Exogenous melatonin modifies rate of sexual maturation in domestic pullets.
ABSTRACT Growing pullets were maintained on 14-h photoperiods and given diets supplemented with 25 mg of melatonin (MEL)/kg during the final 7 h of the photo-period to investigate the role of MEL in sexual development. Melatonin diets were fed to 70 d (to mimic a transfer from 7 to 14 h at 70 d), from 105 d onward (to mimic a transfer from 14 to 7 h at 105 d), or throughout the trial (to mimic constant 7-h photoperiods). Control birds, which were fed normal diets, were maintained on 7 or 14 h, transferred from 7 to 14 h at 70 d, or transferred from 14 to 7 h at 105 d. The MEL groups matured 6 to 11 d later than the constant 14-h controls. The group mimicking a transfer from 7 to 14 h matured 35 d later than photostimulated controls, the group mimicking a 14 to 7-h change at 105 d matured 41 d earlier than birds given a decrease in day length; the third group matured 13 d earlier than constant 7-h controls. Although these data suggest that the birds did not perceive the final 7 h of the photoperiod as being part of the night, when given MEL diets, residual plasma MEL during the first 7 h of the photoperiod was atypically high, possibly preventing an interpretation of day and night. However, continuously high plasma MEL did not result in birds responding as if in constant darkness, because birds transferred from darkness to 14 h at 70 d would not have matured at a similar time to birds changed from 14 h to darkness at 105 d. Plasma LH concentrations for birds mimicking a 7 to 14 h change at 70 d were not significantly different from constant 7-h controls after the transfer to normal diets. The later maturity of the experimental groups, compared with constant 14-h controls, clearly indicated that MEL had some influence over hypothalamic activity and gonadal development.
Exogenous Melatonin Modifies Rate of Sexual Maturation in Domestic Pullets
P. D. Lewis,*,1B. A. Middleton,† and R. M. Gous*
*Animal and Poultry Science, School of Agricultural Sciences and Agribusiness, University of KwaZulu-Natal, Private Bag
X01, Scottsville 3209, South Africa; and †School of Biomedical and Molecular Sciences, University of Surrey, UK
photoperiods and given diets supplemented with 25 mg
of melatonin (MEL)/kg during the final 7 h of the photo-
period to investigate the role of MEL in sexual develop-
from 7 to 14 h at 70 d), from 105 d onward (to mimic a
transfer from 14 to 7 h at 105 d), or throughout the trial (to
mimic constant 7-h photoperiods). Control birds, which
were fed normal diets, were maintained on 7 or 14 h,
transferred from 7 to 14 h at 70 d, or transferred from 14
to 7 h at 105 d.
The MEL groups matured 6 to 11 d later than the con-
stant 14-h controls. The group mimicking a transfer from
the group mimicking a 14 to 7-h change at 105 d matured
41 d earlier than birds given a decrease in day length;
the third group matured 13 d earlier than constant 7-h
Growing pullets were maintained on 14-h
Key words: pullet, sexual maturity, melatonin
2006 Poultry Science 85:117–122
Although the hormonal events that occur within the
avian hypothalamus and pituitary gland in response to a
change in photoperiod are well understood (Etches, 1996)
and although the effects that these endocrine changes sub-
have been adequately reported (Lewis et al., 1994, 1998,
1999), the mechanismby which the hypothalamus receives
photic information to effect these changes is still unclear.
Melatonin (MEL), which is synthesized in the pineal gland
in both mammalian and avian species and, additionally,
is synthesized in the retina of birds, is released during the
hours of darkness in response to the activity of serotonin-
N-acetyltransferase, the enzyme that catalyzes the synthe-
sis of MEL in both the retina and pineal gland (Binkley et
al., 1973). During the day, the light-induced production of
dopamine within the retina suppresses the production of
serotonin in the photoreceptors and, as a consequence,
2006 Poultry Science Association, Inc.
Received July 20, 2005.
Accepted September 18, 2005.
1Corresponding author: email@example.com
controls. Although these data suggest that the birds did
not perceive the final 7 h of the photoperiod as being part
of the night, when givenMEL diets, residual plasma MEL
during the first 7 h of the photoperiod was atypically
high, possibly preventing an interpretation of day and
night. However, continuously high plasma MEL did not
result in birds responding as if in constant darkness, be-
cause birds transferred from darkness to 14 h at 70 d
would not have matured at a similar time to birds
changed from 14 h to darkness at 105 d. Plasma LH con-
centrations for birds mimicking a 7 to 14 h change at
70 d were not significantly different from constant 7-h
controls after the transfer to normal diets. The later matu-
rity of the experimental groups, compared with constant
14-h controls, clearly indicated that MEL had some influ-
ence over hypothalamic activity and gonadal devel-
suppresses the biosynthesis of MEL (Morgan et al., 1995;
Zawilska et al., 2004). The switch from day to night mode,
and vice versa, takes place over a remarkably narrow illu-
minance range of 0.1 to 4 lx (Morgan et al., 1995), making
the circadian cycle of MEL release an ideal candidate for
the circennial changes in MEL rhythms possible indicators
statter, 2003). The involvement of MEL in the control of
reproductive activity has been extensively demonstrated
in a variety of long-day [ferrets–Herbert et al. (1978); ham-
sters, Hoffman and Reiter (1965), Bonnefond et al. (1989);
voles–Farrar and Clarke (1976)] and short-day [sheep–Bitt-
man et al. (1983), Arendt et al. (1983)] breeding mammals.
Exogenous MEL has also been demonstrated to modify
the timing of oestrus in pigs, although pigs are not gener-
ally being regarded as seasonal breeders (Diekman et al.,
1991), and a partial link between MEL and gonadal devel-
salmon (Amano et al., 2000). Whereas the chemical sup-
pressionof MELreleaseduring thefirst 4hof thescotoper-
iod of an 8-h light:16-h dark regimen successfully initiated
testicular growth in quail (Ohta et al., 1989), the control of
plete in birds. For example, the provision of exogenous
LEWIS ET AL.
MEL during a stimulatory photoperiod only reduced, but
didnotprevent, testicular developmentin quail (Jusset al.,
1993; Guyomarc’h et al., 2001) and blackheaded buntings
(Kumar, 1996), and failed to prevent testicular recrudes-
cence in quail given stimulatory light pulses during the
night of an 8-h light:16-h dark regimen (Meyer, 1998).
Most avian investigations have involved the use of
males, but there is a difference between males and females
in the distribution of encephalic MEL binding sites, at least
and preoptic areas than females (Aste et al., 2001). There-
males and females in their response to the photic informa-
tion generated by photoperiodically induced MEL circa-
In a variety of avian species, the manipulation of MEL
biosynthesis by removal of the pineal gland, with or with-
out concomitant ocular enucleation, or the implantation of
radio-luminous beads close to the pineal (Harrison, 1968;
Menaker et al., 1970; Siopes and Wilson, 1974; Cogburn
and Harrison, 1977; Homma et al., 1980; Sharp et al., 1981;
Siopes and Underwood, 1987) has had equivocal effects
of MEL in birds is that, whereas these are the most im-
portant sites, they are not the only areas of MEL synthesis.
origin (Underwood et al., 1984). It follows, therefore, that
supplementation of MEL during periods when it would
be naturally low, rather than trying to eliminate it from
to investigating its role as a transducer of lighting informa-
tion for sexual development.
In the domestic hen, MEL receptors have been found in
and the anterior lobe of the pituitary (Murayama et al.,
1998), demonstrating that systems are in place that could
enable MEL to exert both direct and indirect control over
GnRH and gonadotrophin release and the timing of rapid
This paper reports the findings of a trial that tested the
hypothesis that changes in plasma MEL rhythm, rather
than direct illumination, influence the hypothalamic con-
trol of gonadotrophin release from the pituitary and influ-
trol birds were fed normal diets and were maintained on
7-h (group F) or 14-h photoperiods (group G), were trans-
ferred from 7 to 14 h at 70 d (group B), because this mark-
edly advances AFE (Lewis et al., 2002), or were transferred
from 14 to 7 h at 105 d (group D), which produces a
mental groups were maintained on 14-h photoperiods and
given MEL-supplemented diets from 7 to 70 d (group A
simulating group B), from 105 d onward (groupC simulat-
group F). Nonsupplemented diets were given to group C
up to 105 d and to group A from 70 d. The lighting and
dietary treatments are summarized in Figure 1. A 25-mg/
kg supplementation was used because it had been demon-
strated, in a short preliminary trial, to be the appropriate
dose to achieve typical nocturnal plasma MEL concentra-
tions in illuminated birds. Similar dietary doses had been
used for chicks (Nøddegaard and Kennaway, 1999), and
an equivalent dose was given in the drinking water to
turkeys (Moore and Siopes, 2002).
MATERIALS AND METHODS
A total of 112 Hyline brown egg-type pullets were
placed, 8 birds to a cage, in 6 similar light-proof rooms at
1 d of age, and exposed to an initial 2 d of continuous
illumination followed by 5 d of 18-h photoperiods. At 7
riods (0800 to 1500 h); the remaining 80 birds, stocked 20
per room, were transferred to 14-h photoperiods (0100 to
1500 h). Illumination was provided by 60-W incandescent
lamps (33 ± 1.1 lx at feed trough) with lamps located at a
height of 2 m. The stocking density was reduced to 4 birds
percage at56 dand toone birdper cageat84d.All groups
were allowed unrestricted access to a non-supplemented
chick starter mash for the first 7 d. Subsequently, whereas
the birds on 7-h photoperiods continued to be allowed
free access to feed, the birds in the 4 rooms given 14-h
photoperiods (0100 to 1500 h) had access to feed limited
to a 7.25-h period between 0730 and 1445 h by covering
the troughs at 1445 h and uncovering them at 0730 h next
morning. The increase in photoperiod at 70 d for group B
was achieved by transferring birds from a 7-h room to a
14-h room, and the decrease in photoperiod at 105 d for
group D was achieved by transferring birds from a 14-h
room to a 7-h room. The MEL-supplemented diets were
produced by dissolving MEL (Melatonin 97%, Sigma-Ald-
rich, Steinheim, Germany) in alcohol and mixing with pro-
prietary commercial chick starter and grower mash diets
at the rate of 25 mg/kg of diet. After mixing, the diets
were left exposed to allow the alcohol to evaporate as
described by Diekman et al. (1991).
A 2-mL blood sample was taken from a brachial vein
of 8 birds in groups A and G during the 30 min before the
birds were allowed access to feed and from the remaining
8 birds of these groups between 2 and 3 h after the start
of feeding on d 66. The sample was centrifuged at 500 ×
g for 15 min, and the sera were frozen. Similarly, samples
were taken from groups E and G at 77 d of age. Subse-
quently, the sera were chloroform-extracted and assayed
for plasma MEL concentration using an iodinated tracer
and a method that had been modified from Fraser et al.
(1983) for use with chickens to confirm that ingestion of
taken from 8 birds in groups A, B, and F at 69 d and
again from the same birds at 72 and 76 d for subsequent
luteinizing hormone(LH) radioimmunoassayaccording to
the method described by Sharp et al. (1987). Regressions
of the SEM for plasma LH and MEL concentrations on the
corresponding means for each line × lighting treatment
indicated that the SEM increased in direct proportion to
the mean; therefore, this heterogeneity of variance was
MELATONIN AND SEXUAL MATURITY IN DOMESTIC PULLETS
Figure 1. Dietary and photoperiodic treatments for Hyline brown pullets; black bars represent normal 7-h photoperiod with normal diet. White
bars represent 14-h photoperiods with normal diet. Gray bars represent 14-h photoperiod with melatonin (MEL)-supplemented diet.
removed by transforming concentrations to log10values
prior to statistical analysis. Age at first egg was recorded
for individual birds, together with BW at, and weight of,
the first egg. Sexual maturity data were analyzed using a
residual maximum likelihood model from Genstat Sixth
Edition (Lawes Agricultural Trust, 2002) to check for room
effects. However, no significant effects were detected;
a model from Genstat Sixth Edition (Lawes Agricultural
Mean AFE was similar for the 3 groups maintained on
14-h photoperiods and given MEL-supplemented diets,
regardless of the timing of supplementation. All matured
between 6 and 11 d later than the normally fed, constant
14-h controls, athough the difference was only significant
for those given a MEL-supplemented diet up to 70 d or
from 105 d onward (Table 1). The group given a MEL diet
up to 70 d matured 35 d later than birds transferred from
7- to 14-h photoperiods at 70 d. The group given a MEL
diet from 105 d onward matured 41 d earlier than birds
transferred from 14- to 7-h photoperiods at 105 d. The AFE
for the birds given MEL diets throughout rearing was 13
Table 1. Mean age at first egg (AFE), change in plasma luteinizing hormone (LH) concentration between −1 and
Hyline brown pullets maintained on 7- or 14-h photoperiods from 7 d, transferred from 7- to 14-h photoperiods
at 70 d or transferred from 14- to 7-h photoperiods at 105 d, or maintained on 1-h photoperiods from 7 d and
given a diet supplemented with 25 mg of MEL/kg from 7 to 70 d or from 7 or 105 d onward
Plasma MEL (pg/mL)
relative to feeding
(n = 8)
(n = 8) TreatmentAFE (d)Before 2 h after
14-h photoperiod, MEL diet from 7 to 70 d (group A)
7- to 14-h photoperiod at 70 d (group B)
14-h photoperiod, MEL diet >106 d (group C)
14- to 7-h photoperiod at 105 d (group D)
14-h photoperiod, MEL diet >7 d (group E)
Constant 7-h photoperiod control (group F)
Constant 14-h photoperiod control (group G)
147 ± 2.8c
112 ± 1.5e
145 ± 3.5c
186 ± 3.7a
142 ± 2.6cd
155 ± 2.2b
136 ± 1.9d
+2 ± 14.2b
+169 ± 27.1a
−14 ± 13.9b
360 ± 123a
320 ± 77a
12 ± 1.8b
22 ± 4.1b
a,bWithin a column, means without a common superscript are significantly different at P < 0.05.
1Calculated from individual changes in plasma LH concentration.
2Not included in the analysis because the data were not normally distributed. Comparisons can be made
between and within columns of MEL data.
d earlier than that for constant 7-h controls. In the control
groups given normal diets, those transferred from 7 to 14
h at 71 d matured 43 d earlier than constant 7-h controls,
and those changed from 14 to 7 h at 105 d matured 50
d later than the birds maintained on 14-h photoperiods.
Constant 7-h controls matured 24 d later than birds main-
tained on 14-h photoperiods.
Notwithstanding that the mean AFE for the 3 MEL-fed
from each other, there were noticeable differences among
them for that way in which the individual AFE were dis-
tributed (Figure 2). Whereas the first bird in each experi-
mental group matured at a similar time to the first of the
constant 14-h birds, 125 d (group A), 126 d (group C), 128
d (groups E and C), and 125 d (group G), the 2 groups
that were given MEL diets for only part of the rearing
period had much wider ranges of individual AFE (49 d
for group A and 60 d for group C) than the group that
received MEL diets continuously (group E, 31 d).
The percentage change in plasma LH (69 to 76 d) for
the group transferred from MEL-supplemented to normal
diets at 70 d was not significantly different from that for
constant 7-h controls (Table 1) and in neither group was
the change significantly different from zero. In contrast,
plasma LH for the birds transferred from 7- to 14-h photo-
LEWIS ET AL.
Figure 2. Distribution of individual ages at first egg in 10-d classes
for 16-bird groups of Hyline brown pullets in 6 treatment groups. Con-
trol birds were fed normal diets and were maintained on 7-h (group
F) or 14-h photoperiods (group G), were transferred from 7 to 14 h at
70 d (group B), or were transferred from 14 to 7 h at 105 d (group D).
All experimental groups were maintained on 14-h photoperiods and
givenmelatonin-supplemented dietsfrom7to 70d(group Asimulating
group B), from 105 d onward (group C simulating group D), or continu-
ously from 7 d (group E simulating group F). Non-supplemented diets
were given to group C up to 105 d and to group A from 70 d.
periods rose significantly by 169% within 6 d of the photo-
Plasma MEL concentration in the illuminated period
immediately prior to the start of feeding was significantly
higher for the birds on a MEL-supplemented diet than for
the 14-h birds given normal diets (Table 1). Plasma MEL
concentration in blood sampled 2 to 3 h after feeding had
started was consistently higher than the 500-pg/mL upper
limit of the assay for the birds consuming MEL-supple-
mented diets. Therefore, the data could not be analyzed
because they were not normally distributed. Plasma MEL
for the 14-h controls (group G) before and after feeding
were not significantly different.
The 43-d advance in AFE for the birds transferred from
7 to 14 h at 70 d (group B vs. group F) and the 50-d delay
for those transferred from 14 to 7 h at 105 d (group D
vs. group G), relative to birds maintained on the initial
et al., 2002), as is the 19-d difference between the constant
7-h (group F) and 14-h (group G) controls (Lewis and
The +35-d difference in mean AFE between groups A
and B, the −41-d difference between groups C and D, and
supplemented diet were not interpreted as 7-h photoperi-
ods. Therefore, groups A, C, and E did not, respectively,
mimic groups B, D, and F. The changes in plasma LH
concentration for group A birds during the 6 d following
their transfer to a normal diet and the same changes for
the constant 7-h controls (group F) over the same period
were nonsignificant, but a highly significant change was
observedin LH for birds transferred from 7- to 14-h photo-
periods at 70 d (group B). This result is further evidence
that the experimental birds did not read the change from
a MEL-supplemented to a normal diet as being a transfer
to from a 7- to 14-h day length. Conversely, none of the 3
groups ignored the exogenous MEL, because all matured
later than the constant 14-h controls (group G). These data
ment continued to occur, albeit at a rate that was slower
than might have been expected, for quail exposed to 12-h
photoperiods, despite the birds being injected daily for 3
wk with 10 ?g of MEL 2 h before, and again at, dawn or
dusk (Juss et al., 1993). The quail had clearly not read the
MEL signal as darkness, but neither had they ignored it.
This, the researchers suggested, might indicate that MEL
an internal messenger that is coupled to the environmental
Melatonin concentrations in the sera obtained from the
experimental birds during the period that the lights were
on, but before they had started feeding, were higher than
expected (<40 pg/mL; Lewis et al., 1989, 2001) for the
diurnal part of a 14L:10D regimen. Although the short
preliminary trial and results from other investigations
(Nøddegaard and Kennaway, 1999; Moore and Siopes,
2002) indicated that 25 mg/kg of diet was an appropriate
concentration to achieve physiological circulating MEL
concentrations, these trials had not given exogenous MEL
for such a prolonged period as in the current experiment.
When periods of illumination are brighter than 4 lx, reti-
nally produced dopamine suppresses serotonin and MEL
synthesis in both the ocular and pineal photoreceptors of
birds (Morgan et al., 1995); therefore, these abnormally
Presumably, at the end of the night, the concentration of
MEL was so high that the liver was unable to remove the
accumulated surplus within the 7 h of illumination that
MELATONIN AND SEXUAL MATURITY IN DOMESTIC PULLETS
injection of exogenous MEL at dusk of a 12L:12D regimen
resulted in a 100% increase in peak nocturnal MEL and
persistence for 2 d (Bothorel et al., 2002). However, in the
current trial, the situation is likely to have been worse,
becausethe birdsreceiveddailyintakes ofexogenous MEL
over a prolonged period. The failure of any of the 3 MEL
or as transfers between these photoperiods is understand-
able with such saturated MEL systems. It is possible that
the MEL photic signal was read as some kind of constant
condition and not of a 7- or 14-h photoperiod. The AFE
data tend to support this suggestion. Birds given MEL-
supplemented diets throughout the rearing period (group
E) had a mean AFE that was intermediate between the
nonstimulatory 7-h control (group F) and the stimulatory
14-h controls (group G). However, the birds do not appear
to have perceived the permanently high plasma MEL as
permanent darkness (DD), because transfers from DD to
14 h at 70 d and from 14 h to DD at 105 d and constant
DD would not have resulted in similar sexual maturities
(Lewis et al., 2002). An alternative method of elevating
MEL during the second half of the photoperiod, such as
a smaller dietary dose than 25 mg/kg, absorption into
cracked wheat grains (Nøddegaard and Kennaway, 1999),
a daily subcutaneous injection of MEL (Juss et al., 1993),
or the use of a dopamine receptor antagonist to nullify the
neurotransmitter’s suppressive influence over serotonin
synthesis (Zawilska et al., 2004), might have resulted in
the bird having normal daytime concentrations of MEL
during the first half of the 14-h photoperiod and interpre-
ting the lighting regimen as 7L:17D.
Unfortunately, no clear conclusions can be drawn from
sion of photic information to the hypothalamus and its
involvement in the control of sexual maturation in domes-
tic pullets. However, it is apparent from these results and
those from the other avian experiments that, unlike the
situation in mammals (Bonnefond et al., 1989), MEL in
avian species does not provide a photoperiodic time mea-
surement to the hypothalamus to influence gonadotropin-
releasing hormone release and down-stream gonadotro-
phin release from the pituitary. It is probable that the more
complicated avian system for producing MEL (mammals
do not synthesis MEL in the retina) may be part of the
tion among avian species for the way in which MEL con-
trols the circadian system. For example, the pineal gland
seems to play the main role in house sparrows (Heigl and
Gwinner, 1995), and retinal photoreceptors predominate
in quail, but both sites are important in the pigeon (Un-
derwood et al., 2001). Differences also appear to exist in
turnal elevations in MEL, later maturity, and inferior egg
production compared with birds that had had a bilateral
ocular enucleation or were subjected to both procedures
(Siopes and Underwood, 1987). In contrast, the removal of
the pineal in domestic fowl, while still producing a re-
tarding effect on sexual maturity in cockerels (Cogburn
and Harrison, 1977) and broiler pullets, does not affect
post-peak egg production or modify the response to a
transfer from 6- to 20-h photoperiods (Sharp et al., 1981).
The release of the recently identified hypothalamic neu-
ropeptide, gonadotrophin-inhibitory hormone, which de-
presses the release of LH and follicle-stimulating hormone
in the pituitary of domestic fowl in vitro (Ciccone et al.,
of MEL in quail in vivo (Ubuka et al., 2005). The failure
of the change from ordinary to MEL-supplemented diets
and vice versa to mimic transfers from long to short days
and short to long days, respectively, in this experiment
might be indicative of another interspecies difference or
hormone is onlypart of a very complicated series of events
that control avian gonadal development.
We wish to express our appreciation to Dean Backhouse
and Ann Kinsey for diligently covering and uncovering
feed troughs at the correct times each day for almost 6
mo; and to Philip Knight, University of Reading, UK, for
conducting the LH radioimmunoassay.
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