Influence of melatonin on the initiation of the breeding season of the marsupial bandicoot, Isoodon macrourus
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Influence of melatonin on the initiation of the breeding
season of the marsupial bandicoot, Isoodon macrourus
R. T. Gemmell
Department of Anatomy, University of Queensland, St Lucia, Brisbane, Queensland 4067, Australia
Summary. Melatonin implants were administered to 6 female bandicoots during the
months of May and July. These animals, together with 6 control bandicoots were
housed in large outside enclosures with mature males. Births were observed in the 6
control animals from 26 July to 2 September, but no births were observed in the 6
bandicoots with melatonin implants. These results would suggest that photoperiod,
which is known to influence melatonin concentrations, may be a factor in the initiation
of births in the bandicoot. However, the gradual build-up of births would suggest that
other factors such as temperature and rainfall may also have some influence.
Introduction
The bandicoots which reside along the Eastern Australian coast are all seasonally breeding
marsupials, most of the births occurring in the spring and summer months (Heinsohn, 1966;
Gordon, 1971; Stoddart & Braithwaite, 1979; Gemmell, 1982; Barnes & Gemmell, 1984). The cycle
of breeding activity is more pronounced as the latitude increases. In Tasmania, Victoria and New
South Wales definite periods of non-breeding or anoestrus were observed, but in Queensland
lactating northern brown bandicoots (Isoodon macrourus) were observed throughout the year
(Hall, 1983), although there was a decrease in breeding during the months April to June (Gemmell,
1982, 1986b). This reduction in the degree of seasonality of reproduction in the bandicoot as the
latitude decreases would indicate that the bandicoot is exhibiting a 'high degree of flexibility and
opportunism associated with the breeding of most small mammals' (Bronson, 1985). A total of 197
births were monitored from January 1980 to December 1984 in a semi-captive population of
northern brown bandicoots housed in Queensland. The complete histogram of the monthly fre-
quency of births indicated that the breeding rate was depressed from March to June, with a gradual
increase in births during July and August. Examination of the annual record revealed a variation in
the start of the breeding season with the first births occurring after at least a 1 month period of no
births, on 1 August 1980, 7 July 1981, 27 May 1983 and 28 July 1984. Births occurred throughout
the year of 1982 (Gemmell, 1986b).
Correlations between breeding activity and environmental variations such as daylength, tem-
perature and rainfall have shown that there is a strong association between the number of births
and the rate of change of minimum temperature (Barnes & Gemmell, 1984). A subsequent study of
plasma testosterone concentrations in the male bandicoot suggested that the annual plasma tes-
tosterone profile correlated well with the rate of change of daylength, an increasing daylength being
associated with an increase in plasma testosterone concentration (Gemmell et al., 1985). From the
above observations, a possible mechanism has been proposed for triggering the start of the breed-
ing season in the bandicoot in Queensland in which the rate of change of daylength may play some
part in initiating the breeding season, although the more variable factors such as temperature and
rainfall may also be involved (Gemmell, 1986b).
The rate of change in daylength influences the body metabolism of various mammals and is
thought to be mediated via the secretion of melatonin by the pineal gland (Reiter, 1980; Kennaway,
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via free access1984). The bandicoot is a long-day breeder and if daylength influences reproduction births would
be initiated by an increase in daylength and a subsequent decrease in melatonin concentrations. In
this study the effect of melatonin implants on the initiation of the breeding season of the northern
brown bandicoot was examined.
Materials and Methods
Twelve adult female and 4 adult male bandicoots, /. macrourus housed in 2 enclosures were used in this study. Three
control bandicoots without implants and 3 bandicoots with implants were housed with 2 adult male bandicoots in
each enclosure. Details of capture and maintenance of bandicoots have been described previously (Gemmell, 1982).
The pouches of the female bandicoots were examined weekly. The head lengths of newly born pouch young were used
to estimate their day of birth.
Melatonin implants
Bandicoots 1-6 were adult females which did not receive an implant. Bandicoots 7-12 received (under halothane
anaesthesia) a subcutaneous implant of melatonin, on the backs between the shoulders. These implants consisted of a
sealed envelope of Silastic sheeting, surface area 25 cm2 (500-1 sheeting, Dow Corning, Midland MI, U.S.A.) contain¬
ing 0-2 g melatonin (Sigma, Poole, Dorset, U.K.) (Lincoln et ai, 1984). All 6 bandicoots received an implant on 8 May
and a subsequent implant on 4 July. Blood samples were obtained weekly from all 12 female bandicoots until a young
was first observed in the pouches of the 6 control animals or until the end of September in the case of the animals with
melatonin implants.
Progesterone assay
Plasma progesterone concentrations were determined by radioimmunoassay using the method described pre¬
viously for the bandicoot (Gemmell, 1979), using sheep anti-progesterone- 11-hemisuccinate-bovine serum albumin
(antiserum No. 334) kindly donated by Dr R. I. Cox, CSIRO, Prospect, New South Wales, Australia. The antiserum
is highly specific for progesterone, the only significant cross-reaction being that with 11 ß-hydroxyprogesterone
(11-9%). The limit of sensitivity of the assay was 25pg/tube and the intra- and inter-assay coefficients of variation
were 13-5% (n =
5) and 170% (n 10) respectively. The assay buffer blank was less than 0-1 ng/ml and the efficiency
=
of extraction was 830% (n =
10).
Results
Bandicoots 1 and 2 (controls) gave birth on 26 July. Bandicoots 3 and 4 on 24 August, Bandicoot 5
on 1 September and Bandicoot 6 on 2 September. All 6 bandicoots had basal concentrations of
plasma progesterone before their first pregnancy of the breeding season and the cleanliness of the
pouch and the size of the teats did not change until they became pregnant. The weekly plasma
concentrations of progesterone are presented for 3 control bandicoots (Fig. 1).
The plasma progesterone profile of the 6 bandicoots that had received a melatonin implant
(Nos 7-12) remained at basal levels, except in Bandicoot 12 in which concentrations of pro¬
gesterone indicative of an oestrous cycle were observed in September. The pouch morphology of
Bandicoots 7-12 was similar to that of Bandicoots 1-6 in that pouches were clean throughout
August and September. However, the teat size did not increase, with the exception of Bandicoot
12, during September. The weekly plasma concentrations of progesterone are presented for 3
bandicoots with melatonin implants (Fig. 2).
Discussion
Melatonin administered at the start of the breeding season inhibits ovulation and subsequently
pregnancy in the bandicoot. Similar treatment of long-day breeding eutherian mammals has been
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via free access20 r
16
12
May June July Aug. Sept.
Fig. 1. The plasma progesterone concentrations of control animals, Bandicoots 2 (0--0), 4
(·-·) and 6 (Â--A). The number of young born are indicated.
shown to inhibit reproductive activity. When administered to the Djungarian hamster melatonin
prevented the reproductive stimulatory effects of long days (Hoffman, 1973). Similarly, melatonin
administered to male rabbits caused the testicular regression normally initiated by exposure to
short days (Boyd, 1985). However, in Syrian hamsters stimulation and inhibition of reproduc¬
tive activity have been reported with constant-release melatonin implants (Goldman, 1983).
Continuous exposure of animals to melatonin is not mimicking physiological parameters, since
melatonin is normally released as a nocturnal pulse. Melatonin has been administered to two other
marsupial species, the tammer wallaby (Macropus eugenii) and Bennett's wallaby (Macropus
rufogriseus): seasonal diapause in both wallabies was rapidly terminated (McConnell & Tyndale-
Biscoe, 1985; Loudon et ai, 1985). Unlike the wallabies and kangaroos, the bandicoot does not
exhibit embryonic diapause (Gemmell et ai, 1986). The results with the bandicoot would indicate
that the administration of melatonin to long-day breeding mammals, whether marsupial or
eutherian, has the same effect, i.e. the inhibition of ovulation and pregnancy.
Melatonin has also been shown to inhibit sexual development in the male white-footed mouse,
Peromyscus leucopus (Petterborg & Reiter, 1980). The inhibition of development of the testis
obtained with melatonin would also be obtained with exposure to a short photoperiod (Petterborg
& Reiter, 1980; Forger & Zucker, 1985). Sexual maturity in the female bandicoot can also be
delayed. Females born in the months July-September can produce their first litter in the same
season and, give birth at 193-8 + 7-3 days (N =
5) of age. Bandicoots born in the same period of
the year, but for which the first litter is delayed until the next breeding season, give birth at
354-3 ± 7-7 days (N 6) of age (Gemmell, 1986a). If photoperiod and melatonin have a role in
=
controlling seasonality of breeding in the mature bandicoot, it is probable that the same environ¬
mental cues which inhibit breeding in adult females also affect the maturation of juvenile females.
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via free accessMay June July Aug. Sept.
Fig. 2. The plasma progesterone concentrations of Bandicoots 8 (·-·), 9 ( A--A) and 12
(O—O) which received melatonin implants.
A correlation between an increase in plasma progesterone concentration and an increase in teat
size has been reported previously for the bandicoot. Hall (1983) observed that nulliparous females
had small, dry pouches with small teats, although just before birth the teats enlarged and the pouch
became moist. In a later study, Gemmell (1986b) observed that the increase in plasma progesterone
concentration, whether during pregnancy or an oestrous cycle, was always accompanied by an
increase in teat size. In the 6 bandicoots receiving melatonin in the present study, an enlargement of
teats was only seen with Bandicoot 12 during the same weeks that an increase in plasma progester¬
one was obtained. Teat morphology would therefore support the view that a non-pregnant or
oestrous cycle had occurred in September in this female. Photorefractoriness in long-day breeding
mammals involves spontaneous reactivation of the gonads despite continued exposure to short
photoperiod or melatonin (Goldman, 1983). Hamsters do not seem to respond to melatonin while
they are in a photorefractory state and long-term treatment with melatonin of long-day-housed
Syrian hamsters induced testicular regression followed by reactivation (Bittman, 1978). A possible
explanation for the change in hormonal concentration in Bandicoot 12 could be that it entered a
refractory state in which melatonin could no longer suppress ovulation.
The breeding season in this semi-captive colony of bandicoots varies annually (Gemmell,
1986b), but the start of the breeding season in 1985 was similar to that observed during 1981 and
1984. There were no births during the months March to June; the first births occurred late in July
and continued until 2 September. Since the onset of the breeding season in the bandicoot appears as
a gradual build up of births, photoperiod is unlikely to be the only cue influencing breeding activity.
As suggested previously, photoperiod may be the basic factor controlling seasonality in reproduc¬
tion, although other factors, such as temperature and rainfall, probably also have some influence.
I thank the Australian Research Grants Scheme for financial assistance.
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