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Birth in marsupials
Comparative Biochemistry and Physiology Part B 131 (2002) 621–630
Birth in marsupials夞 Robert T. Gemmella,*, Colleen Veitcha, John Nelsonb a
Department of Anatomical Sciences, School of Biomedical Sciences, The University of Queensland, Brisbane, Australia b Department of Biological Sciences, Monash University, Melbourne, Australia Received 9 April 2001; received in revised form 4 July 2001; accepted 5 July 2001
Abstract Birth is an event that allows the relatively immature marsupial to move from the internal environment of the uterus to the external environment of the pouch. The newborn marsupial passes down from the uterus to the urogenital sinus and then makes its way to the pouch and attaches to the teat at a very early stage of development. From the studies available, there appear to be three methods used by the newborn to move from the uterus to the pouch. In marsupials with a forward pouch such as the red kangaroo, tammar wallaby and the brushtail possum, the mother positions her urogenital sinus below the pouch and the newborn climb upward towards the pouch. The young climb with a swimming motion, moving the head from side-to-side and use the forearms in alternate strokes. In the bandicoot with a backward facing pouch, the mother positions the urogenital sinus above the pouch and the young slither down into the pouch. The young do not have a definite crawl, as seen with the macropodids and possum. The third method of birth has been observed in the marsupials without a definite pouch that have a mammary region that develops as the young grow in size. This type of pouch is observed in the dasyurids. The mother was noted to stand on four legs with her hips raised so that the urogenital sinus was above the pouch and the newborn young crawled downwards from the sinus to the pouch. In all species, birth was completed in 2–4 min. 䊚 2002 Elsevier Science Inc. All rights reserved. Keywords: Marsupial; Birth position; Parturition; Macropods; Possum; Bandicoot; Native cat; Newborn; Movement
1. Introduction There are an estimated 250 species of living marsupials (Kirsch and Calaby, 1977) and information concerning reproduction is known for approximately 32 species (Tyndale-Biscoe and Renfree, 1987). Descriptions of birth have been reported for approximately 11 species (Table 1). Thus it is difficult with this paucity of information to give definitive descriptions of the birth process 夞 This paper was originally presented to the Cambridge 2000 symposium ‘Physiological and Biochemical Adaptations to Australasian and Southern African Environments’ held in Cambridge, July 30–August 3, 2000. *Corresponding author. Fax: q07-3365-7261. E-mail address: [email protected] (R.T. Gemmell).
in all marsupials. Nevertheless, from the studies available, there appear to be three differing birth positions. The descriptions of birth in the Virginian opossum (Didelphis virginana) (Reynolds, 1952) and the red kangaroo (Macropus rufus) (Sharman and Calaby, 1964) gave the impression that all marsupials adopted the same birth position. The mother adopted this birth position by sitting on the base of her tail with her tail passed forward between the hind legs. The hind legs were extended with the toes pointing forwards so that they carried no weight (Fig. 1). All females licked the urogenital opening and some also cleaned the pouch as well while in the birth position. Fluid appeared at the urogenital opening before the birth of the young. In all the animals observed, the young appeared
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Table 1 Marsupials in which birth has been observed Opossum Possum Red kangaroo Didelphid Bandicoot Grey kangaroo Kowari Quokka Antechinus Tammar Quoll Bandicoot Possum
Didelphis virginiana Trichosurus vulpecula Macropus rufus Marmosa robinsoni Isoodon macrourus Macropus giganteus Dasyuroides byrnei Setonix brachyurus Antechinus swainsonii Macropus eugenii Dasyurus hallucatus Isoodon macrourus Trichosurus vulpecula
suddenly at the urogenital opening, immediately grasped the surrounding fur, and began to climb towards the pouch. A similar chain of events occurred with other macropodids such as the tammar wallaby (Macropus eugenii) (Tyndale-Biscoe and Renfree, 1987; Renfree et al., 1989). The grey kangaroo (Macropus canguru giganteus) had a slight variation in that the tail was not placed between the legs (Poole and Pilton, 1964) and was extended back from the body. The young still climbed up towards the pouch (Fig. 2). It
Fig. 1. The red kangaroo in the birth position.
Reynolds, 1952 Lyne et al., 1959 Sharman and Calaby, 1964 Barnes and Barthold, 1969 Lyne, 1974 Poole, 1975 Hutson, 1976 Cannon et al., 1976 Williams and Williams, 1982 Renfree et al., 1989 Nelson, 1992 Gemmell, Veitch and Nelson, 1999 Veitch et al., 2000
must be noted that all the macropodids examined have a forward-facing pouch and they have a similar birth position with the young crawling up towards the pouch. Marsupials with a backward facing pouch displayed a different birth position. Lyne (1974) described birth in one bandicoot (Isoodon macrourus). Immediately before giving birth the mother lay on her side with one hind leg raised, steadying herself with her front feet on the floor of the cage, and her head was twisted so that she was facing her rear end. When the mother was in the birth position, the distance between the urogenital opening and the pouch was much less than when she was in a normal standing position. A further description of birth in the bandicoot has been
Fig. 2. A grey kangaroo in the birth position (from Dawson, 1995).
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published recently (Gemmell, Veitch and Nelson, 1999). Dasyurids have a rudimentary pouch and birth has been observed in two species. In both species, the mother stood on four legs with her hips raised so that the urogenital sinus was above the pouch. The young traveled downwards from the sinus to the pouch, birth taking approximately 4 min. The supernumerary young were not eaten but discarded (Hutson, 1976; Williams and Williams, 1982). Thus to date, there are three birth positions described for marsupials (Table 1). In this review we will describe birth in the possum (Trichosurus vulpecula) a marsupial with a forward facing pouch, in the bandicoot (Isoodon macrourus) that has a backward facing pouch and in the native cat (Dasyurus hallucatus) that has a mammary region at birth. The varying birth positions will be contrasted and related to the morphology of the newborn. 2. Forward-facing pouch 2.1. The brushtail possum, Trichosurus vulpecula A breeding colony of Brisbane brushtail possums has been maintained in Brisbane since 1983. The maintenance and reproduction of possums in this colony has been described previously (Gemmell, 1995). Three adult females and one male were housed in fully enclosed outside enclosures measuring 9 m=3 m=2 m. Possums were fed on a diet consisting of fruit and vegetables and dog biscuits (Drimeat dog ration, Provincial Traders Pty. Ltd., Queensland). The possums were examined at least once a week. Each possum was lightly anaesthetized with a halogen:oxygen mixture to facilitate examination and weighing. The possum has a 17.5-day gestation length and 180-day lactation period. If the young were removed from the pouch, the mothers ovulated and mated between 6 and 10 days later and birth was observed 15–18 days after mating. Vaginal smears and the subsequent presence of sperm identified the day of mating. The possum, unlike the bandicoot, has a mating plug after intercourse. Birth occurred between 16 and 18 days later, usually between 14.00 and 18.00 h. Births in possums as well as bandicoots and a native cat were recorded at normal speed using a hand-held digital video camera (Sony DCR-TRV9E), which allowed continuous recording with a digital time record.
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Fig. 3. A pregnant possum just before birth, licking the pouch, the hind legs and the urogenital sinus.
The brushtail possum has a forward facing pouch and just prior to birth the possum sat on the base of her tail with the tail extending forward and the hind legs were placed either side of the tail. The hind legs were not extended and were bent with the feet off the ground (Fig. 3). The pouch faced directly upwards and was open. The distance from the urogenital sinus to the pouch was approximately 3 cm and the sinus was not much lower than the pouch. The possum, like all marsupial mothers, licked vigorously around the urogenital opening before the appearance of the newborn. Several millilitres of fluid were expelled from the urogenital sinus of the possum just prior to the young appearing head down wrapped in membranes. The mother licked the young vigorously. The orientation of the head of the newborn was random on expulsion from the sinus. However, the newborn immediately faced upwards and crawled directly towards the pouch and the mother continued to lick around the urogenital sinus. The mother removed a fluid-filled sac by pulling on the umbilical cord (Fig. 4) and at the same time breaking the cord allowing the newborn to continue towards the pouch. The possum then ate the membranes and the cord. The young possum took approximately 2.5–3 min to reach the pouch. After the young had reached the pouch and attached to the teat (Figs. 5–8), the marsupial mother continued to lick around the urogenital sinus and the pouch. As reported for the opossum, quokka and tammar (Hartman, 1920; Cannon et al., 1976; Renfree et al., 1989) the mother possum (Veitch
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Fig. 4. Mother possum removing the placenta.
et al., 2000) did not lick a path to aid the passage of the newborn from the urogenital sinus to the pouch. 3. Backward-facing pouch
Fig. 6. Young possum reaches the pouch.
The bandicoots used in this study were members of a breeding colony of Isoodon macrourus housed in large 30=30 m outside enclosures at the Native Animal Research Unit, Pinjarra Hills. Details of capture and maintenance of bandicoots have been described previously (Gemmell, 1982). Female bandicoots with pouch young at approximately day 7 were transferred from the large outside enclosure and housed with an adult male bandicoot in a 3=6 m outside enclosure. They were maintained on
dog food (Drimeat dog ration, Provincial traders Pty Ltd, Queensland) and supplied with water ad libitum. The animals were examined at least once a week. Each bandicoot was lightly anaesthetized with a halogen:oxygen mixture to facilitate examination and weighing. The vaginal apparatus of the female marsupial consists of two lateral vaginae, each located between the urogenital sinus and the uterus of the same side. The anterior end of each vagina is separated by a common median septum forming the vaginal culs-de-sac. In the bandicoot, the lateral vaginae are straight and approximately 50 mm
Fig. 5. A newborn possum crawling towards the pouch.
Fig. 7. Newborn possum looking for teat.
3.1. The bandicoot, Isoodon macrourus
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Fig. 8. Newborn possum attached to teat.
long and there are large lateral anterior expansions of the vaginal system, the vaginal caecae (Lyne and Hollis, 1977; Lyne, 1982). During the breeding season bandicoots wean their young at day 58, one day before the birth of the subsequent litter on day 59 (Gemmell and Johnston, 1985). Thus, with a 12.5 gestation period, ovulation and mating must occur approximately day 46 of lactation. Vaginal caecal samples were obtained daily at 08.00 h from bandicoots from day 44 through to day 50 of lactation. Material from the lumen of the vaginal caecae was obtained using the method described by Lyne (1976). A polyethylene tube with an outside diameter of 1.0 mm was passed through the urogenital sinus and along a lateral vagina into a vaginal caecum. The catheter tube, 100 mm in length, was stiffened with a thin flexible wire that was removed following insertion. A syringe with a 23G needle was used to flush 0.1 ml of saline into the caecum and some of the contents were then withdrawn into the catheter tube. This sample was placed on a microscope slide and the presence of motile sperm noted. Birth occurred 12.5 days after mating. Fortunately the majority of births take place between 08.00 and 14.00 h. Before birth the bandicoot lay on one side with one hind leg facing upwards. The mother licked around the urogenital sinus, around the pouch and along the inside of the hind legs. There was no release of fluid just prior to birth of the first young that appeared covered in membranes. The mother licked the young vigorously to remove the mem-
Fig. 9. The mother bandicoot is lying on her side and the three young are emerging from the urogenital sinus and moving down and across towards the pouch.
branes. Young were born singularly or in groups of up to four young (Figs. 9–11). Unlike the red kangaroo, the pathway of the newborn of the bandicoot was mainly downwards with the newborn only having to travel approximately 1 cm to reach the pouch. The newborn of the bandicoot do not have a definite crawl to the pouch as seen in macropodids, but have a snake-like wriggle down a moist 1 cm pathway between the urogenital sinus and the pouch. The mother bandicoot cleans the young, removing the membranes, and lies on one
Fig. 10. Four young bandicoots making their way down from the urogenital sinus to the pouch.
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Fig. 11. All young are in the pouch. The allantoic stalks are prominent.
side, then on the other, positioning the pouch so that the young nearly ‘fall’ into the pouch. As with the macropodids the transfer from the urogenital sinus to the attachment to the teat in the pouch takes approximately 5 min. 4. Rudimentary pouch 4.1. The native cat, Dasyurus hallucatus Native cats or quolls, Dasyurus hallucatus were obtained by trapping at Shipton’s Flats, Queensland. Native cats give birth between 23 and 29 July. The pregnant cats were trapped between 10 and 20 July and held in cages and monitored for birth. Births were thought to mainly take place in the morning, although film of one birth was obtained in the evening. Birth took place inside an enclosure in the canteen of the mining camp at Shipton’s Flats just outside Cooktown on 23 July 1999. The mother was standing on all four legs with the hind legs raised slightly higher than the front limbs (Fig. 12). The release of approximately 20 ml of fluid heralded the birth at 18.24 h. The native cat mother quickly started to lick up the fluid off the floor. At 18.26 h the mother turned round and licked in the pouch region while still on all fours. Her tail was extended backwards but was not held stiffly. A gelatinous mass, approximately 6 cm in length and 0.5 cm in width extended from the urogenital sinus down to the heel of both hind limbs (Fig. 13). This mass was presumably part of the placentae. The mass began
Fig. 12. Native cat giving birth.
to retract at 18.30 h and was approximately 2 cm in length, attached to the sinus by 18.34 h. The mother continued to stand on all four limbs with the haunches raised and emitted soft growls from time to time. The birth took place over approximately 10 min. The mother was injected with anaesthetic (Saffan, 0.5 mlyKg; Pitman–Moore, Australia Limited) and examined at 18.52 h. Eighteen young were observed in the region of the pouch. The large majority of young were immobile. However, frequently one young would move by wriggling violently in an S curve fashion. The native cat newborn moved far more quickly than those of the possum and bandicoot. Some young were
Fig. 13. Placenta of native cat during birth.
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suggesting parturition occurred at night. The housing of the marsupial may influence the timing of birth as photoperiod has been shown to influence marsupial reproduction. Births in the bandicoot and possum suggest that there may be a preference for birth to occur in the physically quieter period of the day. However, the results for the tammar do not support this hypothesis. 5.2. Birth position of mother
Fig. 14. Newborn native cats in the pouch. The young on the edge of the pouch still have to find a teat.
attached to teats and some to hairs (Fig. 14). The last observation was at 18.58 h. The next morning, eight young were attached to the teats and the remaining ten dead young had been abandoned (Fig. 15). The mother did not eat the young. 5. Discussion 5.1. Timing of birth Lincoln and Porter (1976) suggested that the fetus may determine the day of birth through the maturation of the pituitary–adrenal–placental axis and the mother controls the precise hour of birth. These authors reported that the rat gave birth on day 22 of gestation and births mainly took place between 08.00 and 16.00 h. The bandicoot displayed a similar preference for birth in daylight hours, giving birth between 08.00 and 14.00 h (Ns14) (Gemmell et al., 1982). A further four bandicoots gave birth at 11.26 h, 10.09 h, 11.30 h and 12.05 h within the range reported previously (Gemmell, Veitch and Nelson, 1999). The tammar wallaby did not give birth at a definite stage of the day, births being observed throughout the 24 h (Ns26) (Renfree et al., 1989). However, with the brushtail possum the majority of births occurred between 14.00 h and 18.00 h (Veitch et al., 2000). Beeck (1955) has observed parturition in a grey kangaroo in full daylight. Although the time of birth was not reported for the opossum (Didelphis virginiana), Reynolds (1952) observed birth with a five-celled flashlight as a source of illumination,
From the descriptions of birth in marsupials to date, the newborn of mothers with a forwardfacing pouch crawl upwards towards the pouch. The newborn of the bandicoot crawl sideways and down into the backward-facing pouch and in mothers with a mammary area, the newborn crawl down into the pouch. As birth is observed in other species it will be of interest to see whether the correlation between the morphology of the pouch and the method used by the young to reach the teats is maintained. 5.3. Movement of newborn Just as the method of transferring from the uterus to the teat varies, so does the movement of the young as they make their way to the pouch. The newborn macropodid climbs with a swimming motion moving the head from side to side and the forearms alternate to travel across the fur (Renfree et al., 1989; Veitch et al., 2000). Once they leave the sinus the newborn climb steadily towards the pouch. The newborn bandicoots did not have a
Fig. 15. Native cats at day 3 post-partum.
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definite crawl, but had a snake-like wriggle down a moist pathway between the sinus and the pouch. The newborn of the opossum emerged from the urogenital sinus with their forelimbs swinging as though they were swimming. They attached to the first thing, usually hair, and continued to swim up towards the pouch (Reynolds, 1952). The newborn bandicoots moved constantly until they reached the teat (Gemmell, Veitch and Nelson, 1999). Hutson (1976) in his description of birth in the kowari did not report on the movement of the young. However, the newborn antechinus was reported to move with amazing speed (Williams and Williams, 1982). Nelson (1992) described birth in Dasyurus hallucatus observing that the mother sat on her lower back and the newborn were deposited in their amniotic sacs in the pouch. It must be noted that this mother was housed in a cage and this may have influenced birth. With the birth of Dasyurus hallucatus at Shiptons Flats, the movement of the newborn native cats was not observed as they left the urogenital sinus. However, the young in the pouch region displayed periods of inactivity and periods of extreme activity. Their movements were similar to that observed for bandicoots but were far more vigorous. 5.4. Senses required to reach the pouch The senses present in several newborn species have been described. The newborn native cat (Dasyurus hallucatus), brushtail possum (Trichosurus vulpecula), bandicoot (Isoodon Macrourus), rat kangaroos (Potorous tridactylus and Bettongia gaimardi), dunnart (Sminthopsis macroura) and the opossum (Didelphis virginiana) have rudimentary vestibular (Gemmell and Nelson, 1989; Gemmell and Rose, 1989; Krause, 1991; Gemmell and Selwood, 1993) and olfactory systems (Gemmell and Nelson, 1988; Hughes and Hall, 1988; Krause, 1992) and mechanoreceptors (Merkel cells) around the mouth (Jones and Munger, 1985; Gemmell et al., 1988). All or some of these structures may aid the newborn marsupial in the journey from the urogenital sinus to the pouch and in locating the teat. Several attempts have been made to ascertain the senses required by the newborn marsupial to reach the teat. Hartman (1920) was first to suggest that the opossum, Didelphis virginiana, was ‘negatively geotropic’. Cannon et al. (1976) reported that the newborn quokka, Setonix brachyurus,
reached the pouch using gravity as the sole navigational aid and as the newborn had passed within 1 cm of the pouch opening without hesitating in its upward climb, then it is unlikely that olfaction had a role in birth. To determine the senses used by the newborn possum to reach the pouch, young were removed from the anesthetized possum mothers immediately following birth and placed outside the pouch (Veitch et al., 2000). Five mothers were anaesthetized immediately after birth, young removed from the teat, and the mother held in an upright or birth position for the possum. The newborn was then placed on the fur of the mother 3 cm from the pouch and the young always crawled towards the pouch and attached to the teat. This occurred when the young was placed 3 cm below, above, or to either side of the pouch. If the young were placed several cm across from the urogenital sinus, the young crawled upwards and then across to the pouch. However, if the young was placed more than 3 cm above the pouch, the young continued to crawl upwards away from the pouch. From these observations, the newborn possum instinctively crawled upwards. However, when the newborn was in the vicinity of the pouch, odors emanating from the pouch presumably attracted the young. Thus, the senses of gravity and of olfaction were used by the newborn to reach the teat and probably the sense of touch via the mechanoreceptor Merkel cells (Jones and Munger, 1985; Gemmell et al., 1988) around the mouth allowed the young to attach to the teat. The information gained from the removal of newborn possums and observing their subsequent efforts to return to the teat could not be repeated with newborn bandicoots. The young bandicoot following removal from the teat did not make any attempt to crawl to the pouch when placed 2–3 cm from the pouch. 5.5. Fate of the placenta The various marsupial species dispose of the placenta in different ways. The sequence of events at birth were similar for the red kangaroo and the tammar with a few exceptions (Sharman and Calaby, 1964; Renfree et al., 1989). Approximately 1 min before birth several millilitres of yellow fluid from the yolk sac were released and in the red kangaroo the allantois, a spherical sac containing approximately 2 ml of fluid, was secreted prior
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to the appearance of the young. With the tammar the allantois was secreted after the birth of the young (Renfree et al., 1989). The umbilicus became stretched as the newborn climbed towards the pouch and broke. Sharman and Calaby (1964) presumed that the red kangaroo ate the yolk sac membrane. However, remnants of the yolk sac were observed in the birth canal of tammars and potoroos (Renfree et al., 1989). With the possum, shortly after birth, the mother pulled on the chord presumably removing the yolk sac placenta that still contained fluid. The mother ate the membranes. In bandicoots, this placenta is not expelled at the end of gestation but remains within the uterus and is slowly resorbed over approximately eight days (Hill, 1897). With dasyurids, Antechinus swainsonii and Dasyuroides byrnei expelled large amounts of fluid at birth (Williams and Williams, 1982) as did Dasyurus hallucatus. The placenta of the native cat was expelled at birth and was subsequently removed by the mother. 6. Summary The major reasons for the lack of information concerning birth in marsupials are the paucity of breeding colonies. The difficulty in determining when a marsupial is pregnant and when it will give birth if it is pregnant also inhibits the study of birth in marsupials. The available reports of births are on a limited number of species and usually only of one mother. Finally, there are few scientific studies of the birth process, usually just descriptions of birth. With the further study of methods of inducing birth in marsupials, the filming of births in other marsupial species, the manipulation of newborn to detect senses used to attach to the teat, the identification of the chemical signals emanating from the pouch and other related studies, a better understanding of marsupial birth will be obtained. Nevertheless, from the information to date, it is apparent that marsupials have several methods of transferring their young from the uterus to the pouch and the hormonal events that initiate birth and the senses required by the young to reach and attach to the teat are worthy of further investigation. References Barnes, R.D., Barthold, S.W., 1969. Reproduction and breeding behaviour in an experiment colony of Marmosa mitis Bangs (Didelphidae). J. Reprod. Fert. Suppl. 6, 447–482.
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Krause, W.J., 1991. The vestibular apparatus of the opossum (Didelphis virginiana) prior and immediately after birth. Acta. Anat. 142, 57–59. Krause, W.J., 1992. A scanning electron microscopic study of the opossum nasal cavity prior to and shortly after birth. Anat. Embryol. 185, 281–289. Lincoln, D.W., Porter, D.G., 1976. Timing of the photoperiod and the hour of birth in rats. Nature 260, 780–781. Lyne, A.G., 1974. Gestation period and birth in the marsupial Isoodon macrourus. Aust. J. Zool. 22, 303–309. Lyne, A.G., 1976. Observations on oestrus and the oestrous cycle in the marsupials Isoodon macrourus and Perameles nasuta. Aust. J. Zool. 24, 513–521. Lyne, A.G., 1982. The bandicoots Isoodon macrourus and Perameles nasuta their maintenance and breeding in captivity. In: Evans, D.D. (Ed.), Management of Australian Mammals in Captivity, Zoological Board of Victoria, Melbourne pp. 47–52. Lyne, A.G., Hollis, D.E., 1977. The early development of marsupials, with special reference to bandicoots. In: Calaby, J.H., Tyndale-Biscoe, C.H. (Eds.), Reproduction and Evolution, Australian Academy of Science, Canberra pp. 293–302. Lyne, A.G., Pilton, P.E., Sharman, G.B., 1959. Oestrous cycle, gestation period and parturition in the marsupial Trichosurus vulpecula. Nature 183, 622–623. Nelson, J., 1992. Developmental staging in a marsupial Dasyurus hallucatus. Anat. Embryol 185, 335–354.
Poole, W.E., 1975. Reproduction in two species of grey kangaroos, Macropus giganteus Shaw and M. fuliginosus (Desmarest). 11. Gestation, parturition and pouch life. Aust. J. Zool. 23, 333–353. Poole, W.E., Pilton, P.E., 1964. Reproduction in the grey kangaroo, Macropus canguru, in captivity. CSIRO Wildlife Res. 9, 218–234. Renfree, M.B., Fletcher, T.P., Lewis, D.R., et al., 1989. Physiological and behavioural events around the time of birth in macropodid marsupials. In: Jarman, P., Hume, I.D., Grigg, G. (Eds.), Kangaroos, Wallabies and Rat-Kangaroos, Surrey Beatty and Sons Pty. Ltd, Sydney pp. 323–327. Reynolds, H.C., 1952. Studies on reproduction in the opossum (Didelphis virginiana). Univ. Calif. Publ. Zool. 52, 223–284. Sharman, G.B., Calaby, J.H., 1964. Reproductive behaviour in the red kangaroo, Megaleia rufa, in captivity. CSIRO Wildlife Res. 9, 58–85. Tyndale-Biscoe, C.H., Renfree, M.B., 1987. Reproductive Physiology of Marsupials, Cambridge University Press, Cambridge 476. Veitch, C.E., Nelson, J., Gemmell, R.T., 2000. Birth in the brushtail possum, Trichosurus vulpecula (Marsupialia: Phalangeridae). Aust. J. Zool. 48, 691–700. Williams, R., Williams, A., 1982. The life cycle of Antechinus swainsonii (Dasyuridae:Marsupialia). In: Archer, M. (Ed.), Carnivorous marsupials, Royal Zoological Society, Sydney, Australia pp. 89–95.
Birth in marsupials夞 Robert T. Gemmella,*, Colleen Veitcha, John Nelsonb a
Department of Anatomical Sciences, School of Biomedical Sciences, The University of Queensland, Brisbane, Australia b Department of Biological Sciences, Monash University, Melbourne, Australia Received 9 April 2001; received in revised form 4 July 2001; accepted 5 July 2001
Abstract Birth is an event that allows the relatively immature marsupial to move from the internal environment of the uterus to the external environment of the pouch. The newborn marsupial passes down from the uterus to the urogenital sinus and then makes its way to the pouch and attaches to the teat at a very early stage of development. From the studies available, there appear to be three methods used by the newborn to move from the uterus to the pouch. In marsupials with a forward pouch such as the red kangaroo, tammar wallaby and the brushtail possum, the mother positions her urogenital sinus below the pouch and the newborn climb upward towards the pouch. The young climb with a swimming motion, moving the head from side-to-side and use the forearms in alternate strokes. In the bandicoot with a backward facing pouch, the mother positions the urogenital sinus above the pouch and the young slither down into the pouch. The young do not have a definite crawl, as seen with the macropodids and possum. The third method of birth has been observed in the marsupials without a definite pouch that have a mammary region that develops as the young grow in size. This type of pouch is observed in the dasyurids. The mother was noted to stand on four legs with her hips raised so that the urogenital sinus was above the pouch and the newborn young crawled downwards from the sinus to the pouch. In all species, birth was completed in 2–4 min. 䊚 2002 Elsevier Science Inc. All rights reserved. Keywords: Marsupial; Birth position; Parturition; Macropods; Possum; Bandicoot; Native cat; Newborn; Movement
1. Introduction There are an estimated 250 species of living marsupials (Kirsch and Calaby, 1977) and information concerning reproduction is known for approximately 32 species (Tyndale-Biscoe and Renfree, 1987). Descriptions of birth have been reported for approximately 11 species (Table 1). Thus it is difficult with this paucity of information to give definitive descriptions of the birth process 夞 This paper was originally presented to the Cambridge 2000 symposium ‘Physiological and Biochemical Adaptations to Australasian and Southern African Environments’ held in Cambridge, July 30–August 3, 2000. *Corresponding author. Fax: q07-3365-7261. E-mail address: [email protected] (R.T. Gemmell).
in all marsupials. Nevertheless, from the studies available, there appear to be three differing birth positions. The descriptions of birth in the Virginian opossum (Didelphis virginana) (Reynolds, 1952) and the red kangaroo (Macropus rufus) (Sharman and Calaby, 1964) gave the impression that all marsupials adopted the same birth position. The mother adopted this birth position by sitting on the base of her tail with her tail passed forward between the hind legs. The hind legs were extended with the toes pointing forwards so that they carried no weight (Fig. 1). All females licked the urogenital opening and some also cleaned the pouch as well while in the birth position. Fluid appeared at the urogenital opening before the birth of the young. In all the animals observed, the young appeared
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Table 1 Marsupials in which birth has been observed Opossum Possum Red kangaroo Didelphid Bandicoot Grey kangaroo Kowari Quokka Antechinus Tammar Quoll Bandicoot Possum
Didelphis virginiana Trichosurus vulpecula Macropus rufus Marmosa robinsoni Isoodon macrourus Macropus giganteus Dasyuroides byrnei Setonix brachyurus Antechinus swainsonii Macropus eugenii Dasyurus hallucatus Isoodon macrourus Trichosurus vulpecula
suddenly at the urogenital opening, immediately grasped the surrounding fur, and began to climb towards the pouch. A similar chain of events occurred with other macropodids such as the tammar wallaby (Macropus eugenii) (Tyndale-Biscoe and Renfree, 1987; Renfree et al., 1989). The grey kangaroo (Macropus canguru giganteus) had a slight variation in that the tail was not placed between the legs (Poole and Pilton, 1964) and was extended back from the body. The young still climbed up towards the pouch (Fig. 2). It
Fig. 1. The red kangaroo in the birth position.
Reynolds, 1952 Lyne et al., 1959 Sharman and Calaby, 1964 Barnes and Barthold, 1969 Lyne, 1974 Poole, 1975 Hutson, 1976 Cannon et al., 1976 Williams and Williams, 1982 Renfree et al., 1989 Nelson, 1992 Gemmell, Veitch and Nelson, 1999 Veitch et al., 2000
must be noted that all the macropodids examined have a forward-facing pouch and they have a similar birth position with the young crawling up towards the pouch. Marsupials with a backward facing pouch displayed a different birth position. Lyne (1974) described birth in one bandicoot (Isoodon macrourus). Immediately before giving birth the mother lay on her side with one hind leg raised, steadying herself with her front feet on the floor of the cage, and her head was twisted so that she was facing her rear end. When the mother was in the birth position, the distance between the urogenital opening and the pouch was much less than when she was in a normal standing position. A further description of birth in the bandicoot has been
Fig. 2. A grey kangaroo in the birth position (from Dawson, 1995).
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published recently (Gemmell, Veitch and Nelson, 1999). Dasyurids have a rudimentary pouch and birth has been observed in two species. In both species, the mother stood on four legs with her hips raised so that the urogenital sinus was above the pouch. The young traveled downwards from the sinus to the pouch, birth taking approximately 4 min. The supernumerary young were not eaten but discarded (Hutson, 1976; Williams and Williams, 1982). Thus to date, there are three birth positions described for marsupials (Table 1). In this review we will describe birth in the possum (Trichosurus vulpecula) a marsupial with a forward facing pouch, in the bandicoot (Isoodon macrourus) that has a backward facing pouch and in the native cat (Dasyurus hallucatus) that has a mammary region at birth. The varying birth positions will be contrasted and related to the morphology of the newborn. 2. Forward-facing pouch 2.1. The brushtail possum, Trichosurus vulpecula A breeding colony of Brisbane brushtail possums has been maintained in Brisbane since 1983. The maintenance and reproduction of possums in this colony has been described previously (Gemmell, 1995). Three adult females and one male were housed in fully enclosed outside enclosures measuring 9 m=3 m=2 m. Possums were fed on a diet consisting of fruit and vegetables and dog biscuits (Drimeat dog ration, Provincial Traders Pty. Ltd., Queensland). The possums were examined at least once a week. Each possum was lightly anaesthetized with a halogen:oxygen mixture to facilitate examination and weighing. The possum has a 17.5-day gestation length and 180-day lactation period. If the young were removed from the pouch, the mothers ovulated and mated between 6 and 10 days later and birth was observed 15–18 days after mating. Vaginal smears and the subsequent presence of sperm identified the day of mating. The possum, unlike the bandicoot, has a mating plug after intercourse. Birth occurred between 16 and 18 days later, usually between 14.00 and 18.00 h. Births in possums as well as bandicoots and a native cat were recorded at normal speed using a hand-held digital video camera (Sony DCR-TRV9E), which allowed continuous recording with a digital time record.
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Fig. 3. A pregnant possum just before birth, licking the pouch, the hind legs and the urogenital sinus.
The brushtail possum has a forward facing pouch and just prior to birth the possum sat on the base of her tail with the tail extending forward and the hind legs were placed either side of the tail. The hind legs were not extended and were bent with the feet off the ground (Fig. 3). The pouch faced directly upwards and was open. The distance from the urogenital sinus to the pouch was approximately 3 cm and the sinus was not much lower than the pouch. The possum, like all marsupial mothers, licked vigorously around the urogenital opening before the appearance of the newborn. Several millilitres of fluid were expelled from the urogenital sinus of the possum just prior to the young appearing head down wrapped in membranes. The mother licked the young vigorously. The orientation of the head of the newborn was random on expulsion from the sinus. However, the newborn immediately faced upwards and crawled directly towards the pouch and the mother continued to lick around the urogenital sinus. The mother removed a fluid-filled sac by pulling on the umbilical cord (Fig. 4) and at the same time breaking the cord allowing the newborn to continue towards the pouch. The possum then ate the membranes and the cord. The young possum took approximately 2.5–3 min to reach the pouch. After the young had reached the pouch and attached to the teat (Figs. 5–8), the marsupial mother continued to lick around the urogenital sinus and the pouch. As reported for the opossum, quokka and tammar (Hartman, 1920; Cannon et al., 1976; Renfree et al., 1989) the mother possum (Veitch
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Fig. 4. Mother possum removing the placenta.
et al., 2000) did not lick a path to aid the passage of the newborn from the urogenital sinus to the pouch. 3. Backward-facing pouch
Fig. 6. Young possum reaches the pouch.
The bandicoots used in this study were members of a breeding colony of Isoodon macrourus housed in large 30=30 m outside enclosures at the Native Animal Research Unit, Pinjarra Hills. Details of capture and maintenance of bandicoots have been described previously (Gemmell, 1982). Female bandicoots with pouch young at approximately day 7 were transferred from the large outside enclosure and housed with an adult male bandicoot in a 3=6 m outside enclosure. They were maintained on
dog food (Drimeat dog ration, Provincial traders Pty Ltd, Queensland) and supplied with water ad libitum. The animals were examined at least once a week. Each bandicoot was lightly anaesthetized with a halogen:oxygen mixture to facilitate examination and weighing. The vaginal apparatus of the female marsupial consists of two lateral vaginae, each located between the urogenital sinus and the uterus of the same side. The anterior end of each vagina is separated by a common median septum forming the vaginal culs-de-sac. In the bandicoot, the lateral vaginae are straight and approximately 50 mm
Fig. 5. A newborn possum crawling towards the pouch.
Fig. 7. Newborn possum looking for teat.
3.1. The bandicoot, Isoodon macrourus
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Fig. 8. Newborn possum attached to teat.
long and there are large lateral anterior expansions of the vaginal system, the vaginal caecae (Lyne and Hollis, 1977; Lyne, 1982). During the breeding season bandicoots wean their young at day 58, one day before the birth of the subsequent litter on day 59 (Gemmell and Johnston, 1985). Thus, with a 12.5 gestation period, ovulation and mating must occur approximately day 46 of lactation. Vaginal caecal samples were obtained daily at 08.00 h from bandicoots from day 44 through to day 50 of lactation. Material from the lumen of the vaginal caecae was obtained using the method described by Lyne (1976). A polyethylene tube with an outside diameter of 1.0 mm was passed through the urogenital sinus and along a lateral vagina into a vaginal caecum. The catheter tube, 100 mm in length, was stiffened with a thin flexible wire that was removed following insertion. A syringe with a 23G needle was used to flush 0.1 ml of saline into the caecum and some of the contents were then withdrawn into the catheter tube. This sample was placed on a microscope slide and the presence of motile sperm noted. Birth occurred 12.5 days after mating. Fortunately the majority of births take place between 08.00 and 14.00 h. Before birth the bandicoot lay on one side with one hind leg facing upwards. The mother licked around the urogenital sinus, around the pouch and along the inside of the hind legs. There was no release of fluid just prior to birth of the first young that appeared covered in membranes. The mother licked the young vigorously to remove the mem-
Fig. 9. The mother bandicoot is lying on her side and the three young are emerging from the urogenital sinus and moving down and across towards the pouch.
branes. Young were born singularly or in groups of up to four young (Figs. 9–11). Unlike the red kangaroo, the pathway of the newborn of the bandicoot was mainly downwards with the newborn only having to travel approximately 1 cm to reach the pouch. The newborn of the bandicoot do not have a definite crawl to the pouch as seen in macropodids, but have a snake-like wriggle down a moist 1 cm pathway between the urogenital sinus and the pouch. The mother bandicoot cleans the young, removing the membranes, and lies on one
Fig. 10. Four young bandicoots making their way down from the urogenital sinus to the pouch.
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Fig. 11. All young are in the pouch. The allantoic stalks are prominent.
side, then on the other, positioning the pouch so that the young nearly ‘fall’ into the pouch. As with the macropodids the transfer from the urogenital sinus to the attachment to the teat in the pouch takes approximately 5 min. 4. Rudimentary pouch 4.1. The native cat, Dasyurus hallucatus Native cats or quolls, Dasyurus hallucatus were obtained by trapping at Shipton’s Flats, Queensland. Native cats give birth between 23 and 29 July. The pregnant cats were trapped between 10 and 20 July and held in cages and monitored for birth. Births were thought to mainly take place in the morning, although film of one birth was obtained in the evening. Birth took place inside an enclosure in the canteen of the mining camp at Shipton’s Flats just outside Cooktown on 23 July 1999. The mother was standing on all four legs with the hind legs raised slightly higher than the front limbs (Fig. 12). The release of approximately 20 ml of fluid heralded the birth at 18.24 h. The native cat mother quickly started to lick up the fluid off the floor. At 18.26 h the mother turned round and licked in the pouch region while still on all fours. Her tail was extended backwards but was not held stiffly. A gelatinous mass, approximately 6 cm in length and 0.5 cm in width extended from the urogenital sinus down to the heel of both hind limbs (Fig. 13). This mass was presumably part of the placentae. The mass began
Fig. 12. Native cat giving birth.
to retract at 18.30 h and was approximately 2 cm in length, attached to the sinus by 18.34 h. The mother continued to stand on all four limbs with the haunches raised and emitted soft growls from time to time. The birth took place over approximately 10 min. The mother was injected with anaesthetic (Saffan, 0.5 mlyKg; Pitman–Moore, Australia Limited) and examined at 18.52 h. Eighteen young were observed in the region of the pouch. The large majority of young were immobile. However, frequently one young would move by wriggling violently in an S curve fashion. The native cat newborn moved far more quickly than those of the possum and bandicoot. Some young were
Fig. 13. Placenta of native cat during birth.
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suggesting parturition occurred at night. The housing of the marsupial may influence the timing of birth as photoperiod has been shown to influence marsupial reproduction. Births in the bandicoot and possum suggest that there may be a preference for birth to occur in the physically quieter period of the day. However, the results for the tammar do not support this hypothesis. 5.2. Birth position of mother
Fig. 14. Newborn native cats in the pouch. The young on the edge of the pouch still have to find a teat.
attached to teats and some to hairs (Fig. 14). The last observation was at 18.58 h. The next morning, eight young were attached to the teats and the remaining ten dead young had been abandoned (Fig. 15). The mother did not eat the young. 5. Discussion 5.1. Timing of birth Lincoln and Porter (1976) suggested that the fetus may determine the day of birth through the maturation of the pituitary–adrenal–placental axis and the mother controls the precise hour of birth. These authors reported that the rat gave birth on day 22 of gestation and births mainly took place between 08.00 and 16.00 h. The bandicoot displayed a similar preference for birth in daylight hours, giving birth between 08.00 and 14.00 h (Ns14) (Gemmell et al., 1982). A further four bandicoots gave birth at 11.26 h, 10.09 h, 11.30 h and 12.05 h within the range reported previously (Gemmell, Veitch and Nelson, 1999). The tammar wallaby did not give birth at a definite stage of the day, births being observed throughout the 24 h (Ns26) (Renfree et al., 1989). However, with the brushtail possum the majority of births occurred between 14.00 h and 18.00 h (Veitch et al., 2000). Beeck (1955) has observed parturition in a grey kangaroo in full daylight. Although the time of birth was not reported for the opossum (Didelphis virginiana), Reynolds (1952) observed birth with a five-celled flashlight as a source of illumination,
From the descriptions of birth in marsupials to date, the newborn of mothers with a forwardfacing pouch crawl upwards towards the pouch. The newborn of the bandicoot crawl sideways and down into the backward-facing pouch and in mothers with a mammary area, the newborn crawl down into the pouch. As birth is observed in other species it will be of interest to see whether the correlation between the morphology of the pouch and the method used by the young to reach the teats is maintained. 5.3. Movement of newborn Just as the method of transferring from the uterus to the teat varies, so does the movement of the young as they make their way to the pouch. The newborn macropodid climbs with a swimming motion moving the head from side to side and the forearms alternate to travel across the fur (Renfree et al., 1989; Veitch et al., 2000). Once they leave the sinus the newborn climb steadily towards the pouch. The newborn bandicoots did not have a
Fig. 15. Native cats at day 3 post-partum.
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definite crawl, but had a snake-like wriggle down a moist pathway between the sinus and the pouch. The newborn of the opossum emerged from the urogenital sinus with their forelimbs swinging as though they were swimming. They attached to the first thing, usually hair, and continued to swim up towards the pouch (Reynolds, 1952). The newborn bandicoots moved constantly until they reached the teat (Gemmell, Veitch and Nelson, 1999). Hutson (1976) in his description of birth in the kowari did not report on the movement of the young. However, the newborn antechinus was reported to move with amazing speed (Williams and Williams, 1982). Nelson (1992) described birth in Dasyurus hallucatus observing that the mother sat on her lower back and the newborn were deposited in their amniotic sacs in the pouch. It must be noted that this mother was housed in a cage and this may have influenced birth. With the birth of Dasyurus hallucatus at Shiptons Flats, the movement of the newborn native cats was not observed as they left the urogenital sinus. However, the young in the pouch region displayed periods of inactivity and periods of extreme activity. Their movements were similar to that observed for bandicoots but were far more vigorous. 5.4. Senses required to reach the pouch The senses present in several newborn species have been described. The newborn native cat (Dasyurus hallucatus), brushtail possum (Trichosurus vulpecula), bandicoot (Isoodon Macrourus), rat kangaroos (Potorous tridactylus and Bettongia gaimardi), dunnart (Sminthopsis macroura) and the opossum (Didelphis virginiana) have rudimentary vestibular (Gemmell and Nelson, 1989; Gemmell and Rose, 1989; Krause, 1991; Gemmell and Selwood, 1993) and olfactory systems (Gemmell and Nelson, 1988; Hughes and Hall, 1988; Krause, 1992) and mechanoreceptors (Merkel cells) around the mouth (Jones and Munger, 1985; Gemmell et al., 1988). All or some of these structures may aid the newborn marsupial in the journey from the urogenital sinus to the pouch and in locating the teat. Several attempts have been made to ascertain the senses required by the newborn marsupial to reach the teat. Hartman (1920) was first to suggest that the opossum, Didelphis virginiana, was ‘negatively geotropic’. Cannon et al. (1976) reported that the newborn quokka, Setonix brachyurus,
reached the pouch using gravity as the sole navigational aid and as the newborn had passed within 1 cm of the pouch opening without hesitating in its upward climb, then it is unlikely that olfaction had a role in birth. To determine the senses used by the newborn possum to reach the pouch, young were removed from the anesthetized possum mothers immediately following birth and placed outside the pouch (Veitch et al., 2000). Five mothers were anaesthetized immediately after birth, young removed from the teat, and the mother held in an upright or birth position for the possum. The newborn was then placed on the fur of the mother 3 cm from the pouch and the young always crawled towards the pouch and attached to the teat. This occurred when the young was placed 3 cm below, above, or to either side of the pouch. If the young were placed several cm across from the urogenital sinus, the young crawled upwards and then across to the pouch. However, if the young was placed more than 3 cm above the pouch, the young continued to crawl upwards away from the pouch. From these observations, the newborn possum instinctively crawled upwards. However, when the newborn was in the vicinity of the pouch, odors emanating from the pouch presumably attracted the young. Thus, the senses of gravity and of olfaction were used by the newborn to reach the teat and probably the sense of touch via the mechanoreceptor Merkel cells (Jones and Munger, 1985; Gemmell et al., 1988) around the mouth allowed the young to attach to the teat. The information gained from the removal of newborn possums and observing their subsequent efforts to return to the teat could not be repeated with newborn bandicoots. The young bandicoot following removal from the teat did not make any attempt to crawl to the pouch when placed 2–3 cm from the pouch. 5.5. Fate of the placenta The various marsupial species dispose of the placenta in different ways. The sequence of events at birth were similar for the red kangaroo and the tammar with a few exceptions (Sharman and Calaby, 1964; Renfree et al., 1989). Approximately 1 min before birth several millilitres of yellow fluid from the yolk sac were released and in the red kangaroo the allantois, a spherical sac containing approximately 2 ml of fluid, was secreted prior
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to the appearance of the young. With the tammar the allantois was secreted after the birth of the young (Renfree et al., 1989). The umbilicus became stretched as the newborn climbed towards the pouch and broke. Sharman and Calaby (1964) presumed that the red kangaroo ate the yolk sac membrane. However, remnants of the yolk sac were observed in the birth canal of tammars and potoroos (Renfree et al., 1989). With the possum, shortly after birth, the mother pulled on the chord presumably removing the yolk sac placenta that still contained fluid. The mother ate the membranes. In bandicoots, this placenta is not expelled at the end of gestation but remains within the uterus and is slowly resorbed over approximately eight days (Hill, 1897). With dasyurids, Antechinus swainsonii and Dasyuroides byrnei expelled large amounts of fluid at birth (Williams and Williams, 1982) as did Dasyurus hallucatus. The placenta of the native cat was expelled at birth and was subsequently removed by the mother. 6. Summary The major reasons for the lack of information concerning birth in marsupials are the paucity of breeding colonies. The difficulty in determining when a marsupial is pregnant and when it will give birth if it is pregnant also inhibits the study of birth in marsupials. The available reports of births are on a limited number of species and usually only of one mother. Finally, there are few scientific studies of the birth process, usually just descriptions of birth. With the further study of methods of inducing birth in marsupials, the filming of births in other marsupial species, the manipulation of newborn to detect senses used to attach to the teat, the identification of the chemical signals emanating from the pouch and other related studies, a better understanding of marsupial birth will be obtained. Nevertheless, from the information to date, it is apparent that marsupials have several methods of transferring their young from the uterus to the pouch and the hormonal events that initiate birth and the senses required by the young to reach and attach to the teat are worthy of further investigation. References Barnes, R.D., Barthold, S.W., 1969. Reproduction and breeding behaviour in an experiment colony of Marmosa mitis Bangs (Didelphidae). J. Reprod. Fert. Suppl. 6, 447–482.
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