CSIRO PUBLISHING

www.publish.csiro.au/journals/rfd Reproduction, Fertility and Development, 2004, 16, 491–501

Nutritional and environmental effects on reproduction

in small ruminants

G. B. MartinA,B,C , J. Rodger A and D. Blache A

A School of Animal Biology, Faculty of Natural and Agricultural Sciences, The University of Western Australia,
Crawley, WA 6009, Australia.
B CRC for Plant-based Management of Dryland Salinity, University of Western Australia,

Crawley, WA 6009, Australia.

CTo whom correspondence should be addressed. email: gmartin@agric.uwa.edu.au

Abstract. Animals live in environments that are both complex and continually changing, so they have to respond
to short- and long-term variations in a wide range of factors, such as photoperiod, nutrition and sociosexual signals.
Before they were domesticated, animals developed reproductive strategies that coped with these changes and often
took advantage of them. The physiological processes that implement these strategies have been modified to some
extent during several millennia of controlled breeding, but most persist. Thus, many genotypes still exhibit profound
responses to external inputs, such as the induction of ovulation by sociosexual signals and the doubling of litter size
by a change in nutrition. The complexity in these responses is now becoming clearer. For example, with sociosexual
signals, we now need to consider the stimulatory effects of males on females, of females on males and of females
on females. Similarly, the impact of nutrition has been extended beyond the control of puberty and the production
of gametes to include phenomena such as ‘fetal programming’, with its potentially profound effects on the life-long
performance of the animals. Fortunately, our capacity to research these phenomena has been greatly enhanced
by technical improvements in hormone assays, molecular and cellular biology, and real-time ultrasound. This has
brought us a better understanding of several of the environmental influences on reproduction, including: the cellular
processes within ovarian follicles that mediate the effect of nutrition on ovulation rate; the neuroendocrine pathways
through which nutritional inputs affect the brain centres that control appetite and reproduction; and the intracerebral
pathways through which sociosexual signals (olfactory and non-olfactory) stimulate the reproductive axis. Impor-
tantly, we are now beginning to realise that, as well as considering interactions between environmental inputs and
genotype, we need to take into account interactions between the environmental factors themselves, just as the ani-
mals do. We still have a long way to go for a complete understanding, but we are nevertheless in a position where we
can begin to use this information to develop new management systems for our animals to improve their productivity.

Extra keywords: female effect, fetal programming, male effect, pheromone, season.

Introduction
During evolution, animals developed reproductive strate-
gies to ensure that periods of abundant food coincide with
late pregnancy and lactation. The typical view is that this
is achieved by linking sexual activity to changes in pho-
toperiod, a reliable predictor of the seasons and, therefore,
future food supplies. However, this view is not universally
applicable for three reasons. First, photoperiods may change
imperceptibly in regions close to the equator, where many
sheep and goats are used in production systems. Second,
in many environments, the annual pattern of food supply is
determined by factors other than photoperiod, particularly
rainfall. Third, in semi-arid environments in particular, the
pattern of food supply varies greatly from year to year because
the timing of rainfall is very unpredictable. Animals that are
adapted to these situations have developed strategies that
are opportunistic and relatively flexible with respect to the
timing and intensity of reproductive effort. These opportunis-
tic strategies usually have an underlying annual cycle driven
by photoperiod, but the final reproductive outcome is mod-
ified by responses to other environmental inputs. This was
elegantly demonstrated by Bronson (1985), who studied the
reproductive strategies of species of rodent, lagomorph and
deer in a wide range of environments between the equator
and the arctic circle. The same perspective can be used to
study the domestic ruminants, as we have done by compar-
ing the Suffolk and Merino genotypes. Suffolk rams follow
the ‘photoperiod-driven’ model typical of animals that were
developed in temperate regions, whereas Merino rams fol-
low changes in food availability more than photoperiod and

© CSIRO 2004 10.1071/RD04035 1031-3613/04/040491

492 Reproduction, Fertility and Development G. B. Martin et al.

their annual cycle can be completely overridden by sociosex-
ual interactions (Martin et al. 1999, 2002; Walkden-Brown
et al. 1999; Blache et al. 2003). The same applies to the many
breeds of sheep and goats that have their origins in the cli-
matic zones between 35◦ N and 35◦ S, probably one-third of
the world’s population; hence, our argument against ‘temper-
ate chauvinism’ in research into seasonal breeding (Martin
et al. 1994; Martin 1995).
In the first part of this paper, we will present a brief
overview of the physiological linkages that animals use to
coordinate their reproductive output with environmental fac-
tors, with a particular focus on the roles of nutrition. A more
detailed coverage of this area, taking into account interactions
with genotype, can be found in the recent review by Blache
et al. (2003), although that paper only dealt with neuroen-
docrine integration. Thus, in the second part of the present
paper, we will also mention several effects of nutrition on the
reproductive system that cannot be easily linked into brain-
controlled reproductive strategies for coping with seasonal
environments. They are perhaps more easily seen in the con-
text of survival of a shortfall in nutrition and may even fit into
the category of stress responses. The final part of the paper
will deal with sociosexual stimuli. Most of the information
we use will be derived from studies with sheep, particularly
Merinos, but the physiological principles and most of the
reproductive responses can be applied to all ruminants.
Environmental inputs into reproduction: general
considerations
Most reproductive responses to environmental factors are
coordinated at brain level, where all external and internal
inputs ultimately converge into a final common pathway that
controls the secretion of gonadotrophin-releasing hormone
(GnRH). In turn, this neurohormone controls the secretion
of the gonadotrophins, the pituitary hormones that determine
the activity of the reproductive axis (Fig. 1). The activity of
these neurons is coordinated and synchronised so GnRH is
released as a stream of pulses, the frequency of which is crit-
ical: a high frequency promotes gonadal activity and a low
frequency allows gonadal activity to subside. Each pulse of
GnRH releases a pulse of the gonadotrophin luteinising hor-
mone (LH) from the pituitary gland. In the male, each LH
pulse stimulates the Leydig cells in the testes to release a
pulse of testosterone, which completes the loop by exerting
‘negative feedback’ on the hypothalamic control system to
reduce the frequency of the GnRH and LH pulses (Fig. 1).

Sociosexual signals Food supply

Photoperiod
including pheromones

Auditory Olfactory Vision Pineal

system system system system

GnRH Apetite
pulsar Orexin, NPY ... control
GnRH centres
Preoptic−hypothalamic
? continuum

GnRH Negative
dependent feedback
Leptin, insulin
LH, FSH Sex steroids

Gametes
Uterus and feto-
placental unit

Nutrients,
Gametogenic Endocrine GnRH
metabolites and
functions functions independent?
metabolic hormones

Gonad Mammary gland Colostrum

Fig. 1. Environmental inputs into reproduction operate through a variety of pathways, many of which
ultimately affect the activity of the ‘GnRH Pulsar’ (Martin 1984) and, thus, the pulsatile secretion
of gonadotrophin-releasing hormone (GnRH). The relative importance of these GnRH-dependent
responses to photoperiod and nutritional and sociosexual stimuli depends largely on genotype (for
reviews, see Martin et al. 1986; Blache et al. 2000, 2002, 2003). In addition, there are nutritional and
other inputs into gonadal, uterine and mammary function that also affect reproductive output.
Environment, nutrition and reproduction Reproduction, Fertility and Development 493

In the female, each LH pulse stimulates the follicles to release
a pulse of oestrogen and this steroid fills a role equivalent to
that of testosterone in the feedback loop. A major difference
between the sexes is that, during the breeding season, the
female gonad also produces progesterone and the feedback
loop relies primarily on this steroid and its synergistic interac-
tion with oestradiol (for a review, see Martin 1984). However,
recent research is revealing a key similarity between the sexes:
in male sheep, oestradiol is arguably more important in neg-
ative feedback than testosterone and the testosterone from
the Leydig cells effectively acts as a prohormone and is con-
verted to oestradiol by aromatase in testicular, hepatic and
brain tissues (Sharma et al. 1999; T. P. Sharma, D. Blache,
C. E. Roselli and G. B. Martin, unpublished observations).
In our studies of environmental effects on the reproductive
system, we have focused on pulsatile LH secretion because it
is a simple and effective bioassay of GnRH cellular activity
and, therefore, an excellent indicator of responses to inputs
from the sensory systems that detect external stimuli. The
obvious risk of this approach is that it ignores the other major
endocrine loop that controls reproduction – that involving
pituitary follicle-stimulating hormone (FSH) and the actions
of gonadal hormones at pituitary level. The secretion of FSH
is not pulsatile, so it does not provide the same type of infor-
mation about cerebral responses, but it is vital in controlling
the production of gametes as well as the secretion of sex
steroids and inhibin. In addition, it may play a role in the
‘GnRH-independent’ pathways that seem to be particularly
important in the effects of nutrition (Fig. 1), as discussed
below.
Because of the feedback loop, the hypothalamic–
pituitary–gonadal system is theoretically in equilibrium, but
the balance can be shifted by exteroceptive factors, such as
nutrition, sociosexual signals and photoperiod. The role of
photoperiod and the physiological systems linking this input
with the brain–pituitary–axis have been extensively covered
elsewhere (see Tricoire et al. 2003), so will not be detailed in
the present paper. However, we must emphasise the impor-
tance of the interaction between photoperiod and genotype.
Many of the responses of the hypothalamic–pituitary system
to other inputs, including nutritional and sociosexual signals,
depend on the degree to which the genotype under consid-
eration responds to photoperiod (Blache et al. 2003). For
example, in genotypes that are very responsive to photope-
riod, nutritional inputs can be dominated to the point where
rams can be gaining testicular mass at the same time as they
are losing body mass (Martin et al. 2002).
Effects of nutrition on the reproductive process
The importance of nutrition in the breeding of production
animals has probably been understood since domestication,
although serious scientific investigation and documentation
only began approximately 100 years ago (for a review, see
Clark 1934). Nutrition was known to affect many aspects of
the reproductive process (Fig. 2) and much research effort
was devoted to puberty, gamete production (particularly ovu-
lation rate), placental growth and lactation. In recent years,
there have been major developments in two more areas of
the process, namely fetal development (‘fetal programming’)
and colostrum production in relation to survival of offspring.
The various responses to nutrition, as indicated in Fig. 2, can
be incorporated into management practices, as we have dis-
cussed elsewhere (Martin et al. 2004) so, here, we will outline
it only briefly as a means of emphasising our views on where
more research is needed.

Nutritional inputs

?
Ovulation
Peri-
rate
conceptual
programming?
Sperm Embryo
production survival Fetus and placenta Colostrum
– fetal programming? production Pubertal development
Bloomfield period? ? ? ?

Weeks ⫺8 0 6 12 18 24 30
Mating Pregnancy Birth Lactation Wean

Fig. 2. Periods during the reproductive process of small ruminants when supplementary feeding may affect the reproductive success of the flock.
Generally, nutritional supplements are beneficial, but early embryo development may be an exception because there is some evidence that overfeeding
during that process can provoke embryo mortality. The postulated impact of undernutrition during the 90-day periconceptual period, as evidenced
by Bloomfield et al. (2003), is also indicated. Modified after Martin et al. (2004).
494 Reproduction, Fertility and Development
Gamete production
The effects of nutrition on testicular growth and sperm pro-
duction in mature males has been researched in some detail
(for a review, see Martin and Walkden-Brown 1995), but there
is still a great need for fundamental investigations into the
physiological processes involved. For the GnRH-dependent
pathway (Fig. 1), we still have a poor grasp of the links
between nutritional and metabolic inputs and their effects
on gonadotrophin secretion. Different signals and different
target organs seem to be responsible for the short- and long-
term aspects of the response. Short-term dietary treatments
lead to changes in blood concentrations of glucose, fatty
acids, insulin and leptin, as well as in cerebrospinal fluid
(CSF) concentrations of glucose, insulin, leptin and some
amino acids. Among these, the most important factors seem
to be fatty acids, insulin and leptin, all of which can increase
GnRH/LH pulse frequency. Current studies are suggesting
that there are neuroanatomical linkages between the cen-
tres that control reproduction and those that control appetite
(Blache et al. 2002, 2003), with both perhaps controlled by a
‘metabolic sensor and integrator’ (Blache et al. 2000). These
acute neuroendocrine responses stimulate GnRH secretion
within hours of a change in diet and then disappear after
3–4 weeks as the feedback system re-establishes an equilib-
rium. However, as long as the dietary treatment is maintained,
the testes continue to grow and produce more spermatozoa
and these longer-term effects do not depend on changes in
GnRH output (i.e. on brain control) and, thus, depend on the
other pathway that we have labelled ‘GnRH-independent’ in
Fig. 1 (Hötzel et al. 1995).
We know very little about these ‘GnRH-independent’links
between nutritional input and gonadal output, although it is
difficult to avoid a fundamental role for the factors that con-
trol energy balance in the animal (Boukhliq et al. 1997). It has
long been known that metabolites and metabolic hormones
can be absorbed from the blood and will evoke responses in
the uterus and mammary gland with a large degree of inde-
pendence from brain control. Similar pathways are becoming
evident for the gonads. In the female, the process of ovulation
is GnRH dependent, but nutritional effects on ovulation rate
seem be mediated primarily through pathways that depend
very little on a change in the secretion of GnRH, LH or FSH.
A critical observation here is that as little as 4 days of supple-
mentation will increase ovulation rate (Stewart and Oldham
1986), so the mechanism is confined to the final stages of fol-
liculogenesis. There are some reports suggesting that these
acute dietary treatments can stimulate gonadotrophin secre-
tion in ewes (e.g. Rhind et al. 1985), but most have failed to
demonstrate robust and consistent effects (e.g. Rhind et al.
1989) matching those we have seen in males. Progress in this
area over the past 20 years has often been discouraging, per-
haps because experimentation is difficult: ovulation rate is
a discrete variable with a narrow range and follicular activ-
ity is difficult to study without complex models, such as the
G. B. Martin et al.
ovarian transplant. However, sustained incremental refine-
ments in hormone assays, cell biology and ultrasound have
greatly improved our capacity for testing new hypotheses.
Ultrasound has proven to be particularly valuable for fre-
quent and repeated measurements of ovarian follicles in the
same animal during pre-ovulatory growth and development
(Viñoles et al. 2002).
Two current areas of focus are: (1) the roles of intrafollic-
ular energy metabolism (glucose transport, cytokine activity)
in follicle development; and (2) the role of apoptosis in fol-
licular atresia. Both these processes can respond rapidly to
extra-ovarian stimuli and, thus, may be able to explain, for
example, the increase from one to two follicles entering the
pre-ovulatory stage after only 3 days of supplementary feed-
ing. Scaramuzzi et al. have been working on the hypothesis
that short-term nutritional supplements increase ovulation
rate in the ewe by increasing the glucose supply (e.g. Downing
et al. 1995). At the same time, Iglesias et al. (1996) showed
that a glucogenic drench also increases ovulation rate in
sheep. Before these reports, most workers had been con-
centrating on the roles played by the gonadotrophins, but
the glucose work extended the scope of fundamental stud-
ies on folliculogenesis to include several metabolic factors,
such as insulin, growth factors, glucosamine and leptin, many
of which appear to play a role in the effects of nutrition
on ovarian output (Williams et al. 2001; Muñoz-Gutiérrez
et al. 2002). We are being convinced that, for the control
of ovulation rate, the actions of nutritional signals inside the
ovarian follicle are far more important than nutrition-induced
changes in the activity of the centres in the brain that control
GnRH secretion.
Effect of nutrition on sexual behaviour
The sexual behaviour of small ruminants does not seem to be
affected by nutrition unless there has been an extreme change
in body mass and energy reserves that has affected motor
activity. In the ram, sexual behaviour decreases with severe
undernutrition simply because of the general weakness of the
animal (Parker and Thwaites 1972). Conversely, overnutri-
tion decreases the effectiveness of mating behaviour because
overweight animals become clumsy (Okolski 1975). Among
adult ewes, severe undernutrition may alter the expression of
sexual behaviour because the oestrous cycles have become
irregular or even arrested (Hafez 1952; Allen and Lamming
1961; Lamond et al. 1972). It is not clear whether this is
due to a specific behavioural response or to a reduction in
GnRH pulse frequency that prevents the cascade of events
leading to ovulation: these same events are necessary for the
induction of behavioural oestrus (for a review, see Blache
and Martin 1995). We need to be careful not to confuse
the incidence of oestrus detected in a flock with quantifi-
cation of the behaviour displayed by a female (e.g. duration
and intensity, as measured by Fabre-Nys and Venier (1987)).
There is no evidence showing that undernutrition affects the
Environment, nutrition and reproduction
pre-ovulatory surge of LH or the release of oestrogen, but
it does affect the responsiveness of ovariectomised ewes to
exogenous oestrogen (Gibson and Robinson 1971). Overnu-
trition appears to have little influence on the sexual behaviour
of the ewe because overweight ewes mainly stand still during
sexual encounters. However, proceptivity may be impaired
because overweight ewes may not be able to actively search
for a male. Similarly, the behavioural interactions that under-
pin male–female interactions in the ‘male effect’ (see below)
may be compromised in animals with low levels of activity
and this may explain the poor responses seen in underfed
ewes by Wright et al. (1990). There is very little literature in
this area for small ruminants and more research is needed to
at least define the importance, or otherwise, of the issues.
Periconceptual losses
Severe undernutrition is one of the many factors suggested
as a cause of embryo loss in sheep but, paradoxically, there
is also evidence that overfeeding in the first few weeks after
fertilisation can cause problems. This is apparently due to an
increase in the clearance of progesterone and, thus, a degra-
dation of the uterine environment (Martin et al. 2004). A
recent study from New Zealand has generated a lot of inter-
est in this part of the reproductive process (Bloomfield et al.
2003). When ewes were underfed from 60 days before until
30 days after conception (Fig. 2), there was a marked increase
in premature births, with some lambs being born before Day
130 of pregnancy and half the group delivering at more than
two standard deviations earlier than normal. Remarkably, the
underfeeding was not severe (the ewes only lost 15% of their
body mass) and all ewes had regained normal body mass
at the time of parturition. In the underfed ewes, the lambs
that were born at the normal time had a normal birth weight.
Under extensive management, it seems unlikely that the very
premature births would have been noted, so this phenomenon
may be quite common.
This whole area is obviously fundamental to production
systems because there may be a conflict between strategies
used to increase ovulation rate and strategies that promote
early embryo survival. Moreover, there may be long-term
consequences for the embryos that survive because of the
phenomenon of ‘fetal programming’.
Fetal programming
In addition to the potential impact on periconceptual devel-
opment, nutrition plays a vital role in the development of the
placenta (for a review, see Bell 1984) and other organs in the
fetus between Days 60 and 120 of pregnancy. Undernutrition
can have serious effects on these processes and the conse-
quences may not become evident until much later in life,
by which time the link between cause and effect may have
been lost. This ‘fetal programming’ is currently receiving a
lot of attention in human medical research. In humans, it is
usually linked to susceptibility to disease, but at least three
Reproduction, Fertility and Development 495
aspects of sheep production are affected by nutrition during
pregnancy (review: Martin et al. 2004): (1) the initiation and
development of secondary fibre follicles in the skin, a key
determinant of wool quality in later life; (2) the formation
of muscle fibres, perhaps a major determinant of growth and
carcass quality; and (3) the differentiation and development
of the reproductive system (in this case, we still need studies
that test whether any effects of nutrition during this process
have long-term consequences on reproductive efficiency).
For the effects of nutrition on some of the aspects of the
reproductive process, we have a reasonable idea of the physi-
ological mechanisms involved. However, we do not have solid
hypotheses for periconceptual losses and fetal programming,
particularly with respect to responses to long-term nutritional
deprivation. There is a reasonable possibility that long-term
stress mechanisms are brought into play, particularly the hor-
mones that are involved in responses to metabolic stress and
the control of metabolic homeostasis.
Perinatal mammary function
In sheep, a nutritional supplement during the final week of
pregnancy can double the volume of colostrum that will be
available to the lamb at birth, even in ewes grazing high-
quality pasture (Banchero et al. 2002, 2004). In addition to
supplying food energy and immunity, distension of the gut by
colostrum improves the ability of a lamb to recognise its own
mother and, therefore, contributes to the early establishment
of the ewe–lamb bond (Goursaud and Nowak 1999). Under
extensive management systems, these outcomes are probably
most important for multiple births.
There are two parallels between the effects of nutrition
in the very early and very late stages of pregnancy. First, in
both situations, the supplement appears to act by hastening
the clearance of progesterone (Parr 1992; Parr et al. 1993;
Banchero et al. 2002); in early pregnancy, this may lead to
poor implantation but, at the end of pregnancy, it acceler-
ates the onset of lactogenesis. Second, as in early pregnancy,
there is a potential disadvantage of a nutritional supplement
in the period leading up to parturition. If a supplement that is
designed to promote colostrum production is fed for too long,
it may cause excessive fetal growth and, therefore, dystocia
and an increase in lamb mortality.
Responses to sociosexual signals
We can control the timing of events in the reproductive
process by using the male effect: in sheep and goats, the
sudden introduction of novel males can induce ovulation in
females that are reproductively quiescent because they are
out of season or lactating (for reviews, see Martin et al.
1986; Walkden-Brown et al. 1999; Álvarez and Zarco 2001).
The male effect may also work for advancing the first cycle
in young ewes, although this needs experimental verifica-
tion because the relevant literature is conflicting. Sexual
behaviour accompanies the first ovulation in goats, but is
496 Reproduction, Fertility and Development G. B. Martin et al.

delayed until after the first long cycle in ewes because pro- physiological mechanisms involved so we can manipulate
gesterone priming is needed for the expression of sexual them to improve their value in animal management.
behaviour in that species (for a review, see Martin et al. 1986).
In male sheep and goats, mating behaviour is always instan- Effects of genotype on responses to nutrition
taneously induced by encounters with females, even during and sociosexual stimuli
the non-breeding season.
To reveal the nature of the genotype by environment interac-
In mature females, the induced ovulations are sufficiently
tions that affect the reproductive axis, we have compared the
synchronised in a herd or flock to allow the use of artificial
responses of Merino and Suffolk rams to the female effect
insemination, as well as focused feeding for litter size, fetal
under two levels of nutrition and in different seasons (Fig. 3).
programming and neonatal survival (Martin et al. 2004). In
As expected, Merino rams responded to the female effect
addition to the synchrony of births, the male effect has a
in both seasons, although the response was not significant
second advantage of control over the season of births, so
with the high diet in the breeding season, perhaps because
we can take advantage of seasonal changes in lamb markets.
the pulse frequencies were already very high, making it dif-
Finally, with research and development, it may allow us to
ficult to evoke any further increase. In contrast, Suffolk rams
avoid the use of exogenous hormones in controlled breeding
showed little sign of an increase in LH secretion under any
programmes: this seems to be an almost inevitable trend in
circumstance. Their reproductive axis is very strongly inhib-
modern export markets.
ited by photoperiod in the non-breeding season (Martin et al.
We need to find out why some acyclic females do not
ovulate, how to ensure oestrous behaviour and normal luteal
phases, and how to maintain cyclicity following the ini- (a) Non-breeding season
tial induced ovulation. These questions are discussed by * *
5
Ungerfeld et al. (2004), who have recently combined ultra-
sound with endocrine and behavioural data to greatly improve
LH pulses per 8 h

4
the prospects of successful research in this field.
We would like to focus on three other areas of research: 3
(1) the contribution of social behavioural interactions to the
outcome of the male effect; (2) interactions between genotype 2
and nutrition that affect the GnRH/LH response; and, at a
1
more fundamental level, (3) the neural pathways that link
sociosexual signals with the GnRH secretory system. 0
— ⫹ — ⫹ — ⫹ — ⫹
Social–behavioural interactions Low diet High diet Low diet High diet
In addition to the ‘male effect’, in which sexually active males (b) Breeding season
induce pulses of GnRH/LH and then ovulation in anoestrous 5
females, there is also a ‘female effect’, in which oestrous
*
4
LH pulses per 8 h

females induce pulses of GnRH, LH and testosterone in

males, and also a ‘female–female effect’ in which oestrous
3
females improve the induction of ovulation in anoestrous herd
mates (goats: Walkden-Brown et al. 1993; Restall et al. 1995; 2
Álvarez et al. 1999; ewes: Zarco et al. 1995). These interac-
tions are self-reinforcing and enhance the final reproductive 1
outcome in the flock (Walkden-Brown et al. 1999). A further
level of complexity is added by social interactions. For exam- 0
— ⫹ — ⫹ — ⫹ — ⫹
ple, in red deer (Cervus elaphus), dominant females become
Low diet High diet Low diet High diet
pregnant earlier than subordinates apparently because they
respond more rapidly to the male effect (Clutton-Brock et al. Merino Suffolk
1986). A recent study in goats has shown that the domi- Fig. 3. Effect of introduction of oestrous ewes on the frequency of
nant females establish closer contact with newly introduced pulses of luteinising hormone (LH) in Merino and Suffolk rams fed
bucks and, therefore, ovulate earlier than subordinate females to maintenance (low diet) or with a high energy and protein supple-
(Álvarez et al. 2003). In experiments on the female–female ment (high diet) for 13 days during (a) the non-breeding season and
(b) the breeding season. The frequencies were measured for 8 h (09.00–
effect, Álvarez (2000) has also observed that the subordinate
17.00 h) over consecutive days in the absence and presence of oestrous
does tend to ovulate later than their dominant partners. We ewes. Significant (P < 0.05) ‘female effects’ are indicated (J. S. Fisher,
need to determine how these interactions affect reproductive M. J. Hötzel, S. W. Walkden-Brown and G. B. Martin, unpublished
efficiency and we need an understanding of behavioural and observations).
Environment, nutrition and reproduction
1999, 2002; Hötzel et al. 2003) so, in contrast with the Meri-
nos, they show no response to either sociosexual inputs or
nutritional supplements (Fig. 3). This difference between
the breeds may be an important tool for future research
because, by comparing the neurosensory pathways involved,
we may be able to pinpoint genetic interferences and, thus,
develop ways to overcome the block in the genotypes that are
dominated by photoperiod.
Despite the effect of level of nutrition on the activity of the
reproductive axis in the Merino rams (Fig. 3; for a review, see
Martin and Walkden-Brown 1995), nutritional treatments did
not affect the size of the increase in GnRH/LH secretion that
was induced by the female effect, so it seems likely that inde-
pendent physiological processes mediate responses to these
two factors. Interestingly, this outcome differs from that in
Australian cashmere goats (Walkden-Brown et al. 1994), sug-
gesting variation between the two species, although there are
several major differences in experimental design that may
also explain the difference.
However, in contrast with Merino rams, the ovulatory
response of Merino ewes to the male effect seems to be better
in ewes of good body condition (score 3 on a scale of 5) than
in ewes of poor body condition (score 1.5; Fisher et al. 1993).
Similar sorts of studies need to be performed with the male
effect and the female–female effect in other genotypes.
Neural pathways linking sociosexual signals
to GnRH secretion
In sheep, the critical GnRH cells for sociosexual inputs
seem to be those located in the mediobasal hypothala-
mus (Boukhliq et al. 1999), but we have little idea of
how the olfactory and visual signals from rams reach that
region. Obviously, the same applies to the female effect and
the female–female effect. This will be relatively difficult
research, but not as difficult as unravelling the interactions
with photoperiod, nutrition and genotype (Fig. 1; Blache et al.
2003). Perhaps most intriguing of all are the roles played by
novelty and familiarity and, thus, learning.
Olfactory inputs
In rodents, the pheromones that advance puberty and block
pregnancy stimulate the vomeronasal organ through a set of
specific receptor molecules for which the genes have now
been identified (for a review, see Dulac 2000). This organ
innervates the accessory olfactory bulbs, which, in turn, have
connections to the anterior medial hypothalamus. The main
olfactory bulbs also have connections to the hypothalamus:
they apparently terminate in lateral areas, well away from
the centres that control gonadal function, although the main
olfactory bulb and the lateral hypothalamus can respond to
male odours and apparently have some connection with the
centres that control GnRH release (for a review, see Martin
et al. 1986). Thus, there are two sets of linkages through
which chemical signals could affect the secretion of GnRH.
Reproduction, Fertility and Development 497
Jansen et al. (1998) and Lévy et al. (1999) have traced afferent
and efferent pathways between the olfactory bulbs and the
rest of the brain in female sheep and found that they are
similar to those in rodents. However, sheep seem to differ
fundamentally from rodents because their main tract mediates
the male effect and the female effect does not seem to involve
odours at all (Cohen-Tannoudji et al. 1989; Gonzalez et al.
1991a). For maternal recognition of offspring in sheep, there
is disagreement over which tract is most important (Lévy
et al. 1995; Booth and Katz 2000).
Visual, tactile and auditory inputs
Non-olfactory signals are important in both the male and
female effects in goats and sheep (Shelton 1980; Cohen-
Tannoudji et al. 1986, 1989; Gonzalez et al. 1991a). As
well as stimulus substitution, we must remember that there
are synergistic and additive effects among the various sig-
nals and that efficient reproductive outcomes may depend on
these combinations (Shelton 1980; Pearce and Oldham 1988).
Auditory signals play a role in several aspects of behaviour in
sheep, so they need to be taken into consideration. Tactile sig-
nals may be important because placing a wire fence between
the males and females can reduce the efficacy of the male
effect (Shelton 1980; Pearce and Oldham 1988; Bartlewski
et al. 2002). Visual stimuli have not been linked to GnRH
secretion either, but it is clear that sheep can visually assess,
identify and remember individuals (Kendrick et al. 2001);
can they visually differentiate males from females?
Sex steroid inputs
In the sheep model, we have shown that males can
increase LH pulse frequency in ovariectomised females, but
the response is difficult to detect and greatly improved when
the ovariectomised females are pretreated with oestradiol (for
a review, see Martin et al. 1986). This suggests that, some-
where among the brain pathways, there is a confluence of
these two major inputs into the control of GnRH activity
(Fig. 1). The GnRH cells themselves do not seem to con-
tain receptors for oestradiol in any species, so there must be
at least one set of interneurons involved. For female sheep,
Goubillon et al. (2000) have begun to develop a neuroanatom-
ical framework for steroid inputs, but rams and ewes have
different types of network and this may explain differences
between them in their responses to all environmental inputs,
including sociosexual stimuli. In any case, it seems likely that
the sex steroids amplify the responses in ewes by sensitising
the olfactory pathways to the sociosexual stimulus. There is
evidence for this sort of interaction in mice (Halem et al.
2001) and a recent study with voles has shown that changes
in photoperiod can change the sensitivity of female olfactory
pathways to a male urinary stimulus (Hairston et al. 2003).
This is interesting because there are also strong interactions
between inputs from photoperiod and those from sex steroids,
498 Reproduction, Fertility and Development
nutrition and sociosexual stimuli into the reproductive axis
of sheep (Blache et al. 2003).
The role of learning
The importance of learning is evident from the need for
unfamiliar males to elicit endocrine and ovulatory responses
in the male effect and from the fact that previous experience
with mature rams seems to improve the responses of young
ewes to the male stimulus (Bartlewski et al. 2002; Gelez et al.
2003). Similarly, with the female effect, sexually experienced
rams are more responsive than inexperienced rams (Gonzalez
et al. 1991b). Olfactory learning is also important for recog-
nition of kin, mates and offspring; for example, ewes rely on
learned olfactory signals to distinguish their own offspring
from others, a process mediated by the main olfactory tract
(Lévy et al. 1995, 1999). A similar process may also underpin
the male effect. The ram pheromone is a mix of long-chain
fatty acids, so may be sufficiently complex to carry the signa-
ture of an individual (for a review, see Walkden-Brown et al.
1999).
The olfactory bulb itself is capable of the long-term synap-
tic changes that lead to the learning of important odours. In
addition, memory development may involve the generation of
new neurons. New neurons originate from proliferating cells
in the subventricular zone, then migrate rostrally towards the
main olfactory bulb along a pathway known as the rostral
migratory stream (Rochefort et al. 2002). On arrival, they
differentiate into local interneurons and functionally inte-
grate into circuits (Carlen et al. 2002). Integration is faster
after stimulation by novel odours. In addition to this process,
environmental factors modulate the constitutive turnover of
neurons in many brain regions, including the hypothalamus,
as observed in female voles exposed to males (Fowler et al.
2002) and in hamsters following a change in photoperiod
(Huang et al. 1998).
Discussion of this topic is very speculative because it is
based primarily on rodent literature. It is clear that we now
need similar studies with small ruminants to address the role
of memory and the issue of ‘novelty’, at least for the male
effect.
Conclusions
Animals live in complex environments in which they are
continually confronted with short- and long-term changes
in a wide range of factors, such as photoperiod, nutrition
and sociosexual signals. The complexity of their responses to
these factors is now becoming clearer. With sociosexual sig-
nals, we now need to consider the stimulatory effects of males
on females, of females on males and of females on females.
The impact of nutrition has been extended beyond the con-
trol of puberty and the production of gametes to include,
for example, ‘fetal programming’ with its potentially pro-
found effects on the life-long performance of the animals.
G. B. Martin et al.
To balance the problem of complexity, there has been a coa-
lescence of techniques for working with animals, cells and
molecules, plus the emergence of new perspectives about the
ways that animals and their tissues respond to the wide variety
of inputs that confront them every day. This has brought us to
the brink of a better understanding of the importance of, for
example, the role played by cellular processes within ovarian
follicles in the effect of nutrition on ovulation rate, the neu-
roendocrine pathways through which nutritional inputs affect
the brain centres that control appetite and reproduction, and
the intracerebral pathways through which sociosexual signals
(olfactory and non-olfactory) stimulate the reproductive axis.
A paper this brief cannot be thorough (e.g. we have not
dealt with issues as important as stress), but it can point
out areas of research priority. Indeed, we hope that we have
revealed the threshold of an exciting new era of investigation
into ways that external factors affect the reproductive sys-
tem of farm animals. Inevitably, a paper such as this gives
an impression of complexity. It is no surprise that animals
live in a complex world and it is equally no surprise that
researchers often study only one factor at a time. Compre-
hensive, balanced, multifactorial experiments are technically
difficult to manage, analyse and interpret and it may be that
we should turn to mathematical models as a guide for future
research programmes (Blanc et al. 2001). In the meantime,
we can use much of the information that we already have to
develop management systems to improve the productivity of
our animals.
Acknowledgments
For the discussion that led to many of these ideas, we thank our
colleagues, particularly Lorenzo Álvarez, Rex Scaramuzzi,
John Milton and Carolina Viñoles. Much of the work from
our laboratory was funded through the Australian Research
Council and the National Health and Medical Research
Council of Australia.
References
Allen, D. M., and Lamming, G. E. (1961). Nutrition and reproduction
in the ewe. J. Agric. Sci. 56, 69–79.
Álvarez, R. L. (2000). ‘Efecto de la anosmia y la conducta social sobre la
secreción de LH y ovulación de cabras anéstricas inducidas a ciclar
mediante el efecto hembra.’ MSc Thesis. (Universidad Nacional
Autónomo de México: Mexico.)
Álvarez, R. L., and Zarco, Q. L. (2001). Los fenómonos de biostimu-
latión sexual en ovejas y cabras. Vet. Méx. 32, 117–129.
Álvarez, R. L., Ducoing, W. A. E., Zarco, Q. L., and Trujillo, G. A. M.
(1999). Conducta estral, concentraciones de LH y función lútea en
cabras en anestro estacional inducidas a ciclar mediante el contacto
con cabras en estro. Vet. Méx. 30, 25–31.
Álvarez, L., Martin, G. B., Galindo, F., and Zarco, L. A.
(2003). Social dominance of female goats affects their response
to the male effect. Appl. Anim. Behav. Sci. 84, 119–126.
doi:10.1016/J.APPLANIM.2003.08.003
Banchero, G. E., Quintans, G., Milton, J. T. B., and Lindsay, D. R. (2002).
Supplementation of Corriedale ewes with maize during the last week
Environment, nutrition and reproduction
of pregnancy increases production of colostrum. In ‘Proceedings
of the Australian Society of Animal Production Vol. 24’. p. 273.
(Australian Society of Animal Production: Melbourne, Australia.)
Banchero, G. E., Vazquez, A., Gigena, F., Quintans, G., Lamanna, A.,
Lindsay, D. R., and Milton, J. T. B. (2004). Supplementation of ewes
with maize or barley during the last week of pregnancy doubles
production of colostrum. In ‘Proceedings of the 15th International
Congress on Animal Reproduction, Porto Seguro, Brazil, August
2004’. (Brazilian College of Animal Reproduction: Belo Horizonte,
Brazil.) (In press.)
Bartlewski, P. M., Beard, A. P., Cook, S. J., and Rawlings, N. C. (2002).
Ovarian activity during sexual maturation and following introduc-
tion of the ram to ewe lambs. Small Ruminant Res. 43, 37–44.
doi:10.1016/S0921-4488(01)00253-X
Bell, A. W. (1984). Factors controlling placental and fetal growth and
their effects on future production. In ‘Reproduction in Sheep’. (Eds
D. R. Lindsay and D. T. Pearce.) pp. 144–152. (Australian Academy
of Sciences: Canberra, Australia.)
Blache, D., and Martin, G. B. (1995). Neural and endocrine mechanisms
underlying the synchrony of sexual behaviour and ovulation in the
sheep. In ‘Oxford Reviews of Reproductive Biology. Vol. 17’. (Ed.
H. M. Charlton.) pp. 205–254. (Oxford University Press: New York,
USA.)
Blache, D., Chagas, L., Blackberry, M.A.,Vercoe, P. E., and Martin, G. B.
(2000). Metabolic factors affecting the reproductive axis in male
sheep. J. Reprod. Fertil. 120, 1–11. doi:10.1530/REPROD/120.1.1
Blache, D., Adam, C. L., and Martin, G. B. (2002). The mature male
sheep: a model to study the effects of nutrition on the reproductive
axis. Reprod. Suppl. 59, 219–233.
Blache, D., Zhang, S., and Martin, G. B. (2003). Fertility in males:
modulators of the acute effects of nutrition on the reproductive axis
of male sheep. Reprod. Suppl. 61, 387–402.
Blanc, F., Martin, G. B., and Bocquier, F. (2001). Modelling reproduction
in farm animals: a review. Reprod. Fertil. Dev. 13, 337–353. doi:
10.1071/RD01038
Bloomfield, F. H., Oliver, M. H., Hawkins, P., Campbell, M.,
Phillips, D. J., Gluckman, P. D., Challis, J. R. G., and Harding, J. E.
(2003). A periconceptional nutritional origin for noninfectious
preterm birth. Science 300, 606. doi:10.1126/SCIENCE.1080803
Booth, K. K., and Katz, L. S. (2000). Role of the vomeronasal organ in
neonatal offspring recognition in sheep. Biol. Reprod. 63, 953–958.
Boukhliq, R., Martin, G. B., White, C. L., Blackberry, M. A., and
Murray, P. J. (1997). Role of glucose, fatty acids and protein in the
regulation of testicular growth and the secretion of gonadotrophin,
prolactin, somatotrophin and insulin in the mature ram. Reprod.
Fertil. Dev. 9, 515–524. doi:10.1071/R96113
Boukhliq, R., Goodman, R. L., Berriman, S. J., Adrian, B., and
Lehman, M. N. (1999). A subset of gonadotropin-releasing hormone
neurons in the ovine medial basal hypothalamus is activated during
increased pulsatile luteinizing hormone secretion. Endocrinology
140, 5929–5936. doi:10.1210/EN.140.12.5929
Bronson, F. H. (1985). Mammalian reproduction: an ecological perspec-
tive. Biol. Reprod. 32, 1–26.
Carlen, M., Cassidy, R., Brismar, H., Smith, G. A., Enquist, L. W., and
Frisen, J. (2002). Functional integration of adult-born neurons. Curr.
Biol. 12, 606–608. doi:10.1016/S0960-9822(02)00771-6
Clark, R. T. (1934). Studies of reproduction in sheep. I. The ovulation
rate of the ewe as affected by the plane of nutrition. Anat. Rec. 60,
125–134.
Clutton-Brock, T. H., Albon, S. D., and Guinness, F. E. (1986). Great
expectations: dominance, breeding success and offspring sex ratios
in red deer. Anim. Behav. 34, 460–471.
Cohen-Tannoudji, J., Locatelli, A., and Signoret, J.-P. (1986). Non-
pheromonal stimulation by the male of LH release in the
Reproduction, Fertility and Development 499
anoestrous ewe. Physiol. Behav. 36, 921–924. doi:10.1016/0031-
9384(86)90453-1
Cohen-Tannoudji, J., Lavenet, C., Locatelli, A., Tillet, Y., and
Signoret, J. P. (1989). Non-involvement of the accessory olfac-
tory system in the LH response of anoestrous ewes to male odour.
J. Reprod. Fertil. 86, 135–144. doi:10.1530/JRF.0.0860135
Downing, J. A., Joss, J., and Scaramuzzi, R. J. (1995). Ovulation rate
and the concentrations of gonadotrophins and metabolic hormones
in ewes infused with glucose during the late luteal phase of the
oestrous cycle. J. Endocrinol. 146, 403–410.
Dulac, C. (2000). Sensory coding of pheromone signals in mam-
mals. Curr. Opin. Neurobiol. 10, 511–518. doi:10.1016/S0959-
4388(00)00121-5
Fabre-Nys, C., and Venier, G. (1987). Development and use of a method
for quantifying sexual behaviour in ewes. Appl. Anim. Behav. Sci.
17, 289–304. doi:10.1016/0168-1591(87)90153-5
Fisher, J. S., Martin, G. B., Oldham, C. M., and Gray, S. J. (1993). Long-
term effects of nutrition on spontaneous ovulation in Merino ewes
and their responses to the ‘ram effect’. In ‘Proceedings of the 7th
World Congress on Animal Production, Edmonton, Canada. Vol. 2’.
pp. 32–33.
Fowler, C. D., Liu, Y., Ouimet, C., and Wang, Z. (2002). The effects of
social environment on adult neurogenesis in the female prairie vole.
J. Neurobiol. 51, 115–128. doi:10.1002/NEU.10042
Gelez, H., Lindsay, D. R., Blache, D., Martin, G. B., and Fabre-
Nys, C. (2003). Temperament and sexual experience affect female
sexual behaviour in sheep. Appl. Anim. Behav. Sci. 84, 81–87.
doi:10.1016/S0168-1591(03)00145-X
Gibson, W. R., and Robinson, T. J. (1971). The seasonal nature of
reproductive phenomena in the sheep. I. Variation in sensitivity to
oestrogen. J. Reprod. Fertil. 24, 9–18.
Gonzalez, R., Levy, F., Orgeur, P., Poindron, P., and Signoret, J.-P.
(1991a). Female effect in sheep. 2. Role of volatile substances from
the sexually-receptive female: implication of the sense of smell.
Reprod. Nutr. Dévelop. 31, 103–109.
Gonzalez, R., Orgeur, P., Poindron, P., and Signoret, J.-P. (1991b).
Female effect in sheep. 1. The effects of sexual receptivity of females
and the sexual experience of the rams. Reprod. Nutr. Dévelop. 31,
97–102.
Goubillon, M.-L., Forsdike, R. A., Robinson, J. E., Ciofi, P., Caraty, A.,
and Herbison, A. E. (2000). Identification of neurokinin B-
expressing neurons as an highly estrogen-receptive, sexually dimor-
phic cell group in the ovine arcuate nucleus. Endocrinology 141,
4218–4225. doi:10.1210/EN.141.11.4218
Goursaud, A. P., and Nowak, R. (1999). Colostrum mediates the devel-
opment of mother preference by the new born lamb. Physiol. Behav.
67, 49–56. doi:10.1016/S0031-9384(99)00037-2
Hafez, E. S. E. (1952). Studies on the breeding season and reproduction
of the ewe. J. Agric. Sci. 42, 189–265.
Hairston, J. E., Ball, G. F., and Nelson, R. J. (2003). Photoperiodic
and temporal influences on chemosensory induction of brain fos
expression in female prairie voles. J. Neuroendocrinol. 15, 161–172.
doi:10.1046/J.1365-2826.2003.00963.X
Halem, H. A., Baum, M. J., and Cherry, J. A. (2001). Sex difference and
steroid modulation of pheromone-induced immediate early genes in
the two zones of the mouse accessory olfactory system. J. Neurosci.
21, 2474–2480.
Hötzel, M. J., Walkden-Brown, S. W., Blackberry, M. A., and
Martin, G. B. (1995). The effect of nutrition on testicular growth
in mature Merino rams involves mechanisms that are independent
of changes in GnRH pulse frequency. J. Endocrinol. 147, 75–85.
Hötzel, M. J., Walkden-Brown, S. W., Fisher, J. S., and Martin, G. B.
(2003). Determinants of the annual pattern of reproduction in mature
male Merino and Suffolk sheep: responses to a nutritional stimulus
500 Reproduction, Fertility and Development
in the breeding and non-breeding seasons. Reprod. Fertil. Dev. 15,
1–9. doi:10.1071/RD02024
Huang, L., DeVries, G. J., and Bittman, E. L. (1998). Photoperiod
regulates neuronal bromodeoxyuridine labeling in the brain of a sea-
sonally breeding mammal. J. Neurobiol. 36, 410–420. doi:10.1002/
(SICI)1097-4695(19980905)36:3<410::AID-NEU8>3.0.CO;2-Z
Iglesias, R. M. R., Ciccioli, N. H., Irazoqui, H., and Giglioli, C. (1996).
Ovulation rate in ewes after a single oral glucogenic dosage during
a ram-induced follicular phase. Anim. Reprod. Sci. 44, 211–221.
doi:10.1016/0378-4320(96)01564-3
Jansen, H. T., Iwamoto, G. A., and Jackson, G. L. (1998). Central con-
nections of the ovine olfactory bulb formation identified using wheat
germ agglutinin-conjugated horseradish peroxidase. Brain Res. Bull.
45, 27–39. doi:10.1016/S0361-9230(97)00279-7
Kendrick, K. M., Da Costa, A. P., Leigh, A. E., Hinton, M. R., and
Peirce, J. W. (2001). Sheep don’t forget a face. Nature 414, 165–166.
doi:10.1038/35102669
Lamond, D. R., Gaddy, R. G., and Kennedy, S. W. (1972). Influence of
season and nutrition on luteal plasma progesterone in Rambouillet
ewes. J. Anim. Sci. 34, 626–629.
Lévy, F., Locatelli, A., Piketty, V., Tillet, Y., and Poindron, P. (1995).
Involvement of the main but not the accessory olfactory system in
maternal behavior of primiparous and multiparous ewes. Physiol.
Behav. 57, 97–104. doi:10.1016/0031-9384(94)00200-O
Lévy, F., Meurisse, M., Ferreira, G., Thibault, J., and Tillet, Y.
(1999). Afferents to the rostral olfactory bulb in sheep with spe-
cial emphasis on the cholinergic, noradrenergic and serotonergic
connections. J. Chem. Neuroanat. 16, 245–263. doi:10.1016/S0891-
0618(99)00005-8
Martin, G. B. (1984). Factors affecting the secretion of luteinizing
hormone in the ewe. Biol. Rev. 59, 1–87. doi:10.1086/413673
Martin, G. B. (1995). Reproductive research on farm animals
for Australia: some long-distance goals. Reprod. Fertil. Dev. 7,
967–982.
Martin, G. B., and Walkden-Brown, S. W. (1995). Nutritional influences
on reproduction in mature male sheep and goats. J. Reprod. Fertil.
Suppl. 49, 437–449.
Martin, G. B., Oldham, C. M., Cognié, Y., and Pearce, D. T. (1986). The
physiological responses of anovulatory ewes to the introduction of
rams: a review. Livestock Prod. Sci. 15, 219–247. doi:10.1016/0301-
6226(86)90031-X
Martin, G. B., Walkden-Brown, S. W., Boukhliq, R., Tjondronegoro,
S., Miller, D. W., Fisher, J. S., Hötzel, M.-J., Restall, B. J., and
Adams, N. R. (1994). Non-photoperiodic inputs into seasonal breed-
ing in male ruminants. In ‘Perspectives in Comparative Endocrinol-
ogy’. (Eds K. G. Davey, R. E. Peter and S. S. Tobe.) pp. 574–585.
(National Research Council of Canada: Ottawa.)
Martin, G. B., Tjondronegoro, S., Boukhliq, R., Blackberry, M. A.,
Briegel, J. R., Blache, D., Fisher, J. A., and Adams, N. R. (1999).
Determinants of the annual pattern of reproduction in mature male
Merino and Suffolk sheep: modification of endogenous rhythms by
photoperiod. Reprod. Fertil. Dev. 11, 355–366.
Martin, G. B., Hötzel, M. J., Blache, D., Walkden-Brown, S. W.,
Blackberry, M. A., Boukhliq, R., Fisher, J. S., and Miller, D. W.
(2002). Determinants of the annual pattern of reproduction in mature
male Merino and Suffolk sheep: modification of responses to pho-
toperiod by an annual cycle in food supply. Reprod. Fertil. Dev. 14,
165–175. doi:10.1071/RD02010
Martin, G. B., Milton, J. T. B., Davidson, R. H., Banchero, G. E.,
Hunzicker, G. E., Lindsay, D. R., and Blache, D. (2004). Natural
methods of increasing reproductive efficiency in sheep and goats. In
‘Proceedings of the 15th International Congress on Animal Repro-
duction, Porto Seguro, Brazil, August 2004’. (Brazilian College of
Animal Reproduction: Belo Horizonte, Brazil.) (In press.)
G. B. Martin et al.
Muñoz-Gutiérrez, M., Blache, D., Martin, G. B., and Scaramuzzi, R. J.
(2002). Folliculogenesis and the ovarian expression of mRNA for
aromatase in anoestrous sheep after 5 days of glucose or glu-
cosamine infusion or supplementary lupin feeding. Reproduction
124, 721–731.
Okolski, A. (1975). Effect of different amounts of protein in the diet
on sexual behaviour and properties of semen in rams. Acta agrar.
silvest. Ser. zootech. 15, 101–121.
Parker, G. V., and Thwaites, C. J. (1972). The effects of undernutrition
on libido and semen quality in adult Merino rams. Aust. J. Agric.
Res. 23, 109–115.
Parr, R. A. (1992). Nutrition–progesterone interactions during early
pregnancy in sheep. Reprod. Fertil. Dev. 4, 297–300.
Parr, R. A., Davis, I. F., Miles, M. A., and Squires, T. J. (1993). Liver
blood flow and metabolic clearance rate of progesterone in sheep.
Res. Vet. Sci. 55, 311–316.
Pearce, G. P., and Oldham, C. M. (1988). Importance of non-olfactory
ram stimuli in mediating ram-induced ovulation in the ewe.
J. Reprod. Fertil. 84, 333–339. doi:10.1530/JRF.0.0840333
Restall, B. J., Restall, H., and Walkden-Brown, S. W. (1995). The
induction of ovulation in anovulatory goats by oestrous females.
Anim. Reprod. Sci. 40, 299–303. doi:10.1016/0378-4320(95)
01433-0
Rhind, S. M., Leslie, I. D., Gunn, R. G., and Doney, J. M. (1985). Plasma
FSH, LH, prolactin and progesterone profiles of Cheviot ewes with
different levels of intake before and after mating, and associated
effects on reproductive performance. Anim. Reprod. Sci. 8, 301–313.
doi:10.1016/0378-4320(85)90046-6
Rhind, S. R., Martin, G. B., McMillen, S., Tsonis, C. G., and McNeilly,
A. S. (1989). Effect of level of food intake of ewes on the secre-
tion of luteinizing hormone (LH) and follicle-stimulating hormone
(FSH) and on the pituitary response to gonadotrophin-releasing
hormone (GnRH) in ovariectomized ewes. J. Endocrinol. 121,
325–330.
Rochefort, C., Gheusi, G., Vincent, J. D., and Lledo, P. M. (2002).
Enriched odor exposure increases the number of newborn neurons
in the adult olfactory bulb and improves odor memory. J. Neurosci.
22, 2679–2689.
Sharma, T. P., Blache, D., Blackberry, M. A., and Martin, G. B. (1999).
Role of peripheral and central aromatization in the control of
gonadotrophin secretion in the male sheep. Reprod. Fertil. Dev. 11,
293–302. doi:10.1071/RD99084
Shelton, M. (1980). Goats: influence of various exteroceptive factors on
initiation of estrus and ovulation. Int. Goat Sheep Res. 1, 156–162.
Stewart, R., and Oldham, C. M. (1986). Feeding lupins for 4 days dur-
ing the luteal phase can increase ovulation rate. In ‘Proceedings of
the Australian Society of Animal Production Vol. 16’. pp. 367–370.
(Australian Society of Animal Production: Melbourne, Australia.)
Tricoire, H., Møller, M., Chemineau, P., and Malpaux, B. (2003). Ori-
gin of cerebrospinal fluid melatonin and possible function in the
integration of photoperiod. Reprod. Suppl. 61, 311–321.
Ungerfeld, R., Forsberg, M., and Rubianes, E. (2004). Overview of the
response of anoestrous ewes to the ram effect. Reprod. Fertil. Dev.
16, 479–490.
Viñoles, C., Forsberg, M., Banchero, G., and Rubianes, E. (2002). Ovar-
ian follicular dynamics and endocrine profiles in Polwarth ewes with
high and low body condition. Anim. Sci. 74, 539–545.
Walkden-Brown, S. W., Restall, B. J., and Henniawati, H. (1993). The
male effect in the Australian cashmere goat. 3. Enhancement with
buck nutrition and use of oestrous females. Anim. Reprod. Sci. 32,
69–84. doi:10.1016/0378-4320(93)90058-Y
Walkden-Brown, S. W., Restall, B. J., Norton, B. W., and
Scaramuzzi, R. J. (1994). The ‘female effect’ in Australian cashmere
goats. Effect of season and diet quality on the LH and testosterone
Environment, nutrition and reproduction
response of bucks to oestrous does. J. Reprod. Fertil. 100, 521–531.
doi:10.1530/JRF.0.1000521
Walkden-Brown, S. W., Martin, G. B., and Restall, B. J. (1999). Role
of male–female interaction in regulating reproduction in sheep and
goats. J. Reprod. Fertil. Suppl. 52, 243–257.
Williams, S. A., Blache, D., Martin, G. B., Foot, R., Blackberry, M. A.,
and Scaramuzzi, R. J. (2001). Effect of nutritional supplementation
on quantities of glucose transporters 1 and 4 in sheep granulosa and
theca cells. Reproduction 122, 947–956.
Wright, P. J., Geytenbeek, P. E., and Clarke, I. J. (1990). The influence of
nutrient status of post-partum ewes on ovarian cyclicity and on the
http://www.publish.csiro.au/journals/rfd
Reproduction, Fertility and Development 501
oestrous and ovulatory responses to ram introduction. Anim. Reprod.
Sci. 23, 293–303. doi:10.1016/0378-4320(90)90043-F
Zarco, Q. L., Rodríguez, E. F., Angulo, M. R. B., and Valencia, M. J.
(1995). Female to female stimulation of ovarian activity in the
ewe. Anim. Reprod. Sci. 39, 251–258. doi:10.1016/0378-4320(95)
01384-C
Manuscript accepted 23 March 2004.