Functional interactions between coat structure and colour in the determination of solar heat load on arid living kangaroos in summer: balancing crypsis and thermoregulation.

Interactions of solar radiation with mammal fur are complex. Reflection of radiation in the visible spectrum provides colour that has various roles, including sexual display and crypsis, i.e., camouflage. Radiation that is absorbed by a fur coat is converted to heat, a proportion of which impacts on the skin. Not all absorption occurs at the coat surface, and some radiation penetrates the coat before being absorbed, particularly in lighter coats. In studies on this phenomenon in kangaroos, we found that two arid zone species with the thinnest coats had similar effective heat load, despite markedly different solar reflectances. These kangaroos were Red Kangaroos (Osphranter rufus) and Western Grey Kangaroos (Macropus fuliginosus).Here we examine the connections between heat flow patterns associated with solar radiation, and the physical structure of these coats. Also noted are the impacts of changing wind speed. The modulation of solar radiation and resultant heat flows in these coats were measured at wind speeds from 1 to 10 m s-1 by mounting them on a heat flux transducer/temperature-controlled plate apparatus in a wind tunnel. A lamp with a spectrum like solar radiation was used as a proxy for the sun. The integrated reflectance across the solar spectrum was higher in the red kangaroos (40 ± 2%) than in the grey kangaroos (28 ± 1%). Fur depth and insulation were not different between the two species, but differences occurred in fibre structure, notably in fibre length, fibre density and fibre shape. Patterns of heat flux within the species' coats occurred despite no overall difference in effective solar heat load. We consider that an overarching need for crypsis, particularly for the more open desert-adapted red kangaroo, has led to the complex adaptations that retard the penetrance of solar radiation into its more reflective fur.

The burden of size and growth for the juveniles of large mammalian herbivores: Structural and functional constraints in the feeding biology of juveniles relative to adults in red kangaroos, Osphranter rufus.

Juvenile mammals in their postweaning developmental stages face many challenges in transitioning to adulthood. Among large grazing species such as ruminant bovids and cervids, an overarching challenge is acquiring and processing sufficient nutrients to survive and grow, with a gut that may not yet be fully developed. Marsupial kangaroos of Australia face similar challenges; they also digest vegetation by fermentation in a large foregut. In red kangaroos, Osphranter rufus (=Macropus rufus), the dominant species of Australia's arid interior, females may breed continuously; however, juvenile recruitment to the adult population is irregular and coincident with sporadic rainfall.As compared with adult females, the nutritional requirements of juvenile O. rufus are high in relation to their body mass (BM), largely due to the cost of their rapid growth. We examined processes that juveniles have in their morphology, physiology, and behaviors to meet their elevated nutritional needs, by comparing recently weaned juveniles of both sexes and adult female O. rufus in their desert habitat. Features studied include relative body sizes, relative dimensions, and capacities of principal gut regions, the foregut, small intestine, caecum, and large intestine with rectum. Also examined were digesta attributes and rates of digesta excretion. Additionally, the rates of change in skull parameters and dental characteristics to maturity were assessed. Field determinations of diet choice were made for both age classes.In juveniles, the content masses of major gut structures were related to body mass (BM), as were those of adult females, that is, ~BM1.0. In both age classes, the digesta mass of the foreguts exceeded 75% of the total digesta mass. Diets of both juvenile and adult O. rufus largely focused on grasses. Juveniles had higher rates of digesta excretion while foraging than adults. In addition, the foregut contents in juveniles occupy proportionally less of the total gut than in adult females. Together, the higher excretion rate and smaller relative foregut of juveniles suggest that they necessarily focus on forage that can be rapidly digested, such as young, green grasses, or herbage.Comparison of the skulls of juveniles and adults revealed how this harvest can occur. Relative to BM, juveniles had skulls of larger volume than adults. Additionally, during growth the skull lengthens proportionally faster than increasing BM. By weaning, the dimensions of the incisor bite of juveniles neared those of adult females. The area of wear on premolars/molars increased only slowly relative to the development of incisors, further pointing to juveniles selecting more digestible forage than adults. The intermittent availability of such forage, principally young grasses, appears key to the significant recruitment into the O. rufus population in their arid habitat.

Thermal implications of interactions between insulation, solar reflectance, and fur structure in the summer coats of diverse species of kangaroo.

Not all of the solar radiation that impinges on a mammalian coat is absorbed and converted into thermal energy at the coat surface. Some is reflected back to the environment, while another portion is reflected further into the coat where it is absorbed and manifested as heat at differing levels. Substantial insulation in a coat limits the thermal impact at the skin of solar radiation, irrespective where in the coat it is absorbed. In coats with low insulation, the zone where solar radiation is absorbed may govern the consequent heat load on the skin (HL-SR). Thin summer furs of four species of kangaroo from differing climatic zones were used to determine how variation in insulation and in coat spectral and structural characteristics influence the HL-SR. Coat depth, structure, and solar reflectance varied between body regions, as well as between species. The modulation of solar radiation and resultant heat flows in these coats were measured at low (1 m s-1) and high (6 m s-1) wind speeds by mounting them on a heat flux transducer/temperature-controlled plate apparatus in a wind tunnel. A lamp with a spectrum similar to solar radiation was used as a proxy for the sun. We established that coat insulation was largely determined by coat depth at natural fur lie, despite large variations in fibre density, fibre diameter, and fur mass. Higher wind speed decreased coat insulation, but depth still determined the overall level. A multiple regression analysis that included coat depth (insulation), fibre diameter, fibre density, and solar reflectance was used to determine the best predictors of HL-SR. Only depth and reflectance had significant impacts and both factors had negative weights, so, as either insulation or reflectance increased, HL-SR declined, the larger impact coming from coat reflectance. This reverses the pattern observed in deep coats where insulation dominates over effects of reflectance. Across all coats, as insulation declined, reflectance increased. An increase in reflectance in the thinnest coats was not the sole reason for the limited rise in HL-SR. Higher reflectance should increase the depth of penetrance of solar radiation, thus increasing HL-SR. But in M. antilopinus and Macropus rufus, which had the highest of coat reflectances, penetrance was relatively shallow. This effect appears due to high fibre density (M. rufus) and major modifications in the fibre structure (M. antilopinus). The differing adaptations likely relate to the habitats of these species, desert in the case of M. rufus and monsoon tropical woodland with M. antilopinus.

The kangaroo's tail propels and powers pentapedal locomotion.

When moving slowly, kangaroos plant their tail on the ground in sequence with their front and hind legs. To determine the tail's role in this 'pentapedal' gait, we measured the forces the tail exerts on the ground and calculated the mechanical power it generates. We found that the tail is responsible for as much propulsive force as the front and hind legs combined. It also generates almost exclusively positive mechanical power, performing as much mass-specific mechanical work as does a human leg during walking at the same speed. Kangaroos use their muscular tail to support, propel and power their pentapedal gait just like a leg.

The fur of mammals in exposed environments; do crypsis and thermal needs necessarily conflict? The polar bear and marsupial koala compared.

The furs of mammals have varied and complex functions. Other than for thermoregulation, fur is involved in physical protection, sensory input, waterproofing and colouration, the latter being important for crypsis or camouflage. Some of these diverse functions potentially conflict. We have investigated how variation in cryptic colouration and thermal features may interact in the coats of mammals and influence potential heat inflows from solar radiation, much of which is outside the visible spectral range. The coats of the polar bear (Ursus maritimus) and the marsupial koala (Phascolarctus cinereus) have insulative similarities but, while they feature cryptic colouration, they are of contrasting colour, i.e. whitish and dark grey. The reflectance of solar radiation by coats was measured across the full solar spectrum using a spectroradiometer. The modulation of incident solar radiation and resultant heat flows in these coats were determined at a range of wind speeds by mounting them on a heat flux transducer/temperature-controlled plate apparatus in a wind tunnel. A lamp with a spectral distribution of radiation similar to the solar spectrum was used as a proxy for the sun. Crypsis by colour matching was apparent within the visible spectrum for the two species, U. maritimus being matched against snow and P. cinereus against Eucalyptus forest foliage. While reflectances across the full solar spectrum differed markedly, that of U. maritimus being 66 % as opposed to 10 % for P. cinereus, the heat influxes from solar radiation reaching the skin were similar. For both coats at low wind speed (1 m s(-1)), 19 % of incident solar radiation impacted as heat at the skin surface; at higher wind speed (10 m s(-1)) this decreased to approximately 10 %. Ursus maritimus and P. cinereus have high and comparable levels of fur insulation and although the patterns of reflectance and depths of penetrance of solar radiation differ for the coats, the considerable insulation limited the radiant heat reaching the skin. These data suggest that generally, if mammal coats have high insulation then heat flow from solar radiation into an animal is much restricted and the impact of coat colour is negligible. However, comparisons with published data from other species suggest that as fur insulation decreases, colour increasingly influences the heat inflow associated with solar radiation.

High muscle mitochondrial volume and aerobic capacity in a small marsupial (Sminthopsis crassicaudata) reveals flexible links between energy-use levels in mammals.

We investigated the muscle structure-function relationships that underlie the aerobic capacity of an insectivorous, small (~15 g) marsupial, Sminthopsis crassicaudata (Family: Dasyuridae), to obtain further insight into energy use patterns in marsupials relative to those in placentals, their sister clade within the Theria (advanced mammals). Disparate hopping marsupials (Suborder Macropodiformes), a kangaroo (Macropus rufus) and a rat-kangaroo (Bettongia penicillata), show aerobic capabilities as high as those of 'athletic' placentals. Equivalent muscle mitochondrial volumes and cardiovascular features support these capabilities. We examined S. crassicaudata to determine whether highly developed aerobic capabilities occur elsewhere in marsupials, rather than being restricted to the more recently evolved Macropodiformes. This was the case. Treadmill-trained S. crassicaudata attained a maximal aerobic metabolic rate ( or MMR) of 272 ml O2 min(-1) kg(-1) (N=8), similar to that reported for a small (~20 g), 'athletic' placental, Apodemus sylvaticus, 264 ml O2 min(-1) kg(-1). Hopping marsupials have comparable aerobic levels when body mass variation is considered. Sminthopsis crassicaudata has a basal metabolic rate (BMR) about 75% of placental values but it has a notably large factorial aerobic scope (fAS) of 13; elevated fAS also features in hopping marsupials. The of S. crassicaudata was supported by an elevated total muscle mitochondrial volume, which was largely achieved through high muscle mitochondrial volume densities, Vv(mt,f), the mean value being 14.0±1.33%. These data were considered in relation to energy use levels in mammals, particularly field metabolic rate (FMR). BMR is consistently lower in marsupials, but this is balanced by a high fAS, such that marsupial MMR matches that of placentals. However, FMR shows different mass relationships in the two clades, with the FMR of small (<125 g) marsupials, such as S. crassicaudata, being higher than that in comparably sized placentals, with the reverse applying for larger marsupials. The flexibility of energy output in marsupials provides explanations for this pattern. Overall, our data refute widely held notions of mechanistically closely linked relationships between body mass, BMR, FMR and MMR in mammals generally.

The high aerobic capacity of a small, marsupial rat-kangaroo (Bettongia penicillata) is matched by the mitochondrial and capillary morphology of its skeletal muscles.

We examined the structure-function relationships that underlie the aerobic capacities of marsupial mammals that hop. Marsupials have relatively low basal metabolic rates (BMR) and historically were seen as 'low energy' mammals. However, the red kangaroo, Macropus rufus (family Macropodidae), has aerobic capacities equivalent to athletic placentals. It has an extreme aerobic scope (fAS) and its large locomotor muscles feature high mitochondrial and capillary volumes. M. rufus belongs to a modern group of kangaroos and its high fAS is not general for marsupials. However, other hopping marsupials may have elevated aerobic capacities. Bettongia penicillata, a rat-kangaroo (family Potoroidae), is a small (1 kg), active hopper whose fAS is somewhat elevated. We examined the oxygen delivery system in its muscles to ascertain links with hopping. An elevated fAS of 23 provided a relatively high maximal aerobic oxygen consumption ( ) in B. penicillata; associated with this is a skeletal muscle mass of 44% of body mass. Ten muscles were sampled to estimate the total mitochondrial and capillary volume of the locomotor muscles. Values in B. penicillata were similar to those in M. rufus and in athletic placentals. This small hopper had high muscle mitochondrial volume densities (7.1-11.9%) and both a large total capillary volume (6 ml kg(-1) body mass) and total capillary erythrocyte volume (3.2 ml kg(-1)). Apparently, a considerable aerobic capacity is required to achieve the benefits of the extended stride in fast hopping. Of note, the ratio of to total muscle mitochondrial volume in B. penicillata was 4.9 ml O(2) min(-1) ml(-1). Similar values occur in M. rufus and also placental mammals generally, not only athletic species. If such relationships occur in other marsupials, a fundamental structure-function relationship for oxygen delivery to muscles likely originated with or before the earliest mammals.

Ventilation patterns in red kangaroos (Macropus rufus Desmarest): juveniles work harder than adults at thermal extremes, but extract more oxygen per breath at thermoneutrality.

Juvenile mortalities in large mammals are usually associated with environmental extremes, but the basis for this vulnerability is often unclear. Because of their high surface area to volume ratio, juveniles are expected to suffer greater thermal stresses relative to adults. Coping with thermal stress requires the ventilatory system to accommodate increases in oxygen demand and respiratory water loss at thermal extremes. Because juveniles are smaller than adults, these demands may set up different constraints on their ventilatory system. Using red kangaroos (Macropus rufus Desmarest), an arid zone species, we compared the ventilatory capabilities of juveniles and adults at thermoneutral (25 degrees C) and extreme (-5 degrees C and 45 degrees C) ambient temperatures. We used an allometry to compare juvenile to adult ventilation, using predicted body mass scaling exponents for oxygen consumption (0.75), respiration rate (-0.25), tidal volume (1.0), ventilation rate (0.75) and oxygen extraction (0.0). At ambient 25 degrees C, the juveniles' resting metabolic rate was 1.6 times that of the mature females (ml min(-1) kg(-0.75)), accommodated by significantly higher levels of oxygen extraction of 21.4+/-1.8% versus 16.6+/-1.9% (P<0.05). At thermal extremes, juveniles showed typical mammalian responses in their ventilation, mirrored by that of adults, including higher metabolic and ventilation rates at ambient -5 degrees C and shallow panting at 45 degrees C. However, at thermal extremes the juvenile kangaroos needed to work harder than adults to maintain their body temperature, with higher rates of ventilation at ambient -5 degrees C and 45 degrees C, accomplished via larger breaths at -5 degrees C and higher respiratory rates at 45 degrees C.

Dehydration, with and without heat, in kangaroos from mesic and arid habitats: different thermal responses including varying patterns in heterothermy in the field and laboratory.

Field data showing the daily patterns in body temperature (T(b)) of kangaroos in hot, arid conditions, with and without water, indicate the use of adaptive heterothermy, i.e. large variation in T(b). However, daily T(b) variation was greater in the Eastern Grey Kangaroo (Macropus giganteus), a species of mesic origin, than in the desert-adapted Red Kangaroo (Macropus rufus). The nature of such responses was studied by an examination of their thermal adjustments to dehydration in thermoneutral temperatures (25 degrees C) and at high temperature (45 degrees C) via the use of tame, habituated animals in a climate chamber. At the same level of dehydration M. rufus was less impacted, in that its T(b) changed less than that for M. giganteus while it evaporated significantly less water. At a T(a) of 45 degrees C with water restriction T(b) reached 38.9 +/- 0.3 degrees C in M. rufus compared with 40.2 +/- 0.4 degrees C for M. giganteus. The ability of M. rufus to reduce dry conductance in the heat while dehydrated was central to its superior thermal control. While M. giganteus showed more heterothermy, i.e. its T(b) varied more, this seemed due to a lower tolerance of dehydration in concert with a strong thermal challenge. The benefits of heterothermy to M. giganteus were also limited because of thermal (Q(10)) effects on metabolic heat production and evaporative heat loss. The impacts of T(b) on heat production were such that low morning T(b)'s seen in the field may be associated with energy saving, as well as water saving. Kangaroos respond to dehydration and heat similarly to many ungulates, and it is apparent that the accepted notions about adaptive heterothermy in large desert mammals may need revisiting.

Forage fibre digestion, rates of feed passage and gut fill in juvenile and adult red kangaroos Macropus rufus Desmarest: why body size matters.

Using red kangaroos Macropus rufus Desmarest, a large (>20 kg) marsupial herbivore, we compared the digestive capabilities of juveniles with those of mature, non-lactating females on high-quality forage (chopped lucerne Medicago sativa hay) of 43+/-1% neutral-detergent fibre (NDF) and poorer quality, high-fibre forage (chopped oaten Avena sativa hay) of 64+/-1% NDF. On chopped lucerne apparent dry matter (DM) digestibilities by young-at-foot (YAF) red kangaroos (an age that would normally be taking some milk from their mother), weaned juveniles and mature females were similar (55-59%). On chopped oaten hay apparent DM digestibility was lower in the YAF (35.9+/-2.3%) followed by weaned (43.4+/-2.8%) and mature females (44.6+/-1%). The digestion of NDF and its components (mainly cellulose and hemicellulose) was lowest among the YAF followed by weaned and then mature females. The YAF and weaned kangaroos could not sustain growth on the poor-quality diet, and appeared to be at or near maximal gut fill on both forages; the values being 114-122 g DM for YAF and 151-159 g DM for weaned kangaroos. Mean retention times (MRT) of particle and solute markers were significantly longer for the YAF and weaned kangaroos on oaten hay than on lucerne hay, and DM intake (g d(-1)) was approximately 50% lower on the oaten hay. In contrast, solute and particle MRTs in the mature females were not significantly affected by diet; they maintained DM intakes by increasing DM gut fill from 264+/-24 g on chopped lucerne to 427+/-26 g DM on chopped oaten hay. Clearly, the mature female kangaroos did not maximise gut fill on the high-quality forage, presumably as a consequence of their proportionally lower energy requirements compared with still-growing juveniles. Overall, we have provided the first mechanistic link between the physiological constraints faced by juvenile red kangaroos in relation to their drought-related mortalities, rainfall and forage quality.

Endogenous nitrogen excretion by red kangaroos (Macropus rufus): effects of animal age and forage quality.

Red kangaroos (Macropus rufus) are large (>20 kg) herbivorous marsupials common to arid and semiarid Australia. The population dynamics of red kangaroos are linked with environmental factors, operating largely through juvenile survival. A crucial period is the young-at-foot (YAF) stage, when juveniles have permanently left the mother's pouch but still take milk from a teat in the pouch. Forage quantity and quality have been implicated in drought-related mortalities of juvenile kangaroos. Here we compared how forage quality affected nitrogen (N) intake and excretion by YAF, weaned, and mature, nonlactating female red kangaroos. On high-quality forage (chopped lucerne hay, Medicago sativa) low in neutral-detergent fiber (43%+/-1%) and high in N (2.9%+/-0.1%), YAF and weaned kangaroos had ideal growth rates and retained 460-570 mg dietary N kg(-0.75) d(-1). But on poor-quality forage (chopped oaten hay, Avena sativa) high in neutral-detergent fiber (64%+/-1%) and low in N (0.9%+/-0.1%), YAF and weaned kangaroos could not sustain growth and were in negative N balance at -103+/-26 mg and -57+/-31 mg N kg(-0.75) d(-1), respectively. Notably, the YAF kangaroos excreted 64% of their truly digestible N intake from forage as nondietary fecal N (NDFN). By weaning age, the situation had improved, but the juveniles still lost 40% of their truly digestible N intake as NDFN compared with only 30% by the mature females. Our findings support field observations that forage quality, and not just quantity, is a major factor affecting the mortality of juvenile red kangaroos during drought.

Water use and the thermoregulatory behaviour of kangaroos in arid regions: insights into the colonisation of arid rangelands in Australia by the Eastern Grey Kangaroo (Macropus giganteus).

The Eastern Grey Kangaroo (Macropus giganteus) occurs mostly in the wetter regions of eastern Australia. However, in the past 30-40 years it has moved into more arid regions (rainfall < 250 mm), thus increasing its overlap zone with the xeric adapted Red Kangaroo (Macropus rufus). An increased access to water (supplied for domestic stock) may explain this range extension, but changes in the availability of preferred feed could also be involved. The water use, drinking patterns and thermoregulatory behaviour of these two species of kangaroo have been examined in a semi-free range study, during summer at an arid rangeland site. Foraging was largely nocturnal in both species and during the day they behaved to reduce heat loads. This was especially so for M. giganteus, which showed greater shade seeking. However, it still used more water (72 +/- 2.6 mL kg(-1) day(-1), mean +/- SE) than M. rufus (56 +/- 7.6 mL kg(-1) day(-1)) and drank twice as frequently. Although M. giganteus produced a less concentrated urine (1422 +/- 36 mosmol kg(-1)) than M. rufus (1843 +/- 28 mosmol kg(-1)), kidney physiology did not explain all of the differences in water metabolism between the species. Water from the feed and faecal water retention also appear to be involved. Broadly, a better access to reliable water and the utilisation of mesic microhabitats has enabled M. giganteus to make inroads into the changing rangelands of eastern Australia. However, changes in the vegetation, due to stock grazing, have also favoured M. giganteus, which is a grass eating specialist.

Aerobic characteristics of red kangaroo skeletal muscles: is a high aerobic capacity matched by muscle mitochondrial and capillary morphology as in placental mammals?

Marsupials and placentals together comprise the Theria, the advanced mammals, but they have had long independent evolutionary histories, with the last common ancestor occurring more than 125 million years ago. Although in the past the marsupials were considered to be metabolically 'primitive', the red kangaroo Macropus rufus has been reported to have an aerobic capacity (VO2max) comparable to that of the most 'athletic' of placentals such as dogs. However, kangaroos travel at moderate speeds with lower relative cost than quadrupedal placentals. Given the long independent evolution of the two therian groups, and their unusual locomotor energetics, do kangaroos achieve their high aerobic capacity using the same structural and functional mechanisms used by (athletic) placentals? Red kangaroo skeletal muscle morphometry matched closely the general aerobic characteristics of placental mammals. The relationship between total mitochondrial volume in skeletal muscle and VO2max during exercise was identical to that in quadrupedal placentals, and differed from that in bipedal humans. As for placentals generally, red kangaroo mitochondrial oxygen consumption at VO2max was 4.7 ml O2 min(-1) ml(-1) of mitochondria. Also, the inner mitochondrial membrane densities were 35.8 +/- 0.7 m2 ml(-1) of mitochondria, which is the same as for placental mammals, and the same pattern of similarity was seen for capillary densities and volumes. The overall data for kangaroos was equivalent to that seen in athletic placentals such as dogs and pronghorns. Total skeletal muscle mass was high, being around 50% of body mass, and was concentrated around the pelvis and lower back. The majority of the muscles sampled had relatively high mitochondrial volume densities, in the range 8.8-10.6% in the major locomotor muscles. Again, capillary densities and capillary blood volumes followed the pattern seen for mitochondria. Our results indicate that the red kangaroo, despite its locomotion and extreme body form, shows fundamental aerobic/muscular relationships that appear common to both marsupials and placentals. The evolution of such metabolic relationships apparently predates the divergence of the therian groups in the early Cretaceous, and perhaps evolved in the mammal-like reptiles during the Triassic (220 million years ago) before the actual evolution of the mammals.