Reprod Dom Anim 43 (Suppl. 2), 129–136 (2008); doi: 10.1111/j.1439-0531.2008.01152.
x
ISSN 0936-6768
The Importance of Interactions Among Nutrition, Seasonality and Socio-sexual
Factors in the Development of Hormone-free Methods for Controlling Fertility
RJ Scaramuzzi1,2 and GB Martin3
1
UMRPhysiologie de la Reproduction et des Comportements, L’Institut National de la Reproduction, Nouzilly, France; 2Department of Veterinary
Basic Sciences, Royal Veterinary College, Hertfordshire, UK; 3Animal Production Systems, UWA Institute of Agriculture, The University of
Western Australia, Crawley, WA, Australia
Contents
Around the world, consumers are demanding animal products
that are produced to agreed standards for human health,
environmental management and animal welfare. This has led to
the development in Australia of the concept of ‘clean, green and
ethical’ (CGE) animal production based on the manipulation of
nutrition (‘focus feeding’) and the application of phenomena,
such as the ‘male effect’, to provide ‘natural’ methods for
managing small ruminant production systems. With respect to
the management of fertility, CGE involves utilization of the
inherited responses of animals to environmental factors to
manipulate their reproductive processes. The successful
development and implementation of this new generation of
management tools depends on a thorough yet holistic
understanding of the interactions among environmental factors
and the ways these interactions affect reproductive physiology
and behaviour of the animal. For sheep and goats, a central
aspect of CGE management is the way in which ovarian function
is affected by three major factors (nutrition, photoperiod and
socio-sexual signals) and by interactions among them. Nutrition
can exert two profound yet contrasting types of effect on ovarian
activity: (i) the complete inhibition of reproduction by under-
nutrition through the hypothalamic mechanism that controls
ovulation and (ii) the enhancement of fecundity by nutritional
supplementation, through a direct ovarian mechanism, in
females that are already ovulating. A similarly profound control
over ovarian function in female sheep and goats is exerted by the
well-known endocrine responses to photoperiod (seasonality)
and to male socio-sexual signals. The ‘male effect’ already has a
long history as a valuable technique for inducing a synchronized
fertile ovulation during seasonal and post-partum anoestrus in
sheep and goats. Importantly, experimentation has shown that
these three major environmental factors interact, synergistically
and antagonistically, but the precise nature of these interactions
and their significance to reproductive outcomes are not well
understood. Most research to date has been with small
ruminants but CGE principles can be applied to any species in
a managed environment. For example, a male effect has been
reported for lactating cattle and, in the horse, the pattern of
seasonality of oestrus can be altered by nutrition. Well-fed mares
have a longer breeding season and some animals become non-
seasonal. Similar observations have been reported for sheep and
goats. By working towards a holistic perspective of the physi-
ology, nutrition, genetics and behaviour of our animals, we will
be able to formulate ways to manipulate the animals’
environment that will improve management, productivity and
profitability and, simultaneously, promote a CGE industry.
Introduction
Animal industries around the world are being chal-
lenged by changing attitudes in the market place, and
consumers are increasingly demanding products that are
produced to agreed standards for human health,
 2008 The Authors. Journal compilation  2008 Blackwell Verlag
environmental management and animal ethics and
welfare. This is particularly evident in high-profit,
discerning markets that are influenced by discretionary
spending power. Our challenge is to turn these develop-
ments to advantage, improve productivity and profitabil-
ity and, simultaneously, promote ‘clean, green and ethical
(CGE) production’ (Martin et al. 2004a; Kadokawa and
Martin 2006; Martin and Kadokawa 2006). Importantly,
these issues need not pose difficulties or increase costs – on
the contrary, they offer excellent opportunities. For
extensively managed sheep and goats, we are developing
management tools, such as ‘focus feeding’ and the ‘male
effect’, for controlling reproduction and quantitative
breeding values for improving temperament (Martin
et al. 2004a).
This paper reviews current information, mainly for
sheep and goats, on a central aspect of the CGE system –
the way in which ovarian function is affected by three
major factors (nutrition, photoperiod and socio-sexual
signals) and by interactions among them. We review the
way in which nutrition can influence the ‘decision to
reproduce’ through the hypothalamic mechanism that
controls ovulation and the ‘decision for fecundity’
through a direct ovarian mechanism in females that are
already ovulating. In addition, we review the ways in
which the endocrine responses to photoperiod
(seasonality) and to male socio-sexual signals interact,
synergistically and antagonistically, with nutritional
inputs. It is increasingly clear that the multi-dimensional
nature of these interactions are often far more important
than the responses to the individual environmental input
(Blache et al. 2007).
Most research to date has been with small ruminants
but the ‘CGE principle’, in which manipulation of the
environment is used to control reproductive processes,
can be applied to all species. For example, a male effect
has been reported for cattle (review: Ungerfeld 2007)
and, in this review, we will describe nutrition–reproduc-
tion interactions in the horse.
Thus, the aim of this review is to outline the state of
our knowledge on the interactions among environmen-
tal facts that affect reproductive processes, and to point
out research that is needed for refining CGE manage-
ment of farm animals, particularly with respect to
management of the nutritional inputs.
Nutrition and Ovarian Function
All major measures of reproductive performance (pro-
lificacy, fertility and fecundity) are affected by genetics
130
and by a variety of environmental factors including:
(i) nutrition, energy balance and diet; (ii) photoperiod
and seasonality; (iii) socio-sexual factors; (iv) tempera-
ture and relative humidity and (v) stress. Nutrition
appears to have bi-directional effects on ovarian function
and the nature of these effects we suggest are inhibitory at
a hypothalamic level (allowing or preventing ovulation)
and stimulatory at an ovarian level (affecting ovulation
rate) and, furthermore, may differ between ruminant and
monogastric species. With respect to prolificacy, small
ruminants are generally regarded as seasonal monocot-
ous species, although natural twinning is not uncommon,
and there is considerable variation in the incidence of
twin ovulations and twin births among and within breeds.
The component of the diet that is probably the most
important with respect to ovarian function is energy
particularly that derived from glucose, although the
evidence in favour of any particular nutrient is still
controversial and the precise interrelationships between
ovarian function and the components of the diet are
obscure.
Nutritional effects on ovarian function are bi-directional
Nutritional deprivation of the female, whether as a
result of an insufficient supply of energy in the diet, or a
reduced availability of energy because of excessive
demands for energy (extreme physical activity, energy-
demanding processes such as lactation), inhibits hypo-
thalamic GnRH release and thus leads to reduced
secretion of pituitary LH and eventually to anovulation
and anoestrus. The hypothalamic GnRH pulse-generat-
ing system in monogastric species (rats, primates and
humans) appears to be more sensitive to nutritional
deprivation than in ruminants (sheep, goats and cattle).
In monogastric species, undernutrition and associated
hypoglycaemia quickly leads to suppression of the
GnRH system and a cessation of LH pulsatility (Bron-
son 1988; Cagampang et al. 1990). Farmed ruminants
rarely develop hypoglycaemia and thus appear to be
somewhat protected against nutritional anovulation,
although LH pulsatility is inhibited when they are made
hypoglycaemic under experimental conditions (Down-
ing and Scaramuzzi 1997; Szymanski et al. 2007) or as a
result of lactation (Rhodes et al. 1995). On the contrary,
for animals in normal body condition, nutritional
supplementation appears to have little direct influence
on hypothalamic GnRH secretion or pituitary gonado-
trophin secretion in the female and there is little
unambiguous evidence to show that nutritional supple-
mentation stimulates gonadotrophin secretion by a
primary hypothalamic mechanism or pituitary mecha-
nism.
Thus, for ovulation, primarily a GnRH-dependent
process, the effects of nutrient supplementation are not
simply the opposite to the effects of nutrient deprivation.
On the contrary, nutritional supplementation can stim-
ulate folliculogenesis (Webb et al. 2004; Scaramuzzi
et al. 2006) and thus increase prolificacy (Knight et al.
1975; Wang et al. 2004; Gaskins et al. 2005), but this
appears to involve direct nutritional influences on the
follicle itself. Follicular responses to increased nutrient
supply are not always positive and although increased
 2008 The Authors. Journal compilation  2008 Blackwell Verlag
RJ Scaramuzzi and GB Martin
folliculogenesis is associated with either short-term
nutritional supplementation or moderate increases in
body weight, extreme increases in body weight (obesity)
and rapid fluctuations in nutrient supply, such as
repeated cycles of ‘binge-eating’ followed by starvation,
have inhibitory effects on ovarian function and reduce
fertility (Hartz et al. 1979; Lake et al. 1997; Wolfe 2005).
Thus, there appears to be a nutritional threshold
below which reproduction is inhibited because of the
suppression of the GnRH pulse-generating system to a
level of activity below that required to maintain regular
ovarian cycles. At the hypothalamic level, nutritional
influences on reproduction are qualitative determining
fertility by assessing whether an animal ovulates or not.
However, once this threshold is reached and ovarian
cycles are occurring, nutritional regulation becomes
quantitative and operates at the level of the follicle to
determine the rate of reproduction – ovulation rate,
prolificacy or litter size.
Dietary supplementation, flushing and dietary signals
Flushing, a form of dietary supplementation, is a
practice that has been used in ruminant production
systems since at least the beginning of the 19th century
(Youatt 1837). Despite, or perhaps because of, its
widespread use, there appears to be a variety of
nutritional practices covered by the term, ‘flushing’. In
the absence of a precise definition of flushing, the
interpretation of published information and attempts to
elucidate the mechanism of nutritional influences on
ovarian function have been problematic. The metabolic
outcomes of a period of short-term (3–7 days) nutri-
tional supplementation are very different to those for a
6- to 8-week period of supplementation. Similarly, the
metabolic consequences of dietary supplementation of
animals in negative energy balance will be very different
from those for animals in positive energy balance. It is
therefore very likely that the effects on ovarian follicu-
logenesis and the GnRH pulse-generating system will
also depend on the metabolic state of the animal and the
nature of the supplementation. For example, Nottle
et al. (1997a) reported an experiment with ewes that had
been previously managed for 6 months as separate
flocks on either a high or low plane of nutrition. The two
flocks were recombined 17 days before mating and given
short-term nutritional supplementation with lupin grain
for the 10 days prior to mating. The short-term supple-
ment increased the ovulation rate by 54% in the
underfed group, compared with only 23% in the well-
fed group, and the interaction between previous nutri-
tional history and short-term supplementation was
significant (Nottle et al. 1997a). Another experiment
(Leury et al. 1990) reported an opposite finding; lupin
grain supplementation in ewes fed 1.2 times mainte-
nance increased ovulation rate by 22% compared with
ewes fed at 0.8 times maintenance where lupin grain
supplementation increased ovulation rate by 10%. The
reasons for this difference are not immediately apparent
and additional investigation is obviously required.
There has been considerable speculation and some
research attempting to identify the critical components
of the diet that influence ovarian function. The diet of
Nutritional Interactions and Reproduction
mammals is made up of complex mixtures of proteins,
fats and simple and complex carbohydrates as well as
trace elements, vitamins and other micronutrients, and
all of these components have the potential to influence
reproduction, either directly or indirectly. The current
consensus suggests that dietary energy is a very impor-
tant component of the diet with respect to nutritional
influences on ovarian function. The short-term admin-
istration of glucose or other energy-yielding substrates
can increase ovulation rate in ewes (Nottle et al. 1988;
Teleni et al. 1989; Downing et al. 1995a,b; Viñoles et al.
2005). However, there are other published reports in
which the increased supply of glucose did not increase
ovulation rate in ewes (Iglesias et al. 1996) and further-
more, in the male, the published data suggest that the
increased spermatogenesis seen in response to feeding a
lupin grain supplement is not caused by an increased
availability of glucose (Blache et al. 2002).
From the above remarks it follows that, when
examining the effects of nutrition on ovarian function
and folliculogenesis, there is an obvious need for a more
detailed description of both animals’ diets and metabolic
states than is customary.
Sources of metabolic glucose that affect ovarian function
Glucose for the generation of ATP is derived from either
dietary sources or from gluconeogenesis, either with or
without accompanying glycogen synthesis. Monogastric
species derive their glucose principally from dietary
sources rather than from gluconeogenesis, whereas the
ruminant species reduce their dietary glucose in the
anaerobic conditions of the rumen and derive their
glucose almost exclusively by gluconeogenesis, from
diet-derived long-chain fatty acids and short-chain
volatile fatty acids. Compared with monogastrics, this is
probably a highly significant functional difference with
respect to the effects of nutrition on ovarian function
because ruminants, animals with highly efficient gluco-
neogenesis rarely become hypoglycaemic or, for that
matter, hyperglycaemic. For example, dairy cows with a
high genetic merit for milk production do not become
hypoglycaemic at the peak of lactation, although they can
be in severe negative energy balance. Indeed, hypoglyca-
emia is usually only seen in ruminants in the most extreme
situations such as pregnancy toxaemia (twin lamb
disease) in sheep and in lactating first-calf beef heifers
that are still growing. Hypoglycaemic beef heifers have an
extended period of post-partum anovulation associated
with reduced LH pulsatility, because the hypoglycaemia
inhibits the GnRH pulse-generating system. The situation
with monogastric species appears to be quite different
because they depend on the diet for supplies of glucose
and have a limited capacity for gluconeogenesis com-
pared with ruminants. Monogastric species readily
become hypoglycaemic when deprived of dietary energy
and the consequence is a reduced GnRH ⁄ LH pulse
frequency and thus anovulation.
Seasonality and Ovarian Function
Seasonal patterns of reproduction are relatively com-
mon among the mammals including the domestic
 2008 The Authors. Journal compilation  2008 Blackwell Verlag
131
livestock – sheep, goats, horses and, under some
circumstances, cattle and pigs show seasonal rhythms
of ovarian function that are driven primarily by photo-
period. These patterns and the processes that underpin
them, especially in sheep, have been extensively inves-
tigated and there are a number of detailed reviews on the
subject (e.g.: Yeates 1949; Hafez 1952; Karsch et al.
1984; Malpaux 2006).
Interactions between nutrition and seasonality
Photoperiod and nutrition both exert major influences
on reproduction so it seems axiomatic that seasonal
rhythms in ovulation will be influenced by nutrition. It is
highly probable that photoperiodic and nutritional
inputs to the hypothalamus interact at the level of the
GnRH neuron (Hötzel et al. 2003; Blache et al. 2007),
yet there are relatively few published investigations of
the interaction between nutrition and photoperiodism in
females. There are few controlled studies with ewes
investigating the relationship between nutrition and the
pattern of seasonality, although there are reports of
alterations in the seasonal pattern of cyclic ovulatory
activity associated with nutritional conditions in previ-
ous seasons (Hunter 1962; Smith 1965; Oldham et al.
1990). In one study carried out over 13 months (Hulet
et al. 1986), ewes at pasture had a lower proportion
ovulating in the months of anoestrus (May, June and
July) compared with ewes in a drylot that were
supplemented with alfalfa hay (Fig. 1). The pasture-
fed ewes had a higher proportion of anovulatory ewes in
February suggesting that they were entering anoestrous
sooner. Similarly, in August, the pasture-fed ewes had a
lower proportion of anovulatory ewes, again suggesting
that they were slower to resume ovarian cyclicity at the
start of the new breeding season. In another study, the
seasonal pattern of ovarian cyclicity was determined in
Rasa Aragonesa ewes maintained at two levels of body
condition (Forcada et al. 1992; Forcada and Abecia
2006). This study showed that the duration of anoestrus
was reduced by approximately 2 months in the ewes
100 Pasture
90 Dry lot
80
Ewes ovulating (%)
70
60
50
40
30
20
10
0
Feb May Jun Jul Aug Sep
Time of the years
Fig. 1. The proportion of ewes ovulating in February (entering
anoestrus), May to July (during anoestrus) and August and September
(the start of the next breeding season) in two groups of fine-wool ewes.
One group was managed on rangeland and the other group was
managed with alfalfa hay in drylot. The within month treatment effects
were significant for all months except September. Data taken from
Hulet et al. (1986)
132
maintained in good body condition (BCS, 2.8) com-
pared with ewes maintained in poor body condition
(BCS, 2.3).
More extensive data are available for two other
seasonal species, the horse and the goat. In a study just
completed at the INRA laboratory at Nouzilly, Salazar-
Ortiz and Guillaume studied the effect of nutrition on
the seasonal rhythm of ovarian activity in mares kept
under natural photoperiod (Salazar-Ortiz 2006). The
pattern of ovarian cyclicity over three consecutive years
was determined from weekly blood progesterone mea-
surements in two groups of mares. One group was well
fed and the other group was received a diet calculated to
keep the mares thin but in good health. At the start of
the experiment, the average body weight of the two
groups was approximately 300 kg. The well-fed mares
gained approximately 20 kg in the first year after which
their mean live weight did not change for the remainder
of the experiment. The restricted mares lost approxi-
mately 65 kg in the first year and then their live weight
also stabilized for the remainder of the experiment. The
nutritional regime had a profound effect on the pattern
of ovarian cyclicity (Fig. 2) – the well-fed mares had a
much longer period of ovarian cyclicity and six of the 10
mares had no period of winter anovulation in the 3-year
experiment. This was in contrast with the restricted
group in which the winter period of anovulation was
longer and present in all the 10 mares.
Zarazaga et al. (2005) studied the effect of nutrition
on the seasonal pattern of sexual activity in female
Payoya goats kept under natural photoperiod over a
period of 20 months. The does were maintained on two
levels of nutrition: a high group fed 1.5 times their
calculated maintenance requirements and a low group
fed to maintenance. The pattern of seasonality was then
determined by daily monitoring for oestrus and for
ovulation using progesterone measured in blood twice a
week. The length of anoestrus was 32 days shorter in
does on the high diet and this difference was significant
because of both a delayed entry into anoestrus and an
earlier resumption of ovarian cyclicity at the end of
anoestrus.
Although domestic Bos taurus cattle are non-seasonal,
one study (Montgomery et al. 1985) reported an inter-
action between season and nutrition on the resumption
of ovarian cyclicity post-partum. In this study, an effect
100
Anovulatory mares (%)
80
60
40
20
0 one of the groups received a supplement (950 g lucerne
Sum Aut Win Spr Sum Aut Win Spr Sum Aut Win Spr Sum
Season
Fig. 2. The weekly proportion of anovulatory mares over a 3-year
period. The data for the mares on a high plane of nutrition are shown
by the solid line and that for the mares on a low plane of nutrition by
the dashed line. Redrawn from Salazar-Ortiz (2006)
 2008 The Authors. Journal compilation  2008 Blackwell Verlag
RJ Scaramuzzi and GB Martin
of the season of calving (winter versus spring at latitude
45 south) was observed only under conditions of low
nutrition. The same seems to apply to laboratory rats, in
which undernutrition seems to be able to modulate
reproductive responses to photoperiod through a pineal-
dependent pathway (Walker and Bethea 1977).
What do all these observations tell us? Most impor-
tantly, that there is an interaction in which nutrition
affects the seasonal pattern of ovarian cyclicity in sheep,
goats and horses; the variety of species suggests that
nutritional influences on patterns of seasonal reproduc-
tion are probably present in most, if not all, seasonal
breeding mammals, including non-seasonal species such
as beef cattle. However, the studies done to date with
female animals do not shed any light on the mechanisms
that underlie this interaction or on how the interaction
can be usefully incorporated into systems of CGE
animal production.
Socio-sexual Signalling and Ovarian Function
The ‘male effect’ is a well-studied phenomenon in sheep
and goats and there are a number of excellent recent
reviews of the subject (Martin et al. 2004b; Ungerfeld
et al. 2004; Chemineau et al. 2006; Ungerfeld 2007). In
summary, sexually active males produce a pheromone
that stimulates the secretion of GnRH pulses and ovarian
activity and can induce anovulatory females to ovulate.
Interactions between nutrition and socio-sexual signals
As with photoperiod, socio-sexual signals are a major
factor controlling ovulation in seasonal species and,
because nutrition also has major influences on
ovulation, it also seems highly probable that nutrition
would influence the efficacy of the ‘male effect’ and that
the site of the interaction is again the GnRH neuron in
the hypothalamus (Martin et al. 2004b; Blache et al.
2007). When a group of female goats were divided
according to bodyweight, it was observed that the
oestrus response to the ‘buck effect’ was reduced in the
does with the lowest body weight compared with those
with medium and heavy weights (Véliz et al. 2006).
Similar findings have been reported for ewes (Lassoued
and Khaldi 1990). Similarly, in beef cattle, the socio-
sexual influence of bulls can affect growth rate and the
age of puberty in heifers (Roberson et al. 1991), and
nutrition modifies the ability of bulls to reduce the
duration of post-partum anoestrus (Monje et al. 1992;
Stumpf et al. 1992).
In a recent experiment, we have investigated the
interaction between nutrition and the ‘male effect’ in
anoestrous female goats (De Santiago-Miramontes et al.
2008). Two groups of 25 anoestrous female goats grazed
very poor quality natural vegetation from 09:00 to
16:00 h daily. Overnight, they were housed in pens and
hay, 290 g rolled corn and 140 g soy bean per animal
daily) for 7 days before exposure to bucks. The propor-
tion of does ovulating, the proportion in oestrus and the
ovulation rate at the first ovulation detected within
5 days of exposure to males were all greater in supple-
mented than in the control females (Fig. 3). The effect of
Nutritional Interactions and Reproduction 133

2.0 100 Ovulating

Oestrus
1.6 80

Ovulation rate

Response (%)
1.2 60

0.8 40

0.4 20
Fig. 3. The ovulation rate
(mean ± SEM; n = 25), interval 0.0 0
(mean ± SEM days) from the
8.0 100
introduction of bucks to the onset

Does with short cycles (%)

Interval to oestrus (days)
of oestrus, and the proportions of
does ovulating, showing oestrus 80
and having short cycles at the first 6.0
ovulation following buck
60
introduction in does that were
either given nutritional supple- 4.0
mentation or not given nutritional 40
supplementation for 7 days before
the introduction of sexually active 2.0
20
bucks. All between-treatment
comparisons are significant. Data
taken from De Santiago- 0.0 0
Miramontes et al. (2008) Control Supplemented Control Supplemented

supplementation did not persist and the proportion of more of supplemented does ovulated over the first
does in oestrus was not different if ovulation occurred 5 days compared with the non-supplemented does
after 5 days (Fig. 4) and neither was the ovulation rate because most does responding in the first 5 days have
(De Santiago-Miramontes et al. 2008). We concluded a short cycle (Chemineau et al. 2006; Delgadillo et al.
that short-term feed supplementation before the ‘male 2006). These findings are consistent with the suggestion
effect’ can increase the proportion of females responding that a shorter delay from male introduction to the first
and their ovulation rate. However, the stimulatory effect ovulation is associated with an increased proportion of
of supplementation did not persist and was not observed short cycles (Pearce et al. 1985). The nutritional supple-
at the subsequent ovulation. The increase in ovulation ment appears to have accelerated the follicular phase
rate suggests that the supplement promoted the growth induced by the ‘buck effect’ and the shorter period of
of a greater number of ovulatory follicles or reduced the follicular development (Fig. 4) leads to either a non-
rate of atresia among the existing cohort of follicles. functional CL or, perhaps, to uterine entrainment for an
Somewhat surprisingly, supplementation also increased early luteolytic signal.
the proportion of does showing short cycles after the Somewhat similar findings have been reported for
first male-induced ovulation and this response was ewes. In one study, Nottle et al. (1997b) reported that
associated with a reduced interval from the introduction supplementation of Merino ewes daily with 500 g lupin
of bucks to oestrus (Fig. 3). The effect of nutritional grain from Days 12 to 26 after the introduction of rams
supplementation on the proportion of short cycles significantly increased the ovulation rate from 1.26 to
induced by the male effect could be due to the fact that 1.46 at the second ovulation following ram introduction.
Working with lactating Sarda ewes, Molle et al. (1995)
also observed an increase in ovulation rate following
60 supplementation starting 2 weeks before the ‘ram effect’,
but only with a supplement of soya bean meal and not
Does in oestrus (%)

50 a
with whole corn grain. In a later study, Molle et al.
40
(1997) reported that short-term supplementation for
30 only 7 days before the introduction of rams increased
20 ovulation rate from 1.36 to 1.66 but, in this case,
10 the difference was not significant, possibly because of the
group size of 15 ewes per treatment was too small. These
0
outcomes contrast with those from a factorial study with
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15
Time relative to the introduction of bucks (days)
390 Merino ewes (Fisher et al. 1993) – there were no
significant effects of short-term supplementation with
Fig. 4. The daily proportion of does showing oestrus for 15 days after lupin grain on the proportion of the flock responding,
the introduction of sexually active bucks on day 0 and following a ovulation rate or the frequency of short cycles in ewes
nutritional supplementation for 7 days before the introduction of the stimulated with the ‘ram effect’. This outcome was
bucks. The data for the supplemented group are shown by the dashed
line and for the non-supplemented (control) group by the solid line; the independent of the previous nutritional history of the
letter ‘a’ = p < 0.05 compared with the control group at the same ewes, although the percentage of ewes ovulating was
time. Redrawn from De Santiago-Miramontes et al. (2008) higher in ewes in good condition than in ewes in poor

 2008 The Authors. Journal compilation  2008 Blackwell Verlag

134
condition. There is no obvious explanation for the
differences in outcomes among these various studies.
Nutritional studies are difficult because they require
strict control of previous nutritional history. The mech-
anism behind the reproductive response to nutritional
supplementation is still problematic because we do not
have experimental models to explain the variability in
the response to a nutritional supplementation, the male
effect and their interaction.
Overall, it is clear that the efficacy of the ‘male effect’
is influenced by nutritional and metabolic factors in the
females. Thus, optimization of the efficacy of the ‘male
effect’ for CGE management requires a very clear
understanding of how nutrition influences the respon-
siveness of females to socio-sexual signals.
Conclusions
This brief review of nutritional interactions with sea-
sonal rhythms and the ‘male effect’ draws attention to
the importance of nutrition as a major factor influencing
reproductive outcomes and points to critical areas of
future research. There are some reports, often only
descriptively documenting the nature of these interac-
tions but there has been very little research exploring the
underlying processes. We need molecular genetic expla-
nations of the reproductive, metabolic, behavioural and
physiological processes that underpin, for example, the
influence of nutritional inputs on the melatonin-driven
seasonal rhythms of ovarian cyclicity, and on female
responsiveness to the ‘male effect’ at both brain and
ovarian levels. By working towards a holistic perspective
of the physiology, nutrition, genetics and behaviour of
our animals, we will be able to formulate ways to
manipulate their environment that will improve man-
agement, productivity and profitability and, simulta-
neously, promote a CGE industry.
Acknowledgements
RJ Scaramuzzi is the recipient of a Marie Curie Chair of Excellence
from the European Union (SUSTREPRO: FP6-2005-Mobility-
10 ⁄ 42499) and their support is gratefully acknowledged. GB Martin
was funded by Meat and Livestock Australia (Project MS.027;
‘LambMax’). Thanks are due to Dr B Malpaux and Dr D Guillaume
for their constructive comments on the manuscript.
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136 RJ Scaramuzzi and GB Martin

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Author’s address (for correspondence): RJ Scaramuzzi, UMR Phys-
iologie de la Reproduction et des Comportements, Centre INRA de
Tours, 37380 Nouzilly, France. E-mail: rscara@rvc.ac.uk
Conflicts of interest: Much of GBM’s research is funded by Meat &
Livestock, Australia; RJS has not declared any conflict of interests.

 2008 The Authors. Journal compilation  2008 Blackwell Verlag