We sincerelly thank the unconditional
collaboration of the authors, and the kind disposition of the Mexican
Association of Animal Nutrition (AMENA), and the Latin American
College of Animal Nutrition (CLANA). Because of their support, Engormix.com
brings closer the result of years of international research to the service of
the animal producer.
E. J. Clowes1, K. T. Soltwedel2, T. S. Stahly3,
F. X. Aherne4, and J. E. Pettigrew5.
1Alberta Agriculture, Food and Rural Development, Edmonton; 2University
of Illinois, Urbana; 3Iowa State University, Ames; 4 Emeritus,
University of Alberta, Edmonton
Inadequate nutrient intake by the sow during lactation impairs subsequent fertility.
Evidence for this can be found in both the results of controlled experiments
(reviewed by Prunier and Quesnel, 2000) and in practical experience. This symposium
deals with the biological mechanisms that connect nutrient intake to fertility,
and this paper focuses on those mechanisms at the whole-animal level. We also
give some attention to the influence of body nutrient stores at farrowing on
the sow’s response to inadequate nutrient intake.
Inadequate nutrient intake occurs when the sow fails to consume enough nutrients
to meet the enormous needs for milk production. Sow unit managers often restrict
feed to lactating sows, especially during the early stages of lactation. However,
the bigger concern is that sows fail to consume enough feed even when they have
ad libitum access to it. We believe that the sow’s voluntary feed intake
is not fixed, but that it is subject to management. Proper management of the
animal and its environment, by controlling the effective thermal environment,
feeding management, and diet formulation, can increase voluntary feed intake
in lactating sows in many cases (Pettigrew and Esnaola, 2000). We also believe
that pig producers around the world have increased the voluntary feed intake
of their lactating sows substantially during the past decade, largely through
attention to these management factors. We suspect that this increase in feed
intake has contributed in some measure to the recent widespread improvement
in reproductive efficiency in the USA (National Agricultural Statistics Service,
2003). The logical conclusion to this is that the problem of inadequate nutrient
intake, and the associated mobilization of body tissues, is less severe than
it was a decade ago.
The striking exception to this conclusion lies in hot climates. It is impossible
to manage the environment to eliminate heat stress in many Latin American climates.
In those situations, it is imperative that managers of lactating sows employ
all management techniques at their disposal to enhance feed intake, but inadequate
intake and excessive mobilization of body tissues may still occur. That fact
focuses attention on the subject of this symposium.
Body Condition vs. Metabolic State
The detrimental effects of inadequate nutrient intake on fertility may be mediated
through effects on at least the following:
1. Metabolic state, broadly defined;
2. Rate of mobilization of body protein and/or fat;
3. Amount of body protein and/or fat in the sow at weaning/rebreeding.
The concept of metabolic state as used here is quite broad. It encompasses
the concentrations of several metabolites and metabolic hormones, a subject
reviewed in depth in this symposium by Dr. Quesnel, and tissue sensitivity to
these hormones. Tissue sensitivity to these hormones is an important component
of metabolic state, which can alter the signal transmitted by the circulating
hormones, and affects the hypothalamo-pituitary-ovarian axis either directly
or indirectly. Metabolic state also encompasses the concept of total oxidizable
substrates (Wade and Schneider, 1992; Wade et al., 1996), and measures of the
metabolic conditions of body tissues (especially protein and fat) themselves,
such as the size of the tissue reserve and the rate of tissue mobilization (synthesis/degradation).
The fact that many factors are involved in the regulation of reproductive function
is not a surprise, as most complex functions have multiple regulators. So it
would be unusual if only one component of metabolic state regulated such an
important and complex physiological function as reproduction.
It is practically important to know whether metabolic state (1), and its associated
effects on rate of body tissue mobilization (2), or the amount of reserves remaining
at weaning (3) is more important for subsequent fertility. If a sow’s
subsequent fertility depends largely on a high level of body reserves at weaning,
it would be practical to feed the sow liberally during pregnancy to ensure development
of adequate body tissues to compensate for tissue mobilization during lactation.
However, excessive feeding during pregnancy reduces feed intake during lactation,
presumably because of excessive fatness (Xue et al., 1997; Revell et al., 1998;
Sinclair et al., 2001), and this results in an increased rate of tissue mobilization.
To help determine the appropriate feeding strategy during pregnancy it is necessary
to discover whether metabolic state, and its associated effects on the rate
of tissue mobilization, or the amount of body protein and/or fat remaining at
weaning/re-breeding is more important. As described below, it is likely that
all these factors are important.
Frisch (1984) proposed that a threshold amount of body fat is necessary for
fertility. But, no consistent threshold of body fat has been associated with
post-weaning reproductive problems. This, together with the fact that these
observations are purely correlative, reduces the confidence in the hypothesis
that the size of the body fat reserve is a primary controller of fertility in
the pig. However, we do present evidence that the size of body protein stores
at farrowing impacts on the sow’s subsequent reproductive performance.
Experimental treatments imposed only during lactation cannot distinguish between
metabolic state and its associated effects on the rates of tissue mobilization
and the amount of tissue remaining at weaning, because the two are perfectly
confounded. However, direct experimental evidence indicates that the metabolic
state (or rate of tissue mobilization) of the sow during lactation may be more
important than the size of the sow’s body stores of protein and/or fat
in influencing fertility. Two examples of such evidence are described below.
First, Mullan and Williams (1989) fed first-parity sows at three levels of intake
during pregnancy, then at two levels during lactation. Two of the treatments
(high intake during pregnancy and a low intake during lactation vs. medium intake
in gestation and a high intake during lactation) had similar body weights (~125
kg) and composition (~23mm P2 backfat depth) at weaning, but very different
subsequent reproductive performance. The clear advantage lay with the treatment
that had a high feed intake during lactation. These sows likely exhibited a
lower rate of tissue mobilization, and were in a less severe catabolic state
Second, Zak et al. (1997a,b) fed sows to appetite during the first 21 d of lactation
and then restricted intake to 50% of the to appetite level during the last week,
or restricted feed intake during the first 21 d of lactation and fed to appetite
during the last week. Sows on both treatments lost a similar amount of body
weight and backfat depth during lactation. However, follicular fluid taken at
proestrus (~3 d post-weaning) from sows restrict-fed at the end of lactation
supported poorer generic oocyte maturation and the oocytes from these sows matured
to a lesser degree in generic follicular fluid (Table 1). Sows on this treatment
also showed lower mean LH levels at the end of lactation and a lower embryo
survival rate (Table 1). These sows lost more body weight in the last week of
lactation and perhaps had a higher protein mobilization rate compared to sows
on the other treatment. This indicates that a more catabolic state during the
last week of lactation enhances both the environment (follicular fluid) surrounding
the oocyte as well as the potential of the oocyte to mature, resulting in increased
embryo survival. However, any period of nutritional insult in lactation is likely
to impede follicular fluid quality and oocyte maturation, because an antral
follicle may be recruited into the pre-ovulatory pool in the span of 19 to 21
days (Morbeck et al., 1992). But if the nutritional/metabolic insult is too
severe, improved nutrition just prior to weaning will only allow partial recovery
of the sow’s reproductive status (Table 1).
Body Tissue Mobilization
A reduction in subsequent reproductive performance (Aherne and Kirkwood, 1985;
Prunier et al., 1993) occurred in sows after loss of 10 to 15% of their body
weight during lactation; a loss of 18 to 26 kg of body weight in a 180 kg sow.
This body weight loss is composed of both protein and fat containing tissue.
A review of the literature available several years ago (King, 1987) indicated
that excessive protein mobilization during lactation is more detrimental to
subsequent fertility than is excessive fat mobilization. More recently, a regression
analysis of data from 16 published experiments indicates that the fractional
loss of body protein during lactation accounts for almost half the variation
in the sow’s post-weaning reproductive performance (wean-to-estrus interval;
Figure 1a). In contrast, less than a quarter of the variation in the same measure
was accounted for by loss of body fat (Figure 1b). Post-weaning reproductive
performance also appears to decline when sows are fed less than 500 to 600 g
CP/d in lactation (Figure 1c).
Further analysis of this data set suggests that loss of more than 16% of a sow’s
body protein mass is associated with a progressive decline in subsequent reproductive
performance, as indicated by an extended wean-to-estrus interval (Figure 2).
Mobilization of about 15% of an animal’s protein mass has also previously
been implicated in reduced lactational performance in the dairy cow (Botts et
al., 1979) and rat (Pine et al., 1994abc). Similarly, marked reductions in many
indices of ovarian function at weaning (Clowes et al., 2003a) were associated
with loss of 12% or more of the sow’s protein mass. A slight impairment
of the reproductive axis appeared to occur in sows that sustained about a 9%
loss in body protein (Table 2). Furthermore, the increase in subsequent litter
size achieved by breeding first-parity sows at their second rather than first
estrus after weaning was attributed to changes in the sow’s protein metabolism
(Clowes et al., 1994). These observations confirm the detrimental effects to
fertility of the metabolic conditions associated with rapid protein mobilization.
Physiological mechanisms of effects of protein loss on reproduction. Subsequent
litter size is a function of ovulation rate and embryo survival. Amino acid
deficiency during lactation has equivocal effects on ovulation rate in the sow,
and causes either no effect (King and Williams 1984ab; Yang et al., 1989; Zak
et al., 1998) or a reduction (Zak et al., 1997a; van den Brand et al., 2000;
Mejia-Guadarrama et al., 2002) in ovulation rate. Thus, rapid maternal protein
loss likely reduces the sow’s subsequent reproductive performance by reducing
embryo survival. These effects of body protein loss on reproduction are presumed
to impact the hypothalamic-pituitary axis and/or the ovary, causing poor follicle
and oocyte development, and ultimately reducing embryo survival and subsequent
Central inhibition of the reproductive axis is indicated by a reduction in LH
pulsatility, probably due to a reduction in the rate of GnRH release from the
hypothalamus. Lower LH pulsatility in lactation (King and Martin, 1989; Jones
and Stahly, 1999b, Yang et al., 2000b) and after weaning (King and Martin, 1989)
was observed in first-parity sows fed similar energy levels but low protein
(~ 400 g/d) and total lysine (16 g/d) intakes in lactation, compared to adequately
fed controls. These restricted sows likely mobilized a larger proportion of
their protein mass, and had higher rates of muscle protein mobilization throughout
The quality of the follicle, and the oocyte within that follicle, are important
for normal oocyte maturation and early embryonic development (Ding and Foxcroft,
1994). The oocyte’s ability to be fertilized and develop into an embryo
is influenced by the concentration of a complex mixture of serum proteins and
factors such as IGF-1 and EGF, and steroid hormones such as estradiol (Gougeon,
1996; Driancourt and Thuel, 1998) in follicular fluid. These factors may be
altered by nutrition, and this provides a direct connection between nutritional
inadequacy and inhibition of the reproductive axis at the ovarian level.
Three recent studies have implicated excessive maternal protein loss in lactation
and/or a higher protein mobilization rate at the end of lactation with reduced
ovarian function post-weaning (Zak et al., 1997b; Yang et al., 2000a, Clowes
et al., 2003a). The first experiment (Zak et al., 1997b) was described in an
earlier section. It showed detrimental effects of severe feed restriction during
the last week of lactation on the quality of follicular fluid and the oocyte.
In the second experiment, follicular fluid taken at pro-estrus from first-parity
sows fed 16 compared to 36 and 56 g/d of total lysine was less able to support
oocyte maturation (Yang et al., 2000a). These sows lost the most body protein
during lactation and had a higher fractional myofibrillar protein breakdown
rate (5.6 vs. < 4.2%) at the end of the 15-day lactation. Sows on this experiment
were fed isoenergetic diets (~ 46 MJ ME/d) during lactation, lost only a small
amount of body fat (-1.4 to -2.2mm of backfat), but as dietary lysine intake
decreased, sows lost progressively more live weight (-15, -19, and –22
In the third experiment, few differences were observed between sows that lost
9% and those that lost 7% of their protein mass, in a variety of ovarian variables
at weaning and the ability of follicular fluid to advance in vitro maturation
of oocytes (Clowes et al., 2003a; Table 2). However, marked reductions in many
indices of ovarian function were observed in sows that had lost more (~15%)
body protein and exhibited higher rates of muscle protein mobilization (Clowes
et al., 2000). A poor uterine environment may also be implicated in the reduced
embryonic survival in sows with excessive protein loss, especially when superimposed
upon embryos developing from poorly matured oocytes.
The Importance of Body Protein Reserves at Farrowing
While there is ample reason to believe that the sow’s metabolic state
during lactation, is a critical link between nutrition and fertility, there
is also convincing evidence that the amount of body stores at farrowing is important.
Two examples of that evidence are described below.
First, the factorial experiment of Mullan and Williams (1989) evaluating the
effects of feeding level during both pregnancy and lactation found the poorest
reproductive performance in sows given the very low feed allowances during both
Second, a more recent experiment by Clowes et al. (2003b; Table 3) repeated
this observation, but with three important differences. First, the sows were
managed to have at farrowing similar relative fatness but different levels of
body weight (193 vs. 165 kg) and body protein (30.0 vs. 24.3 kg). Second, the
measurements were extended to include specific measures of ovarian development.
Third, measures of gene expression confirmed that sows that were small at farrowing
and restricted during lactation had the greatest up-regulation of gene expression
in the main proteolytic pathway in muscle, and the lowest capacity for protein
synthesis in muscle (Clowes et al., 2002).
Pettigrew et al. (1992) proposed a mathematical model of the metabolism of lactating
sows that incorporated two key concepts related to the amount of body protein
reserves in the sow. There was (and remains) inadequate quantitative data to
support parameterization of these aspects of the model with confidence, but
the concepts remain useful.
The first of these concepts is that both protein synthesis and degradation can
be expressed per unit of protein mass. As undernutrition depletes the amount
of body protein during lactation, the body protein mass shrinks. In this case,
a constant fractional rate of net mobilization would therefore result in a reduced
rate of total amino acid release. Maintenance of a constant supply of amino
acids then requires a stronger catabolic stimulus to achieve a greater fractional
rate of mobilization. At some point, the protein reserve may become so depleted
and/or the rate of mobilization may reach a physiologic maximum that the total
supply of amino acids:
- will not meet the needs of the lactating mammary gland to maintain milk
- will not provide sufficient amino acid precursors for biosynthesis of proteins
associated with ovarian function
As a result, milk production will fall and/or milk protein composition will
decline, and embryo survival will also decline.
A corresponding relationship holds with regard to initial body protein mass.
Sows with smaller body protein stores would require a stronger catabolic stimulus
to provide the same supply of amino acids to the mammary glands. This more catabolic
state may have severely detrimental effects on the reproductive system. Recent
data on gene expression in muscle (Clowes, 2001; Clowes et al., 2002) appear
to confirm the predicted impact of both initial protein mass and degree of protein
mobilization on the fractional protein mobilization rate.
The second concept is that the animal protects itself from excessive depletion
of its body stores. The physiological mechanisms for sensing the degree of depletion
(or of remaining tissue) and orchestrating the protective response are unknown,
as are the quantitative relationships between rate of mobilization and the size
of the remaining tissue reserve. However, the result is the protection of the
sow’s body at the expense of both milk production and the metabolic conditions
necessary for subsequent fertility.
Both of these concepts suggest that depletion of body reserves would progressively
reduce the supply of nutrients supplied from further tissue mobilization, and
there is strong empirical support for this relationship. Several studies (Mullan
and Williams, 1989; Jones and Stahly, 1999a; Kusina et al., 1999; Clowes et
al., 2003a) have shown that excessive tissue depletion progressively reduces
milk yield as lactation continues, and that both the amount of stores at farrowing
and the nutrient supply during lactation are important in this regard. Furthermore,
a loss of body protein, beyond a 9 to 12% loss, results in a continued decline
in milk yield, and may even result in a reduction in milk protein composition
(Clowes et al., 2003 a,b). But, feeding first-parity sows to above their ad
libitum intake appeared to have no beneficial effect on milk production (Pluske
et al., 1998) or reproductive performance (Zak et al., 1998) in some situations.
The implication of the importance of body stores at farrowing is that sows should
be fed generously enough during pregnancy to develop a protective level of body
stores. Excessive fatness reduces feed intake during lactation, so the aim should
be to develop a larger body protein reserve but a moderate body fat reserve
(Pettigrew and Yang, 1997). Producing heavier gilts at farrowing, by breeding
at a heavier weight and/or feeding a higher energy/protein intake during gestation,
could be a useful management tool if poor appetite and subsequent reproductive
performance are a problem in a commercial herd. However, the economic impact
of these findings and the effects on overall animal productivity need to be
Management to Maximize Feed Intake
A general theme of this discussion is that adequate nutrient intake of the lactating
sow relative to her needs is important for achieving the desired metabolic state
that will support subsequent fertility. As mentioned above, we believe that
proper management is important in encouraging a high level of feed intake. The
challenge of getting sows to eat enough during lactation is more acute when
the sow is heat-stressed, but proper management can help.
We suggest the proper management factors to encourage a high level of feed intake
fall into three categories (Pettigrew and Esnaola, 2000):
Minimizing heat stress.
The first requirement is for adequate and effective ventilation. Natural ventilation
systems in hot climates should incorporate high roofs, with the roof extending
far enough to provide shade to all animals. The buildings should be far enough
apart to allow adequate air movement. Among fan-powered ventilation systems,
tunnel ventilation is especially effective in high temperatures. Circulating
fans within the building are also effective.
Evaporative cooling can be useful. Evaporative systems include the enormously
effective dripping of water on the sow, wetting the roof, and pulling incoming
air through water-soaked pads. Floors made of materials that conduct heat away
from the sow contribute to cooling.
It is important to feed lactating sows frequently; we suggest at least three
times daily. Ensure feed is available during the coolest times if daytime temperatures
are high. Use feeders that allow comfortable access to the feed. An adequate
supply of water is essential, and that includes an adequate flow rate through
nipple waterers. Wet/dry feeding systems, in which the sow can mix feed and
water, appear to increase feed intake in both finishing pigs and lactating sows.
Various methods of wet-feeding, providing feed mixed with water to form a gruel,
are used effectively to encourage a high level of feed intake, especially in
It is necessary to provide adequate dietary levels of all essential amino acids.
It is also important to minimize the total protein content of the diet, to minimize
the heat production associated with elimination of excess nitrogen. For these
reasons, crystalline amino acids are especially useful during hot weather.
The heat increment of fat is low, so fat supplementation of lactation diets
is especially important during hot weather. The heat increment of fiber is high,
so fibrous diets should be avoided.
Excessive levels of minerals should be avoided, and providing an appropriate
cation:anion ratio may be useful.
Excessive mobilization of body tissues by the lactating sow appears avoidable
in many situations, but probably not in hot climates. The metabolic state of
the sow and its associated rate of mobilization of body tissues appears more
important for subsequent fertility than the amount of body stores in the sow
at weaning/re-breeding. Rapid mobilization of body protein during lactation
appears more detrimental than excessive mobilization of body fat. Sows can mobilize
up to about 10% of their initial body protein mass during lactation without
significant detriment to fertility, but more severe mobilization is damaging.
The consequences of inadequate amino acid intake appear to include effects on
the hypothalamic/pituitary axis and direct effects on the ovary that reduce
the quality of the developing follicles. A large body protein reserve at farrowing
appears to be protective. Management practices to encourage a high level of
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Effects of pattern of feeding over a 28-day lactation
on post-weaning fertility in first-parity sows bred at first post-weaning estrus
(from Zak et al., 1997ab)
|Feed level d 0 to 21:
|Feed level d 21 to 28:
|Zak et al., 1997a
|Weight change d 0 to 28, kg
|Weight change d 21 to 28, kg
|Backfat change d 0 to 28, mm
|Backfat change d 21 to 28, mm
|d 28 mean LH, ng/ml
|Embryo survival rate, %
|Ovulation rate, %
|# embryos at d 28
|Zak et al., 1997b
|Weight change d 0 to 28, kg
|Weight change d 21 to 28, kg
|Backfat change d 0 to 28, mm
|Backfat change d 21 to 28, mm
|% oocytes matured to Metaphase II:
|Generic oocytes matured in treatment follicular fluid
|Treatment oocytes matured in generic follicular fluid
Within a row, means without a common superscript letter differ by xy
P < 0.01,
P < 0.054.
Change in weight and backfat depth between d 21 and 28, and the # of embryos at
d 28 were not statistically analysed in these papers
Lactational and reproductive performance of first-parity
sows that lost a high, moderate, or low amount of body protein in lactation (From
Clowes et al., 2003a)
Protein Loss in Lactation
|Lysine intake in lactation, g/d
|Loss in lactation:
| Body protein a, kg
| Body protein a, % parturition mass
|Follicular fluid volume b, µL
|Follicular fluid E2 z, ng/mL
|Uterine weight d, g
|Piglet growth rate (d 0 to 23), g/d
|% GR change, d 0-20 to d 20-23
Body protein and fat mass predicted from the equations of Whittemore and Yang
Average follicular fluid volume from the largest 16 follicles (largest eight
from each ovary) measured at weaning..
Follicular fluid variables were measured on the largest eight follicular fluid
volumes collected at weaning.
Tissues were collected 2 to 4 h after weaning, on d 23 of lactation, at the
time of slaughter.
Within a row, means without a common superscript letter differ by
the P-value in that row.
Reproductive performance, and muscle parameters at weaning,
in first-parity sows with either a standard (165 kg) or high (193 kg) body mass
at farrowing, that lost a high amount of protein during lactation (From Clowes
et al., 2002 and 2003b)
||Standard body mass
(165 kg at farrowing)
|High body mass
(193 kg at farrowing)
|Calculated lactation lossa:
| Protein, %
| Fat, %
|Skeletal muscle variables at weaning:
|Muscle’s main proteolytic pathway mRNA expression
| Ubiquitin, 1.2 kb
| 14-kDa E2
|Follicular fluid estradiol, ng/mL
|% largest 16 follicles > 3.5mm diameter
Body protein and fat mass calculated from the equations of Whittemore and Yang
Within a row, means without a common superscript letter differ by P < 0.05
Regression analysis of subsequent wean-to-estrus interval
against the sow’s estimated whole-body a) protein and b) fat loss in lactation,
and c) lactational crude protein intake. Body protein and fat mass are presented
as a percentage of the parturition tissue mass, and were estimated from the equations
of Whittemore and Yang (1989).
Adapted from Clowes, (2001)
Break–point analysis of maternal protein loss
versus wean-to-estrus interval (WEI) on retrospective data from 16 published experiments
using two-phase regression. Adapted from Clowes et al. (2003a).