Digestive performance and digesta passage in the omnivorous greater bilby, Macrotis lagotis (Marsupialia: Peramelidae)

Omnivores such as the greater bilby (Macrotis lagotis) consume a variety of dietary items and often are faced with large changes in the nutrient composition of their food. This paper explores the basis for the dietary flexibility of the bilby by comparing digestive performance and digesta retention patterns of captive bilbies fed either an insect diet (mealworm larvae) or a plant diet (mixed seeds). Mean retention times (MRTs) of particle and solute markers in the gastrointestinal tract did not differ significantly between the two diets, but MRT of the particle marker was significantly longer than that of the solute marker on both the mealworm (particle: 23.5 h; solute: 17.9 h) and mixed seed (particle 33.0 h; solute: 30.2 h) diets. Lack of selective retention of solutes and small particles in the bilby gastrointestinal tract probably restricts them to relatively low-fibre diets, such as those based on seeds rather than leaves and stems of plants. It was observed radiographically that the major sites of digesta retention were the caecum, proximal colon and distal colon, and thus the hindgut is probably the principal site of microbial fermentation. The mealworms were more digestible than the mixed seeds, but digestible energy intake (mealworm: 939 kJ · kg^−0.75 · d⁻¹; mixed seed: 629 kJ · kg^−0.75 · d⁻¹) was high enough for maintenance of body mass and positive nitrogen balance on both diets. Thus, although bilbies may be limited in their ability to utilize high-fibre diets by a lack of selective retention of solutes and small particles in their hindgut, their digestive strategy is flexible enough to accommodate at least some diets of both animal and plant origin. Such a strategy should benefit an animal inhabiting environments in which food resources are unpredictable in their relative abundance. Accepted: 26 May 2000     

Ecophysiology and nutritional niche of the bilby (Macrotis lagotis), an omnivorous marsupial from inland Australia: a review

The bilby (Macrotis lagotis) is a small omnivorous marsupial that was once widespread but is now restricted to the most arid margins of its former range. It feeds on a mixture of invertebrates (mainly ants and termites) and plant material (mainly seeds and bulbs), most of which is below ground. Measurements of the energy and water requirements of free-living bilbies and of the maintenance nitrogen requirements of captive animals provided the basis for an explanation for its continued survival in the Australian arid zone. Measurements of the mean retention times of inert markers for the solute and particulate phases of digesta revealed no selective retention of solutes and small particles in the caecum. Lack of selective digesta retention in the bilby hindgut helps to explain why the plant component of their diet consists predominantly of seeds and bulbs of relatively low fibre content. This is in contrast to the stems and leaves eaten by other bandicoots, all of which appear to have a colonic separation mechanism that not only selectively retains small particles in the caecum but also facilitates the passage of large fibrous particles through the colon. The ability of the bilby to survive in the Australian arid zone is related to low water and nitrogen requirements and the abundance of ants, termites, bulbs and seeds. Foraging efficiency is maximised by exploiting the underground nests of seed-harvesting ants.     

The phylogenetic relationships of the bilby, Macrotis lagotis (Peramelimorphia: Thylacomyidae), to the bandicoots- DNA sequence evidence

Partial sequencing of the 12S ribosomal RNA gene was used to test two competing hypotheses concerning the phylogenetic relationship of the bilby (Macrotis lagotis) to the Australian and New Guinean species of bandicoot. The first hypothesis proposes that the Australian and New Guinean bandicoots are in a monophyletic clade to the exclusion of the bilbies, whereas the second hypothesis proposes that the bilby is monophyletic with the Australian bandicoots to the exclusion of the New Guinean bandicoots. Phylogenies determined by both maximum-likelihood and neighbour-joining approaches supported the first hypothesis in which the bilby is excluded from the clade represented by the Australian and New Guinean bandicoots. Monophyly of the Australian and New Guinean bandicoots is consistent with the biogeographical scenario in which Australia and Papua New Guinea have undergone repeated connection and disconnection over the last 20 million years.     

Responses of the digestive tract of the omnivorous northern brown bandicoot, Isoodon macrourus (Marsupialia: Peramelidae), to plant- and insect-containing diets

The gastrointestinal tract of omnivores such as bandicoots (Marsupialia: Peramelidae) must be able to process foods as different as invertebrates, fungi and plant material. We studied the mechanisms involved in the utilisation by captive northern brown bandicoots (Isoodon macrourus) of insect larvae and milled lucerne (Medicago sativa) hay incorporated into a basal diet of a commercial small carnivore mix. Animals on the plant-basal mix digested less dry matter, energy, lipid, fibre and total nitrogen, but consumed 79% more dry matter than those on the insect-basal mix. Consequently intake of digestible energy (i.e. energy absorbed) was not significantly different between diets. Mean retention time (MRT, the mean time a marker remains in the tract) of a large particle marker was shorter on the plant-basal mix, reflecting its higher intake, but MRT of a solute marker was not significantly different between diets. Consequently the solute marker was retained longer than the particle marker on the plant-basal mix, indicating selective retention of solutes and very small particles in the caecum on this diet. This was confirmed by a higher proportion of small particles in the caecum than the distal colon of road-killed I. macrourus. Thus the main responses by I. macrourus to the plant-basal mix appeared to be an increase in gastrointestinal tract capacity (from radiographic evidence), selective retention of solutes and very small particles in the caecum, and facilitated passage of less tractable large particles through the colon. As a consequence, food intake was higher on the plant-basal mix, which compensated for its lower digestibility, and intake of digestible energy was similar to that on the insect-basal mix. This considerable flexibility of the morphologically rather simple digestive tract of northern brown bandicoots helps to explain their ability to cope with naturally variable diets consisting of mainly invertebrates in summer to much more plant and fungal material in winter, and to survive in nutritionally dynamic environments such as heathlands where there can be dramatic changes in food type and availability following periodic wildfires. Accepted: 14 April 1999     

Milk composition in the northern brown bandicoot, Isoodon macrourus (Peramelidae, Marsupialia)

Milk samples were obtained at regular intervals throughout lactation from northern brown bandicoots, Isoodon macrourus, in captivity. Total concentration of milk solids was initially 7% (w/w) and increased linearly to 45% (w/w) by 55 days. Carbohydrate, lipid and protein concentrations increased from about 2% (w/w) to about 7-8% (w/w) at 30 days. Thereafter they diverged, with lipid increasing to between 25-30% (w/w) at 56 days, protein reaching maximal values of 10-15% (w/w) at just over 40 days and carbohydrate gradually declining to about 5% (w/w) at 56 days before a rapid fall to 1-2% (w/w) at the completion of lactation. The milk of the bandicoot exhibits a similar pattern of change during the course of lactation to that shown by other marsupials.     

Monitoring physiological stress in semi-free ranging populations of an endangered Australian marsupial,the Greater Bilby (Macrotis lagotis)

Rapid and reliable physiological evaluation of stress is necessary for understanding the potential impacts of environmental changes on managed populations of threatened mammals. In situ populations of Australia’s iconic marsupial, the greater bilby (Macrotis lagotis), are nearing extinction due to the impacts of competition and predation by feral animals and unpredictable climatic events (summer heat waves). In this study, we focussed our aim to identify a non-invasive method to measure adrenal activity in the species and also to identify potential factors that should be considered when comparing physiological stress in semi-free ranging populations of the species. We validated an enzyme immunoassay (EIA) for detecting fecal cortisol metabolites (FCM) from fresh fecal pellets taken from bilbies within four captive sites and two semi-free ranging populations around Queensland and New South Wales, Australia. Our FCM EIA successfully detected the ‘raise and fall’ pattern of FCM levels within 3 days of exogenous adrenocorticotropic hormone (ACTH) challenge. Mean FCM levels differed significantly between the captive sites and between sexes. All male bilbies grouped outdoor in captivity expressed the highest mean FCM level in comparison to all captive males that were housed individually or as groups indoors. Also, semi-free ranging bilbies expressed higher mean FCM levels than the captive bilbies. Overall, our study successfully validated a non-invasive tool for monitoring physiological stress in the greater bilby. In the future, it will be worthwhile to consider factors such as housing conditions, sex and location when comparing the adrenal sensitivity to environmental changes, to help evaluate the success of management interventions (such as predator free enclosures) and support the survival of the species.     

Genetic population structure of the Greater Bilby Macrotis lagotis, a marsupial in decline

The Greater Bilby has shown a rapid decline in range during this century and now occupies only a small isolated area in south-western Queensland (QLD) and a larger, but mostly low-density area in the north-western deserts of the Northern Territory (NT) and Western Australia (WA). We have examined variation in the control region of mitochondrial DNA (mtDNA) and at nine microsatellite loci in order to investigate the extent of current and historical subdivision across the species range, and to provide a preliminary assessment of genetic structuring and mating system on a finer scale within the QLD population. Both mtDNA and microsatellite loci had substantial variation within and among populations, with mtDNA divergence being greater between QLD and NT than between NT and WA. The QLD population had two unique and divergent mtDNA lineages, but there was no evidence for strong phylogeographical structure across the range. The available evidence suggests that the bilby should be considered as a single Evolutionarily Significant Unit consisting of multiple Management Units. Augmentation of the remnant QLD population from the NT does not appear necessary at this stage, at least not on genetic grounds. Finer-scale analysis of microsatellite variation for two QLD colonies revealed a deficiency of heterozygotes and significantly greater relatedness within than between colonies. However, structuring was observed only for males; relatedness values for females did not depart from those expected under panmixia. Parentage exclusion analysis for one colony allowed the construction of a partial pedigree which indicated strong polygyny, with one male fathering all but one of the eight offspring assigned. The extent to which fine-scale genetic structuring and differences between sexes is due to sex-biased dispersal vs. effects of mating system remain to be determined.     

Effects of long-term captivity on thermoregulation,metabolism and ventilation of the southern brown bandicoot (Marsupialia: Peramelidae)

Thermoneutral metabolic and ventilatory parameters were measured every 3 months over 2 years for southern brown bandicoots held in captivity, and from a nearby reserve. Captive bandicoots were 130 g (9.9%) heavier than wild bandicoots. Long-term captivity had no effect on body temperature, basal metabolic rate (oxygen consumption), thermal conductance or respiratory ventilation, but there was an effect on carbon dioxide production, respiratory exchange ratio and total evaporative water loss (values were between 15 and 25% higher for captive than for wild bandicoots). Diet may be influencing these aspects of captive bandicoot physiology; the diet of captive bandicoots would be considerably different to that of wild bandicoots. Water availability seems to have a minimal effect. This study has important implications regarding physiological measurement for captive and wild mammals. For bandicoots at least, captive animals are equivalent to wild animals for some physiological parameters at thermoneutrality (body temperature, resting metabolic rate and thermal conductance), but not others.     

The effect of supplementary food on home range of the southern brown bandicoot,Isoodon obesulus (Marsupialia: Peramelidae)

The study investigated the relationship between home range and food abundance in a population of the southern brown bandicoot. Isoodon obesulus, in Western Australia. Home range areas were estimated seven times between 1986 and 1988 by live-trapping, spool-and-line devices and fluorescent pigment tracking. The abundance of invertebrate food was measured simultaneously by placing pitfall traps within the home ranges of individual animals, and by sampling invertebrates in topsoil and litter. Home range areas tended to be negatively correlated with food abundance, especially in the autumn and winter of 1986 and 1987. The influence of food on home range was investigated further in September 1988 by providing eight individual I. obesulus with a supplementary food mixture. Contrary to expectation, the added food caused an increase in home range area, home range overlap and displacement, as well as an influx of new individuals to food stations. In contrast, home range parameters in control (non-fed) individuals changed little during the experiment. The shuffling of home ranges due to feeding suggests that the home range system of I. obesulus is relatively flexible, with individuals monitoring and exploiting resources in an opportunistic manner. In contrast to previous studies, we found no evidence that I. obesulus was territorial. We speculate that individuals may be territorial at low population density if resources are defendable and intruder pressure is low, but occupy overlapping ranges if population density is high.     

An electrophoretic comparison of Physaloptera Rudolphi, 1819 (Nematoda: Physalopteridae) from two species of Australian bandicoot (Marsupialia: Peramelidae)

An electrophoretic study was conducted on nematodes of the genus Physaloptera that occur in the stomachs of two species of Australian bandicoot, Perameles nasuta and P. gunnii. Each nematode was genetically characterised at 28 enzymes encoding a presumptive 30 loci. No fixed genetic differences were detected between the nematodes in P. gunnii from two localities. A comparison of nematodes from the two host species, however, revealed fixed genetic differences at 15 (50%) loci. This suggests that each host species is infected by a different species of Physaloptera.     

Effect of season on thermoregulation, metabolism and ventilation of the southern brown bandicoot Isoodon obesulus (Marsupialia: Peramelidae)

Seasonal variation in various thermoregulatory, metabolic and ventilatory parameters was examined for southern brown bandicoots (Isoodon obesulus fusciventer) from a Mediterranean climate near Perth, Western Australia. There was significant seasonal variation over the four annual seasons at thermoneutrality (Ta=30 degrees C) in body temperature, oxygen consumption, carbon dioxide production, respiratory exchange ratio, total evaporative water loss, wet and dry thermal conductance and tidal volume but not mass, ventilatory frequency, minute volume or oxygen extraction efficiency. Only carbon dioxide production and respiratory exchange ratio showed an annual pattern that was significantly related to season, with both being significantly higher in winter, presumably as a result of greater and higher quality food availability.     

Sex chromosome elimination,X chromosome inactivation and reactivation in the southern brown bandicoot Isoodon obesulus (Marsupialia: Peramelidae)

Cytogenetic studies have shown that bandicoots (family Peramelidae) eliminate one X chromosome in females and the Y chromosome in males from some somatic tissues at different stages during development. The discovery of a polymorphism for X-linked phosphoglycerate kinase (PGK-1) in a population of Isoodon obesulus from Mount Gambier, South Australia, has allowed us to answer a number of long standing questions relating to the parental source of the eliminated X chromosome, X chromosome inactivation and reactivation in somatic and germ cells of female bandicoots. We have found no evidence of paternal PGK-1 allele expression in a wide range of somatic tissues and cell types from known female heterozygotes. We conclude that paternal X chromosome inactivation occurs in bandicoots as in other marsupial groups and that it is the paternally derived X chromosome that is eliminated from some cell types of females. The absence of PGK-1 paternal activity in somatic cells allowed us to examine the state of X chromosome activity in germ cells. Electrophoresis of germ cells from different aged pouch young heterozygotes showed only maternal allele expression in oogonia whereas an additional paternally derived band was observed in pre-dictyate oocytes. We conclude that reactivation of the inactive X chromosome occurs around the onset of meiosis in female bandicoots. As in other mammals, late replication is a common feature of the Y chromosome in male and the inactive X chromosome in female bandicoots. The basis of sex chromosome loss is still not known; however later timing of DNA synthesis is involved. Our finding that the paternally derived X chromosome is eliminated in females suggests that late DNA replication may provide the imprint for paternal X inactivation and the elimination of sex chromosomes in bandicoots.     

Effects of temperature on metabolism,ventilation, and oxygen extraction in the southern brown bandicoot Isoodon obesulus (Marsupialia: Peramelidae)

The effects of ambient temperatures (T(a)) from 10 degrees to 35 degrees C on metabolism, ventilation, and oxygen extraction were examined for the southern brown bandicoot (Isoodon obesulus). Oxygen consumption (VO2) followed the pattern typical for endotherms, decreasing with increasing T(a) from 10 degrees to 25 degrees C. It did not significantly change between Ta=25 degrees and 35 degrees C (the thermoneutral zone). VO2 was approximately 2.4 times higher at Ta=10 degrees C (0.967 mL O(2) g(-1) h(-1)) compared with basal (0.410 mL O(2) g(-1) h(-1)) at Ta=30 degrees C. While the metabolic rates of the bandicoots were basal at Ta=30 degrees C, respiratory frequency (f(R)) was 24.6 breaths min(-1), tidal volume (V(T)) was 7.79 mL, minute volume (V(I)) was 191.3 mL min(-1), and oxygen extraction efficiency (EO2) was 26.8%. Increased VO2 at Ta< or =25 degrees C was associated with a large increase in V(I) due to increases in V(T) and f(R). A greater proportion of the change was due to the increase in tidal volume. EO2 was constant at approximately 26% for all T(a) up to and including 30 degrees C. At Ta=35 degrees C, EO2 decreased to 17.7%, f(R) increased to 35.6 breaths min(-1), and V(T) decreased to 7.22 mL. The metabolic and ventilatory physiology of the southern brown bandicoot are typical of an unspecialized medium-sized marsupial.     

Y Chromosome mosaicism in pouch young of the marsupial,greater glider (Marsupialia: Petauridae)

Y chromosome elimination was studied in three tissues from 13 pouch young greater gliders. There was no sex chromosome loss from the liver, spleen or bone marrow of female pouch young ranging in age from approximately 4 to 80 days. All liver cells in a 15 day old male were XY but only 75 to 80% of the cells were found to be XY in older pouch young. The Y chromosome was eliminated from a higher percentage of spleen cells, with 45 to 50% of the cells retaining the Y chromosome in 60-100 day old animals. — Y chromosome elimination in greater gliders appears to most closely resemble the X and Y chromosome elimination system of the marsupial bandicoots. There are no clear resemblances to the kinds of sex chromosome elimination which occur in eutherian mammals.     

Body temperature variation of free-ranging and captive southern brown bandicoots Isoodon obesulus (Marsupialia: Peramelidae)

To investigate patterns of thermoregulation in free-ranging and captive southern brown bandicoots Isoodon obesulus, we measured abdominal body temperature (T_b) of five free-ranging bandicoots over 42 days using implanted data loggers and T_b of three captive bandicoots over 3 months using implanted temperature-sensitive radio transmitters. Bandicoots in the wild had a mean T_b of 36.5±1.0 °C (range 33.4–39.8 °C) and showed a pronounced nychthemeral pattern with two distinct temperature phases. T_b increased at 13:30±2.6 h each day and remained high for 10.65±2.07 h, suggesting a crepuscular and early evening activity pattern. Daily T_b variation of I. obesulus would save considerable energy by reducing daytime thermoregulatory costs in the wild. Captive bandicoots had a similar mean body temperature (36.9±0.2°C) and range (33.0–39.9°C) as free-ranging bandicoots. However, the nychthemeral T_b pattern of captive bandicoots was different from free-ranging bandicoots, with a less pronounced daily cycle and the nocturnal rise in T_b occurring mainly at sunset and the daily decline occurring mainly at dawn.     

Klossiella quimrensis (Apicomplexa: Klossiellidae) causes renal coccidiosis in western barred bandicoots Perameles bougainville (Marsupialia: Peramelidae) in Western Australia

Previous studies have described a range of Klossiella species parasitic in marsupial hosts. Klossiella quimrensis is the etiologic agent of renal coccidiosis in the peramelid marsupial hosts Isoodon obesulus and Perameles gunnii in Eastern Australia, but there is no previous report of klossiellosis in Western Australian peramelids. This study describes klossiellosis diagnosed by histology of renal tissue sections collected during necropsy of 20 Perameles bougainville between 2000 and 2005. Sporonts, sporoblasts, and macrogametes were identified within parasitophorous vacuoles of epithelial cells located near the renal corticomedullary junction. The prevalence of renal coccidiosis in P. bougainville diagnosed by renal histology is estimated at 30%. Only a single unsporulated sporocyst was detected by examination of cystocentesis-collected urine, indicating that microscopic evaluation of urine samples is an insensitive diagnostic test for detection of K. quimrensis in P. bougainville. This infection in P. bougainville is indirectly associated with mild multifocal interstitial lymphohistiocytic nephritis and is likely to be only minimally pathogenic in otherwise healthy individuals. Our study also extends the host and geographic range of K. quimrensis to include P. bougainville and Western Australia.     

Morphological and molecular characteristics of a species of Hepatozoon Miller, 1908 (Apicomplexa: Adeleorina) from the blood of Isoodon obesulus (Marsupialia: Peramelidae) in Western Australia

Examination of blood films as part of a study to assess the health status of the southern brown bandicoot Isoodon obesulus (Shaw) in Western Australia revealed the gamonts of a haemogregarine parasite in some samples, the first to be recognised in a bandicoot in this state. Light microscope morphological characteristics and partial sequence of the 18S rRNA gene were used to describe these organisms. Morphological characters did not differentiate the organism in the current study from previously reported Hepatozoon peramelis (Welsh & Dalyell, 1909). Phylogenetic analysis has not previously been reported for any species of Hepatozoon from Australian marsupials and consequently could not be used to confirm the identity of the organism in the current study as that described in the 1900s. If this organism is H. peramelis, then it has a wide distribution, being found in three species of bandicoot, in western and eastern Australia and the in island state of Tasmania.