animal feed science and technology 126 (2006) 259-276

8/19/2019 Animal Feed Science and Technology 126 (2006) 259-276

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Animal Feed Science and Technology

126 (2006) 259–276

Nutrition and fertility in ruminant livestock

J.J. Robinson ∗, C.J. Ashworth, J.A. Rooke,L.M. Mitchell, T.G. McEvoy

Scottish Agricultural College, Sustainable Livestock Systems Group, Ferguson Building,

Craibstone Estate, Bucksburn, Aberdeen AB21 9YA, UK

Abstract

In this review fertility is taken to be the successful establishment of pregnancy. Nutritional effects on

fertility therefore embrace the formation of the foetal gonads, their post-natal development, the timing

of puberty and in multiple ovulating species, their ovulation rates. The interval from parturition to

rebreeding, ovum quality, embryo development and embryo survival are the other major contributors

to fertility. In each of these areas there have been significant advances. For example recent research

in ewes has demonstrated that during its early development the foetal ovary is remarkably sensitive

to maternal nutrition with subsequent lifetime effects on ovulation rate. The timing of puberty in both

sexes and adult ovulation rates in ewes are influenced by post-natal nutrition. Nutrition during the

period when ovarian follicles emerge from the primordial pool (approximately 6 months before they

ovulate in ewes and 3–4 months in cows) can influence ovulation rate in ewes and oocyte quality

in cattle. Donor nutrition, in particular selenium status, can affect the resilience of spermatozoa to

freezing and thawing. In contrast to spontaneously ovulating animals in which high-plane feed imme-

diately before ovulation enhances oocyte and embryo quality the opposite is the case in superovulated

donor animals and those from which oocytes are harvested for in vitro embryo production. In high

yielding dairy cows excessive negative energy balance reduces insulin and IGF-1 concentrations and

increases growth hormone leading to delays in oestrous cyclicity and impaired oocyte quality andcorpus luteum function. Recent research into diets specifically designed to stimulate insulin secretion,

increase progesterone production by the corpus luteum and enhance the antiluteolytic mechanism is

Abbreviations: BMP, bone morphogenetic protein; FSH, follicle stimulating hormone; GnRH, gonadotrophin-

releasing hormone; IGF, insulin-like growth factor; LH, luteinising hormone; PGF2∝, prostaglandin F2∝; Zn, Co

and Se, zinc, cobalt and selenium This paper is part of the special issue entitled Feed and Animal Health, Guest Edited by Professor Kjell

Holtenius.∗ Corresponding author. Tel.: +44 1224 711052; fax: +44 1224 711292.

E-mail address: [email protected] (J.J. Robinson).

0377-8401/$ – see front matter © 2005 Elsevier B.V. All rights reserved.

doi:10.1016/j.anifeedsci.2005.08.006


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260 J.J. Robinson et al. / Animal Feed Science and Technology 126 (2006) 259–276

providing new opportunities for improving dairy cow fertility with associated benefits for suckling

beef cows. The move to a more mechanistic approach in dealing with nutritional studies of fertility

is providing information that can readily be adapted for the formulation of more efficient feeding

strategies across a diverse range of ruminant species and production systems.© 2005 Elsevier B.V. All rights reserved.

Keywords: Fertility; Nutrition; Ruminants

1. Introduction

Nutrition influences ruminant fertility directly by the supply of specific nutrients required

for the processes of oocyte and spermatozoa development, ovulation, fertilization, embryosurvival and the establishment of pregnancy. It also influences fertility indirectly through

its impact on the circulating concentrations of the hormones and other nutrient-sensitive

metabolites that are required for the success of these processes.

Current research on nutrition and ruminant fertility extends from whole animal responses

to the intricate cellular and molecular events that control gamete production, embryo

development, conceptus growth and implantation. It also deals with effects during embry-

onic and foetal life on the timing of puberty and subsequent adult fertility. The research

embraces a diversity of animal species, food types and management systems. Increasingly

it tests the impact of dietary-induced shifts in the end products of rumen fermentation on the

metabolism of gametes and embryos, and on the ability of their associated cellular structuresand secretions to secure their normal development. A further dimension to recent nutritional

research on ruminant fertility is the identification of feeding strategies that improve the

cryopreservation qualities of spermatozoa in males and superovulatory responses and

embryo quality in females involved in multiple ovulation and embryo transfer programmes.

In keeping with the recognised importance of the subject, nutrition and ruminant fer-

tility has been the topic of numerous recent original research papers and authoritative

reviews. Indeed more than half of the 36 review papers in the recent book volume enti-

tled Reproduction in Domestic Ruminants V (2003), either have nutrition as their main

theme or contain a section on the effects of nutrition on some aspect of fertility.

The aim of this review is to bring together recent research findings on the impact of

nutrition on the establishment of pregnancy in ruminants and to interpret the findings in

the context of the diversity of management systems that characterise the ruminant animal

industries.

2. Nutrition and male fertility

The durations of spermatogenesis in the bull, ram and goat are 54, 49 and 48 days,

respectively (Saunders, 2003); hence the recommendation for all three species that theyreceive adequate nutrition and are free from any deficits in the supply of specific nutrients

during the 2 months prior to breeding.


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J.J. Robinson et al. / Animal Feed Science and Technology 126 (2006) 259–276 261

Beneficial effects of ‘supra-nutritional’ supplementary trace minerals (Zn, Co and Se)

on sperm motility, percentage of live sperm and sperm membrane integrity in ram lambs

have been observed by Kendall et al. (2000). These benefits, which were accompanied

by an improved antioxidant status in the form of increased concentrations of glutathioneperoxidase in seminal plasma, were attributed to selenium on the basis that there was no

effect on seminal plasma zinc, and that a link between cobalt and Vitamin B 12 status and

male fertility has not been documented. A beneficial effect of selenium supplementation

(50 mg as barium selenate by s.c. injection) of rams on the viability and motility of their

semen has also been observed by Anderson et al. (1996). Interestingly the beneficial effect

in terms of the proportion of normal sperm was more pronounced following freezing and

thawing than in fresh semen.

In bulls, significant reductions with age in their sperm concentrations of the polyun-

saturated fatty acids, arachidonic 20:4n-6 and docosahexaenoic 22:6n-3, along with an

associated reduction in the antioxidant enzyme systems in their seminal plasma (Kelso et

al., 1997) have stimulated commercial interest in the use of dietary fish oil supplements and

higher inclusion rates for the antioxidant, Vitamin E, to improve fertility. These fatty acids

are important for sperm membrane integrity, sperm motility and viability, as well as cold

sensitivity. Their addition, in the form of tuna oil (30 g/kg diet) to boar diets resulted in an

increase, after a 5-week feeding period, in the proportions of progressively motile sperm

and those with a normal acrosome score as well as a decrease in those showing abnormal

morphologies (Rooke et al., 2001). In terms of the composition of sperm phospholipids, fish

oil supplementation also prevented the age-related replacement of docosahexaenoic acid

with docosapentaenoic acid 22:5n-6 that accompanies the decrease in sperm quality withadvancing age (Speake et al., 2003).

Where there are known adverse effects on sperm production and quality caused by

dietary ingredients such as cottonseed which contains the toxic polyphenolic pigment,

gossypol, there is evidence from studies with bulls that these can be reversed by feeding

4000 IU per day of Vitamin E (Velasquez-Pereira et al., 1998). Amongst other mecha-

nisms this protection by Vitamin E may be through the prevention of lipid-membrane

damage.

3. In utero nutrition and subsequent fertility

The effect of in utero nutrition on the timing of puberty and on adult fertility is currently

stimulating considerable research interest. For example, Da Silva et al. (2001) observed a 5-

week delay in the onset of puberty in intrauterine growth retarded male lambs (2.8 kg at birth)

compared with controls (5.2 kg). Although, not tested for its effect on subsequent fertility,

Alejandro et al. (2002) found that male lambs from ewes that gained 17% in bodyweight

during the second half of pregnancy had significantly more Sertoli cells in their testes at

birth than those from ewes that just maintained their bodyweight over the corresponding

period.

In the case of female offspring, Rae et al. (2002a) have reported that a low feeding level(0.5×maintenance) during the first 3 months of the 5-month pregnancy in ewes resulted

in their female offspring, at 20 months of age, having a lower mean ovulation rate (1.17


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Fig. 1. Critical periods during gestation in sheep for the expression of effects of maternal undernutrition

(0.5×maintenance vs. 1.0×maintenance) on foetal ovarian development (summarised from experiments reported

by Borwick et al. (1997) and Rae et al. (2001, 2002a)). After McEvoy and Robinson (2002).

versus 1.46) than those from adequately nourished (1.0×maintenance) controls. This effect

occurred in the absence of a significant difference in birthweight. This reduction in ovulation

rate due to early in utero nutrition occurred in the absence of any shift, either during foetal

or adult life, in pituitary gonadotrophins (Rae et al., 2002b; Borwick et al., 2003; Da Silva

et al., 2003). It therefore appears to be the result of a direct effect on the development of

the foetal ovary (see Fig. 1 for summary of foetal ovarian effects).

4. Post-natal nutritional effects

Nutrition during the early post-natal period can also have a permanent effect on adult

litter size in sheep and by inference probably so too in other multiple-ovulating ruminant

species such as the goat. For example, undernutrition in the form of an 8-week growth

arrest from 6 weeks of age in ewe lambs reduced their adult ovulation rates for up to 3

years (Williams, 1984) and in a more recent study a pre-weaning growth restriction of 12%

in hill ewe lambs caused a significant permanent reduction in their subsequent prolificacy

as adult ewes (Rhind et al., 1998). These observations and those for the in utero nutritional

effects referred to in the previous section have important implications for optimising

the allocation of the limited feed resources that characterise many of the world’s sheep

systems. This is particularly so for breeding females that are born and reared on harsh hilland mountain areas and then transferred to lowground farms where there is an abundance

of high quality forage and where a high reproductive rate is essential for profitability.


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Studies of the influence of post-natal nutrition on the timing of puberty are numerous.

In general they demonstrate that feed restriction delays puberty. In this regard the recent

study by Chelikani et al. (2003) of Holstein dairy heifers provides a useful illustration

with those animals growing at 1.1, 0.8 and 0.5 kg/day from 100 kg liveweight reachingpuberty at 9, 11 and 16 months of age, respectively. However, for many ruminant species,

seasonal effects in the form of changing nutrient supply or changing photoperiod, in their

natural habitats, modify the timing of puberty with those animals failing to achieve puberty

in one season having to wait another 12 months for the appropriate nutritional and/or

photoperiodic cues to trigger its expression (Adam and Robinson, 1994). Thus in many

natural environments there is enormous diversity in age at puberty both within a species

and indeed a breed. For example, in short-day breeders such as sheep and goats puberty

can occur under the declining daylength of their first autumn (5–6 months of age) provided

they are grown rapidly. If early growth rate is restricted puberty is likely to be delayed until

the following autumn. Interestingly there is some evidence that the timing of puberty in

feral sheep breeds may be less sensitive to nutrition and more sensitive to photoperiod than

those breeds selected for improved production (Adam et al., 1998). That photoperiod should

be the over-riding trigger for puberty in feral breeds is perhaps understandable. It may be

a natural mechanism to prevent nutritionally induced advances in puberty, and therefore

lambing, compromising the survival of the newborn lamb as a result of an inadequate food

supply and adverse weather conditions (Adam et al., 1998). In this regard red deer, in their

natural environment, are also highly dependent on declining daylength as a cue for the

timing of puberty (Adam, 1991). Due to their 2-month longer gestation than sheep, calving

takes place in the early summer, thus preventing the attainment of threshold sizes for theexpression of puberty in their first autumn. Thus ages at puberty are 9–10 months older than

those for sheep and goats.

Due to the restrictions imposed by their cold environment on food availability, Tibetan

yak only achieve puberty during the warmer summer months (Zi, 2003). For those that are

well nourished this can be as young as 13 months but if nutrition during the growing phase

is poor it can be as old as 36 months. In buffalo the range can be even higher (15 months to 5

years) with high temperatures and the associated low availability and quality of forage being

major inhibitors, as evidenced by a reduction from 39 to 23 months by improved nutrition

that resulted in daily weight gains increasing from 240 to 650 g (reviewed by Nandra et

al. (2003)). In buffalo, inadequate dietary protein leading to sub-optimal yields of rumenmicrobial protein often delays the timing of puberty (Kaur and Arora, 1995). On the basis

of a recent sheep study comparing 80 and 180 g/kg DM crude protein diets at the same level

of energy intake, this effect is likely to be the result of a reduced pituitary synthesis and

release of LH but not FSH (Polkowska et al., 2003).

5. Nutritional effects on the oocyte

Research into methods of improving the efficiency of ruminant multiple ovulation and

embryo transfer programmes and, more recently, in vitro systems of embryo production fromoocytes obtained by aspirating ovarian follicles is providing new information on the impact

of oocyte-donor nutrition on oocyte quality when using these reproductive technologies.


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Fig. 2. Effect of plane of nutrition and diet type during oocyte maturation on ruminant embryo development

following superovulation and/or in vitro embryo production (from data reviewed by Boland et al. (2001) and

McEvoy et al. (2001) with more recent observations by Adamiak et al. (2003) and Lozano et al. (2003)).

Fig. 2 provides an illustration of the main findings from these studies. Unlike spontaneously

ovulating sheep and cattle for which high-plane feeding is beneficial to oocyte quality the

opposite is the case in superovulated animals and those donating oocytes for in vitro embryo

production. The adverse effect is accentuated in animals in good body condition (Adamiak

et al., 2003) and those given large amounts of high-starch concentrates that are rapidly

fermented in the rumen (Yaakub et al., 1999).

Dietary excesses of rumen degradable protein given in discrete feeds lead to elevated

concentrations of ammonia in follicular fluid and are associated with reduced in vitro pro-

duction of blastocysts. The adverse effect on the oocyte is likely to involve inhibition in

the growth and metabolism of the oocyte-supporting granulosa cells (Rooke et al., 2004).It also appears to be follicle stage and size specific with pre-antral and medium-sized folli-

cles being most affected. Since medium-sized follicles can be induced to ovulate by giving

gonadotrophins, this may also explain why the adverse effect seems to be more prevalent

in gonadotrophin-stimulated than spontaneously ovulating animals. An associated feature

of the preceding dietary effects during oocyte development is cellular stress expressed as

up-regulation of embryo metabolism which in turn is not considered to be conducive to

good preimplantation embryo survival (Leese, 2002).

In high-yielding dairy cows the excessive negative energy balance of early lactation

coincides with a critical window in the development of oocytes that establish the next

pregnancy. Furthermore the oocyte develops in a changing biochemical environment withinthe follicle that reflects nutritionally mediated changes in the blood serum concentrations

of metabolites that indicate the energy, protein and mineral status of the cow (Leroy et al.,


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2004a). It is therefore perhaps understandable that cows that lose a lot of body condition in

early lactation (Snijders et al., 2000) and those with high hepatic triacylglycerol contents

which are indicative of excessive fat mobilisation at this time (Kruip et al., 2001) produce

oocytes of inferior quality as measured by their reduced ability to develop in vitro. Recently,Jorritsma et al. (2004) observed that high concentrations of non-esterified fatty acids, which

are a characteristic feature of undernutrition, reduced the in vitro proliferation of granulosa

cells, delayed oocyte maturation, and impaired blastocyst production. Thus a nutritional

effect on oocyte quality may contribute to the low fertility (Royal et al., 2000) of high

yielding Holstein dairy cows. There is also the suggestion however that there may be a

specific genetic component to the effect (Leroy et al., 2004b).

6. Ovulation rate

In addition to the foetal and early post-natal nutritional effects on adult ovulation rate

referred to earlier in this review there are times during adult life when ovulation rate is also

particularly sensitive to nutrient supply (Table 1).Inewesoneofthesetimesis6monthsprior

to mating when ovarian follicles emerge from the primordial pool and become committed

to growth. Undernutrition at this time reduces the number of follicles that emerge and

therefore the number that is available to ovulate. There is now evidence that the reduction

in ovulation rate can be prevented by improved nutrition (flushing) in the 10-day period

prior to mating. Indeed the critical window for the stimulatory effect of improved nutrition

may be even shorter than 10 days. Thus in a recent review of the scientific literature on

short-term nutritional flushing Viñoles Gil (2003) concluded that its beneficial effect couldbe imparted over as short a period as from Day 8 to Day 4 before ovulation (i.e. Days 10–14

of the oestrous cycle). This period coincides with the emergence of the ovulatory follicular

wave. Oestrous synchronisation permits precision in the application of nutritional inputs.

However the variable mating times that occur in a spontaneously ovulating flock means that

in order for all ewes to receive the nutritional stimulus a more extended period of improved

feeding commencing 10 days before the introduction of rams to the flock, is required.

Table 1

Critical windows during which ovulation rate in ewes is particularly sensitive to nutrition

Nutritionally sensitive window Target tissue/organ Mechanism

Foetus

Days 50–65 Foetal ovary Alteration in germ cell meiosis

Neonate

Pre-weaning N/D N/D

Adult

6 months prior to ovulation Ovary Alteration in the number of follicles

leaving the primordial pool

The 10 days preceding ovulation Hypothalamus, pituitary Changes in ovarian follicular growth and

atresia, oocyte quality, ovulation rate

Days 8–4 preceding ovulation Ovary Changes in ovarian follicular growth and

atresia, oocyte quality, ovulation rate

From data reviewed by Robinson et al. (2002a) and Viñoles Gil (2003). N/D: not determined.


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At the experimental level there are many examples of the beneficial effects of nutritional

flushing on ovulation rate in ewes. A selection of these is given in Table 2 to illustrate

the effect of diet type and different end products of digestion on the ovulatory response.

An interesting feature of the data in Table 2 is the very marked response in ovulation rateto a dietary supplement of ruminally undegraded starch by the carriers of the Booroola

fecundity gene, but not the non-carriers. This ‘fecundity’ gene has now been identified as a

point mutation in the intracellular serine threonine kinase signalling domain of the BMP-

1 receptor (reviewed by McNatty et al. (2003)). Its response to a specific feed component

promises to bring a new level of sophistication to our understanding of the role of nutrition

in controlling ovarian function and ovulation rate.

For veterinary practitioners carrying out commercial multiple ovulation and embryo

transfer programmes the recent observation by Mitchell et al. (2004) that the cobalt/Vitamin

B12 status of donor ewes affected ovulation rate is important. In this study ewes with mean

circulating B12 concentrations of 1483 and 182 pmol/l had mean±S.E. ovulation rates of

14.4± 1.28 and 9.9± 1.55, respectively, following superovulation.

7. The parturition to rebreeding interval

In sheep and goats, the vast majority of which have an approximate 7-month interval

from parturition to rebreeding, the main role of nutrition is to ensure that they achieve their

target condition score (3–3.5 on a five point scale) at mating for maximum ovulation rate.

Following the lactational depletion of body reserves this can be a slow process requiringrealimentation periods of approximately 90 and 65 days, respectively, in ewes consuming

forages with 8 and 12 MJ of metabolizable energy per kg dry matter at intakes equivalent

to twice maintenance (Robinson et al., 2002a). When lambing is made to coincide with

the natural mating season, suckling does not impair post-partum oestrous cyclicity. Under

these conditions Mitchell et al. (2003a) f ound that the replacement of 300 g/kg maize grains

with 300 g/kg sugar beet pulp in the concentrate portion of the lactation diet advanced the

mean±S.E. interval to oestrous cyclicity from 35± 3.1 to 26± 2.1 days.

For cattle (both dairy and beef) post-partum nutrition plays a major role in the timing of

the onset of oestrous cyclicity after calving, the normality of its expression and conception

rate. So too does body condition at calving. In beef cows suckling a single calf, those in goodbody condition at calving and those receiving high food intakes after calving have shorter

anoestrous periods than their thinner and less well nourished contemporaries (Wright et al.,

1992). Supplementary dietary protein in the form of digestible undegraded protein (DUP)

above that required for maximum microbial protein synthesis interacts with body condition

and ME intake to modify these effects (Sinclair et al., 1994). Thus at high body condition

extra DUP tends to reduce the post-partum interval to oestrus whereas at low body condition

it increases it (Fig.3) with the increase being more pronounced in those suckling twin calves.

In modern high yielding dairy cows for which fertility at first insemination has been

falling by up to 1% per year (Royal et al., 2000), there has been a major research effort to

identify nutritional strategies that will reverse this trend. This involves attempts to minimisethe incidence of delayed ovulation arising from the suppressing effect that a severe negative

energy balance (NEB) has on hypothalamic gonadotrophin releasing hormone activity and


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Table 2

Examples of the effect of a feed type (lupin grain), a compound feed (alfalfa hay, barley and soya bean meal), a protein su(ruminally undegradable starch) and products of digestion (acetate, glucose, branched-chain amino acids) on ovulation rate in

Treatment Ewe breed Control Supp

or in

Lupin grain (500 g/day)

Days prior to ovulation

15–9 Merino 1.03± 0.06 1.43

11–5 1.08± 0.08 1.53

7–0 1.10± 0.07 1.40

0.7 kg/day of a 60:30:10 mixture of alfalfa hay, barley

and soya bean meal for 14 days prior to ovulation

Rasa Aragonesa 1.50± 0.16 2.22

0.1 k g/day of fish meal for 14 days prior to ovulation Rasa Aragonesa 1.50± 0.16 1.88

100 g/day of ruminally undegraded starch for 22 days

prior to ovulation

FecB 2.46± 0.31 3.29

Non-FecB 1.36± 0.34 1.44

1122 mM/day of intravenous acetate for 9 days prior

to ovulation

Merino 1.32 1.51

60–65 mM/h of intravenous glucose from Days 9 to 4

prior to ovulation

Border LeicesterxMerino 2.0± 0.00 2.4±

12.3, 9.5 and 11.3 g/day of leucine, valine and isoleucine,

respectively, from Days 9 to 4 prior to ovulation

Border LeicesterxMerino 1.54± 0.16 2.35

Modified from Robinson et al. (1999). FecB and Non-FecB refer to Booroola crossbred ewes that are carriers and non-carrier

gene. Values are means±S.E.


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Fig. 3. Schematic illustration of how the interactions between body condition at calving and the metabolizable

energy (ME) and supplementary digestible undegradable protein (DUP) intakes during the post-partum period

influence the post-partum interval to first ovulation in beef cows.

the post-partum resumption of LH pulsatility (Roche et al., 2000). An important controller

of the magnitude of the NEB is body condition at calving which in turn is a reflection of

nutrition in the pre-calving ‘dry’ period. The late-pregnancy studies of Kruip et al. (2001),

albeit involving nutritional extremes, illustrate the point. High plane feeding (119 MJ of

ME/day for the last 8 weeks of pregnancy) leading to over condition at calving resulted in

lower voluntary feed intake and a larger and more protracted NEB during early lactation than

a late-pregnancy feeding level (49 MJ of ME/day) that just maintained energy balance. The

large NEB was accompanied by elevated hepatic concentrations of triacylglycerol (TAG)

which in turn were positively correlated with the interval to first ovulation. A recent study,

involving more subtle differences in late pregnancy nutrition in the form of a basal dietalone or supplemented daily with either 0.8 kg DM from milled barley or 0.75 kg DM from

a high DUP vegetable protein, showed no significant effects on the interval to first ovulation

(Pushpakumara et al., 2003). Although not significantly different, intervals to conception

were higher for those receiving the barley and DUP supplements than the basal diet alone

(123 and 105 days versus 90 days).

Attempts have been made to reduce the extent of negative energy balance and shorten

the post-partum interval to oestrus by boosting the energy concentration of the diet with

fats possessing varying degrees of protection from rumen biohydrogenation. In some cases

there have been benefits but in others associated reductions in forage intake or increases

in milk production have exacerbated the energy deficit and been counterproductive to fer-tility (Staples et al., 1998). Thus in a recent study, involving a grass-based system of milk

production, fewer cows receiving a protected fat supplement that increased milk yield had


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an early resumption of oestrous cyclicity than those receiving a fat supplement that did not

increase yield (McNamara et al., 2003).

Given that a severe negative energy balance is a primary cause of a delayed resumption of

normal oestrous cyclicity in high-yielding dairy cows (Lucy, 2003) and that a major limitingfactor is glucose supply (Beever et al., 2001), the role of nutrition for improved reproduc-

tion could be regarded as one of maximising the production of glucose precursors; in other

words the production of propionate and gluconeogenic amino acids. There is also the need

however to ensure a rumen fermentation pattern that will provide sufficient acetate for milk

fat synthesis. An example of the beneficial effect on ovarian function of boosting the glucose

supply is seen in the experimental approach of daily drenching of dairy cows from 7 to 42

days of lactation with 500 ml of propylene glycol (Miyoshi et al., 2001). Compared with

controls this treatment reduced the interval to first oestrus, eliminated the short initial luteal

phase and increased conception rate. Rather than being the result of a reduction in negative

energy balance, these beneficial effects were attributed to a significant increase in plasma

insulin. Thus dietary regimens and ingredients that aim to correct a specific weakness in

the nutritionally sensitive modulators of hypothalamic/pituitary/ovarian function at critical

times post-partum may provide opportunities to improve dairy cow fertility. The results of

the more recent study by Gong et al. (2002) support this view. By formulating diets with

the same ME and crude protein concentrations but with contrasting fermentation character-

istics (acetate versus propionate, 100 g versus 260 g starch/kg DM) they found that, in the

absence of any shift in milk yield or energy balance, the ‘propionate’ diet increased insulin

concentrations and reduced the interval from calving to first ovulation. In autumn-lambing

ewes, Mitchell et al. (2003b) found that a propionate-producing diet which increased insulindecreased the incidence of short luteal phases.

While insulin may be the main modulator of the post-partum nutritional effect on the

resumption of ovarian activity, IGF-1, growth hormone and leptin are also likely to be

involved in that their concentrations are correlated with nutritionally induced changes in the

timing of first post-partum oestrus (Armstrong et al., 2003). For example, undernutrition is

associated with elevated growth hormone, reduced IGF-1, an uncoupling of the link between

growth hormone and IGF-1 and failure of the dominant ovarian follicle to produce enough

oestradiol to generate the preovulatory LH surge. Protracted intervals to first oestrus are

also associated with delays in the recovery of leptin concentrations after calving (Kadokawa

et al., 2000) and low concentrations of leptin have been observed in cows with abnormalpost-partum reproductive cycles (Mann and Blache, 2002). With regard to their relative

importance, Armstrong et al. (2003) found that following GnRH administration increases

in insulin concentrations preceded increases in IGF-1 which in turn preceded increases in

leptin. Another metabolite with experimental observations linking it to energy balance and

changes in nutritional status is ghrelin, a peptide that is mainly produced by the gut ( Blache

et al., 2003). It has not yet been thoroughly investigated in ruminants.

8. Embryo development and survival

Fig. 4 provides a simplified schematic illustration of the diversity of routes by which

nutrition influences embryo development and survival. Many of these are not solely about the


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Fig. 4. Some examples of the routes by which nutrition influences embryo development and survival in ruminants.

direct provision of essential nutrients in the histotroph (oviductal and uterine secretions)

that nurtures the early embryo; rather they involve indirect effects on the histotroph of

nutritionally sensitive hormones such as progesterone and growth factors such as IGF-1.

Others not shown in Fig. 4 are growth hormone, insulin and the IGF-binding proteins and

proteases that modify the IGF responses.

As a result of its stimulating effect on follicle growth (Fig. 4) improved preovulatory

nutrition increases the size of the ovulatory follicle and the progesterone-secreting ability of

the resulting corpus luteum. However, following ovulation high plane feeding can suppressblood progesterone concentrations to levels that compromise embryo survival (Robinson et

al., 2002a). This is particularly so in ewes; thus a maintenance level of feeding during the

first month of pregnancy is now considered optimum for embryo survival in this species

(Robinson et al., 2002a). For cattle the evidence for an adverse effect of high-plane feeding

on progesterone is equivocal. Nonetheless in cattle, enhanced embryo development (Mann

et al., 2003) and increased production of the trophoblastic antiluteolysin, interferon tau

(Wathes et al., 2003), which are prerequisites for good embryo survival, are positively

correlated with progesterone concentrations on Days 4 and 5 following ovulation. This

feeding strategy would seem the most practical for maximising progesterone production,

although Kuran et al. (1999) have shown enhanced luteal progesterone in ewes given dietarysupplements of fatty acids (palmitic, stearic and oleic) in the form of a rumen-protected

calcium soap.

In the more controlled feeding systems applied to dairy cows dietary inclusions of calcium

soaps of saturated fatty acids which enhance progesterone through increased cholesterol

provision (Staples et al., 1998) are easily implemented. However, with growing interest

in the use of dietary polyunsaturated fatty acids (PUFA) to increase the unsaturated fatty

acid content of milk for improved human health, research is now focussed on the effect

of dietary PUFA supplementation on dairy cow fertility. Fish oil, a rich source of two

of the targeted PUFAs (eicosapentaenoic 20:5n-3, and docosahexaenoic 22:6n-3) caused

a significant decrease in the oxytocin-induced release of PGF2∝ (Thatcher et al., 2001)on Day 15 following oestrus, an effect which would be conducive to improved embryo

survival. A similar in vivo effect was observed on Day 17, but not Days 15 or 16 in cows


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given the polyunsaturated fatty acid, linoleic, 18:2n-6 (Robinson et al., 2002b). Endometrial

explants from cows given a predominantly n-6 supplement also had a lower capacity to

produce PGF2∝, PGE2 and 6-keto-PGF1∝ (Cheng et al., 2001). However linoleic acid

supplementation reduced early luteal progesterone concentrations despite there being alarger dominant follicle and higher IGF-1 and cholesterol concentrations. Care should thus

be taken lest some fatty acid-rich supplements compromise embryo survival. This concern is

also relevant at the earliest stages of development because, on the basis of in vitro research

findings, bovine embryos are sensitive to the adverse effects of fatty acid accumulation

unless given adequate antioxidant protection (Reis et al., 2003).

High protein diets are a common feature of dairy cow nutrition. Their associated high

blood urea concentrations coupled with sub-optimal early luteal progesterone concentra-

tions have been found to have a detrimental effect on embryo survival (Butler, 2001).

Elevation of plasma urea and ammonia by feeding 250 g/day of a urea supplement to dairy

cows from insemination had a deleterious effect on the quality of Day 7 embryos (Dawuda et

al., 2002) and ammonium chloride addition to culture medium caused quantitative changes

in bovine embryo amino acid metabolism (Orsi and Leese, 2004). Interestingly, introducing

the supplement 10 days before insemination had no adverse effect on embryo development,

or on insulin, IGF-1 and early luteal-phase progesterone concentrations (Dawuda et al.,

2004), implying that the cows had adapted to the high urea. Thus, the practical implica-

tion of the findings is to avoid the spring turnout to high nitrogen grass coinciding with

rebreeding.

Numerous micronutrients are involved in embryo development and survival. Those for

which deficiencies, and in the case of Vitamin A excesses, are linked to impaired embryodevelopment and poor embryo survival in practical farming systems are shown in Fig. 5

Fig. 5. Micronutrient involvement in embryo development and survival.


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along with their functions and modes of action. For a comprehensive and detailed review

the reader is refereed to Underwood and Suttle (1999). As with all nutrients but perhaps

more so with the trace minerals there is considerable variation in the dietary requirements

for maximum embryo survival. Contributing factors are the interactions between differentmineral elements in their absorption and use, animal breed and genotype effects, the diver-

sity of farming systems (intensive to organic) and the application of improved breeding

technologies.

Finally, the impact of nutrition on embryo survival in ruminants extends beyond the

supply of essential nutrients and the modification of the hormones and growth factors

that influence embryo development. Unlike simple stomach species, abrupt changes in the

composition of diets fed to ruminants or rapid fluctuations in feeding level and pattern of feed

intake can disrupt rumen function and metabolic homeostasis with adverse consequences

for embryo survival.

9. Conclusions

In this review, recent research on nutrition for improved fertility in ruminants has been

considered in the context of nutritionally sensitive periods in the production of gametes and

viable embryos. This approach provides a conceptual framework from which to develop long

term feeding strategies which enable animals to maximise their fertility. In high-producing

animals such as the dairy cow, the demand on nutrients for milk production creates a level of

negative energy balance during early lactation that compromises ovarian follicular growth,

oocyte quality, corpus luteum function and embryo survival. As a result of recent research

into how specific dietary ingredients influence the steroid and peptide hormones that control

ovulation and embryo survival, there are now opportunities for improving dairy cow fertility,

with associated benefitsforbeef cows. The move from an empirical to a mechanistic research

approach should bring greater precision to the formulation of diets and feeding regimens

that embrace the diversity of ruminant species and genotypes, the farming systems within

which they are kept and the breeding technologies to which they are subjected.

Acknowledgements

The authors thank the Scottish Executive Environment and Rural Affairs Department

and the United Kingdom Department for Environment, Food and Rural Affairs for funding

studies on nutrition and reproduction at SAC.

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