The Northern Bettong clearly depended heavily on fungus for food. This was implied by analysis of faeces from wild-caught animals, and confirmed by stable isotope analysis which showed that most of the nitrogen, and perhaps more than half the carbon, assimilated into body tissue by this species was derived from hypogeous fungi. A high degree of fungus consumption has also been recorded (by faecal analysis) in other bettongs and potoroos (Johnson 1994b; Claridge & May 1994). Fungus made a modest and seasonally variable contribution to the diet of the Rufous Bettong, with faecal analysis indicating a peak in consumption during the wet season. However, stable isotope analysis suggested that Rufous Bettongs derive comparatively little of their dietary nitrogen from fungus. Both faecal analysis and stable isotope analysis indicated that mycophagy was of little significance to the diet of the Northern Brown Bandicoot. Our results agree with previous studies of bandicoot diets (e.g. Quin 1988; Claridge et al. 1991) in demonstrating the importance of invertebrates together with the marginal value of fungi for this species, but differ in showing that unlike bandicoots in southern forests (i.e. the Long Nosed Bandicoot, Perameles nasuta, and Southern Brown Bandicoot, I. obesulus), the Northern Brown Bandicoot eats grass to a substantial extent, especially during the dry season. Again, the significance of grass was confirmed by the stable isotope analysis, which suggested that around half the carbon assimilated into body tissue by Northern Brown Bandicoots was derived from grass.
MYCOPHAGY AND DIGESTIVE STRATEGIES IN SMALL MAMMALS
Most small herbivorous and omnivorous mammals have simple stomachs and, if they possess a capacity for microbial fermentation, it usually occurs in the hindgut (Cork 1994). The lack of extensive microbial fermentation in small mammals is thought to be a consequence of the scaling of gut capacity and energy requirements in relation to body size (Demment & Van Soest 1985): small mammals have low gut capacity relative to body mass; this limits their ability to retain ingesta in the gut for long enough to allow microbial fermentation to take place; and in addition their high mass-specific energy requirements demand a high rate of assimilation of energy. Therefore, small herbivorous mammals are obliged to feed selectively for high-quality items and often have mixed diets (Foley & Cork 1992). Under these circumstances, foregut fermentation is considered to be positively disadvantageous because it results in fermentation of highly digestible cell contents, which could more efficiently be absorbed directly across the small intestine (Van Soest 1982; Cork & Foley 1991). Hindgut fermentation avoids this cost, while still allowing some fermentation of less digestible material further along the gut (Cork 1994).
Cork & Kenagy (1989a) and Claridge & Cork (1994) show that sporocarps of hypogeous fungi have a high energy and nitrogen content, but that much of this energy and nitrogen is locked up in cell wall constituents and requires microbial processing before it can be used by mammals. Rat-kangaroos have an enlarged, elaborate forestomach in which microbial processing takes place (Hume 1982). Our results for the Northern Bettong, together with Claridge & Cork’s (1994) feeding trials on the Long-nosed Potoroo Potorous tridactylus, show that foregut fermentation allows rat-kangaroos to extract energy and nutrients from hypogeous fungi with a high degree of efficiency. Rat-kangaroos, most of which weigh between 1 and 2 kg, are much smaller than most foregut fermenters such as sheep, deer and kangaroos. Their nutritional ecology is therefore of general interest as it seems that the match of their digestive adaptations with the chemical and ecological properties of hypogeous fungi represents the very lowest threshold of body size at which foregut fermentation is a viable ecological strategy. Bandicoots have simple stomachs, with capacity for microbial fermentation in the hindgut only (Hume 1982), and in these respects resemble most other herbivorous/omnivorous small mammals. One of the supposed disadvantages of hindgut fermentation is the limitation it places on the assimilation of nitrogen that has been processed by microbes: foregut fermenters can absorb this microbial nitrogen across the small intestine, but hindgut fermenters, unless they are coprophagic or caecotrophic, lose much of it in faeces (Foley & Cork 1992). Rat-kangaroos possess a further advantage over many hindgut fermenters, which is that an important source of microbial protein comes from urea which is endogenously recycled from the blood into the forestomach (Wallis 1990). Thus, urea recycling enhances the efficiency of nitrogen use and enables the animals to feed on foods which are low in nitrogen. This may be an important factor governing the ecology of rat-kangaroos as nitrogen is often a limiting nutrient in the diets of herbivores, and its digestibility and retention is crucial (Loeb, Schwab & Demment 1991). In contrast to rat-kangaroos, many small hindgut-fermenting mammals are known to select diets that are high in protein and low in fibre, which reduces their dependence on microbial fermentation (Miller, Xia & Norrie 1990; Campbell & Macarthur 1996), although exceptions to this trend are known (e.g. Vickery et al. 1994). Such foods should be rich in a source of readily available nitrogen which can be readily absorbed without microbial processing. This may explain the limited use of fungus by bandicoots, and their extensive consumption of invertebrates.
The digestive system of the Rufous Bettong is similar to that of the Northern Bettong, yet in our study the Rufous Bettong used fungus to a much lesser extent than the Northern Bettong. One hypothesis that might explain differences in the use of fungi by the two species is that a partitioning of resources has enabled their coexistence. However, if this were the case, we might expect a substantial overlap in the distribution of the two species. This hypothesis is unlikely as the natural range of two species shows almost no overlap, despite similarities in their habitat requirements (Carpenter, Gillison & Winter 1994). A more likely hypothesis is suggested from differences in body size of the two species. Rufous Bettongs are, at 3 kg, about two to three times heavier than Northern Bettongs, and it may be that they lie closer to some threshold of body size above which foraging on hypogeous sporocarps ceases to be energetically efficient. Hypogeous sporocarps are small (usually less than 10-g dry mass) and the little that is known of their patterns of fruiting suggests that they occur patchily and often ephemerally (Johnson 1994a). They are, however, readily detectable because many of them produce powerful aromas when mature, and these aromas are demonstrably attractive to small mammals (Donaldson & Stoddart 1994). Therefore a mammal that passes close to a patch of hypogeous sporocarps will quickly become aware of it, but it may then have a large area to search before locating another patch. We speculate that a mammal of the Northern Bettong’s size might be able to satisfy its daily requirements by locating just one or a small number of patches of sporocarps, but a larger species such as the Rufous Bettong with greater absolute food requirements may need to search for a larger number of sporocarps, the patchy distribution of which would result in low foraging efficiency. This argument may explain why the Rufous Bettong devotes most of its feeding to grasses and roots, which are much more abundant and evenly distributed than hypogeous sporocarps. Confirmation of the hypothesis is needed with experiments comparing the availability, food preference and nutritional value of these food items to both species.
All three mammal species in this study relied on grass to a substantial degree. This is also of comparative interest, as our study animals are much smaller than typical grazers. There is extensive evidence that suggests that grazing is generally feasible for large herbivores only, because of the very extensive microbial processing that is required to convert grass into chemical forms that can be assimilated by mammals (Demment & Van Soest 1985). In response to these constraints, our study species appear to graze very selectively. In most samples, more than 70% of grass fragments belonged to one species, Cockatoo Grass Allopteropsis semilata. This species has a swollen stem base. Observation of grazed plants suggested that these stem bases were eaten in preference to leaves, and that the animals somehow separated coarse fibres from them before ingesting the less fibrous and liquid fractions. In the field it was common to see a chewed bolus of coarse fibres lying beside a grazed plant. The three mammals also seemed to select swollen stem bases when eating lilies, but apparently did not separate coarse fibres as they did with Cockatoo Grass.
The behaviour of ingesting just the soluble components of grass may have led to underestimation of its importance to the diet through faecal analysis. At the dry site (site B), both the Northern Bettong and Rufous Bettong showed a distinct reduction in stable isotope ratios for N and an increase in C ratios from the dry through to the wet season, indicating a decline in the use of fungus and an increase in the importance of grasses over this period. However, faecal analysis suggested the reverse trend was true for both species. An explanation for this might be that both bettongs take advantage of grasses when grass biomass increases substantially during the wet season, to maximize either energy, nutrient or water gain while minimizing overall fibre intake, which could potentially delay food retention times and digestion rates.
INTERPRETATION OF STABLE ISOTOPE VALUES IN FUNGI
Sporocarps of ectomycorrhizal fungi are known to be enriched in 15N relative to other forest ecosystem components (Gebauer & Dietrich 1993). Part of the explanation for the elevated δ15N values in fungi relative to plant items may lie in differences between the sources of nitrogen in ectomycorrhizal fungi and plants which possess either no mycorrhiza or vasicular arbuscular (VA) mycorrhizal symbionts (most grasses, forbs and lilies; Allen et al. 1995). Non-mycorrhizal plant roots and VA mycorrhizal fungi can absorb only inorganic forms of nitrogen from the soil, such as nitrate and ammonia. In contrast, ectomycorrhizal fungi can potentially utilize organic forms of nitrogen such as free amino acids, proteins and peptides (Abuzinadah & Read 1989; Read, Leake & Langdale 1989; Marschner & Dell 1994). Utilization of organic N occurs through the secretion of extracellular acid proteinases which degrade organic compounds into simple and polymeric N sources that can be assimilated by the fungi (Maijala, Fagerstedt & Raudaskoski 1991). Thus, ectomycorrhiza provide host plants with access to N sources that are normally unavailable to non-ectomycorrhizal infected plants. This may be an important factor influencing the δ15N values in ectomycorrhizal fungi as all the major pathways of N loss from the soil (denitrification, ammonia leaching and nitrate leaching) discriminate against 15N, leaving organic components of the soil enriched in 15N (Turner, Bergersen & Tantala 1983; Nadelhoffer & Fry 1988; Schulze, Chaplin & Gebauer 1994). Thus, differences in δ15N values between ectomycorrhizal fungi and plants with VA mycorrhiza or non-mycorrhizal plants probably reflect which components of the N pool are utilized. Similar patterns of 15N enrichment have been observed between saprophytic and autotrophic plants with differences due to the assimilation of organic sources of N which are available only to saprophytes (Virginia & Delwiche 1982).
Hogberg et al. (1996) found an 15N enrichment of between 1·7 and 2·0‰ in the fungal sheaths of ectomycorrhizal fungi when compared with non-mycorrhizal roots. Based on the higher percentage N of fungal sporocarps, they suggested that fungal material should be 3–11% more enriched than plant material. Differences between δ15N values in fungi and plant items observed in this study are consistent with this prediction.
It is not clear whether the large differences observed in δ15N between food items in this study are solely due to differences in sources of N uptake, or whether other processes, such as isotope fractionation during the assimilation of N, also influence δ15N values. An experimental study by Hogberg et al. (1994) using 15N-labelled NH4+ showed that differences in the δ15N of ectomycorrhizal and non-ectomycorrhizal plants were due to variations in N uptake, and that isotope fractionation appeared to be unimportant. Given this, it appears that δ15N values provide a useful marker for measuring the organic component and source of N uptake in ectomycorrhizal fungi in the field.
In addition to soil composition, the relative differences in 15N ratios of hypogeous fungi and non-ectomycorrizal plants will be influenced by features such as plant life form (Virginia & Delwiche 1982), vertical depth of plant roots in soil profile (Gebauer & Schulze 1991), ability of plants to fix nitrogen (Peoples et al. 1991) and the extent of mineralization processes (Read et al. 1989; Handley & Raven 1992) which are in turn influenced by soil properties, rainfall, fire and biotic interactions within the soil. We predict that high δ15N values in ectomycorrhizal fungi should occur in forests where the soil is rich in organic N such as many eucalypt and conifer forests (Marschner & Dell 1994). Many of these forests are nutrient limited (Schulze et al. 1994) because rates of decomposition are low because of either low temperatures or low moisture (Van Cleve et al. 1991). In such forests, particularly those with acid organic soils (Abuzinadah & Read 1989), ectomycorrhiza are expected to provide plants with an important means of N acquisition, and in addition, an important food source for mycophagous mammals.