' .
Chapter
2:
Seasonal variation in reproductive performance of commercial herdsLiterature review '•·
Seasonal infertility - the disorder and its causes
Seasonal infertility (SI) is the tenn used to describe a complex syndrome with multiple causes which affects reproductive perfonnance of sows and boars (Hennessy, 1 987a) during summer and autumn. Production losses associated with the problem are more serious in continental climates than in Mediterranean and tropical climates (Leman, 1986). The condition has been reported from many European countries-Greece (Menegatos, 1 987), Portugal (Vieira and Vieira, 1 987), Spain (Perez and Gutierrez, 1 987), Yugoslavia (Cerne, 1 987), Italy (Mattioli, 1 987), U. S. A. (Hurtgen and Leman, 1 980) but is not considered to be a serious problem in Ireland (Lynch and Kearney, 1986) and Belgium (Robijns, 1 987). It occurs in large pig breeding units in Britain (Stone, et al., 1 986; Wrathall, 1 987) and has also been reported in one other island country, New Zealand (Sprey, 1980). The prevalence of seasonal infertility is highest in late summer and early autumn, but in some herds, signs are present throughout the whole year. In the northern hemisphere, fertility may be reduced by 10-30% during June to September, compared with the rest of the year.
According to Hennessy (1 987a), the signs of a seasonal infertility problem include:
• an increased weaning to mating interval
• delayed onset of puberty and/or poor oestrus expression in gilts
• decreased litter size
• increased prevalence of stillbirths and/or mummified foetuses
Love ( 1 9 8 1 a) considered the following signs to be indicative of a seasonal infertility problem:
• delayed onset of oestrus after weaning in a larger proportion of sows
• an increased number of sows with mating to return oestrus intervals greater than
24 days
• increased incidence of abortions
• an increased number of sows "not in pig" shortly before expected farrowing date
He did not consider a higher proportion of returns to oestrus at intervals of 1 8-24 days, or a reduction in litter size to be reliable indicators of a seasonal infertility problem (Love, 1 981 a).
•
Observed anoestrus is more likely to be due to reduced behavioural expression of oestrus rather than a true anoestrus, since it is usually accompanied by ovulation (Love, 1 98 l a). By far the most important aspect of the seasonal infertility is a reduced farrowing rate (Love et al., 1 993), commonly evidenced by delayed (>24 days) return to oestrus (usually 25 to 35 days after mating) (Love, 1981a). In summer the incidences of failure to maintain pregnancy and delayed return to oestrus are increased (Dial and Xue, 1 993). Wrathall ( 1 987) noted that
'·
problems associated with summer included depressed fertility in boars, delayed puberty in
gilts (Carneron, 1 980), delayed post-weaning oestrus and a higher incidence of returns to oestrus following mating (Cameron, 1 980). Te Brake and Aalbers ( 1987) reported that the proportion of sows coming into oestrus within seven days of weaning was lowest during the summer months. They also reported that conception rates to first mating and litter sizes were lowered during spring and winter time respectively. On the other hand, analyses of 33 herds through 1 980-1983 in North-western Germany indicated that the smallest litters were born in summer and the largest in winter; and that the age at first mating and the weaning to oestrus interval reached a maximum in summer and autumn and a minimum in winter (Plonait and Lahrmann, 1 987). Wrathall (1987) suggested that environmental temperatures might not be causally associated with autumn abortions as autumn abortions have been reported predominantly from cooler parts (more northerly latitudes) of Europe and North America
Using plasma progesterone levels 1 8-21 days after mating as the criterion for diagnosis, Williarnson et al. ( 1 980) were able to categorise seasonal infertility into 3 distinct classes:
• high progesterone levels indicating pregnancy or a luteinized ovarian cyst
• low progesterone levels indicating non-pregnancy
• high progesterone levels 1 0 days after the first test indicating cycling with undetected oestrus
More recently, Claus and Weiler (1994) have hypothesised that seasonal infertility results from the effects of stressors that cause early embryonic deaths, luteinized ovarian cysts, small ovarian cysts, poor oestrus expression or undetected early abortions, and caution against it being regarded simply as a consequence of embryonic death, or endocrine imbalance.
The majority of sows returning to oestrus during summer do so between 25 and 38 days post service (Love, 1981b; Leman, 1 986; Reilly and Roberts, 1 99 1 ) with a secondary small peak occurring between 46 and 57 days (Reilly and Roberts, 1991 ). This phenomenon appears to be associated with the maximum daily temperatures during the period and to be unrelated to minimum daily temperature or daily duration of sunlight (Reilly and Roberts, 1 991). A retrospective study of pig farms in the U. K. showed that SI did not decrease liner size (Reilly and Roberts, 1 99 1 ). Conversely, Martinat-Botte (1 987) recorded reduced litter sizes in sows
in Brittany which were mated during the latter part of winter/spring period, lower fertility with summer matings.
Multiparous sows returned to oestrus after weaning earlier than did primiparous sows but the risk of post-weaning oestrus failure was higher in primiparous sows, especially during summer and autumn (Hurtgen et al., 1980b; Hurtgen and Leman, 1980; Love, 1 98 l a). The interval between weaning and oestrus was shortest in autumn at 5 -6 days, and extended to more than 30 days after weaning in summer (Ciaus and Weiler, 1987). These authors also reported improved conception rates in autumn/early winter matings and then again in May/June in Germany. However Hurtgen et al. (1 980a) pointed out that while most sows have a normal weaning to oestrus interval, a minority of sows (and in particular the parity one group) have considerably prolonged weaning to oestrus intervals (>30 days) and thus increase the mean interval. Wu ( 1986) found the incidence of delayed puberty in gilts was highest in summer, particularly for pure-bred Hampshire and Landrace gilts (Wu, 1986). Seasonal variations in litter size were more pronounced in sows than in gilts (te Brake and Aalbers,
1 987).
Many researchers have analysed data from case studies, but cohort studies have also been conducted to evaluate the effect of heat treatments, changes in the photoperiod, alterations to animal husbandry procedures, other stressors known to cause hormonal changes and changes in eating habits. Some authors consider seasonal infertility to be a natural phenomenon with the signal for reduced fertility coming from decreasing day length (Leman, 1 986).
The literature review to this point has clearly shown that SI is essentially a collective term which conveniently describes a wide range of infertility manifestations in pigs including the following:
• increased weaning to oestrus intervals
• delayed onset of puberty in gilts and/or poor oestrus expression in gilts and sows
• increased incidence of return to service in gilts/sows
• increased incidence of abortions
• increased incidence of "not in pig" gilts/ sows
• increased prevalence of stillbirths and/or mummified foetuses
• decreased litter sizes and/or numbers of pigs born alive
Seasonal infertility on boars
While there is not universal agreement on the issue, some authors classify the following conditions in boars as seasonal infertility:
• decreased libido
• decreased sperm concentration and/or total sperm count
• decreased volumes per ejaculate
Causes of seasonal infertility
For purposes of discussion, the various causes of seasonal infertility may be conveniently classified as:
�
I
• effects of photoperiod on SI • effects of heat on SI • effects of housing on SI • effects of stress on SI• effects of season on hormonal system
• effects of nutrition on SI
• effects of the boar on SI
Photoperiod and seasonal infertility (SI)
Pigs are essentially short-day breeding animals (Peacock et al., 1 987) and the seasonal breeding effect is largely determined by changes in the daily photoperiod. Photoperiodism is the outstanding environmental factor involved in seasonal alterations to reproductive responses (Mauget, 1 987; Love et al., 1 993).
High light intensity and neural pathways
The natural light mechanisms which influence seasonal breeding in farm animals are complex and subject to dynamic change. The length of day (or night) has a greater influence on photoperiodic responses than light quality (Fraser and Broom, 1990) and photoperiodism induced breeding responses are readily produced if the natural day length is extended with artificial lighting of very low intensity. While the duration of the photoperiod is more
important than the intensity of light, adequate light intensity is critical for the generation of • � distinct circadian rhythms of melatonin which play an impt>rtant role in regulation of fertility
(Love et al., 1 993). Love et al. ( 1 993) also points out that while the critical light intensity has not yet been precisely determined, reliable induction of a nocturnal melatonin rise appears to require a light intensity of 200-300 lux.
light is received by the eye and transmitted initially to the brain via the optic nerve. One of the first fields of projection is the suprachiasmatic nucleus (SCN) in the hypothalamus. This site must be considered of paramount importance for light-induced rhythms, including
reproductive rhythms. From the SCN, fibres project to the paraventricular nucleus (PVN) of the hypothalamus and from there using the medial forebrain bundle (MFB) via the reticular formation into the intermediolateral cell column (IML) of the spinal cord. An important
· ...
outflow of fibres from the IML is to the superior cervical ganglion; which in turn uses the nervi conarii to direct the potential signal into the pineal gland.
_,. A signal is also sent from the retina to the pineal gland via the sympathetic pathways. In the
pineal gland, the neural message is changed to a humoral message (indoleamine melatonin) which affects the photoperiodic response in both long-day and short-day breeders. All mammals have a daily nocturnal rise in melatonin concentration (Peacock et al., 1987). The pineal gland has an important role in the transduction of photoperiodic information and parenchymatous pinealomas are associated with depressed gonadal function. It is considered that light is transmitted to the mammalian pineal via sympathetic fibres and it is probable that dark is transmitted via cholinergic pathways (Maxwell et al., 1991). Light provides an inhibitory stimulus to the sympathetics and reduces pineal activity while augmented activity of the gland during darkness is due to a normally high tonic rate of somatic activity. In addition, the pineal gland may have its own independent rhythms of activity. The pineal is believed to have an antigonadal effect in mammals and a progonadal effect in birds (Maxwell et al., 1 99 1 ). In various domestic mammals, the light photoperiod facilitates the release of gonadotropic hormones whereas the dark photoperiod results in their increased synthesis. Prolongation of the light photoperiod causes decreased gonadotropin production consequent to a fatigue phenomenon brought about by inadequate duration of the dark photoperiod (Maxwell et al., 1 991). Long photoperiods increase the sensitivity of the GnRH pulse generator to the negative feedback effects of oestrogen, markedly decreasing LH pulsatility. In the absence of ovarian steroids, long photoperiods have considerably less influence on LH pulsatility (Love et al., 1 993). Evidence that the pineal gland may exert its antigonadotropic effect via the hypothalamic areas concerned with gonadotropin-releasing factors came from an experiment which demonstrated that the degree of acceleration of pubertal onset in female rats was the same following pinealectomy as for rats with anterior-basal hypothalarnic lesions. The pineal gland does not induce persistent oestrus in constant light but has a role in controlling cycle length when photoperiods are shorter (Maxwell et al., 1991).
Melatonin
significance when animals are transferred to new latitudes (Yeates et al., 1 975). Photoperiod influences melatonin secretion and English et al. (1 986) suggest that the duration of melatonin secretion is an important factor in the transduction process of photoperiod information in sheep. Ewes must be exposed to a minimal period of long days before they are able to respond to short days, either by early pubertal development or by an early onset of oestrous cycles in adults (English et al., 1 9 86). In immature female rats melatonin causes a decrease in ovarian growth. Melatonin has been found to be concentrated not only in the pineal gland, but also in the iris, ovary, brain, pituitary and vagina In humans, melatonin has been shown to increase progesterone synthesis by the corpus luteum and stimulate the incorporation of acetate-l -14C into androstenedione in the ovarian stroma Melatonin thus seems capable of exerting a direct stimulatory effect on human ovarian steroidogenesis (Maxwell et al., 1 99 1 ).
Ellendorff and McConnell ( 1987) report that melatonin secretion in pigs remained at baseline levels in both short - dark ( 1 6 h light : 8 h
dark)
or long - dark (8 h light : 16 h dark) conditions, but there was a clear nocturnal surge of melatonin under 1 2 h light : 1 2 h dark conditions in 4 of 5 animals investigated in spring and in 2 of 4 animals following a 9 day adaptation period in autumn. Love et al. (1993) considers that nocturnal increases in melatonin are most likely to occur in pigs maintained under high light intensities and fed ad libitum.The effects of duration of light periods on fertilily
In a study of seasonal infertility in Cornwall (a mild climate county in the
UK)
Hancock ( 1 988) reported that the period of subfertility coincided with the period of maximum total monthly hours of direct sunlight.In a study by Peacock et al. ( 1 987) in which sows were exposed to 1 6 h, 8 h, and natural photoperiods, no difference was found in weaning-to-oestrus interval, conception rate, farrowing rate or litter size. The same authors found that gradual reduction of light from 15 h 20 minutes by 20 minutes per week for 1 month resulted in a reduction of the weaning-to-oestrus interval from 23.6 days with natural photoperiod to 5 .7 days under the lighting programme (Peacock et al., 1 987).
It seems that pigs are unable to respond appropriately to sudden changes in photoperiod (Love et al., 1 993). Perera et al. (1980) showed that sows exposed to a 24 hour-light regime exhibited behavioural oestrus for a longer period than those in a 12 hour-light : 12 hour-dark regime. The number of days to oestrus from weaning, conception rate, and litter size were the same for both light regimens and maximum serum levels of LH and oestrogen showed no differences. Mattioli et al. (1 987) reported that a constant long day photoperiod (14 h light :
..
• •
I 0 h dark) did not affect the weaning to oestrus interval but significantly improved the farrowing rate throughout the year (see summary information in Table 2-1 ). In line with previous proposals by Maxwell et aL (1991), Relkin (1976) proposed that the duration of the dark photoperiod, rather than the amount of light per day or the light : dark ratio, determines reproductive organ activity.
Table
2-1:
Summary information· for 3 separate studies on the effect of various light periods on sow fertilityPeacock et Peacock et al. (1987) Peacock et al. (1987) Mattiole
aL (1980) et aL (1987)
Time exposed 24 h 16 h 8 h natural 1 5 h 20 min. 14 h
to light (-20 minJweek for 1 mth.)
Wean-to- none none none none reduced from none
service interval 23.6 d to 5.7 d
Conception none none none none
rate
Farrowing none none none improved
rate
Liner none none none none
size
Oestrous longer than
behaviour 12 h
Onset of puberty
Increasing day length advances the onset of puberty in gilts but temperature may interact with photoperiod in a more complex way. Thus while spring-born animals are stimulated to reach puberty earlier, this photoperiod effect is inhibited by high environmental temperature. Conversely, autumn-born gilts are stimulated by lower temperatures and inhibited by a shorter photoperiod (Enne and Greppi, 1993).
Photoperiod and boar fertility
Peacock et al. (1987) noted that for boars the total number of spermatozoa per ejaculate was higher in short day conditions than in long day conditions. They concluded that photoperiod changes sperm production by influencing the hypothalamo/pituitary axis, whereas high temperature has a direct destructive effect on the germ cells. They pointed out that in a trial conducted in Germany, boars showed improvement in libido, ejaculate volume, number of
spermatozoa per ejaculate and number of insemination doses obtained per ejaculate when exposed to short light conditions. In bulls, sperm production was related to the length of the photoperiod although there was individual variation in sensitivity to day length. When the influence of the duration of the photoperiod and average monthly temperature on bull sperm production was investigated, greater variation was observed in relation to the photoperiod than to the temperature and humidity changes (Predojevic et al., 1 988). In the boar the pineal gland is not only involved in short-photoperiod-induced testicular regression, but it also participates in mediating the accelerating effects of long photoperiods on testicular development (Maxwell et al., 1991).
Supplementary light
Wrathall ( 1 975) reported that the average ovulation rate in gilts held in continuous light for one complete oestrous cycle did not differ from those in gilts kept in natural light. Conditions of light during lactation were found to have no effect on the weaning-to-oestrus interval in sows (Wrathall, 1975) but Hughes and Varley (1 980) suggested that a lighting regime of 1 2 hours on and 1 2 hours o ff i n the service house was optimal. Leman ( 1 986) recommended 1 6 hours of light and 8 hours of darkness i n breeding herds throughout the year with 1Jz watt for each square foot of living space. Tsoutsis ( 1 986) recommended a minimum of 8 hours light for pregnant sows and 12 hours or more for others, while Lahrmann and Plonait (1 984) favoured a constant 12 to 14 hour-day or an increasing photoperiod. The latter authors also suggested a tendency for smaller variations in fertility due to husbandry methods and seasonal factors if the service area was provided with more natural light. Wrathall (1 987) recommended a regular 1 2-14 hours of light; 500-1 000 lux at pig eye level each day to counteract the rapid decline in daylength in late summer and autumn which may induce the autumn abortion syndrome.
The duration of oestrus tends to be slightly longer in gilts when they receive extra light. When light treatments were continued post-mating into pregnancy, there were consistent increases, both in the number of embryos at 25 days, and in the number of piglets born at term. Light has a stimulating effect on corpora lutea and the increased progesterone levels from this effect result in enhanced embryo survival. A day length of 1 7 hours was found to be adequate (Wrathall, 1 975). Supplementary lighting to give a 1 7 hour photoperiod increased the number of boars and gilts reaching puberty. earlier .than under normal natural light (Comes, 1984). Continuous exposure to light does not affect ovulation rates but continuous darkness has been reported to hasten the onset of puberty (Peacock et al., 1 987). The feedback interplay between gonadal hormone and gonadotrophin is seasonally modified
by a photoperiodic alteration of hypothalarnic-pituitary activity (Mauget, 1982). In wild sows, the secretion of prolactin (Prl) was apparently influenced by seasonal variation in
.,_
..
daylight and/or temperature. As i n cyclic ewes, Prl of wild cyclic sows i s high during anoestrus and sexual inactivity but it has not been clearly demonstrated that Prl causes anoestrus. The influence of light on Prl secretion in domestic pigs is low (Ravault et al.,
1 982).
Both length of day and light quality influence photoperiodic response. The pineal gland has an important role in photoperiodic _information transduction. It does not induce persistent oestrus in constant light but has a role in controlling cycle length when photoperiods are shorter. In sheep, melatonin secretion is an important factor in the transduction process of
-. photoperiod information. In pigs, a nocturnal surge of melatonin was found under 1 2h light: 1 2 h dark condition.
The pineal gland is believed to mediate or control an anti-gonadal effect in mammals. Prolongation of the light photoperiod causes decreased gonadotropin production as a