Torpor and activity patterns in free-ranging sugar gliders Petaurus breviceps (Marsupialia)

Almost all studies on daily torpor in mammals have been conducted in the laboratory under constant environmental conditions. We investigated torpor and activity patterns in free-ranging sugar gliders (Petaurus breviceps, 100 g) using temperature telemetry and compared field data with published information obtained in the laboratory. Body and/or skin temperature and activity patterns of 12 sugar gliders were monitored from autumn to spring. Healthy sugar gliders were active between sunset and sunrise, but on cold or rainy nights activity was substantially reduced. Animals in poor condition occasionally foraged during the day. Eleven gliders were monitored for 8–171 days and all of these entered daily torpor. Torpor was observed on 103 days (17% of observation days), usually occurred on rainy or cold nights, and frequency of torpor changed with season. Torpor bouts lasted between 2 and 23 h (average 13 h) and the body temperature fell to a minimum of 10.4°C. Torpor was thus much deeper, longer and more frequent than in laboratory studies on the same species. Our study shows that cold or wet conditions curtail foraging in wild sugar gliders and that they employ daily torpor regularly during adverse weather. This suggests that minimisation of energy loss by the use of torpor in sugar gliders is pivotal for their survival in the wild. Received: 8 July 1999 / Accepted: 23 December 1999     

The dorsal paracloacal gland and its relationship with seasonal changes in cutaneous scent gland morphology and plasma androgen in the marsupial sugar glider (Petaurus breviceps; Marsupialia: Petauridae)

A study spanning two breeding seasons was carried out to examine changes in the size of the dorsal paracloacal glands and testes in the marsupial sugar glider Petaurus breviceps Waterhouse 1839. These changes were related to seasonal increases in the plasma testosterone concentration and to morphological changes in the frontal and gular cutaneous scent glands of males.
Both dorsal paracloacal glands and testes underwent a seasonal cycle of development which reached its maximum during the June-September breeding season. These changes coincided with an increase in the plasma testosterone concentration and with the increase in activity of certain cell types within the frontal and gular glands.
Castration caused a significant decrease in the size of the dorsal paracloacal glands, while androgen replacement was effective in restoring the glands to their pre-castration size thus demonstrating the influence of androgens upon the activity of these glands.
The synchronization which exists between plasma testosterone concentration, cutaneous scent gland morphology and the size of the dorsal paracloacal glands of males, suggests that the dorsal paracloacal glands, or more likely their secretions, are important in social organization in this species.     

Seasonally constant field metabolic rates in free-ranging sugar gliders (Petaurus breviceps)

Sugar gliders, Petaurus breviceps (average body mass: 120 g) like other small wild mammals must cope with seasonal changes in food availability and weather and therefore thermoregulatory and energetic challenges. To determine whether free-ranging sugar gliders, an arboreal marsupial, seasonally adjust their energy expenditure and water use, we quantified field metabolic rates (FMR) and water flux at a seasonal cool-temperate site in eastern Australia. Thirty six male and female sugar gliders were labelled with doubly labelled water for this purpose in spring, summer and autumn. The mean FMR was 159 ± 6 kJ d^? 1 (spring), 155 ± 8 kJ d^? 1 (summer), and 152 ± 20 kJ d^? 1 (autumn) and the mean FMR for the three seasons combined was 158 ± 5 kJ d^? 1 (equivalent to 1.33 kJ g^? 1 d^? 1 or 780 kJ kg^? 0.75 d^? 1). The mean total body water was 83 ± 2 g, equal to 68.5% of body weight. Mean water flux was 29 ± 1 mL day^? 1. Season, ambient temperature or sex did not affect any of the measured and estimated physiological variables, but body mass and total body water differed significantly between sexes and among seasons. Our study is the first to provide evidence for a constant FMR in a small mammal in three different seasons and despite different thermal conditions. This suggests that seasonal changes in climate are compensated for by behavioural and physiological adjustments such as huddling and torpor known to be employed extensively by sugar gliders in the wild.     

Seasonal changes in the thermoenergetics of the marsupial sugar glider, Petaurus breviceps

Little information is available on seasonal changes in thermal physiology and energy expenditure in marsupials. To provide new information on the subject, we quantified how body mass, body composition, metabolic rate, maximum heat production, body temperature and thermal conductance change with season in sugar gliders (Petaurus breviceps) held in outdoor aviaries. Sugar gliders increased body mass in autumn to a peak in May/June, which was caused to a large extent by an increase in body fat content. Body mass then declined to minimum values in August/September. Resting metabolic rate both below and above the thermoneutral zone (TNZ) was higher in summer than in winter and the lower critical temperature of the TNZ occurred at a higher ambient temperature (Ta) in summer. The basal metabolic rate was as much as 45% below that predicted from allometric equations for placental mammals and was about 15% lower in winter than in summer. In contrast, maximum heat production was raised significantly by about 20% in winter. This, together with an approximately 20% decrease in thermal conductance, resulted in a 13 degrees C reduction of the minimum effective Ta gliders were able to withstand. Our study provides the first evidence that, despite the apparent lack of functional brown adipose tissue, sugar gliders are able to significantly increase heat production in winter. Moreover, the lower thermoregulatory heat production at most TaS in winter, when food in the wild is scarce, should allow them to reduce energy expenditure.     

The frontal and gular dermal scent organs of the marsupial sugar glider (Petaurus breviceps)

A study spanning two breeding seasons was carried out to examine the role of androgens in the control of the frontal and gular scent glands of the marsupial sugar glider Petaurus breviceps Waterhouse in a wild population. Animals were captured at monthly intervals and from these blood samples were taken and tissue biopsy samples were collected from the scent glands.
Several histological parameters underwent seasonal changes which were related to changes in the plasma concentration of free plus albumin bound ('biologically active') testosterone. The parameters which showed significant change did so during the July-September breeding season coinciding with the peak in biologically active testosterone concentration.
Castration caused a significant decrease in the nuclear diameters of gular and frontal apocrine and sebaceous gland cells, and a decrease in gular apocrine cell height. These decreases were reversed with androgen replacement therapy.
The nuclear diameters of apocrine tissue cells in both scent organs are positively correlated with the plasma level of biologically active testosterone. In the gular organ, but not in the frontal organ, the depth of apocrine tissue was significantly correlated with nuclear diameter. In castration and androgen replacement studies gular apocrine tissue responded more dramatically than did frontal apocrine tissue. This suggests that the gular organ is more sensitive to testosterone than is the frontal.     

Effects of helium/oxygen and temperature on aerobic metabolism in the marsupial sugar glider, Petaurus breviceps

Helox (79% helium and 21% oxygen) has often been used for thermobiological studies, primarily because helium is thought to be metabolically inert and to produce no adverse effects other than increasing heat loss. However, these assumptions have been questioned. As basal metabolic rate (BMR) represents maintenance energy requirements for vital body functions, potential physiological effects of helox should be reflected in changes of BMR. In this study, sugar gliders were subjected to both air and helox atmospheres over a wide range of T(a)'s, including the thermoneutral zone (TNZ), to determine (1) whether helox has any influence other than on heat loss and (2) the maximum heat production (HP(max)) and thermal limits of this species. Although thermal conductance in the TNZ increased in helox, BMR was similar in air and helox (0.55+/-0.07 and 0.57+/-0.06 mL g(-1) h(-1), respectively). The TNZ in helox, however, was shifted upwards by about 3 degrees C. Below the TNZ, sugar gliders were able to withstand an effective temperature of -24.7+/-7.3 degrees C with an HP(max) of 3.14+/-0.36 mL g(-1) h(-1). The low effective temperature tolerated by sugar gliders shows that they are competent thermoregulators despite their apparent lack of functional brown fat. Similarities of BMRs in air and helox suggest that the effect of helox is restricted to an increase of heat loss, and, consequently, helox represents a useful tool for thermal physiologists. Moreover, the lack of increase of BMR in helox despite an increase in thermal conductance of sugar gliders suggests that BMR is not a function of body surface.     

Molecular systematics and evolutionary origins of the genus Petaurus (Marsupialia: Petauridae) in Australia and New Guinea

The glider genus Petaurus comprises a group of arboreal and nocturnal marsupial species from New Guinea and Australia. Molecular data were generated in order to examine phylogenetic relationships among species within the genus and explore the time-scale of diversification and biogeographic history of the genus in Australia and New Guinea. All known species and subspecies of Petaurus (with the exception of P. biacensis) were sequenced for two mitochondrial genes (ND2 and ND4) and one nuclear marker (omega-globin gene). Phylogenetic analyses confirmed the monophyly of the genus relative to other petaurids and showed a sister relationship of P. australis to the rest of Petaurus. The analyses revealed that currently recognised species of Petaurus formed distinct mitochondrial DNA (mtDNA) clades. Considerable mtDNA diversity and seven distinct clades were identified within the species P. breviceps, with the distribution of each clade showing no correspondence with the distributional limits of known subspecies. Molecular dating analyses using BEAST suggested an early to mid-Miocene origin (18–24 mya) for the genus. Ancestral area reconstructions, using BayesTraits, did not resolve the location for the centre of origin of Petaurus, but provided evidence for at least one dispersal event from New Guinea to Australia that led to the evolution of extant Australian populations of P. breviceps, P. norfolcensis and P. gracilis. The timing of this dispersal event appears to pre-date the Pleistocene, adding to the growing number of studies that suggest faunal connections occurred between Australia and New Guinea in the Late Miocene to Pliocene period.     

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.     

Rileyella petauri gen. nov., sp. nov. (Pentastomida: Cephalobaenida) from the lungs and nasal sinus of Petaurus breviceps (Marsupialia: Petauridae) in Australia

A new cephalobaenid pentastome, Rileyella petauri gen: nov., sp. nov. from the lungs and nasal sinus of the petaurid marsupial, Petaurus breviceps, is described. It is the smallest adult pentastome known to date, represents the first record of a mammal as the definitive host of a cephalobaenid and may represent the only pentastome known to inhabit the lungs of a mammal through all its instars, with the exception of patent females. Adult males, non-gravid females and nymphs moulting to adults occur in the lungs; gravid females occur in the nasal sinus. R. petauri is minute and possesses morphological features primarily of the Cephalobaenida but the glands in the cephalothorax and the morphology of the copulatory spicules are similar to some members of the remaining pentastomid order, the Porocephalida. This unusual combination of features distinguish the new genus from other genera in the Cephalobaenida. The occurrence of only seven fully-formed larvae in eggs in the uterus, each representing about 10% of the length of the patent female, and her presence in the nasal sinus of a dependent juvenile P. breviceps (36 gm) implies a direct life cycle.     

The sugar glider (Petaurus breviceps): a laboratory host for the nematode Parastrongyloides trichosuri

Parastrongyloides trichosuri is a nematode parasite of the Australian brush-tailed possums that can be propagated through many generations in vitro. This makes P. trichosuri uniquely suited for genetic investigations, including those involving transgenesis. However, an obstacle to its use as an experimental model has been the fact that its host is limited to Australia and New Zealand and that it cannot be exported because of its status as a protected species or agricultural pest, respectively. In previous studies, conventional laboratory animals such as rats, mice, rabbits, ferrets, and chickens have failed to support infections. In the present study, gerbils and short-tailed opossums proved similarly refractory to infection. In contrast, the sugar glider (Petaurus breviceps, family Petauridae) proved to be a good host for P. trichosuri. Patent infections resulted using as few as 6 infective larvae (L3i) and as many as 2,000 L3i. Large numbers of L3i (1,000-2,000) produced patent infections of much shorter duration than those seen when 100 L3i were initially given to the sugar glider. In one case, an infection initiated with 100 L3i was patent for over 1 yr. Parastrongyloides trichosuri is easily cryopreserved using a method developed for Strongyloides stercoralis. Thus, we have identified an experimental host for P. trichosuri that will make it possible to conduct research on this parasite in laboratories outside the endemic sites.     

A set of microsatellite primers for the striped possum,Dactylopsila trivirgata (Petauridae: Marsupialia)

The New Guinean endemic dactylopsilines are members of the Petauridae possum family, represented in Australia only by the striped possum Dactylopsila trivirgata. The shy nature and low density of this species have hampered studies of its ecology to date, so we developed nine highly variable polymorphic microsatellite markers to enable molecular genetic analysis of population structure and mating system parameters. This will add substantially to our understanding of the behavioural ecology of this species. The low degree of cross‐amplification of the primers in other petaurid species lends weight to other evidence suggesting that this family underwent a relatively early radiation.     

Social dominance and serum testosterone concentration in dyads of male Macaca fascicularis

The relationship between social dominance and serum testosterone concentration was evaluated in 24 male Macaca fascicularis in 14 dyads at 2-week intervals over an 8-month period. No associations between testosterone concentration and dominance ranks were found in dyads with "clear dominance" relationships. A significant positive association was found between testosterone concentration and dominance ranks in dyads that exhibited "contested dominance" or dominance reversals. Thus, higher testosterone concentration corresponded to social dominance in subjects dominant as the result of a contest, rather than a consequence of high relative rank.     

Plasma testosterone and male dominance in a Japanese macaque (Macaca fuscata) troop compared with repeated measures of testosterone in laboratory males

Plasma testosterone levels measured by radioimmunoassay did not correlate with dominance rank or aggressive behavior in 21 adult males of a natural troop of Japanese macaques (Macaca fuscata). The data were replicated during two consecutive breeding seasons. Levels of male dominance and aggressive behavior were highly correlated from year to year, but testosterone levels of individual males were not. Nor were individual levels of testosterone correlated in five laboratory males sampled every 15 min over a 2-hr period. These laboratory males showed multiple, apparently random peaks but the mean testosterone level of 11.73 ng/ml did not vary significantly throughout the 120 min that were studied. By demonstrating that the stress of blood collection did not depress plasma testosterone titers in laboratory males, these data validated the method used in the study of the natural troop.