Reprod Dom Anim 43 (Suppl. 2), 40–47 (2008); doi: 10.1111/j.1439-0531.2008.01141.
x
ISSN 0936-6768
Seasonality of Reproduction in Mammals: Intimate Regulatory Mechanisms and
Practical Implications
P Chemineau, D Guillaume, M Migaud, JC Thiéry, MT Pellicer-Rubio and B Malpaux
UMR Physiologie de la Reproduction et des Comportements, INRA, CNRS, Universite´ F. Rabelais, Haras Nationaux, Nouzilly, France
Contents
Farm mammals generally express seasonal variations in their
production traits, thus inducing changing availability of fresh
derived animal products (meat, milk and cheese) or perfor-
mances (horses). This is due to a more or less marked seasonal
birth distribution in sheep and goats, in horses but not cattle.
Birth peak occurs at the end of winter-early spring, the most
favourable period for the progeny to survive. Most species
show seasonal variations in their ovulation frequency (pres-
ence or absence of ovulation), spermatogenic activity (from
moderate decrease to complete absence of sperm production),
gamete quality (variations in fertilization rates and embryo
survival), and also sexual behaviour. The intimate mechanism
involved is a complex combination of endogenous circannual
rhythm driven and synchronized by light and melatonin.
Profound and long-term neuroendocrine changes involving
different neuromediator systems were described to play a role
in these processes. In most species artificial photoperiodic
treatments consisting of extra-light during natural short days
(in sheep and goats and mares) or melatonin during long days
(in sheep and goats) are extensively used to either adjust the
breeding season to animal producer needs and ⁄ or to com-
pletely overcome seasonal variations of sperm production in
artificial insemination centres. Pure light treatments (without
melatonin), especially when applied in open barns, could be
considered as non-invasive ones which fully respect animal
welfare. Genetic selection could be one of the future ways to
decrease seasonality in sheep and goats.
Products of Animal Origin are Seasonally
Marketed
Availability of animal products for human consumption
was probably seasonal for a long time before domesti-
cation. Although domestication processes generally
reduced seasonality of reproduction compared to what
is observed in their wild counterparts, a majority of
animal-derived products remain accessible only season-
ally. Cycles of reproduction and production are them-
selves seasonal because domestic stock have inherited
the characteristics of the natural populations from
which they originate (see below and Ortavant et al.
1985; Bronson 1989).
Under temperate climates, the quantity of lambs and
kids and the collection of sheep and goat milk greatly
vary throughout the year, which induces high variations
in the price paid to producers and ⁄ or in the ability of
these different products to be processed by the food
industry. For example, in France, goat milk production
is highly seasonal, ranging from over 30 millions litres in
May to approximately 10 millions in November
(Fig. 1). This induces large variations in prices paid to
the producer (53%). Similarly, monthly mean produc-
tion of lambs is low in October and high in April,
 2008 The Authors. Journal compilation  2008 Blackwell Verlag
causing significant changes to the market price of lamb
meat.
In the equine species, the odds ratio for a mare to be
pregnant at the end of the year, relative to the month of
first mating, is approximately 1.4 from January to April,
while it falls to approximately 0.5 after June. Very early
mating (January–February), however, did not totally
valorize this advantage because many mares were not
spontaneously in oestrus at this time (see below).
Autumn mating was rare and lead to poor reproductive
performances (Langlois and Blouin 2004). In the same
species, in all the race and sport competitions, birth
month of the foal has a highly significant effect on its
future sport performances estimated by financial gains
in adult horse. Annual earnings are higher for horses
born in January-February, than for those born from
April to June (Langlois and Blouin 1997, 1998).
Seasonality of animal product availability is the result
of several intricate factors based on the underlying
physiological mechanisms of the adaptation of farm
animals to local environmental conditions. This is due to
a more or less marked seasonal birth peak in sheep and
goats, horses but not cattle, at the end of winter-early
spring, the most favourable period for the progeny to
survive (Fig. 2). We will focus here on the basic
mechanisms involved in the seasonal variations of
reproductive activity, because it is one of the main
remaining constraints within some domestic animal
populations.
Gonadal Activity, Sexual Behaviour and
Littering Vary Seasonally
The frequency of ovulations and oestrous behaviour in
unmated Alpine and Saanen dairy goats, even when
maintained in excellent body condition, present a long
period of sexual rest, the anoestrous season, as it varies
dramatically from 0 (March–September) to 100%
(October to January, Fig. 3; Chemineau et al. 1992).
Ile-de-France ewes show similar variations but isolated
ovulations without associated behaviour are observed in
some females during the anoestrous season (Thimonier
and Mauléon 1969). A majority of mares stop ovulating
from December to May (Palmer and Driancourt 1983).
In pony mares, duration of winter anovulatory season is
increased by undernutrition (Salazar-Ortiz 2006).
Dairy or beef cows, in contrast to sheep and goats,
when not mated, do not stop ovulatory activity. This
indicates that they are potentially able to breed all the
year round. However, the presence of a calf (if calving in
winter), undernutrition and photoperiodic rhythm, syn-
ergistically combine to induce a seasonal pattern of the
Seasonality of Reproduction in Mammals 41

40 0.61 100
Harvest (106 liters) Ovulations

% females showing at least one ovulation/

Price (Euros/liter) Oestrus

80

30 0.53

oestrus per month

60

20 0.46 40

20
Price
10 0.38
Harvest 0
0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32
Oct. Feb. Oct. Feb. Oct. Feb.
0 0.30
Months J F M A M J J A S O N D Months

Fig. 1. Seasonal variations in the harvest and farm price of goat milk Fig. 3. Seasonal variations of the occurrence of ovulations and
in France (year 1992; adapted from Chemineau et al. 1996) oestrous behaviour in Alpine goats (adapted from Chemineau et al.
1992)

post-partum ovulatory activity in beef cattle character-
ized by a limited period of time for ovulations (Ingrand
et al. 2003; Agabriel et al. 2004).
In rams and he-goats, although spermatogenic activ-
ity and sexual behaviour do not stop, they deeply vary
with season. In Soay rams, a primitive breed from North
Scotland, testicular size (which reflects spermatogenic
activity), plasma FSH and testosterone concentrations
as well as sexual ‘flush’ and aggressive behaviour reach
their maximum between August and November, the
‘rut’ season in this breed (Lincoln 1979). Ile-de-France
rams show testicular weight and sperm production per
testis (directly measured at its output) varying from less
than 200 g and 1 billion per day in March, to more than
300 g and 5 billion per day in September, respectively
(Ortavant et al. 1985). Alpine bucks also display dra-
matic variations in sexual behaviour (0–1.5 matings in
10 min), sperm individual motility (2.5–3.5 over 5) and
fertilizing ability (20%–70% of kiddings after AI)
between the spring-summer and autumn-winter periods
(Delgadillo et al. 1992). In this last breed, changes in
ejaculate volume and sperm concentration occur sea-
sonally, which, in this species showing a deleterious
effect of seminal plasma on in vitro sperm survival, has
important implications on semen technology. Finally,
stallions also show seasonal variations in sexual behav-
iour and sperm quality, the lowest season being in
winter and the highest in spring-summer (Magistrini
et al. 1987).
Within a given species, the various breeds may express
variable degrees of seasonality. For example, Soay and
Texel ewes are highly seasonal, while Merino and
Manchega ewes present more discrete expression of
seasonality (Hafez 1952; Santiago-Moreno et al. 2000).
Breeds raised in the Subtropics and in the Tropics
generally present a low seasonality or cycle all the year
round with no anovulatory period (Gonzalez-Stagnaro
1983; Khaldi 1984; Yenikoye 1984; Chemineau 1986;
Mahieu et al. 1989; Arroyo et al. 2007). This is an
interesting trait of these breeds for local farmers who
can then organize the breeding season of their flock all
the year round, without expensive hormonal treatments.
Unfortunately, a marked seasonality is expressed in
these breeds when subjected to the large photoperiodic
variations and temperate climates of northern countries
(Chemineau et al. 2004), preventing the possible use of
these breeds in flocks under temperate latitude. How-
ever, in temperate breeds maintained under environ-
mental conditions similar from which they originate,
intra-breed variability also exists. Some reproductive

Spring Summer Autumn Winter

Horse
Feral horse
Feral cattle
Goat Breeding season

Texel sheep
Soay sheep
Mouflon Birth season

Californian mountain sheep

Alaska mountain sheep
Fig. 2. Timing of the annual
reproductive cycle of some sea- Wild pig
sonal breeders. Breeding season is Mink
indicated as a grey box and deliv-
ering season as a black box J F M A M J J A S O N D J F M A M J J A S O N D
(adapted from Ortavant et al.
1985) Months

 2008 The Authors. Journal compilation  2008 Blackwell Verlag

42 P Chemineau, D Guillaume, M Migaud, JC Thiéry, MT Pellicer-Rubio and B Malpaux
traits including the onset, offset and duration of the
breeding season were found heritable, therefore becom-
ing candidates for genetic selection (Ricordeau 1982;
Quirke et al. 1986; Hanrahan 1987; Smith et al. 1992;
Al-Shorepy and Notter 1997). Indirect traits such as the
presence or absence of ovulatory activity in spring, a
trait found heritable in Merino ewes (Hanocq et al.
1999) could be used for genetic selection.
Neuroendocrine Mechanisms and Combination
of Endogenous Circannual Rhythms with the
Entraining Effects of Photoperiodic Variations
are Responsible for Seasonality
Numerous experiments were done, mainly in sheep to
identify which are the neuroendocrine mechanisms
involved in seasonality of reproduction. A spontaneous
seasonal change in the negative feedback (FB) potency
of gonadal steroids (strong FB in anoestrous season)
was identified as one of the first key-elements of the
system (Pelletier and Ortavant 1975). Ovariectomized-
oestradiol implanted ewes show parallel changes in
plasma LH pulsatility and mean concentration with the
frequency of ovulations of ovary-intact ewes (high LH
pulsatility and mean concentration during the ovulatory
season vs low LH pulsatility and mean concentration
during the anoestrus season; Fig. 4; Legan and Karsch
1980; Karsch et al. 1984). These changes originated
quasi exclusively from changes in LHRH pulsatility at
the brain level (Barrell et al. 2000), which makes the
frequency of LHRH release in the portal system as the
essential message sent by the brain to seasonally control
the whole pituitary–gonadal axis. Seasonal changes in
the steroid transport from the periphery to the brain via
changes in the blood-brain barrier potency could be
responsible for a part of the mechanism (Thiery and
Malpaux 2003; Thiery et al. 2006), but the main part of
the phenomenon probably takes place in various specific
hypothalamic areas bearing identified or putative oes-
tradiol receptors. The Dopaminergic (DA) A15 nucleus
of the retrochiasmatic hypothalamus is probably a
LH plasma concentration in Ovx ewes (n = 6)
LH plasma concentration in Ovx + E2
ewes (n = 6)
UNDETECTABLE
100
% Ewes cycling
50
% entire ewes cycling
(n = 14)
0
Estradiol plasma concentration in Ovx + E2 ewes (n = 6)
Jan Feb Mar Apr May Jun
key-nucleus (Thiery et al. 1989, 1995), intermediate
between oestradiol binding cells and LHRH neurons
of the pre-optic area. Interestingly, these cells are
located in dual sites, the retrochiasmatic hypothalamus
itself (Gallegos-Sánchez et al. 1997) and the ventral pre-
optic area (Anderson et al. 2001).
In ewes, thyroid hormone T4 needs to be present at a
constantly low plasma level (Billings et al. 2002) and
probably acts in the pre-mammillary area of the
posterior hypothalamus for its effect. Seasonal plastic-
ity, identified by changes in PSA-NCAM, has been
demonstrated in the LHRH neurones (Lehman et al.
2002). Concurrent seasonal changes identified by syn-
apsin expression have been shown in the A15 nucleus,
this latter plasticity depending upon thyroid hormone
(Adams et al. 2006). Similarly, changes in the expression
and binding capacity of serotonergic receptor 5HT2A
were observed in association with pulsatile LHRH
activity (Le Corre et al. 1994; Chemineau et al. 2003).
Within a given specific species or breed, the breeding
season appears very stable from one year to another,
with stable dates of onset and offset of female ovulatory
activity and a period of maximum quantitative and
qualitative sperm production. This precise timing is due
to complex mechanisms which allow animals to ‘locate’
their breeding season over the year and express their
sexual activity at the right time, synchronously between
sexes and with external environmental factors. In these
seasonal mammals, similarly to the circadian ‘clock’ (i.e.
with a free-running period close to 24 h which generates
endogenous circadian rhythms), a circannual ‘rhythm’,
endogenous to animals, is likely to generate alternate
periods of sexual activity with periods of sexual rest
throughout the year. These alternate periods can be
experimentally observed when animals are kept under
artificial constant photoperiodic regimens (constant
short days, for example), over at least two consecutive
years (Jansen and Jackson 1993; Malpaux et al. 2001;
Malpaux 2006). Hamsters and sheep are the two
experimental models that have contributed to a better
understanding of the endogenous rhythms governing
LH
Fig. 4. Seasonal variations in E2
negative feedback potency on
plasma LH concentration in
E2 ovariectomized ewes bearing
(Ovx+E2) or not (Ovx) an estra-
diol implant and compared to the
percentage of ovary-intact entire
ewes of the same breed (adapted
Jul Aug Sep Oct from Karsch et al. 1984)
 2008 The Authors. Journal compilation  2008 Blackwell Verlag
Seasonality of Reproduction in Mammals
reproduction (Larkin et al. 2002; Lehman et al. 2002;
Paul et al. 2008) or pelage moult (Paul et al. 2008). This
endogenous rhythm is timed, in ewes, by discrete signals
given by external changes in photoperiod (Barrell et al.
2000). However, the specific physiological mechanisms
underlying this circannual system remain largely un-
known.
The specific role of short days (SD) and long days
(LD) days in timing reproductive activity varies among
species. In long-day breeders (i.e. animals which are
fully sexually active during LD) like horses, LD are
stimulatory and SD inhibitory of sexual activity. In
contrast, LD inhibit while SD stimulate sexual activity
in short-day breeders such as sheep and goats. However
in mammals subjected to a constant photoperiod, the
daylength-specific effect is not permanent. Animals
‘escape’ and become ’refractory’ to the prevailing pho-
toperiod: LD are no longer stimulatory in mares or
inhibitory in sheep and goats, SD are no longer
inhibitory in mares or stimulatory in sheep and goats.
This refractoriness could conceptually be considered as
merely the first step of the expression of the circannual
endogenous rhythm. It can be ‘broken’ by transferring
animals into the opposite photoperiod: refractoriness to
SD, which occurs naturally in sheep in late winter, is
broken by 2 months of exposure to LD in December–
January, allowing the efficiency of stimulatory SD to be
restored. Thus, by subjecting animals to opposite
photoperiods, it is possible to control seasonality of
reproduction. This property is now commonly used in
photoperiodic treatments applied on farms and ⁄ or in
AI centres (see below). The definition of what is really
LD and SD is not straightforward: it is possible to
define a threshold of photosensitivity based on the
number of light hours per day, under which LD are
stimulatory and below which SD are inhibitory (see
reviews Chemineau et al. 1996 and Malpaux et al.
1996). The ‘photoperiodic history’ of each individual
should also be taken into account. Thus, it is now
commonly accepted that LD are days longer than the
preceding ones, and that SD are days shorter than the
preceding ones. This property is interesting under field
conditions: following a period of artificial long days,
animals perceive SD even though natural daylength is
longer than 12 h of light per day. Another interesting
property can be used under farm conditions to apply
long days: the illumination of a specific phase of the
night, the so-called ‘photosensitive phase’, generally
situated 14–16 h after dawn in sheep and 9.5 h after
dusk in mares, allows animals to perceive LD even
though real LD are not applied (see reviews of Malpaux
et al. 1996; Chemineau et al. 1996 in sheep and goats,
and Guillaume 1996 in mares).
More generally, photoperiod, which entrains the
endogenous circannual rhythms of reproduction, exerts
its action through two different but complementary and
dependent pathways by (1) adjusting the phases of
gonadal development with external natural conditions
and (2) by synchronizing the reproductive period
between individuals of the same species. In mammals,
all the photoperiodic input is perceived exclusively
through the eyes then transmitted via a multi-synaptic
pathway to the pineal gland, which transduces the
 2008 The Authors. Journal compilation  2008 Blackwell Verlag
43
photic signal into a chemical one by synthesizing and
secreting melatonin. Synthesized during the night by the
pineal gland, it is thought that melatonin is delivered to
the brain via the cerebrospinal fluid, and to peripheral
tissues by general circulation. To control reproductive
activity in sheep, melatonin acts on the pre-mammillary
hypothalamus where specific receptors transcripts are
expressed (Migaud et al. 2005) and the membrane
receptor is present, which stimulates, approximately
45 days after the onset of daily impregnation (Viguié
et al. 1995), the pulsatile activity of LHRH-LH which in
turn will drive gonadal and behavioural sexual activities
(review by Malpaux 2006; Malpaux et al. 2001). Exter-
nal melatonin can be given to ‘mimic’ short days and has
been of practical use in sheep and goats to stimulate
reproduction in spring. Details of the neuroendocrine
mechanisms responsible for the seasonal and light
control of LHRH pulsatility could not be discussed
extensively here (see Malpaux 2006 for an extensive
review), especially what differs between short-day breed-
ers (sheep and goats) and long-day breeders (horses and
hamsters) to explain their opposite change in LHRH
neuron pulsatility to the same melatonin signal. How-
ever, it is likely that the difference lies in the neural
network connecting hypothalamic melatonin receptor
bearing cells and LHRH neurones, a network that is
also responsible for the long delay of action of melato-
nin on LHRH pulsatility (Viguié et al. 1995). For
example, dopaminergic activity inhibits the LHRH
pulsatility at the end of the neural network during long
days in sheep (Thiery et al. 1989). Interestingly, dopa-
mine from the median eminence is also correlated with
the inhibition of gonadotropin release, which takes place
under short days in these species (Steger et al. 1985;
Glass et al. 1988).
Although molecular mechanisms underlying the cen-
tral control of gonadotrope system by melatonin still
constitute a ‘black box’, numerous experiments using
only photoperiodic variations have lead to proposals to
farmers and artificial insemination centres of specific
light devices, which may be able to control seasonality
of reproduction of their animals.
Using Artificial Photoperiodic Treatments to
Control Seasonality of Reproduction in Farm
Animals
Photoperiodic treatments have been of practical interest
for controlling seasonal reproduction essentially in
sheep, goats and horses. Sheep and goat AI centres,
equipped with dark housing, use alternate light regimes
with 1 month LD and 1 month SD which allow
permanent high semen production in rams and bucks,
with no seasonal variations in sperm quality. Currently,
in the French national genetic improvement scheme, all
bucks (approximately 70 per year) are permanently
treated with rapid alternation LD–SD, which increases
the AI dose production (+40%) per buck and per year
(Delgadillo et al. 1993) and reduces duration of the
breeding period of males (slaughtered after 18 months
of production, or approximately 18 months earlier that
those maintained under natural photoperiod). In other
AI centers which do not require all the year-round
44 P Chemineau, D Guillaume, M Migaud, JC Thiéry, MT Pellicer-Rubio and B Malpaux

production of semen doses, rams raised in open barns
are subjected to 2–3 months extra ‘LD’ (from December
to February) followed either by return to natural
photoperiod, or by subcutaneous treatment with mela-
tonin implants which mimics SD (‘SD’) (Fig. 5). This
succession ‘LD’–‘SD’ stimulates semen output in quan-
tity and quality in spring, thus mimicking the normal
sexual season which itself normally lasts 2–3 months
(Malpaux et al. 1995).
In goat farms, (always in open barns), males and
females are subjected to the second type of treatment
performed in AI centres (succession ‘LD’–‘SD’). This
treatment should be associated with a ‘buck effect’
(introduction of treated bucks for 45 days, after 35–75
‘SD’) in order to induce ovulations and oestrous
behaviour and to get high fertility rate. Under such
conditions, out-of-season fertility and prolificacy can be
kept at high levels (>75% kidding rate with approxi-
mately two kids per kidding) (Chemineau et al. 1996).
This type of treatment could be satisfactorily associated
with AI on fixed-time basis with fertility results equiv-
alent to ‘classical’ hormonal treatment with FGA
sponge and eCG (Pellicer-Rubio et al. 2007, 2008).
For local breeds in subtropical conditions where sea-
sonality is less marked than those raised under temper-
ate latitudes, the treatment of females is not necessary.
When the LD treatment is applied only in bucks used
for the ‘buck-effect’, the percentages of ovulating
females and their fertility after natural mating are high
(Delgadillo et al. 2002, 2004).
In ewes, a majority of out-of-season lambings are still
obtained using ‘classical’ hormonal treatments (FGA
sponges + eCG), but the frequency of utilization of
melatonin implants to get out-of-season breeding is
increasing, especially in Mediterranean countries. The
use of implants also increases fecundity: + 0.20
lamb ⁄ ewe treated ⁄ year has been almost always ob-
served, mainly due to increased proportions of twins
rather than triplets (Chemineau et al. 1996).
Photoperiodic treatments are also applied in mares to
advance the annual breeding season and to provide foals
with a decisive age-related advance when competing
with their contemporaries born the same year (see
above). This is generally performed by exposing mares
to LD or pseudo LD during autumn and winter. Such
treatments allow mares to be fertilized approximately
2–3 months earlier than females kept under a natural
photoperiod (Guillaume 1996).
Thus, photoperiodic treatments are now used in both
sexes of nearly all farm species to control seasonal
reproduction. Whatever the species, they use common
properties of alternations between inhibitory and stim-
ulatory photoperiods, where durations are adapted to
the species and sex. When using pure light treatments
(without melatonin), especially when applied in open
barns, they could be considered as non-invasive which
fully respects animal welfare considerations. It is very
probable that these photoperiodic treatments will be
used more extensively in the future as livestock produc-
tion systems strive to be more sustainable.

(a) Light-proof buildings:

17
h 16

Dusk Progressive 8L
16L
decrease
Dawn

0 60 150 days
January March June

(b) 17
h 16

Dusk
Short days
Dawn

0 60 150 days
January March June

(c) 17
h 16

Dusk
Melatonin
Dawn

0 60 150 days
January March June
"Long days" "Short days"

(d) Open barns:

24
2nd period of suppl. light
Natural dusk
20

16
hours

Natural light
12 or
Melatonin
8 1st period of suppl. light
Natural dawn
4
Fig. 5. Photoperiodic treatments
0
to control sexual activity in small
January February March April May June ruminants raised in closed (a–c) or
open (d) barns (adapted from
"Long days" "Short days" Chemineau et al. 1996)

 2008 The Authors. Journal compilation  2008 Blackwell Verlag

Seasonality of Reproduction in Mammals
Conclusion
The seasonality of animal products release is more the
consequence of interactions between the natural
endogenous rhythmicity of animals and environmental
constraints than a deliberate choice of the farmer to
produce at a definite season. In most seasonal species
and breeds involved in these productions, specific
photoperiodic treatments derived, at least in part,
from the cumulative knowledge of physiological mech-
anisms involved in the control of the reproductive
function, have progressively been proposed to over-
come the problem raised by the seasonal availability of
reproduction-derived products. In mammals, such
treatments should be taken as an interesting alternative
to classical hormonal treatments in a general context
of reduction of hormonal utilization in more sustain-
able animal production systems. The existence of
strong genetic bases for seasonality of reproductive
activity in the main farm animal species should be
further explored to propose selection criteria and ⁄ or
gene markers accessible to primary breeder and pro-
ducer organizations willing to reduce seasonality in
their flocks.
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Author’s address (for correspondence): P Chemineau, UMR Physiol-
ogie de la Reproduction et des Comportements, INRA, CNRS,
Université F. Rabelais, Haras Nationaux, 37380 Nouzilly, France.
E-mail: philippe.chemineau@tours.inra.fr
 2008 The Authors. Journal compilation  2008 Blackwell Verlag
47
Conflict of interest: P Chemineau has received a research grant from
CEVA Animal Health and has no potential conflicts to declare.
J-C Thiéry has received a research grant from ‘‘Institut de Recherche
Servier’’ and has no potential conflicts to declare.
D Guillaume has no potential conflicts to declare.
M Migaud has received a research grant from ‘‘Institut de Recherche
Servier’’ and has no potential conflicts to declare.
M-T Pellicer-Rubio has no potential conflicts-to declare.
B Malpaux has received a research grant from ‘‘Institut de Recherche
Servier’’, from ‘‘CEVA Animal Health’’ and has no potential conflicts
to declare.