Hitherto we have been concerned with the tactics adopted by individuals and the performance of populations, and we have demonstrated a number of applications of evolutionary theory to these levels of organisation. However, one of the most active areas of both theoretical and empirical ecological research concerns the interspecific interactions among individuals and populations. Such interactions fall within the ambit of community ecology or synecology. Most community properties are the sum of the properties of individuals and consequently reflect the separate adaptations of species. This causes difficulty in the application of evolutionary theory to explain the apparent structure and resilience exhibited by some communities with regard to phenomena such as species diversity (for an alternative view see Wilson (1980)). One type of individual selection which can increase the structure and stability of communities is evolutionary change in a trait of the individuals in one population in response to a trait exhibited by the individuals in a second population, followed by an evolutionary response by the second population to the change in the first. This process is called coevolution (Janzen, 1980), and may arise in a number of circumstances, depending on the nature of the effects of the interacting species on each other (Table 7.1).

Where two species interact to the benefit of both, the interaction is termed mutualism. Mutualism and other two-species interactions may arise without coevolution, but coevolution may enhance the relationship to the extent that the species become obligatorily interdependent (symbiosis). A more immediately obvious interaction is one where one species enhances its fitness to the detriment of another through predation or parasitism.

Our purpose in this text is to place the natural history of marsupials within an evolutionary framework. We feel that a synthesis of this sort is warranted for four reasons. First, we freely admit that we are biased towards the view that the questions of greatest utility in ecological theory are those framed in an evolutionary context, and that we are thus concerned with the ways in which individuals in different environments enhance their survival and reproduction. This perspective has been applied to marsupial reproduction only occasionally. Second, most of the literature on marsupial ecology continues to be descriptive, its authors being motivated by the dearth of natural history data for most species. While this descriptive information is desperately needed, the absence of a comparative framework has led to the use of disparate and incomparable methods and this has hindered synthesis. Third, where evolutionary theory has been applied to marsupials, it has often been done unwisely, using assumptions now discarded by evolutionary biologists. Last, we believe that the unique mode of reproduction in marsupials affords an opportunity to examine a number of problems of general relevance. We show that behavioural and ecological convergence between marsupials and eutherians has been as frequent as morphological convergence.

From the foregoing analyses it should be obvious that there are still major deficiencies in our data base for marsupials. Although we would welcome any information, either published or unpublished, which helps to overcome these gaps, we believe the available data point to a number of important theoretical areas worthy of future investigation.

It is clear from Chapter 2 that it is important to distinguish between anecdotal observations on diet and those studies which carefully measure food intake, particularly in relation to food availability. Only a few studies have unequivocally demonstrated food preference by marsupials. In order to interpret the importance of particular food resources it will be necessary to attempt experimental manipulations of resources to determine which of them are limiting to particular populations.

In Chapter 3 we stress the need for increased recognition of allometric and developmental constraints on life history traits in marsupials. We also feel that it is important to consider traits of species in a holistic perspective rather than in terms of exigencies operating on individual species. Our data also point to the need for increasing synthesis of ecological, developmental and physiological approaches to marsupial biology. Specific areas worthy of further research identified in this chapter include the possibility of adaptive brood reduction in polytocous marsupials, measurement of the cost of lactation in eutherians versus marsupials, examination of the sources of the rapid pace of life found in the Peramelidae and interpretation of marsupial growth and development in terms of heterochrony.

In Chapter 4 we review the biology of three well-studied taxa of marsupials which feed predominantly on animal tissue.

It is now appropriate to examine the variation or adaptations which species exhibit within the constraints of being marsupial. Because of the effect of diet on growth and fecundity we will separate the marsupials into those species which feed predominantly upon animal tissue, the polyprotodont marsupials (this chapter), and those species which feed predominantly upon plant material, the diprotodont marsupials (Chapter 5). We have argued that the protein- and energy-rich diet of carnivorous species facilitates growth and reproduction, so in these taxa we might expect comparatively large litters and short periods of maternal investment, subject to the allometric constraints we have discussed previously. The abundance of some animal prey varies seasonally (e.g. arboreal insects; Chapter 2) and unpredictably (e.g. desert foliage-feeding insects) and we would expect this variability to have a strong influence in shaping the life histories of carnivores.

Dasyuridae

Despite their conservative body form and diet, the Dasyuridae have been exceptionally successful in Australia and New Guinea in the range of habitats occupied (Chapter 2), and this success is reflected in the wide range of life history strategies they exhibit. This diversity of life history strategies has aroused considerable interest because of the opportunities it offers for empirical analysis of life history theory (see Chapter 6). A review of these life histories by Lee, Woolley & Braithwaite (1982) recognised six distinct strategies among the thirty species for which there was information on patterns of reproduction and longevity. The strategies were distinguished on the basis of five characters (Fig. 4.1): the frequency of oestrus, the duration and the timing of male reproductive effort, the seasonality of breeding and the age at maturity.

In recent years the study of ecology has undergone a rapid shift in approach. This has been associated with an increased emphasis on evolutionary principles in analysis of ecological relationships. Historically, ecology was biased towards descriptive studies, but now most synthetic ideas are generated from theoretical approaches, often couched in turgid equations which are incomprehensible to biologists who lack mathematical training. Unfortunately, the explosion of mathematical theory has now outstripped the ability of biologists to verify its main predictions empirically. The loose use of the results of theory which may be based on naive assumptions is something of which we should all be careful, and in Chapter 7 we review the growth of competition theory as an example of the inadequate integration of theoretical, experimental and descriptive aspects of science.

A further consequence of these developments has been a decline in the role played by mammals and birds in our understanding of theoretical ecology. Although the ‘fathers’ of evolutionary ecology, David Lack and Robert MacArthur, were both ornithologists, it has become increasingly apparent that invertebrates with simple life histories, simple population structure and short lives are superior empirical tools to most mammals and birds. In this chapter we discuss a fascinating mammalian exception to this pattern. The abrupt male mortality, synchronous breeding and monoestrous reproduction in Antechinus spp. overcomes many of the technical difficulties experienced by population ecologists. Animals may be aged precisely, the distinction between semelparity and iteroparity is clearly defined, and the maternity and survival of young is readily assessed.

In this chapter we consider what it means to be a marsupial. We do this by contrasting the scope of the marsupial and eutherian radiations, and examine hypotheses which attempt to explain why the marsupial radiation appears to be conservative. It is not our intention to enter into the sterile debate over the general advantages of ‘marsupialness’ and ‘eutherianness’. The coexistence of these groups in South America and Australia clearly testifies to the evolutionary viability of both.

However, we feel it is useful to point to a number of deficiencies in previous attempts to contrast the two taxa. Historically, it has often been assumed that marsupials are in some sense inferior to eutherians (Asdell, 1964; Lillegraven, 1975,1979), perhaps as a consequence of the widespread but fallacious belief that marsupials represent an intermediate grade of mammalian organisation between monotremes and eutherians. Both the original work and attempts to destroy the assumption (e.g. Kirsch, 1977a, b; Parker, 1977; Low, 1978), suffer from a lack of quantification and statistical examination, and have given rise to summary statements which are probably incorrect, for example, ‘the nonseasonal opportunism in most marsupials’ (Low, 1978, p. 206), or ‘even modest territorial behaviour in the marsupials is a comparative rarity’ (Lillegraven, 1979, p. 270).

There is a further underlying and unrecognised assumption which pervades this literature. This may be paraphrased: all aspects of an organism are perfectly tuned or adapted to their environments. As we shall see, the case for interpretation of species characteristics in an adaptive framework is by no means always clear, and the application of similar assumptions to the characteristics which distinguish higher taxa is even less justified.

In this chapter we consider the life history strategies of diprotodont marsupials, marsupials which primarily depend upon plant tissues and plant exudates for food. In the previous chapter we assumed that the quality of food resources of marsupials which feed upon animal tissues was uniformly adequate and concluded that differences in the seasonality and predictability of supply were important in shaping their life history strategies. Here, however, we are concerned with animals whose food resources differ and vary markedly in quality as well as in supply (see Chapter 2), and for this reason we have chosen to review the life histories of diprotodont marsupials according to their feeding strategies.

Feeding strategies and life histories

Nectarivore

The two families (Tarsipedidae and Burramyidae) represented in this category appear to have similar life history traits (Table 5.1). These small pygmy possums and gliders are the most fecund of the diprotodonts, usually producing two or three litters a year, each of two to six young. They are unusual among marsupials in that some species breed in the season of birth.

Among these nectarivores the life history of Tarsipes rostratus is best documented. Births occur year-round in T. rostratus (Fig. 5.1), which is found in heathlands where flowering phenologies ensure substantial supplies of nectar and pollen in most months (Scarlett & Woolley, 1980; Wooller et al., 1981). Some females produce at least two, and probably three litters a year. There is a nadir in females carrying pouch young in December, when flowering is least, and a peak in February-March, when flowering increases.

Evolutionary ecology is concerned with the ways in which organisms living in different environments enhance their survival and reproduction. In this text we consider the evolutionary ecology of the marsupials, a group of mammals which have fascinated biologists since the discovery of their unique mode of reproduction. In doing this we do not offer an exhaustive review of all aspects of ecology. Rather, we focus on instances where marsupials elucidate problems in evolutionary ecology and vice versa. Most of our endeavour must be viewed as an attempt to place descriptive data in a standard theoretical framework which we hope leads naturally to the generation of hypotheses which examine the resilience of the framework and provide new directions in marsupial research.

Origins of theoretical ecology

Ernest Haeckel (1866) coined the term ‘Oekologie’ to embrace animal/environment relationships while discussing animal morphology in the light of Charles Darwin's new theory of evolution by natural selection. Despite the early importance of evolutionary theory in distinguishing ecology as a science, a theoretical basis for much of ecological research has been lacking. Mclntosh (1980) points out that there were only two references to theory and one to hypothesis in the pre-1950 cumulative indices of the major American ecological journals Ecology and Ecological Monographs, but that since that time a theoretical literature has burgeoned.

Recent historians of science have commented that this literature gives two distinct views of the organisation of ecosystems, with different historical bases (Ghiselin, 1974; MacFayden, 1975; F. E. Smith, 1975; Harper, 1977; Mclntosh, 1980; Simberloff, 1980).

What skeletons do

Skeletons are support systems; they keep animals from collapsing, and they provide levers on which muscles can act. Skeletons are hard and mechanically rigid, and they can be either internal structures (endoskeletons, as in vertebrates, from fish to mammals) or external (exoskeletons, as in arthropods, from crabs to spiders and insects).

Skeletons are mechanical structures that must withstand the forces that impinge on them, or they fail. The skeleton must support the weight of the animal, or it will fail in compression by crushing. It must withstand the forces due to locomotion, which produce bending and torsion that may cause failure in buckling. Also, a skeleton must withstand the forces of impact, and this may be the most critical requirement.

A heavier skeleton will be stronger, and for animals that do not move about (corals, for example), most of the organism can consist of skeletal material. For animals that move about, a heavy skeleton increases the cost of moving about and also reduces agility and the chances of escape from predators. The size and structure of the skeleton will therefore involve a compromise between the various demands: What should be optimized, strength or lightness?

Scaling mammalian skeletons

Consider a group of vertebrates, mammals, for example, that are similarly organized, although they are not alike. It is familiar to all of us that the bones of an elephant are proportionately heavier and stockier than those of a mouse.