Patterns of parental care and parental investment in marsupials.

Abstract

SummaryI. Information on growth, development and care of young has been assembled for 62 species of marsupial.2. During gestation, development of the marsupial embryo proceeds only so far as to allow the neonate to make its way from the urogenital opening to the mammary area on the abdomen of the female where it attaches to a teat. Specific structural adaptations keep the neonate firmly attached to the teat for at least the first month after birth.3. Six types of pouch are distinguished ranging from lateral folds of skin, which do not cover the mammary area or enclose the developing young, to a fold of skin that covers the mammary area and forms a deep pouch, completely enclosing the developing young.4. Although the young is very small at birth and birth is rapid, specific changes in the behaviour of females occur around the time of birth, and a specific birth position is adopted.5. The time at which marsupial young leave the pouch cannot be equated with birth in eutherians, because of the considerable variations in the type of pouch and in patterns of parental care. From a consideration of the functional development of the young in the pouch, it is suggested that the nearest equivalent to eutherian birth is the time at which the marsupial young achieves homeostasis, when it is well furred and endothermic.6. Maternal behaviour is influenced by the type of pouch. In all species, the mother keeps the young and the pouch clean by licking, especially when the young are wholly within the pouch or attached to the abdomen. In species with reduced pouches where young are left in a nest at an early stage of development, maternal behaviour includes nest building, defence, and retrieving and carrying the young. These functions are performed by the pouch itself in species with large deep pouches in which the young is carried for a much larger part of its development, and other specific maternal behaviours are infrequent.7. The patterns of parental care are reviewed over all families of marsupial. Not all members of a family have the same pattern of parental care, which appears to be influenced by many factors including body size, type of pouch, diet, litter size and other aspects of life history strategy.8. Three patterns of parental care are distinguished:(A) As soon as young begin to release the teat they are no longer carried by the mother, and are left in a nest when still barely furred, ectothermic and before the eyes open. This pattern is found in species with large litter size and a pouch reduced or absent, e.g. some Dasyuridae and some Didelphidae.(B) Young remain in the pouch after they begin to release the teat but are left in a nest, at a later stage of development than in A, when well furred, endothermic and with eyes open. After first pouch exit, there is generally a period when young return to the pouch from time to time. This pattern is found in species with well developed pouches and litters of I or > 1 e.g. Peramelidae, some Didelphidae.(C) Young remain in the pouch after they begin to release the teat. At first pouch exit, the young is well furred and endothermic, and leaves the pouch only for brief periods, gradually spending more time out until permanent pouch exit. It is not usually left in a nest. This pattern is found in species with well developed pouches and litters of one, e.g. Macropodidae.9. Pattern A is seen particularly in the smaller species in any family, where large litter size means that by the time young release the teat, the litter is about 50% of maternal body weight and a considerable burden. In such species, young are left in a nest as soon as possible. In larger species with patterns B or C, litter size is smaller, and by the time they are no longer carried by the female, the litter is still only 20% of maternal weight.10. Whatever the pattern of parental care, mortality from birth to permanent pouch exit is not unusually high in marsupials in comparison with eutherians.11. I suggest that the presence of the pouch and the associated patterns of parental care are important determinants of social organization in marsupials. For much of the period of dependence, the young is small, attached to a teat or in a pouch. The male can make little contribution to parental care, and there is little room for improvement in the care of young in complex social groups. In most species, the female on her own is sufficient caretaker. The male is most likely to increase his own biological fitness by going off to mate again and leaving the female to raise his offspring.12. Patterns of energy expenditure on offspring by female marsupials were assessed throughout the development of young. Investment before birth was assessed by weight of the neonate, during development by growth rate and the time for which the young was carried (pouch life), and total investment by weight of young at weaning and time from birth to weaning. Regression of measures of investment against maternal body weight allowed comparison of investment in animals of different size.13. Investment in young before birth is very small. Neonatal marsupials range in size from 0·01 to 1 g, and the largest is less than 0·2 % of the size of the mother. Larger mothers produce larger young which are smaller relative to the mother than are the young of smaller species. Individual young in the family Dasyuridae are particularly small.14. Growth rates in g/d were calculated over the period from permanent pouch exit to weaning. There is a very close correlation between growth rate and maternal body weight ‐ that of litters increases as the 0·78 power of body weight. During this period the growth rate of individuals is comparable with that of eutherian young during lactation, and in litters it is higher still, suggesting that the difference in patterns of growth are not due to the lower metabolic rate of marsupials. As in eutherians there is considerable individual variation in growth rate; it is very high in litters of small dasyurids, which have individual rates comparable to those of larger species. Young of the family Peramelidae grow and develop rapidly; those of the arboreal folivore Phascolarctos do both slowly.I 5. Pouch life, the period for which the young is carried by the mother, increases with body size; as expected, species with pattern A parental care have shorter pouch lives than species of the same size with patterns B or C, reflecting the early stage of development at which young are left in the nest in pattern A.16. Time from birth to weaning is also longer in larger species. There is a close relationship of age at weaning with maternal weight, with some significant exceptions. For their size, the family Peramelidae have a very short time from birth to weaning, and the time from pouch exit to weaning is particularly short. Many arboreal species have longer periods of dependence than expected from their size.17. The weight at weaning of individual young is closely related to MBW0·71, but the weight of one young relative to maternal body weight shows no trend with size, and ranges from 25–61 %, with a mean of 42 %.18. Parental Investment, as measured by the function Wt. of litter at weaning × 100/MBW, decreases with increasing size of mother as MBW0·28. The highest levels of investment are found in very small species. In many small species of the family Dasyuridae, a litter at weaning is > 300% MBW. By contrast, investment in the family Peramelidae is low ‐ at weaning a litter of three is about 50% MBW, comparable with investment in a single young of the family Macropodidae.19. The evolution of patterns of parental care and investment appears to follow three main lines:(1) Species with large litter size, high levels of investment in litters and in individual young. Investment is directed to growth and not to carrying the young in the pouch, since young are left in a nest at an early stage. Typical of this group is the family Dasyuridae, in which many species make few reproductive attempts per year.(2) Species with litters of more than one, low levels of investment in litters and in individuals, but rapid growth and development of young. Because of the small relative size of young they are carried in the pouch for a large part of the period from birth to weaning. This pattern is shown by the family Peramelidae, and seen as an adaptation to rapid and repeated reproduction in an environment with an extended favourable season.(3) Species with small litter size, lower total investment, but investment in individual young is not low, and investment in carrying young to an advanced stage of development is high. Patterns of this type are found in the Diprotodonta, with extreme development in the Macropodidae.20. Many of the measures of investment have been expressed as a power function of maternal body weight. The exponents of body weight in these functions are such as to suggest that an important underlying variable is metabolic rate.21. It has been suggested elsewhere that the marsupial mode of reproduction evolved as an adaptation to environmental uncertainty, in that it allows a reproductive attempt to be abandoned at any time much more readily than in eutherians, thereby increasing the likelihood that a female will survive to reproduce again. I consider this suggestion in the light of patterns of parental investment. For small, short‐lived species, any reproductive attempt represents a substantial part of its lifetime reproductive output. Investment in any one reproductive attempt is high, and the cost of replacing an abandoned attempt is so high that it seems unlikely that the desertion of offspring would be an important reproductive strategy in small ancestral marsupials, although it may be an important response to environmental uncertainty in certain large modern macropodids.