudes (>56◦ ). In contrast, under controlled nutrition and in absence of males, all Suffolk ewes had a defined anestrus. De Lucas-Tron et al. (1997), observed that Suffolk sheep showed estrus in presence of rams with deviated penis for 123 days (September–January). Therefore, inconsistent with previous information (Yeates, 1949; Hafez, 1952; Jansen and Jackson, 1993) about seasonal breeding ewes that inhabit or are transferred to equatorial or near equatorial regions that express estrous cycles at irregular intervals, or show an undefined ovulatory season; Suffolk ewes have a clearly defined seasonal anestrus. The end of seasonal anestrus in Suffolk ewes was different (P < 0.05) between the 2 years of study. Robinson and Karsch (1984) recorded annual behavioral variations at the beginning of the reproductive season in Suffolk sheep. This behavior is due to the capability of sheep to respond to annual changes in length of photoperiod; that is, it depends on the period at which the ewes become refractory to long inhibitory days (Robinson et al., 1985). It is, therefore, suggested that the neuroendocrine mechanisms involved in seasonal anestrus are functional in this breed, despite the fact that they are at 19◦ N. What are the physiological mechanisms that might determine three distinct patterns of behavior in Pelibuey females? Two hypotheses have been raised for local breeds under tropical latitude: either the females are insensitive to photoperiod, or photoperiodic changes are too small to impact the physiology for the females (Chemineau et al., 2004). Our data support the first hypothesis because even with the subtle changes of the tropical photoperiod, all the Suffolk and 40% of the Pelibuey ewes were capable of interpreting the light signal and experienced anestrus. In these ewes, the GnRH pulse generator is probably exquisitely sensitive to inhibition by estradiol (Karsch et al., 1984); the mechanism that is modulated by hypothalamic neurons that produce neurotransmitters with an inhibitory (dopamine, serotonine) or a stimulatory action (glutamate, aspartate). Within this frame of ideas, a question remains unanswered: what would be the physiological changes in the continuous ovulatory ewes? Probably in these ewes the lateral retrochiasmatic area is less

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sensitive to the negative effect of estradiol. This is possible because it was observed (GallegosS´anchez et al., 1997) that the changes in sensitivity to estradiol reside in these hypothalamic areas in seasonal ewes. In the present research, 3 of 10 Pelibuey ewes showed periods of anestrus both years but in the first year, anestrus occurred between July and December, after the summer solstice (June 21), when daylight hours begin to decrease; that is, there was no synchrony between the ceasing of ovulatory activity of these Pelibuey sheep and the classical photoperiod signal that sets the endogenous rhythm of sheep to initiate and induce cessation of seasonal anestrus (Karsch et al., 1984). In the second year, three sheep had anestrus when light hours increased (January–April), without an explanation of this variation between years, because neither ambient temperature nor changes in body weight could be related to this behavior. In Pelibuey sheep that displayed periods of anestrus during the first year, their endogenous rhythm has signaled for interruption of their ovulatory activity, without the photoperiod having regulated that event. Ambient temperature was not correlated with the ovulatory activity as previously had been demonstrated by Wodzicka-Tomaszewska et al. (1967). We conclude that at 19◦ N, a large proportion of Pelibuey females maintain continuous ovulatory activity throughout the year, whereas Suffolk ewes show seasonal anestrus associated with annual changes of photoperiod, even at low latitudes. Acknowledgments exico Research supported by project PAPIIT-IN205803. L.J. Arroyo thanks to CONACYT-M´ for supporting his Ph.D. studies. References Bartlewski, M.P., Beard, P.A., Cook, J.S., Rawlings, C.N., 1998. Ovarian follicular dynamics during anoestrus in ewes. J. Reprod. Fertil. 113, 275–285. Castillo, R.H., Valencia, Z.M., Berruecos, J.M., 1972. Comportamiento reproductivo del borrego Tabasco mantenido en clima tropical y subtropical. I: Indices de fertilidad. T´ ec. Pec. M´ex. 20, 52–56. Castillo, R.H., Rom´an, P.H., Berruecos, J.M., 1974. Caracter´ısticas del crecimiento del borrego Tabasco. I: Efecto de la edad y peso al destete y su influencia sobre la fertilidad de la madre. T´ ec. Pec. M´ex. 27, 28–32. Cerna, C., Porras, A., Valencia, M.J., Perera, G., Zarco, L., 2000. Effect of an inverse subtropical (19◦ 13′ N) photoperiod on ovarian activity, melatonin and prolactin secretion in Pelibuey ewes. Anim. Reprod. Sci. 60/61, 511–525. Chemineau, P., Daveau, A., Cogni´e, Y., Aumont, G., Chesneau, D., 2004. Seasonal ovulatory activity exists in tropical Creole female goats and Black Belly ewes subjected to a temperate photoperiod. BMC Physiol. 4, 12. Cruz, L.C., Fern´andez-Baca, S., Alvarez, L.J., P´erez, R.H., 1994. Variaciones estacionales en la presentaci´ on de la ovulaci´on, fertilizaci´on y sobrevivencia embrionaria de ovejas Tabasco en el tropico ´ h´umedo. Vet. M´ex. 25, 23–27. De Lucas-Tron, J., Gonz´alez, P.E., Mart´ınez, R.L., 1997. Estacionalidad reproductiva en ovejas de cinco razas en el altiplano central Mexicano. T´ ec. Pec. M´ex. 35, 25–31. Gallegos-S´anchez, J., Delalu, B., Caraty, A., Malpaux, B., Thi´ ery, J.C., 1997. Estradiol acts locally within the retrochiasmatic area to inhibit pulsatile LH release in the female sheep during anestrus. Biol. Reprod. 56, 1544–1549. exico: reproduction in the Pelibuey Gonz´alez-Reyna, A., Valencia, J., Foote, W.C., Murphy, B.D., 1991. Hair sheep in M´ sheep. Anim. Breed. Abstr. 59, 509–524. Gonz´alez, A., Murphy, B.D., Foote, W.C., Ortega, E., 1992. Circannual estrous variations and ovulation rate in Pelibuey ewes. Smal...