Ian D. Hume

The diet and digestive energetics of an Australian short-necked turtle, Emydura macquarii

We described the diet of Emydura macquarii, an omnivorous turtle from south-eastern Australia, compared its digestive performance on diets of fish or plants at two temperatures, and related how both diet and temperature affect its food selection in nature. Filamentous algae constituted 61% of the stomach content of E. macquarii. The turtles rarely fed on motile prey, but selected carrion from the lagoon bottom and terrestrial insects (Diptera, Hymenoptera and Coleoptera) trapped on the surface of the water. Digestive efficiency of E. macquarii was affected little by body temperature, in contrast to consumption rates and rates of passage which were strongly influenced by both temperature and diet. In combination, these responses resulted in a slower rate of digestion at 20 degrees C than at 30 degrees C. Digestive efficiency of E. macquarii on a herbivorous diet at 30 degrees C (49%) was about half that of turtles on a carnivorous diet (91%), but they had longer transit times (118 h on the plant diet versus 70 h). Lower consumption rates and longer mean retention times in turtles fed plants compared those fed fish relate to slower digestive processing of the plant. Rapid processing and higher consumption rates of fish by E. macquarii resulted in higher energy gains compared to turtles consuming plants (almost 100 times more energy at 30 degrees C). The laboratory results suggest that fish carrion and aquatic and terrestrial invertebrates are probably essential dietary items of E. macquarii in the wild, because its metabolic requirements cannot be met from aquatic macrophytes alone.

Digesta Retention and Digestive Performance in Sciurid and Microtine Rodents: Effects of Hindgut Morphology and Body Size

To examine the effects of hindgut morphology and body size on the digestive performance of rodents, we fed diets of three different fiber contents (7%, 22%, and 28%) to three species of sciurids-yellow-pine chipmunks (Eutamias amoenus) (55-60 g body mass), Columbian ground squirrels (Spermophilus columbianus) (600-700 g), and hoary marmots (Marmota caligata) (2,000-3,000 g)-and to Townsend voles (Microtus townsendii) (55-60 g), a microtine rodent. All species generally maintained body mass on all three diets, except that chipmunks lost mass on the high-fiber diet. We measured intake and digestibility of the three diets and compared rates of passage of fluid digesta (marked with Co-EDTA) and large particles (marked with Cr-mordanted plant cell walls) on the 7% fiber diet. For voles, the mean retention time (MRT ± SE) of fluid (14.8 ± 1.9 h) was greater (P = 0.02, paired t-test) than that of large particles (13.1 ± 2.4 h). This indicates separation of digesta phases in the proximal colon and selective retention of fluid digesta, probably in the cecum, which means that small, highly digestible food particles as well as bacteria are preferentially held in the cecum, which results in a more efective digestion by this system. In contrast, in the three sciurids, MRTs of fluid were the same or less than those of large particles, indicating no selective fluid retention. Among all species, MRTs increased with increasing body size. Dry matter digestibility was greater in the voles than in the chipmunks for all three diets and was greater in marmots than in voles for the low-fiber diet. Our results confirm the general prediction that voles can utilize more fibrous foods than chipmunks because of separation of digesta in a more complex proximal colon and selective retention of fluid in a larger cecum. Within the Sciuridae, increasingly larger body size (and hence a larger absolute gut capacity relative to metabolic rate) offsets the disadvantage of the relatively simple sciurid hindgut.

Behavioural, Morphological and Dietary Response of Rabbits to Predation Risk from Foxes

We report on the responses of wild European rabbits (Oryctolagus cuniculus) to a reduction in predation risk from red foxes (Vulpes vulpes) in a predator removal experiment in montane Australia. Specifically we tested whether rabbits in two sites with reduced fox numbers moved further from refuge than rabbits in two sites with abundant foxes. We then compared diet quality by analysing stomach contents, gut morphology and age-specific body mass to determine if release from predation risk enables rabbits to access higher quality food and hence attain higher body mass and condition. During spotlighting on three quarterly surveys in 1994-1995, rabbits in fox removal sites were observed, on average, three times further from refuge compared to rabbits at sites with foxes. However, this freedom to forage far from cover did not translate into a higher quality diet. Analysis of the nitrogen and neutral-detergent fibre content of stomach samples taken from a shot sample of rabbits at their peak densities after fox removal showed no differences in short-term diet quality of male or female rabbits due to fox removal. In contrast, analyses of gut morphologies, which reflect long-term fibre intake, suggested that rabbits in removal sites fed on a diet higher in fibre and hence of lower quality. This was possibly due to the large increases in rabbit density associated with fox removal. Despite this, male rabbits in fox removal sites were heavier for their age, had longer intestines, and heavier stomach and gut contents. We suggest that rabbits in fox removal sites compensated for the lower quality diet by increasing intake which enabled them to maintain higher age-specific body mass but only because predation risk was reduced. This result highlights the untenable link between resource limitation and predation risk.

Effects of habitat fragmentation on the demography, movements and social organisation of the eastern pygmy-possum (Cercartetus nanus) in northern New South Wales

A population of eastern pygmy-possums (Cercartetus nanus) was studied in northern New South Wales for almost 3 years. A total of 98 pygmy-possums was captured, of which 52 were captured only once. The sex ratio of the population did not differ significantly from parity. Mid-way through the study, 1.4 ha of the 4.0-ha study site was cleared. Pre-clearing capture rates in nest boxes averaged 33.5 ± 5.8 captures per 100 box checks per month, and the population was estimated by three methods to be at least 15–20 animals. There was no significant difference in body mass between adult males (23.7 ± 6.3 g) and adult females (27.1 ± 7.7 g). Males had significantly larger short-term home ranges (0.35 ± 0.14 ha) than females (0.14 ± 0.06 ha) and tended to move over greater distances each night. Breeding occurred from summer to early winter, and juveniles and sub-adults entered the population in autumn and winter. The mean number of pouch young was 3.9. The most likely minimum size at which juveniles left their mother was 9–11 g. Adult body mass and condition were highly variable over time, and did not appear to be related to either the breeding season or Banksia flowering. Fourteen pygmy-possums were found torpid during the study. Population troughs occurred in late winter and spring and were associated with low survival and/or seasonal migration, possibly linked to the cessation of Banksia flowering in July and the lack of alternative food sources at this time and/or increased use of nest boxes by Antechinus stuartii during late winter. Post-clearing, capture rates fell to 7.8 ± 1.6 captures per 100 box checks per month, the estimated population size fell to 5–8 animals, and there was an almost total lack of juvenile/sub-adult recruitment into the population. The results support concerns that the long-term survival of the eastern pygmy-possum in New South Wales is threatened by continued land clearing throughout much of its present range.

Physiology of Intermittent Feeding: Integrating Responses of Vertebrates to Nutritional Deficit and Excess*

Food intakes of wild animals may not match their requirements for nutrients and energy but may vary between periods of nutritional excess (hyperphagia) and nutritional deficit (hypophagia) at timescales that vary from days to months. We present a simple model of feeding patterns and requirements of vertebrates. Frequent fasts and high intakes are typical of endothermic predators and migratory birds, whereas slow cycles and long deficits typify feeding patterns of ectothermic predators and ungulates in seasonal environments. We propose that hyperphagia is constrained by the ability to increase processes of digestion, absorption, intermediary metabolism, net deposition in tissue, and excretion to match loads of digesta and metabolites. Hyperphagia on high‐quality diets is limited by the clearance of metabolites, whereas digestive tract capacity and flow limit consumption of low‐quality diets. Of all digestive strategies, small omnivores with simple digestive systems may be the most tolerant of frequent hyperphagia. Tolerance of hypophagia favors large endogenous stores or low mass‐specific rates of metabolism and reproductive output. Large animals may be most able to sustain reproduction during prolonged deficits in seasonal environments. Responses to excessive and deficient intakes of food are constrained by the length of the feeding cycle. Animals adapted to short feeding cycles may be best suited to unpredictable food supplies but at the energetic cost of maintaining spare capacity for digestion and absorption. Predictions of the response to food disruption are best evaluated in the context of body size, nutritional physiology, and life history of the species and the time for internal response.

Effects of diet change on carbon and nitrogen stable-isotope ratios in blood cells and plasma of the long-nosed bandicoot (Perameles nasuta)

Carbon (C) and nitrogen (N) stable isotopes offer a powerful tool for assessing the extent of tissue assimilation of dietary components. However, the method relies on knowledge of diet–tissue isotopic discrimination and how quickly diet shifts become apparent in various tissues. In the present study, blood plasma and blood cells, tissues that are easily obtained under field conditions, were used to validate the stable isotope method over a period of 4–5 weeks using captive long-nosed bandicoots (Perameles nasuta). Diet–tissue discrimination effects appeared to be small. For C, derived diet–tissue isotopic discriminations were 1.4‰ for blood plasma and –0.2‰ for blood cells. For N the values were 2.8‰ and 2.1‰, respectively, and were independent of the nitrogen content of the food. C and N turnover measurements in the blood plasma and cells of the bandicoots indicated that blood plasma provides dietary information integrated over a period of ~3 weeks, whereas blood cells give an impression of the assimilated diet over a period of as much as half a year. These turnover rates were low compared with the little information available for birds and eutherian mammals, and probably relate to the typically low metabolic rate of marsupials.

Effects of dietary fibre on digesta passage, nutrient digestibility, and gastrointestinal tract morphology in the granivorous Mongolian gerbil (Meriones unguiculatus).

To investigate digestive tract performance in Mongolian gerbils (Meriones unguiculatus), food intake and digestibility, digesta passage rate, and gastrointestinal tract morphology were measured in captive animals fed low‐ or high‐fibre diets. We used two markers (Co‐ethylene diamine tetra‐acetic acid for solutes and Cr‐mordanted cell walls for particles) to measure differential passage rates of digesta fractions in order to test for the presence of a colonic separation mechanism (CSM). Although dry‐matter intakes on the high‐fibre diet did not differ from those on the low‐fibre diet, digestibilities of dry matter, neutral‐detergent fibre, acid‐detergent fibre, crude protein, and crude fat were all significantly lower on the high‐fibre diet. Gross energy intake on the high‐fibre diet also did not differ from that on the low‐fibre diet, but energy lost in faeces was much higher than on the low‐fibre diet; thus, energy digestibility and digestible energy intake were significantly lower on the high‐fibre diet. The lengths and dry‐tissue masses of all segments of the gastrointestinal tract tended to enlarge in response to increased dietary fibre, but only the total tract contents, contents of the small intestine, and length and dry‐tissue mass of the caecum increased significantly. The mean retention time (MRT) of the particle marker was significantly greater than that of the solute marker on the low‐fibre but not the high‐fibre diet; the solute/particle differential retention ratio was 0.62 on the low‐fibre diet and 0.90 on the high‐fibre diet. Thus, there was no evidence for selective retention of the solute marker on either diet. The MRT of the particle marker was significantly lower on the high‐fibre diet and in the same direction as the MRT of the solute marker. These results suggest that the granivorous Mongolian gerbil has no CSM but can adjust its digestive tract capacity to accommodate greater quantities of low‐quality food.

Production of Milk and Nutrition of the Dependent Young of Free‐Ranging Koalas (Phascolarctos cinereus)

The production of milk by lactating females, and energy expenditure and foliage intake of their dependent young, were investigated in free‐ranging koalas. Koalas had the lowest mass‐specific daily milk‐energy production at peak lactation so far recorded in a mammal, but the duration of reproduction was 58% longer than the combined marsupial and eutherian average. As a consequence, the total energy input to reproduction in koalas was similar to that in other mammals. We propose that the prolonged lactation and low daily rate of energy transfer to the young by female koalas is an adaptation to the low energy availability from their diet of Eucalyptus foliage. Energy requirements (field metabolic rates) of young koalas were lower than those expected for typical marsupials (only 60% at permanent pouch exit), which may be a necessary preadaptation that allows the low rate of maternal energy transfer. However, the energy requirements of the adult females were no lower than expected for marsupials. This pattern of energy requirements and age resulted in a linear relationship between field metabolic rate and mass for the koalas in this population. Differences in milk production between the years of the study coincided with fluctuations in the availability of preferred young foliage, which suggests that lactational output by koalas may be flexible and affected by diet quality. Despite the interannual differences in milk production, growth of the young was similar in the two years.

Digestive performance and selective digesta retention in the long-nosed bandicoot, Perameles nasuta, a small omnivorous marsupial.

Bandicoots are opportunistic omnivores that feed on invertebrates, fungi and both epigeal and hypogeal plant parts. We examined the performance of the digestive tract of the long-nosed bandicoot (Perameles nasuta) in terms of intake and total digestibility, patterns of excretion of inert digesta markers, and likely sites of digesta retention, on two diets designed to mimic part of their natural plant and insect diets. On the insect diet (mealworm larvae), bandicoots virtually maintained body mass at a digestible energy intake of 511 kJ · kg-0.75 · day-1 and were in strongly positive nitrogen balance. In contrast, on the plant diet (shredded sweet potato), bandicoots ate only one-third as much digestible energy, lost 7% body mass, and were in negative nitrogen balance. Mean retention times of two particle markers on the plant diet (27.5 and 27.0 h) were more than double those on the insect diet (12.4 and 11.2 h), and on both diets the mean retention time of the fluid digesta marker was greater than those of the particle markers, indicating consistent selective retention of fluid digesta in the gut. It was seen radiographically than in mealwormfed bandicoots major sites of digesta retention were the distal colon and rectum, whereas in the sweet potato-fed animals the caecum and proximal colon were principal sites. It was concluded that retention of plant material in the caecum and proximal colon (the main sites of microbial digestion) and the preferential retention of fluid digesta (together with bacteria and small feed particles) in the caecum were important factors in the ability of bandicoots to switch between insect and plant foods, depending on relative availabilities, and thus to exploit nutritionally unpredictable environments.

Seasonal field energetics and water influx rates of the greater bilby (Macrotis lagotis)

Water and energy requirements of free-living male and female greater bilbies (Macrotis lagotis) were measured over two summers and two winters on Astrebla Downs National Park in far south-western Queensland, Australia, by means of the doubly labelled water method. Mean water influx rate of the bilby (mean body mass: summer 928 g; winter 848 g) did not differ between summer (63.1 mL day–1) and winter (53.1 mL day–1), but mean field metabolic rate was significantly higher during summer (617.2 kJ day–1) than in winter (480.3 kJ day–1). The comparatively low water influx rate of the bilby (significantly lower than that predicted for a 887-g marsupial: P < 0.001) indicated that bilbies have the ability to conserve water in the wild. In contrast, field metabolic rate of the bilby did not differ significantly from that predicted for a marsupial of its body mass (P = 0.999). Bilbies were able to obtain sufficient food and water to satisfy energy and water requirements in three out of the four study periods. However, they were in negative energy and water balance during one study period, suggesting that they are susceptible to nutrient and water stress. The relatively low body fat stores of bilbies in the wild also indicate that they are vulnerable to periods of low food availability. The metabolic strategies of the bilby are only partly suggestive of adaptation to arid conditions.