www.elsevier.comrlocateranireprosci
Factors effecting reproduction in the pig: seasonal
effects and restricted feeding of the pregnant gilt
and sow
O.A.T. Peltoniemi
a,), A. Tast
a,b, R.J. Love
b aDepartment of Veterinary Clinical Sciences, Faculty of Veterinary Medicine, UniÕersity of Helsinki,
Pohjoinen Pikatie 800, 04920 Saarentaus, Finland
b
Department of Veterinary Clinical Sciences, UniÕersity of Sydney, Camden NSW 2570, Australia
Abstract
Recent advances in research on seasonal infertility are discussed with a special focus on implications of the generally recommended restricted post-mating feeding strategy of the early pregnant gilt and sow for the physiology of seasonal infertility. The endocrinological basis of seasonal breeding of the wild and domestic pig is being clarified: as in other seasonal breeders, melatonin is relaying photoperiodic information about season to the pituitary–gonadal axis. Earlier confusion on this matter appears to have been caused by a lack of specificity of the melatonin assays employed. Group housing of the pregnant sow is becoming a common practice and, as an important environmental risk factor for seasonal infertility, may lead to an increase in the incidence of seasonal infertility in the future. After an initial progesterone-mediated beneficial effect on embryonic survival, a restricted post-mating feeding strategy may have a negative effect on maintenance of early pregnancy in the gilt and sow in the summer–autumn period. The endocrinological mechanism of seasonal disruption of pregnancy is yet to be determined. However, it is proposed that LH is reduced in the summer–autumn period and this reduction is amplified by the commonly applied restricted post-mating feeding strategy. These changes in LH secretion, although not as such inducing CL regression, may exert a progesterone-mediated detrimental effect on the capability of embryos to produce adequate embryonic signaling. This may lead to a seasonal disruption of pregnancy and a return to oestrus 25–30 days after mating. q2000 Elsevier Science B.V. All rights reserved.
Keywords: Seasonal infertility; Feed restriction; LH
)Corresponding author. Tel.:q358-529-5306; fax:q358-685-1181.
Ž .
E-mail address: [email protected] O.A. Peltoniemi .
0378-4320r00r$ - see front matterq2000 Elsevier Science B.V. All rights reserved.
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1. Introduction
The European wild boar is a true seasonal breeder with a breeding season occurring
Ž .
in early winter with piglets born once a year in late spring Mauget, 1982 . Despite being capable of producing piglets throughout the year, the domestic sow shows a
Ž .
reduction in fertility in late summer and early autumn Love, 1981 , at a time that the
Ž
European wild boar is in seasonal reproductive arrest Mauget, 1982; Claus and Weiler,
.
1985 . The reduction in fertility commonly reported all around the world justifies the use of the term ‘‘seasonal breeder’’ for the domestic pig as well as for the European wild
Ž .
boar Love et al., 1993 . Manifestations of this seasonal infertility include a reduced
Ž .
farrowing rate Xue et al., 1994; Love et al., 1995; Peltoniemi et al., 1999b , delayed
Ž
puberty of gilts Ehnvall et al., 1981; Paterson and Pearce, 1989; Peltoniemi et al.,
. Ž
1999a,b , a prolonged weaning to oestrus interval Hurtgen and Leman, 1980; Benjamin-sen and Karlberg, 1981; Sterning et al., 1990; Prunier et al., 1996; Peltoniemi et al.,
. Ž
1999a and, possibly, a reduced litter size during late summer and early autumn Claus
.
and Weiler, 1985 . Although photoperiod is considered the primary environmental cue
Ž .
to seasonal infertility Love et al., 1993 , a whole variety of other environmental factors seem to interact with season either to exacerbate or to alleviate this infertility. These
Ž
environmental factors include housing group vs. individual; Hurtgen and Leman, 1980;
. Ž . Ž
Love et al., 1995 , feeding level Love et al., 1995 , light conditions Andersson et al.,
. Ž . Ž .
1998 , boar exposure Paterson et al., 1991 , group size Love et al., 1993 , ambient
Ž .
temperature Love, 1978; Stork, 1979; Hurtgen and Leman, 1980; Prunier et al., 1997
Ž .
and interactions between females Wilson and Love, 1990 . The significance of seasonal infertility has increased in recent years as group housing of dry sows has become more
Ž .
common Peltoniemi et al., 1999b . In the present paper, recent advances in seasonal infertility-related research are reviewed. The focus of the present review is on the interaction of nutrition and season in the feed-restricted, early pregnant gilt and sow. A review on the effects of season, housing and nutrition on gonadotrophins is given
Ž .
elsewhere Peltoniemi et al., 1999c .
2. Effector mechanism mediating seasonal effects on the pituitary–gonadal axis
In seasonal breeders other than the pig, the overall mechanism by which seasonal changes in daylight are carried to the hypothalamic–gonadal axis is well-established, although some details of this mechanism still remain to be clarified at the cellular level
ŽKarsch et al., 1984; Lincoln, 1992; Malpaux et al., 1996 . These animals have a.
Ž . Ž . Ž .
Fig. 1. Pattern of light intensity lxs' and mean "SEM serum melatonin concentrations pgrml in European wild boarssland in domestic giltssBover a 48-h period.
In the pig, many researchers have been unable to demonstrate the nocturnal rise in
Ž
melatonin concentration seen in other species Brandt et al, 1986; Peacock, 1991;
. Ž .
Diekman et al., 1992; Bollinger et al., 1997 . However, Paterson et al. 1992 reported a consistent nocturnal rise in melatonin concentration in pigs under varying photoperiodic
Ž .
circumstances and work by Klupiec et al. 1997 implied that the previous confusion had
Ž .
been due to methodological problems. We carried out an experiment Tast et al., 2000b ,
Ž
where individual European wild boars were cannulated by intra-arterial catheters Tast et
.
al., 2000a for frequent blood sample collection. In the same experimental design, we used domestic YorkshirerLandrace crossbred gilts fitted non-surgically with intravenous
Ž .
jugular catheters Peacock, 1991 . Blood sampling was carried out at a 2-h interval for 48 h. The sampling was repeated in each season in Finland to establish seasonal variation in melatonin secretion for these experimental animals. As illustrated in Fig. 1
Žsummer profiles , a consistent and repeatable melatonin profile was found in all of the.
experimental animals. Therefore, it is proposed that this aspect of the neuroendocrino-logical basis of seasonal reproduction in the pig is not different from that of other seasonal breeders.
3. Environmental factors involved in seasonal infertility
As photoperiod functions as the primary cue to seasonal infertility, other
environmen-Ž
tal factors then determine the level of reproductive activity in summer–autumn Love et
.
al., 1993 . Of these environmental facors, housing, ambient temperature and social interactions are considered to be of significance. One of the main environmental cues
Ž
affecting onset of sexual activity in the European wild boar is availablity of feed Pepin
.
and Mauget, 1989 . Likewise, nutrition is considered an important environmental factor in the physiology of seasonal infertility. As a focus of the present review, the role of nutrition in seasonal infertility is dealt with on its own.
3.1. Housing and social stress
acceptable way of housing pigs intensively. Available information on effects of the type of housing on fertility and seasonal fluctuation in fertility of the sow seems very limited.
Ž . Ž
Work carried out in Australia Love et al., 1995 and the USA Hurtgen and Leman,
.
1980; Leman, 1992 suggests that individual housing may in fact protect sows from the seasonal reduction in farrowing rate. Farrowing rates for group-housed sows were clearly reduced during the seasonal infertility period in large production unit, whereas
Ž
individually housed sows showed no seasonal fluctuation in farrowing rates Love et al.,
. Ž .
1995 . This study Love et al., 1995 provided strong evidence for the benefit of individual housing as the experimental animals were maintained within the same buildings and received similar management. However, epidemiological findings in Finland suggest that other manifestations of seasonal infertility, such as a prolonged weaning-to-oestrus interval, may be more common a finding in sows kept in individual
Ž .
stalls Peltoniemi et al., 1999a . On the other hand, the seasonal reduction in farrowing
Ž
rate related to group housing may partly be prevented by feeding measures Peltoniemi
.
et al., 1999b .
There are clear indications that ‘‘social stress’’ or grouping of sows may elevate
Ž
cortisol concentrations, especially in low-ranked sows shortly after grouping Tsuma et
.
al., 1996 . A stress hypothesis for seasonal infertility was proposed by Wan et al.
Ž1994 , who suggested that those pigs with a greater adrenal responsiveness to ACTH.
administration were more likely to suffer from seasonal infertility. This correlation was found to be particularly significant for gilts, which are known to be more susceptible to seasonal infertility than older sows. This hypothesis implies that the environmental determinants of seasonal infertility that are related to stress are likely to be important in the pathophysiology of seasonal infertility. Therefore, effects of grouping density, feed restriction, and heat on gonadotrophins may, at least in part, be mediated via cortisol. To
Ž .
support this, Love et al. 1995 clearly showed that seasonal reduction in farrowing rates was worsened by increased stocking density.
3.2. Temperature
High ambient temperature leading to heat stress has, in many instances, been
Ž .
associated with seasonal infertility Love, 1978; Stork, 1979; Reilly and Roberts, 1992 . However, attempts to alleviate the seasonal infertility of sows by cooling systems have
Ž .
generally failed Stork, 1979; Hurtgen and Leman, 1980 . Furthermore, seasonal infertil-ity has been described across all the continents under a diversinfertil-ity of climatic conditions, yet the severity of the condition does not correlate with any of these variations in temperatures. The strongest argument against temperature being of great significance in the physiology of seasonal infertility is the fact that the duration of seasonal infertility period exceeds long beyond August, when temperatures have fallen and the climatic conditions cannot be described by anything but cool in countries like Finland. Therefore, it can be suggested that temperature may not play a major role in the pathogenesis of seasonal infertility. However, high ambient temperatures reduce the feed intake of sows during lactation, thereby somewhat increasing the weaning-to-oestrus interval in
sum-Ž .
3.3. Boar exposure
Ž
Apart from season affecting fertility of the boar Claus and Weiler, 1985; Andersson
.
et al., 1998 , the male role in the seasonal infertility of gilts and sows is essential in terms of prevention of seasonal infertility. The adverse effect of season on attainment of
Ž
puberty in gilts was largely prevented by proper use of boar stimulation Paterson et al.,
.
1991 . In addition, more educated use of the boar with weaned sows has decreased the
Ž .
weaning-to-oestrus interval in the summer–autumn Love et al., 1993 .
4. Feeding the pregnant gilt and sow — should season be considered?
Weight fluctuation over the production cycle of a sow is to be avoided. This is best achieved by feeding sows ad libitum during lactation and by restricting feeding during
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the following pregnancy Einarsson and Rojkittikhun, 1993 . Thus, a catabolic state of the sow at around time of ovulation may be avoided as much as possible by a liberal feeding during lactation and after weaning and, on the other hand, overconditioning and related problems upon farrowing are prevented by restricting feeding during pregnancy
ŽFoxcroft et al., 1996 . Furthermore, the most important aspect in optimizing embryonic.
survival is to generate an increased number of embryos by a high-plane feeding prior to mating, followed by feeding strategies during the post-mating period, which include
Ž .
restricted feeding, that further support developing embyos Ashworth, 1998 .
These general nutritional considerations, however, may not account for seasonal fertility problems seen in the pig industry. This aspect seems important as seasonal
Ž .
infertility appears to affect the pig industry as a whole Peltoniemi et al., 1999b ,
Ž
especially where pregnant sows are kept in group housing environments Love et al.,
.
1995 . This implies that season should be included as an aspect when planning nutritional programs for pigs. A controversial beneficial effect of a high feeding level for the first 4 weeks of pregnancy was reported on fertility in gilts and sows in two large
Ž .
Australian pig units during the seasonal infertility period of the year Love et al., 1995 . In the present review, endocrinological mechanisms mediating nutritional effects and considered of major significance are discussed, especially focusing on the period beyond
Ž
Day 12 of pregnancy, when CL become dependent on gonadotrophic support Peltoniemi
.
et al., 1995 . As information on nutrition–season interaction in the mated sow is very limited, we acknowledge the fact that the points discussed here may only be a part of the whole endocrinological mechanism mediating nutritional and seasonal effects on fertility of the sow.
4.1. Progesterone-mediated nutritional effects
Nutritional effects on embryonic survival may be mediated via progesterone or direct effects on the conceptus and uterus. In the pig, to exert nutritional effects on embryonic survival, the progesterone-mediated mechanism is thought to be essentially effective
Ž .
Ž .
unlikely for the polyovulatory pig Foxcroft, 1997 . However, unlike for progesterone, it is likely that such a threshold value exists for embryonic oestrogens. This argument stems from the fact that more than a certain number of viable embryos must be present on days 14 and 15 for successful continuation of the function of the corpus luteum
ŽPolge et al., 1966 , implying that there needs to be a quantitative threshold of the.
Ž .
embryonic signal to maintain the corpus luteum Findlay, 1993 . Furthermore, it seems more than a coincidence that in seasonal comparisons, progesterone values fall during
Ž .
autumn Wrathall et al., 1986 and a seasonal disruption of an already established
Ž .
pregnancy is observed Love et al., 1993 , with sows often returning to oestrus between 24 and 30 days after mating. In autumn, it may be that after a period of 12 days of refractoriness, the CL function is somewhat impaired by a seasonal effect, resulting in lower progesterone production. This seasonal effect on CL function may be further suppressed by a commonly used feed restriction, which has been shown to reduce LH
Ž .
pulse frequency in the early pregnant gilt Peltoniemi et al., 1997a .
Detrimental progesterone-mediated effects on embryonic survival related to a high plane of nutrition 3–4 days after mating may be reversed by exogenous progesterone
ŽAshworth, 1991 , demonstrating the direct effector mechanism of progesterone in.
mediating the nutritional effects. We suggest, however, that nutritional effects on progesterone production are more complex than this, when season is accounted for in an applied feeding regime for the pregnant sow. After the short-term beneficial effect of
Ž .
feed restriction for 3–4 days after mating Jindal et al., 1997 , there may be an indirect counteractive effect of feed restriction on progesterone production, mediated via LH secretion as described above.
Ž
Mechanisms by which progesterone concentrations are reduced nutritionally Jindal et
.
al., 1997 may be different from that of a seasonal reduction in progesterone secretion
ŽWrathall et al., 1986 . In the reduction of progesterone associated with a high plane of.
nutrition shortly after mating, the principle mechanisms that may be considered are the increased hepatic blood flow and the metabolic clearance rate of progesterone, and changes in splanchnic circulation diverting blood away from the ovarian circulation
ŽFoxcroft, 1997 . Hepatic blood flow and metabolic clearance rates are unlikely to be.
subject to seasonal photoperiodic changes, whereas LH secretion from the pituitary
Ž .
clearly follows a seasonal pattern of secretion Peacock, 1991; Peltoniemi et al., 1997a .
4.2. LH-mediated nutritional effects
LH is an essential component for maintenance of the corpora lutea and early
Ž
pregnancy in the pig Anderson et al., 1967; Spies et al., 1967; Kraeling and Davis,
.
1974; Kraeling et al., 1992; Peltoniemi et al., 1995 . Therefore, any factor, including nutrition, which affects LH secretion during early pregnancy, may have implications for
Ž .
embryonic survival and maintenance of early pregnancy Peltoniemi et al., 1999c . A lot of research work has emphasized the role of nutrition on gonadotrophin
Ž
secretion during lactation, after weaning, and before and shortly after ovulation for reviews, see Booth, 1990; Einarsson and Rojkittikhun, 1993; Cosgrove and Foxcroft,
.
gonadotrophin secretion related to the follicular phase and ovulation. Little attention has been paid to the role of nutrition as a modulator of gondotrophin secretion during early pregnancy when CLs have become dependent upon pituitary support.
Insulin, glucose, amino acids and free fatty acids provide metabolic signals to the
Ž
brain that influence food intake, energy balance and body weight regulation Oomura,
.
1976; Porte and Woods, 1981; Fernstrom, 1983 . Of these, insulin and glucose are considered to be the most directly and fundamentally involved in the nutritional
Ž .
modulation of the hypothalamic–pituitary–gonadal axis Booth, 1990 .
In the prepubertal gilt, feed restriction to 50% of ad libitum intake clearly reduced
Ž .
LH pulse frequency in long-term Prunier et al., 1993 and short-term experiments
ŽCosgrove et al., 1993 . This degree of feed restriction showed up in metabolic markers.
such as plasma free fatty acid concentrations, plasma insulin concentrations and plasma glucose concentrations. Gilts with restricted feeding had metabolic characteristics of
Ž
animals that had been denied feed low pre-prandial glucose, insulin and urea and high
.
free fatty acid concentrations , a metabolic state that was clearly related to reduced LH
Ž .
pulsatility Prunier et al., 1993 . When low-energy post-mating feeding strategies are
Ž .
applied according to latest recommendations Cosgrove and Foxcroft, 1996 , this should reduce LH pulsatility in the early pregnant gilt, since such a recommendation essentially is equivalent to a 40–50% feed restriction.
As a favourable effect of high feeding level after mating on fertility in summer–
Ž .
autumn was found Love et al., 1995 , we hypothesised this favourable effect was mediated via LH secretion. We therefore conducted studies to determine the effect of
Ž .
commonly used level of feed restriction feed-restricted gilts received 1.8 kgrday on
Ž
LH secretion in pregnant gilts in summer–autumn and spring Peltoniemi et al.,
. Ž .
1997a,b . In spring, the feed-restricted gilts 23.4 MJrday had fewer LH pulses than
Ž . Ž .
control gilts on 3.6 kg 46.8 MJ of feed Peltoniemi et al., 1997a . This reduction in LH pulsatility related to feed restriction, however, was not significant in summer–autumn,
Ž .
when seasonal disruption of pregnancy is observed Peltoniemi et al., 1997b . These studies showed that moderate feed restriction, capable of altering LH secretion, also caused metabolic changes, as indicated by plasma insulin and free fatty acid concentra-tions in experimental feed-restricted gilts. The feed-restricted pregnant gilts tended to show higher preprandial FFA concentrations, lower preprandial insulin concentrations, and a greater pre- vs. post-prandial difference than in animals fed nearly ad libitum
ŽPeltoniemi et al., 1997a . These findings may be considered metabolic characteristics of.
Ž .
pigs deprived of feed Prunier et al., 1993 . Alterations in energy intake correlated with
Ž
weight and back fat changes, and the metabolic changes recorded Peltoniemi et al.,
. Ž
1997b . Furthermore, it was observed that LH characteristics pulse amplitude, pulse
.
frequency and area under the LH curve showed a tendency towards higher values when the gilts had more energy intake and showed the metabolic characteristics of satiated
Ž .
animals Peltoniemi et al., 1997a,b . LH values were highest in animals, which were given a high-density diet to ad libitum, maximising nutrient intake. In conclusion, feed restriction of the usual order after mating may reduce LH pulse frequency in the early
Ž .
pregnant gilt Peltoniemi et al., 1997a . However, the effect of a 50% feed restriction and season as such on LH characteristics found was not considered strong enough to
Ž .
5. Seasonal disruption of pregnancy: the present view
A definition of seasonal disruption of pregnancy, considered as the major economic
Ž .
loss related to seasonal infertility, has been given Love et al., 1993 . This definition contends that affected sows in summer–autumn first conceive, have embryos present for a short period of time, but that within a week after implantation the embryos die and the
Ž .
whole litter is lost Love et al., 1993 . Having undergone this wasteful process, sows typically exhibit signs of oestrus 25–30 days after mating. Furthermore, studies from
Ž . Ž . Ž
Australia Love et al., 1993 , Italy Enne et al., 1979 , and Finland Peltoniemi et al.,
.
1999a,b,c indicate the early embryonic deaths and loss of the whole litter as the cause of the reduced farrowing rate in summer–autumn. In addition, our recent work studying embryonic deaths as a cause for repeated breeding in different seasons in group housing system, indicates that loss of an established early pregnancy, determined by ultrasound
Ž
and progesterone profiles, was rare in spring but common in autumn Tast, Peltoniemi et
.
al., unpublished work .
It seems more than a coincidence that such an irregular oestrus-to-oestrus interval occurs in sows in which embryos are removed by flushing on Days 11, 12 or 13 of
Ž .
pregnancy Meulen et al., 1988 . In these sows, the first phase of the embryonic signal has occurred, an effect that can be mimicked by two injections of oestradiol on Days 12
Ž .
and 13 Pusateri et al., 1996a . A second signal produced by the embryos or further injections of oestradiol is required to extend the life of the corpora lutea beyond 30 days
ŽPusateri et al., 1996b . An interesting question is whether the seasonal disruption of.
Fig. 2. Season–nutrition interaction of hormones involved in embryonic survival and establishment of pregnancy. Seasonally suppressed LH in feed-restricted sows may exert a downward effect on progesterone,
Ž
reducing secretory activity by the endometrium. This results in an inadequate second embryonic signal dotted
.
pregnancy seen in seasonal infertility is due to inadequacy of the embryonic signals or a failure of the maternal response to these signals. The fact that both progesterone
Ž . Ž
secretion Wrathall et al., 1986 and LH pulsatility Peacock, 1991; Smith and Almond,
.
1991; Peltoniemi et al., 1997a in the early pregnant pig are subject to seasonal
suppression during late summer–early autumn would support the latter theory. However, as seasonal and nutritional effects on LH secretion were as such considered too weak to
Ž
cause regression of CL and seasonal disruption of pregnancy Peltoniemi et al.,
.
1997a,b , we have come to the conclusion that LH-mediated effects on progesterone may in fact lead to inadequacy of embryonic signals. This is why the sow fails to respond to the embryonic signalling, leading to a seasonal disruption of pregnancy.
The present view therefore is that LH secretion is reduced in summer–autumn, and this effect is amplified by a restricted post-mating feeding strategy, which suppresses
Ž .
progesterone seretion Fig. 2 . This effect only becomes evident after the CLs become independent of pituitary support after Day 12. The reduced progesterone then has a negative impact on histotrophic secretions from the endometrium, exerting a negative effect on viability of embryos, and, more importantly, capability of the embryos to
Ž .
produce the second embryonic oestrogen signal on Day 18 required for maintenance of pregnancy beyond Day 30. The sow fails to respond to the inadequate embryonic signals, CLs regress and pregnancy is terminated.
6. Conclusion
Seasonal infertility can be seen as a vestige of the distinct seasonal breeding pattern that existed before the pig was domesticated. Thus, it can be understood that in the domestic pig, changing photoperiod is an inherent and effective means by which seasonal information is mediated and this mediation occurs, as in other seasonal breeders, by seasonal changes in melatonin patterns. To this, the pig tends to respond in a way similar to that seen in the wild: reducing its fertility in summer and autumn. The magnitude of reduction in fertility in the female depends on environmental factors such as feeding level, boar exposure, temperature, stress and type of housing. A mechanism for the commonly reported seasonal disruption of pregnancy is given. Seasonally reduced LH secretion in summer–autumn is further suppressed by commonly applied feed restriction after mating. These effects on LH secretion are as such not strong enough to induce regression of CLs; however, these effects of LH may reduce progesterone secretion, which in turn slows down the secretory activity of histotrophs of the endometrium. This cascade of events eventually results in retarded embryos, which are not able to produce adequate secondary oestrogen signal required for maintenance of CL function and pregnancy beyond Day 30. As a result, sows return to oestrus between Days 24 and 30 after mating.
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