Review: Comparative methane production in mammalian herbivores.

Methane (CH4) production is a ubiquitous, apparently unavoidable side effect of fermentative fibre digestion by symbiotic microbiota in mammalian herbivores. Here, a data compilation is presented of in vivo CH4 measurements in individuals of 37 mammalian herbivore species fed forage-only diets, from the literature and from hitherto unpublished measurements. In contrast to previous claims, absolute CH4 emissions scaled linearly to DM intake, and CH4 yields (per DM or gross energy intake) did not vary significantly with body mass. CH4 physiology hence cannot be construed to represent an intrinsic ruminant or herbivore body size limitation. The dataset does not support traditional dichotomies of CH4 emission intensity between ruminants and nonruminants, or between foregut and hindgut fermenters. Several rodent hindgut fermenters and nonruminant foregut fermenters emit CH4 of a magnitude as high as ruminants of similar size, intake level, digesta retention or gut capacity. By contrast, equids, macropods (kangaroos) and rabbits produce few CH4 and have low CH4 : CO2 ratios for their size, intake level, digesta retention or gut capacity, ruling out these factors as explanation for interspecific variation. These findings lead to the conclusion that still unidentified host-specific factors other than digesta retention characteristics, or the presence of rumination or a foregut, influence CH4 production. Measurements of CH4 yield per digested fibre indicate that the amount of CH4 produced during fibre digestion varies not only across but also within species, possibly pointing towards variation in microbiota functionality. Recent findings on the genetic control of microbiome composition, including methanogens, raise the question about the benefits methanogens provide for many (but apparently not to the same extent for all) species, which possibly prevented the evolution of the hosting of low-methanogenic microbiota across mammals.

A continent-wide analysis of the shade requirements of red and western grey kangaroos.

Foraging time may be constrained by a suite of phenomena including weather, which can restrict a species' activity and energy intake. This is recognized as pivotal for many species whose distributions are known to correlate with climate, including kangaroos, although such impacts are rarely quantified. We explore how differences in shade seeking, a thermoregulatory behavior, of 2 closely-related kangaroo species, Macropus rufus (red kangaroos) and M. fuliginosus (western grey kangaroos), might reflect differences in their distributions across Australia. We observed foraging and shade-seeking behavior in the field and, together with local weather observations, calculated threshold radiant temperatures (based on solar and infrared radiant heat loads) over which the kangaroos retreated to shade. We apply these calculated tolerance thresholds to hourly microclimatic estimates derived from daily-gridded weather data to predict activity constraints across the Australian continent over a 10-year period. M. fuliginosus spent more time than M. rufus in the shade (7.6 ± 0.7 h versus 6.4 ± 0.9 h) and more time foraging (11.8 ± 0.5 h vs. 10.0 ± 0.6 h), although total time resting was equivalent (∼8.2 h). M. rufus tolerated 19°C higher radiant temperatures than M. fuliginosus (89°C versus 70°C radiant temperature). Across Australia, we predicted M. fuliginosus to be more restricted to shade than M. rufus, with higher absolute shade requirements farther north. These results corroborate previous findings that M. rufus is more adept at dealing with heat than M. fuliginosus and indicate that M. rufus is less dependent on shade on a continental scale.

Energetic costs of mange in wolves estimated from infrared thermography.

Parasites, by definition, extract energy from their hosts and thus affect trophic and food web dynamics even when the parasite may have limited effects on host population size. We studied the energetic costs of mange (Sarcoptes scabiei) in wolves (Canis lupus) using thermal cameras to estimate heat losses associated with compromised insulation during the winter. We combined the field data of known, naturally infected wolves with a data set on captive wolves with shaved patches of fur as a positive control to simulate mange-induced hair loss. We predict that during the winter in Montana, more severe mange infection increases heat loss by around 5.2-12 MJ per night (1,240-2,850 kcal, or a 65-78% increase) for small and large wolves, respectively, accounting for wind effects. To maintain body temperature would require a significant proportion of a healthy wolf's total daily energy demands (18-22 MJ/day). We also predict how these thermal costs may increase in colder climates by comparing our predictions in Bozeman, Montana to those from a place with lower ambient temperatures (Fairbanks, Alaska). Contrary to our expectations, the 14°C differential between these regions was not as important as the potential differences in wind speed. These large increases in energetic demands can be mitigated by either increasing consumption rates or decreasing other energy demands. Data from GPS-collared wolves indicated that healthy wolves move, on average, 17 km per day, which was reduced by 1.5, 1.8, and 6.5 km for light, medium, and severe hair loss. In addition, the wolf with the most hair loss was less active at night and more active during the day, which is the converse of the movement patterns of healthy wolves. At the individual level, mange infections create significant energy demands and altered behavioral patterns, this may have cascading effects on prey consumption rates, food web dynamics, predator-prey interactions, and scavenger communities.

Environmental osmolality influences sperm motility activation in an anuran amphibian.

Evolutionary theory predicts that selection will favour sperm traits that maximize fertilization success in local fertilization environments. In externally fertilizing species, osmolality of the fertilization medium is known to play a critical role in activating sperm motility, but there remains limited evidence for adaptive responses to local osmotic environments. In this study, we used a split-sample experimental design and computer-assisted sperm analysis to (i) determine the optimal medium osmolality for sperm activation (% sperm motility and sperm velocity) in male common eastern froglets (Crinia signifera), (ii) test for among-population variation in percentage sperm motility and sperm velocity at various activation-medium osmolalities and (iii) test for among-population covariation between sperm performance and environmental osmolality. Frogs were obtained from nine populations that differed in environmental osmolality, and sperm samples of males from different populations were subjected to a range of activation-medium osmolalities. Percentage sperm motility was optimal between 10 and 50 mOsm kg(-1) , and sperm velocity was optimal between 10 and 100 mOsm kg(-1) , indicating that C. signifera has evolved sperm that can function across a broad range of osmolalities. As predicted, there was significant among-population variation in sperm performance. Furthermore, there was a significant interaction between activation-medium osmolality and environmental osmolality, indicating that frogs from populations with higher environmental osmolality produced sperm that performed better at higher osmolalities in vitro. This finding may reflect phenotypic plasticity in sperm functioning, or genetic divergence resulting from spatial variation in the strength of directional selection. Both of these explanations are consistent with evolutionary theory, providing some of the first empirical evidence that local osmotic environments can favour adaptive sperm motility responses in species that use an external mode of fertilization.

Energy, water and space use by free-living red kangaroos Macropus rufus and domestic sheep Ovis aries in an Australian rangeland.

We used doubly labelled water to measure field metabolic rates (FMR) and water turnover rates (WTR) in one of Australia's largest native herbivores, the red kangaroo (Macropus rufus) and one of Australia's dominant livestock species, the wool-breed Merino sheep, under free-living conditions in a typical Australian rangeland. Also, we used GPS technology to examine animal space use, along with the comparisons of urine concentration, diet, diet digestibility, and subsequent grazing pressures. We found smaller space-use patterns than previously reported for kangaroos, which were between 14 and 25 % those of sheep. The FMR of a 25-kg kangaroo was 30 % that of a 45-kg sheep, while WTR was 15 % and both were associated with smaller travel distances, lower salt intakes, and higher urine concentration in kangaroos than sheep. After accounting for differences in dry matter digestibility of food eaten by kangaroos (51 %) and sheep (58 %), the relative grazing pressure of a standard (mature, non-reproductive) 25-kg kangaroo was 35 % that of a 45-kg sheep. Even for animals of the same body mass (35 kg), the relative grazing pressure of the kangaroo was estimated to be only 44 % that of the sheep. After accounting for the energetic costs of wool growth by sheep, the FMRs of our sheep and kangaroos were 2-3 times their expected BMRs, which is typical for mammalian FMR:BMRs generally. Notably, data collected from our free-living animals were practically identical to those from animals confined to a semi-natural enclosure (collected in an earlier study under comparable environmental conditions), supporting the idea that FMRs are relatively constrained within species.

No effect of short-term exposure to high-fibre diets on the gastrointestinal morphology of layer hens (Gallus gallus domesticus): body reserves are used to manage energy deficits in favour of phenotypic plasticity.

Using layer hens, Gallus gallus domesticus, we compared the digestive capabilities of birds on a low-fibre diet (LF, 8.49% neutral detergent fibre; NDF), with those fed a high-fibre diet balanced for energy and protein to match the LF diet (high fibre balanced, HFB; NDF = 15.61%) and those fed a high fibre unbalanced (HFU) diet (NDF = 16.68%). The HFU diet had the lowest apparent dry matter (DM) metabolisability at 58.14 ± 6.46%, followed by HFB, 65.87 ± 3.50 and the LF diet, 70.49 ± 7.07%. Despite significant differences between apparent DM metabolisabilities of LF and HFU diets, no morphometric changes in the gastrointestinal tract (GIT) of layer hens were observed (including crop, gizzard, proventriculus, liver, large intestine, paired caeca and small intestine). Conversely, body mass losses were recorded for animals on HFU diet, while those on the LF and HFB diets actually gained body mass over the 14-day trials. We suggest that the body mass losses seen in the animals fed HFU diets were attributed to losses in adipose tissue, but this was not quantified. Assuming body mass losses were mainly in adipose tissue, we propose that adipose may act to buffer environmental challenges like shortfalls in nutrient acquisition when dietary energy requirements are not met. Compared with smaller birds (e.g. quail), the larger body size of the layer hens may offer them a greater safety margin in terms of body energy reserves before changes in the GIT might be needed to redress energy deficits associated with hard-to-digest, high-fibre diets.

Energy and water use by invasive goats (Capra hircus) in an Australian rangeland, and a caution against using broad-scale allometry to predict species-specific requirements.

Feral goats (Capra hircus) are ubiquitous across much of Australia's arid and semi-arid rangelands, where they compete with domestic stock, contribute to grazing pressure on fragile ecosystems, and have been implicated in the decline of several native marsupial herbivores. Understanding the success of feral goats in Australia may provide insights into management strategies for this and other invasive herbivores. It has been suggested that frugal use of energy and water contributes to the success of feral goats in Australia, but data on the energy and water use of free-ranging animals are lacking. We measured the field metabolic rate and water turnover rate of pregnant and non-pregnant feral goats in an Australian rangeland during late summer (dry season). Field metabolic rate of pregnant goats (601 ± 37 kJ kg(-0.73)d(-1)) was 1.3 times that of non-pregnant goats (456 ± 24 kJ kg(-0.73)d(-1)). The water turnover rate of pregnant goats (228 ± 18 mL kg(-0.79)d(-1)) was also 1.3 times that of non-pregnant goats (173 ± 18 kg(-0.79)d(-1)), but the difference was not significant (P=0.07). There was no significant difference in estimated dry matter digestibility between pregnant and non-pregnant goats (mean ca. 58%), blood or urine osmolality, or urine electrolyte concentrations, indicating they were probably eating similar diets and were able to maintain osmohomeostasis. Overall, the metabolic and hygric physiology of non-pregnant goats conformed statistically to the predictions for non-marine, non-reproductive placental mammals according to both conventional and phylogenetically independent analyses. That was despite the field metabolic rate and estimated dry matter intake of non-pregnant goats being only 60% of the predicted level. We suggest that general allometric analyses predict the range of adaptive possibilities for mammals, but that specific adaptations, as present in goats, result in ecologically significant departures from the average allometric curve. In the case of goats in the arid Australian rangelands, predictions from the allometric regression would overestimate their grazing pressure by about 40% with implications for the predicted impact on their local ecology.

Energy requirements of the red kangaroo (Macropus rufus): impacts of age, growth and body size in a large desert-dwelling herbivore.

Generally, young growing mammals have resting metabolic rates (RMRs) that are proportionally greater than those of adult animals. This is seen in the red kangaroo ( Macropus rufus), a large (>20 kg) herbivorous marsupial common to arid and semi-arid inland Australia. Juvenile red kangaroos have RMRs 1.5-1.6 times those expected for adult marsupials of an equivalent body mass. When fed high-quality chopped lucerne hay, young-at-foot (YAF) kangaroos, which have permanently left the mother's pouch but are still sucking, and recently weaned red kangaroos had digestible energy intakes of 641+/-27 kJ kg(-0.75) day(-1) and 677+/-26 kJ kg(-0.75) day(-1), respectively, significantly higher than the 385+/-37 kJ kg(-0.75) day(-1) ingested by mature, non-lactating females. However, YAF and weaned red kangaroos had maintenance energy requirements (MERs) that were not significantly higher than those of mature, non-lactating females, the values ranging between 384 kJ kg(-0.75) day(-1) and 390 kJ kg(-0.75) day(-1) digestible energy. Importantly, the MER of mature female red kangaroos was 84% of that previously reported for similarly sized, but still growing, male red kangaroos. Growth was the main factor affecting the proportionally higher energy requirements of the juvenile red kangaroos relative to non-reproductive mature females. On a good quality diet, juvenile red kangaroos from permanent pouch exit until shortly after weaning (ca. 220-400 days) had average growth rates of 55 g body mass day(-1). At this level of growth, juveniles had total daily digestible energy requirements (i.e. MER plus growth energy requirements) that were 1.7-1.8 times the MER of mature, non-reproductive females. Our data suggest that the proportionally higher RMR of juvenile red kangaroos is largely explained by the additional energy needed for growth. Energy contents of the tissue gained by the YAF and weaned red kangaroos during growth were estimated to be 5.3 kJ g(-1), within the range found for most young growing mammals.

How important is milk for near-weaned red kangaroos ( Macropus rufus) fed different forages?

Red kangaroos (Macropus rufus) are large (>20 kg) herbivorous marsupials common to the arid and semi-arid regions of inland Australia, where drought is frequent. Young-at-foot (YAF) red kangaroos are the age/size class usually most affected by drought. Kangaroos at this YAF stage are making the transition from a milk-based diet to one of herbivory and an inability to adequately digest high-fibre feeds may contribute to their high mortalities during drought. We examined the role of milk in the nutrition of YAF red kangaroos fed forages of different fibre content and evaluated it as an extra energy and/or nitrogen source. Milk intake had little impact on the digestion of herbage by YAF red kangaroos fed low-fibre chopped lucerne (alfalfa) hay. Organic matter (OM) intake was 210+/-20 g day(-1) and 228+/-22 g day(-1), respectively, by YAF fed lucerne and lucerne with milk. Apparent digestibility of lucerne OM was ca. 55%, regardless of milk intake. Fed lucerne, with and without milk, YAF sustained growth rates of ca. 45 g day(-1). Conversely, even with a milk supplement, YAF red kangaroos ingested only 90+/-11 g day(-1) of high-fibre chopped oaten hay, of which they digested only ca. 36%. Despite milk intake, YAF fed chopped oaten hay lost between 0 and 75 g body mass day(-1) and were in negative nitrogen balance (-0.40+/-0.11 g N day(-1)). On all diets nitrogen loss was primarily as endogenous nitrogen (urinary and faecal) rather than as dietary nitrogen. Endogenous nitrogen losses were elevated in YAF fed chopped oaten hay, primarily as non-dietary faecal nitrogen. Overall, when high-quality feed was available, YAF were not markedly dependent on milk. However, YAF fed poor-quality chopped oaten hay would require up to 540 ml day(-1) of late-stage kangaroo milk to attain intakes of energy and nitrogen, and hence growth rates, comparable with those YAF fed lucerne.

Thermoregulation in juvenile red kangaroos (Macropus rufus) after pouch exit: higher metabolism and evaporative water requirements.

The population dynamics of red kangaroos (Macropus rufus) in the Australian arid zone is tightly linked with environmental factors, which partly operate via the survival of juvenile animals. A crucial stage is the young-at-foot (YAF) stage when kangaroos permanently exit the pouch. We have examined the thermal biology of YAF red kangaroos during ages from permanent pouch exit until weaning. Over a wide range of environmental temperatures (ambient temperature [T(a)] -5 degrees to 45 degrees C), YAF red kangaroos had a mass-specific metabolism that was generally twice that of adults, considerably higher than would be expected for an adult marsupial of their body size. The total energy requirements of YAF red kangaroos were 60%-70% of those of adult females, which were three times their size. Over the same range in T(a), YAF red kangaroos also had total evaporative water losses equal to those of adult females. At the highest T(a) (45 degrees C), differences were noted in patterns of dry heat loss (dry conductance) between YAF red kangaroos and adult females, which may partially explain the relatively high levels of evaporative cooling by YAF. By weaning age, young kangaroos showed little change in their basal energy and water requirements (at T(a) 25 degrees C) but did show reduced mass-specific costs in terms of energy and water use at extremes of T(a) (-5 degrees and 45 degrees C, respectively). In their arid environment, typified by unpredictable rainfall and extremes of T(a), young red kangaroos may need to remain close to water points, which, in turn, may restrict their ability to find the high-quality forage needed to meet their high energy demands.

Thermoregulation by kangaroos from mesic and arid habitats: influence of temperature on routes of heat loss in eastern grey kangaroos (Macropus giganteus) and red kangaroos (Macropus rufus).

We examined thermoregulation in red kangaroos (Macropus rufus) from deserts and in eastern grey kangaroos (Macropus giganteus) from mesic forests/woodlands. Desert kangaroos have complex evaporative heat loss mechanisms, but the relative importance of these mechanisms is unclear. Little is known of the abilities of grey kangaroos. Our detailed study of these kangaroos' thermoregulatory responses at air temperatures (T(a)) from -5 degrees to 45 degrees C showed that, while some differences occur, their abilities are fundamentally similar. Both species show the basic marsupial characteristics of relatively low basal metabolism and body temperature (T(b)). Within the thermoneutral zone, T(b) was 36.3 degrees + or - 0.1 degrees C (X + or - SE) in both species, and except for a small rise at T(a) 45 degrees C, T(b) was stable over a wide range of T(a). Metabolic heat production was 25% higher in red kangaroos at T(a) -5 degrees C. At the highest T(a) (45 degrees C), both species relied on evaporative heat loss (EHL) to maintain T(b); both panting and licking were used. The eastern grey kangaroo utilised panting (76% of EHL) as the principal mode of EHL, and while this was so for red kangaroos, cutaneous evaporative heat loss (CEHL) was significant (40% of EHL). CEHL appeared to be mainly licking, as evidenced from surface temperatures. Both species utilised peripheral vascular adjustments to control heat flow, as indicated by changes in dry conductance (C(dry)). At lower temperatures, C(dry) was minimal, but it increased significantly at T(a) just below T(b) (33 degrees C); in these conditions, the C(dry) of red kangaroos was significantly higher than that of eastern grey kangaroos, indicating a greater reliance on dry heat loss. Under conditions where heat flows into the body from the environment (T(a) 45 degrees C), there was peripheral vasoconstriction to reduce this inflow; C(dry) decreased significantly from the values seen at 33 degrees C in both kangaroos. The results indicated that, while both species have excellent thermoregulatory abilities, the desert red kangaroos may cope better with more extreme temperatures, given that they respond to T(a) 45 degrees C with lower respiratory evaporation than do the eastern grey kangaroos.

Ventilatory accommodation of oxygen demand and respiratory water loss in kangaroos from mesic and arid environments, the eastern grey kangaroo (Macropus giganteus) and the red kangaroo (Macropus rufus).

We studied ventilation in kangaroos from mesic and arid environments, the eastern grey kangaroo (Macropus giganteus) and the red kangaroo (Macropus rufus), respectively, within the range of ambient temperatures (T(a)) from -5 degrees to 45 degrees C. At thermoneutral temperatures (Ta=25 degrees C), there were no differences between the species in respiratory frequency, tidal volume, total ventilation, or oxygen extraction. The ventilatory patterns of the kangaroos were markedly different from those predicted from the allometric equation derived for placentals. The kangaroos had low respiratory frequencies and higher tidal volumes, even when adjustment was made for their lower basal metabolism. At Ta>25 degrees C, ventilation was increased in the kangaroos to facilitate respiratory water loss, with percent oxygen extraction being markedly lowered. Ventilation was via the nares; the mouth was closed. Differences in ventilation between the two species occurred at higher temperatures, and at 45 degrees C were associated with differences in respiratory evaporative heat loss, with that of M. giganteus being higher. Panting in kangaroos occurred as a graded increase in respiratory frequency, during which tidal volume was lowered. When panting, the desert red kangaroo had larger tidal volumes and lower respiratory frequencies at equivalent T(a) than the eastern grey kangaroo, which generally inhabits mesic forests. The inference made from this pattern is that the red kangaroo has the potential to increase respiratory evaporative heat loss to a greater level.