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Received: 9 January 2017    Accepted: 28 March 2017

DOI: 10.1111/rda.12988

ORIGINAL ARTICLE

Extended day length in late winter/early spring, with a return

to natural day length of shorter duration, increased plasma
testosterone and sexual performance in rams with or without
melatonin implants

JA Abecia1  | P Chemineau2 | M Keller2 | JA Delgadillo3

1
Instituto Universitario de Imvestigación en
Ciencias Ambientales (IUCA), Universidad de
Zaragoza, Zaragoza, Spain
2
Physiologie de la Reproduction et
des Comportements, UMR INRA,
CNRS, IFCE, Université de Tours, Nouzilly,
France
3
Centro de Investigación en Reproducción
Caprina, Universidad Autónoma Agraria
Antonio Narro, Torreón, Coahuila, Mexico
Correspondence
José A. Abecia, Instituto Universitario de
Investigación en Ciencias Ambientales (IUCA).
Universidad de Zaragoza, Miguel Servet, 177,
50013 Zaragoza, Spain.
Email: alf@unizar.es
Funding information
MICINN (Spain), Grant/Award Number:
AGL2013-41200-P; DGA (Aragón), Grant/
Award Number: A26
Contents
Sixteen rams were used to quantify the effects of long days, imposed during late win-
ter/early spring, with or without exogenous melatonin, on plasma testosterone con-
centrations and ram serving capacity. Rams were assigned to two groups:
photoperiod-­treated rams (Artificial Photoperiod, AP; n = 8), exposed to 2 months of
long days (16 hr of light/day) between 22 December and 22 February, and control
rams (Natural Photoperiod, NP; n = 8). At the end of the long-­day period, AP rams
were returned to the natural photoperiod, and each ram in the two groups either did
(+M) or did not (-­M) receive three subcutaneous melatonin implants. Four groups were
created as follows: AP+M (n = 4), AP-­M (n = 4), NP+M (n = 4) and NP-­M (n = 4). Thirty
days after of the onset of photoperiodic treatment, AP rams (13.5 ± 2.8 ng/ml) had
significantly (p < .05) lower testosterone levels than NP rams (36.7 ± 1.0), and similar
differences were not apparent at the end of the photoperiod treatment. A month later,
AP rams (24.3 ± 7.9) had higher (p < .10) testosterone levels than NP rams (13.1 ± 5.0),
with no effect of melatonin treatment. Fifty days after melatonin implantations, rams
were exposed for 20 min to three oestrous ewes. AP rams (2.50 ± 0.42) exhibited sig-
nificantly (p < .05) more serves than did NP rams (1.11 ± 0.39), and melatonin treat-
ment had no significant effect; however, the interaction between treatments was
significant. Time to first serve was significantly (p < .05) shorter in AP (2.30 ± 1.20 min)
than it was in NP rams (5.58 ± 0.68 min). In conclusion, exposure to 2 months of long
days in late winter/early spring, with a return to natural day length of shorter duration,
increased plasma testosterone concentrations and sexual performance in rams with or
without exogenous melatonin. This particular management is an option if a non-­
hormonal reproductive strategy is scheduled; yet, if the use of exogenous hormones is
feasible, melatonin implants increase the mating efficiency of rams.

1 |  INTRODUCTION conditions of temperature and food availability are favourable

(Ortavant, Pelletier, Ravault, Thimonier, & Volland-­Nail, 1985).
Small ruminants exhibit seasonal variations in breeding activ- Seasonal changes in sexual activity are under photoperiodic con-
ity, which ensure that births occur in late winter or early spring. trol, which is the environmental factor most responsible for sea-
As such, lambs and kids can survive and grow at a time when sonal reproduction (Yeates, 1949). In sheep, long days can inhibit,

Reprod Dom Anim. 2017;1–6. © 2017 Blackwell Verlag GmbH |  1

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2       ABECIA et al.
and short days can stimulate sexual activity (Karsch et al., 1984;
Lincoln & Short, 1980). Ewes exhibit anovulatory and anoestrous
periods from the end of winter to mid-­summer, and rams exhibit
seasonal variation in behaviour and spermatogenesis. If photope-
riod is short, sexual activity cannot be sustained because refracto-
riness occurs, which stops reproductive activity (Ducker, Bowman,
& Temple, 1973; Ortavant, Maulton, & Thibault, 1964). If sheep
are exposed to the opposite photoperiod (long days), refractori-
ness can be suppressed, which has led to an understanding that
alternating between long and short days is essential for the photo-
periodic control of seasonal reproduction.
Exogenous melatonin, in the form of subcutaneous implants,
mimics the effect of short days, and is used in spring to stimulate
ovarian activity in ewes and improve libido and seminal character-
istics in rams (review Abecia et al. 2011). A preliminary period of
increasing day length or artificially long days should precede mela-
tonin treatment (Zarazaga, Gatica, Celi, Guzmán, & Malpaux, 2010).
In that way, successive long days coupled with melatonin treatment
is more efficient than is successive long days alone, which is more
efficient than is melatonin alone (Chemineau, Normant, Ravault, &
Thimonier, 1986; Chemineau et al., 1988). Chemineau et al. (1988,
1992) reviewed the practical use of photoperiod management and
melatonin implants for out-­of-­season control of sexual activity. In
particular, exposure to 2 months of long days (16-­hr light/day) is very
efficient in activating sexual behaviour in rams, advancing puberty in
young rams, substantially increasing sperm production in adult rams,
which allows these animals to be used in progeny tests for artificial
insemination at an earlier age, and causing a significant increase in
testicular weight (Chemineau et al., 1992). Furthermore, not only do
melatonin implants mimic short days, they improve semen quality,
testosterone and LH secretions and testicular weight (Rosa & Bryant,
2003).
In a recent study, we found that prolonged continuous exposure
to sexually active rams that had been stimulated by artificial photope-
riod and melatonin implants prolonged ovarian activity and increased
oestrous expression in Mediterranean ewes in spring (Abecia et al.,
2015). Furthermore, the introduction at weaning of those sexually ac-
tive rams advanced the resumption of oestrous activity in adult ewes
in spring after weaning at the end of the breeding season (Abecia
et al., 2016b), and their presence advanced puberty in autumn-­born
ewe lambs (Abecia et al., 2016a). That combination of artificial pho-
toperiod and melatonin treatment stimulates testosterone secretion
in Rasa Aragonesa rams in spring (Abecia et al., 2016a). The use of
sexually active males to override the photoperiodic control of female
sexual activity has provided a sustainable method of reproductive
control of small-­ruminant flocks, in which photoperiod is the main
factor influencing the seasonality of reproduction. It remains to be
confirmed whether the use of melatonin implants after exposure
to long days can be avoided as a means of providing a fully non-­
hormonal procedure for rams and ewes. The aim of this study was
to quantify the effects of 2 months of long days, with or without ex-
ogenous melatonin, on plasma testosterone concentrations and ram
serving capacity.
2 | MATERIAL AND METHODS
2.1 | Animals and treatments
The study included 16 sexually experienced, adult Rasa Aragonesa
rams (6–9 years of age), which had an average live weight (LW) of
98 ± 7 kg (mean ± SEM) and a mean body condition score (BCS; on
a scale of 0–5, where 0 = emaciated and 5 = obese; Russel, Doney,
& Gunn, 1969) of 3.75 ± 0.10. Before the photoperiod treatment,
rams were housed in a shaded, open pen under natural photoper-
iod. Individuals were assigned to one of two groups: photoperiod-­
treated rams (Artificial Photoperiod, AP group; n = 8), which were
exposed to 2 months of long days (16 hr of light/day) in a pen
(5 m × 7 m; 8.75 m2/ram) between 22 December and 22 February,
and control rams (Natural Photoperiod, NP; n = 8), which were kept
in a shaded, open pen and exposed to natural photoperiod at 41ºN
(15 hr 12 min, and 9 hr 10 min of light at the summer and winter
solstices, respectively). At the end of the long-­day period (22 Feb),
AP rams were returned to natural photoperiod conditions, and the
rams in the two groups were randomly assigned to groups that
either would (+M) or would not (-­M) receive three subcutaneous
melatonin implants, as recommended by the manufacturer
(Melovine, CEVA Salud Animal, Barcelona, Spain); thus, four experi-
mental groups were created as follows: AP+M (n = 4), AP-­M (n = 4),
NP+M (n = 4) and NP-­M (n = 4).
The AP rams were exposed to artificial light in the morning
(06:00–09:00) and evening (16:00–22:00), which was controlled by
an electronic timer, and light intensity was >300 lx at the eye-­level
of the animals (Chemineau et al., 1992). Plasma testosterone con-
centrations were used to quantify the effects of photoperiod and
melatonin treatments on the sexual status of rams. From the onset
of the photoperiod treatment until 1 month after the resumption
of the natural photoperiod, blood samples were collected monthly.
Samples were collected by jugular venipuncture, placed into hepa-
rinized tubes and centrifuged at 3,500 × g for 30 min. The plasma
fraction was stored at −20°C until testosterone concentrations were
measured.
Rasa Aragonesa is a local breed from northern Spain, whose re-
productive characteristics have been described (Forcada, Abecia,
& Sierra, 1992). The breed, which is typical of the “Mediterranean”
sheep breeds, exhibits a three-­month anestrous season between April
and July, although some (10%–45%) ewes ovulate in spring (Forcada
et al., 1992). Rams exhibit seasonal variation in sperm characteristics
(Cardozo et al., 2006). In our study, rams and ewes were fed to meet
their live weight maintenance requirements (AFRC 1993) and had un-
limited access to water and mineral salts.
2.2 | Serving capacity test
On 30 March, to induce oestrus, 16 adult Rasa Aragonesa ewes
received intravaginal pessaries that contained 30 mg of flug-
estone (Syncro-­Part, CEVA Salud Animal, Spain). Twelve days
later, pessaries were removed and each ewe received 300 IU eCG
ABECIA et al.
(Syncro-­Part PMSG, CEVA Salud Animal, Spain) by intramuscular
injection.
Forty-­eight hours after the removal of pessaries (50 day after
melatonin implantation), ewes were used in an individual ram serving
capacity test (after Kilgour & Whale, 1980; and Damián, Beracochea,
Hötzel, Banchero, & Ungerfeld, 2015). For 20 min, individual rams
were exposed to three oestrous ewes in a 15-­m2 pen, and the num-
ber of mountings with (serve) or without (mount) ejaculation was re-
corded. A mount was defined as the ram straddling and clasping the
ewe, and contacting her rump with his brisket. A serve was defined as
a mount that led to intromission and ejaculation, which was character-
ized by a distinct pelvic thrust and the ram’s head being thrown back,
followed by a short period in which the ram showed no interest in the
ewes (Kilgour & Whale, 1980).
2.3 | Hormonal assay
Plasma testosterone concentrations were measured by radioimmu-
noassay following Hochereau-­de Reviers et al. (1990). Sensitivity was
0.3 ng/ml. Samples were run in a single assay (intra-­assay CV = 6%).
2.4 | Statistical analysis
The experiment was based on a 2 × 2 factorial design in which pho-
toperiod and melatonin treatments were fixed effects. The effects of
the treatments on plasma testosterone concentrations and on serv-
ing capacity were evaluated statistically using the glm proc (spss v. 21)
in a model that included photoperiod (artificial or natural) treatment,
melatonin treatment (with or without melatonin implants) and their
interaction. Post hoc Least Significant Difference (LSD) tests were
used to assess the statistical significance of differences between
groups. Chi-­squared tests were used to assess the statistical signifi-
cance of differences in proportional values. Paired-­sample t tests
were used to detect significant differences in plasma testosterone
levels between one sampling day and the next. Results are expressed
F I G U R E   1   Plasma testosterone concentrations (mean ± SEM) of
vasectomized Rasa Aragonesa rams either housed under the natural
photoperiod at 41ºN (NP) or exposed to an artificial photoperiod (AP)
regime (2 months of long days: 16 hr of light/day; 22 December to 22
February) that either did (+M) or did not (-­M) receive three melatonin
implants at the end of the treatment. a, b: p < .10; c,d: p < .05 within
sampling
|
      3
as mean ± SEM, and the level for statistical significance was set to
p < .05.
3 | RESULTS
3.1 | Testosterone profiles
At the onset of the light treatment (22 December), rams in the four
groups had similar plasma testosterone levels (Figure 1). After 30 days
of the photoperiod treatment, the AP rams had lower testosterone
levels than did NP rams (13.5 ± 2.8 and 36.7 ± 1.0 ng/ml, respec-
tively: p < .05); however, at the end of the exposure to long days (22
Feb), all groups had similar plasma testosterone concentrations. Thirty
days after melatonin implantation, AP rams had higher testosterone
­concentrations than did NP rams (24.3 ± 7.9 and 13.1 ± 5.0 ng/ml,
respectively; p < .10), and melatonin treatment did not have a
­significant effect.
3.2 | Serving Capacity Test
AP rams (2.50 ± 0.42) exhibited significantly (p < .05) more serves than
did NP rams (1.11 ± 0.39), and melatonin treatment had no significant
effect; however, the interaction effect of treatments was significant.
NP+M rams performed significantly (p < .05) more serves than did NP-­M
rams (Table 1). Mating efficiency was significantly (p < .001) higher in
the AP group (0.63 ± 0.10) than it was in the NP group (0.18 ± 0.05);
yet, both photoperiod (p < .0001) and melatonin treatment (p < .01)
had a significant effect. AP+M rams exhibited their first serve the earli-
est and both photoperiod and melatonin treatments had a significant
(p < .01) effect. Time to first serve was significantly (p < .05) shorter in
AP rams (2.30 ± 1.20 min) than it was in NP rams (5.58 ± 0.68 min).
4 | DISCUSSION
In this study, exposure to 2 months of long days before a return to
the natural photoperiod increased testosterone secretion in rams,
but exogenous melatonin did not have a significant effect, and rams
exposed to the artificial photoperiod served the most ewes in the
tests, and the melatonin implants were most effective in rams that
had been exposed to the natural photoperiod. The testosterone pro-
files, which were similar to those in an earlier study (Abecia et al.,
2016a), showed that, in rams exposed to artificially long days, plasma
testosterone concentrations decreased after 30 day of exposure.
Testosterone concentrations increased 30 day after the return to
the natural photoperiod (March-­April), at the beginning of the natural
sexual refractory period. Melatonin treatment did not have a signifi-
cant effect on plasma testosterone concentrations, which indicates
that, after the long-­day treatment, melatonin is not necessary to in-
crease the plasma testosterone concentrations in the natural sexual
refractory period in Rasa Aragonesa rams. In contrast, rams exposed
to the natural photoperiod maintained testosterone levels in January,
although seasonal changes were evident because concentrations
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4       ABECIA et al.

T A B L E   1   Mean (±SEM) number of mountings with (serve) or without ejaculation (mount) during 20 min in an individual (1 ram with three
oestrous ewes) serving capacity test, and mating efficiency (serve/mounts+serves) and time (min) for the first serve by Rasa Aragonesa rams
that had been exposed to 2 months of long days (16 hr of light/day) between 22 December and 22 February (Artificial Photoperiod, AP), and
non-­exposed control rams (Natural Photoperiod, NP), that either did (+M) or did not (-­M) receive three melatonin implants at the end of the
artificial photoperiod

NP-­M NP+M AP-­M AP+M Significance

N 4 4 4 4 Photoperiod Melatonin Interaction

ace f d b
Serves 0.25 ± 0.45 1.80 ± 0.39 3.00 ± 0.33 2.00 ± 0.42 p < .01 ns p < .05
Mounts+Serves 5.25 ± 0.98 6.80 ± 1.50 6.75 ± 1.71 2.25 ± 1.50 ns ns ns
g h i j
Mating efficiency 0.08 ± 0.14 0.29 ± 0.10 0.44 ± 0.04 0.89 ± 0.19 p < .0001 p < .001 p = .10
First serve (min) 12.47 ± 0.0 3.87 ± 1.81 3.03 ± 1.50 1.32 ± 0.64 p < .01 p < .01 p < .10

Same line: ns, non-signifcant; a,b (p < .05); c,d (p < .05); e,f p < .01; g,h,i,j (p < .001) indicate the Post hoc Least Significant Difference (LSD) between groups.

decreased in February and March, when ewes became anestrus natu-
rally, which was similar to the profiles of other Mediterranean breeds
(e.g., Merino) at similar latitudes (Santiago-­Moreno et al., 2005).
Melatonin treatment did not have a significant effect on plasma tes-
tosterone concentrations, which indicated that, at least for the pur-
pose of increasing testosterone concentrations, light treatment alone
was as effective as exogenous melatonin. In an attempt to identify
alternative treatments for increasing testosterone levels, Delgadillo
et al. (2015) observed that continuous light after a long-­day treat-
ment stimulated testosterone secretion in male Alpine goats in the
non-­breeding season as well as did long days followed by a melatonin
treatment. Therefore, the use of continuous light can replace the use
of melatonin implants.
The efficacy of the combination of light treatment and melatonin to
improve sexual activity has been widely described in the buck but not
in the ram. Delgadillo et al. (2001) demonstrated that a 2.5-­mo long-­
day treatment followed by two s.c. melatonin implants induced sexual
activity in male Creole goats that were adapted to subtropical Mexico.
Zarazaga et al. (2010) reported that artificially long days or melatonin
implants at Mediterranean latitudes increased plasma testosterone con-
centrations in bucks in the natural sexual rest period. Although the long-­
day treatment alone was a less effective method of inducing adequate
out-­of-­season sexual activity in the buck, it seems that treating rams with
melatonin implants in late spring, without a priming period of long days
prior to the treatment, is not a sufficient stimulus to cause an increase in
testis growth and sperm production (Rosa, Silva, & Bryant, 2012).
In Rasa Aragonesa rams, artificial photoperiod alone was effective
in increasing the number of ejaculations, although the interaction be-
tween the two factors indicated that melatonin had a positive effect
on rams under the natural photoperiod but had no effect in the AP
group. In another experiment of ours (Abecia et al., 2015), exogenous
melatonin in spring exerted a positive effect on the number of mounts
and services, and in the interval between ejaculations among rams ob-
served for 6-­hr periods under the natural photoperiod. Rosa and Bryant
(2003) reported that melatonin implants had a positive effect on ram
sexual behaviour in spring. Kridli et al. (2007) reported seasonal varia-
tion in the sexual performance of Assaf ewes; specifically, that mount-
ing, female tail-­raising, and mating frequencies were significantly
higher in the autumn than they were in the spring. Furthermore, mat-
ing efficiency (mounts per mating) was lower in spring than it was in
autumn. Although there are no published accounts of serving capacity
tests in Rasa Aragonesa in the breeding season and at the latitude of
our study, it is likely that, in our experiment, artificial photoperiod in
the AP group, and the melatonin treatment in the NP group, induced
sexual behaviour that was comparable to that observed in the breed-
ing season. In both groups, melatonin implants had the most notable
effect on mating efficiency; that is, animals that received implants had
more mounting attempts that finished with an ejaculation than did an-
imals that did not receive an implant. In addition, the time to achieve
the first ejaculation was shorter. Seasonal variation in ejaculate latency
occurs in Algerian rams (Benia et al., 2013), and Rekik et al. (2015)
reported that melatonin treatment increased total activity time and
number of lateral approaches in a sexual behaviour test. Thus, exoge-
nous melatonin might be a more potent signal for ejaculate efficiency
than is a long-­day alone.
5 | CONCLUSION
In conclusion, exposure to 2 months of long days in late winter/early
spring, with a return to natural day length of shorter duration, in-
creased plasma testosterone concentrations and sexual performance
in rams with or without the use of subcutaneous melatonin implants.
This particular management, without an exogenous hormonal support,
is an option if a non-­hormonal reproductive strategy is scheduled;
however, if the use of exogenous hormones is feasible, melatonin im-
plants increase the mating efficiency of rams.
ET HI C AL S TAT EM ENT
The experiment was conducted at the experimental farm of the
University of Zaragoza, Spain (41° 40′N 0° 53′ W). The Ethics
Committee for Animal Experiments at the University of Zaragoza ap-
proved all of the procedures performed in the study. The care and
use of animals were in accordance with the Spanish Policy for Animal
Protection RD1201/05, which meets the European Union Directive
ABECIA et al.
2010/2063 on the protection of animals used for experimental and
other scientific purposes.
CO NFLI CT OF I NTE RE ST
The authors declare no competing financial interests.
ACKNOWLE DG E MEN TS
This study was supported financially by grant AGL2013-­41200-­P
from MICINN (Spain) and A26 from DGA (Aragón). We thank
José Antonio Ruiz and Antonio Barrio for their help in the care
of the animals, and Bruce MacWhirter for the English revision of
the manuscript. We thank Anne-­Lyse Lainé and all of the staff of
the hormonal assays, INRA, Nouzilly, France, for the testosterone
measurements.
AUT HOR CONTRI B UTI O N S
All co-­authors have participated in the design of study, acquisition and
interpretation of data as well as article preparation and have approved
the final draft of this article.
JAA performed the experiment (collected samples, mating tests.).
MK analysed the hormones. JAA, JAD and PC involved in statistical
­analysis and manuscript.
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6       ABECIA et al.

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