The physiology of the honey possum, Tarsipes rostratus, a small marsupial with a suite of highly specialised characters: a review.

Field and laboratory studies of the iconic nectarivorous and 'pollenivorous' honey possum, Tarsipes rostratus, are reviewed with the aim of identifying aspects of its physiology that are as yet poorly understood and needed to implement management strategies for its long-term conservation. Dietary specialisations include the loss of teeth, a modified gut with a high rate of passage, exceptionally low minimum nitrogen requirements, an apparently high basal metabolic rate and a permanently polyuric kidney. In contrast, its reproductive physiology is plesiomorphic, combining aspects such as a post-partum oestrus, embryonic diapause, photoperiodicity and extended maternal care that are usually separate characteristics of other marsupial groups. In common with a number of other marsupials, the honey possum has the potential for trichromatic colour vision and has been the subject of several studies attempting to correlate visual quality with ecological realities. Field physiological studies have established its high rates of nectar and pollen intake needed to maintain energy balance and highlight the need for a constant intake from floral sources. Early allometric studies suggesting that the honey possum's relatively low reproductive rate may be linked to a diet limited in protein have not been supported and nitrogen intakes in the field exceed by a factor of 10 the animal's basic requirements for balance. Measurements of rates of protein turnover in field-caught lactating females suggest that they divert nitrogen from the protein pool to milk production by reducing rates of degradation, rather than by increasing rates of synthesis of protein. Although not yet an endangered species, the honey possum's habitat has been drastically reduced since European occupation of Australia and future-targeted research on the animal's unique physiology and habitat linkage is needed that can be translated into effective management practices. Only then will its long-term survival be assured.

Progesterone and reproduction in marsupials: a review.

Progesterone (P4) profiles throughout pregnancy and the oestrous cycle are reviewed in a wide range of marsupial species, representing 12 Families, and focus on the corpus luteum (CL) and its functioning, compared with its eutherian counterpart. Physiologically, P4 subtends the same fundamental processes supporting gestation in marsupials as it does in eutherian mammals, from its role in stimulating the secretory endometrium, effecting nutritional transfer across the placenta and establishing lactogenesis. Before the formation of the CL, however, secretion of P4 is widespread throughout many Families and the dual roles of P4 in the induction of sexual behaviour and ovulation are exposed. In Dasyuridae, raised levels of P4 are linked with the induction of sexual receptivity and are also present around the time of mating in Burramyidae, Petauridae and Tarsipedidae, but their function is unknown. Only in Didelphidae has research established that the pheromonally-induced levels of pro-oestrous P4 trigger ovulation. This is principally the role of oestradiol in the eutherian and may be an important difference between the marsupial and the eutherian. The deposition of the shell coat around the early marsupial embryo is also a function of P4, but perhaps the most striking difference is seen in the time taken to form the CL. This is not always immediate and the maximum secretion of P4 from the granulosa cells may not occur until some 2 weeks after ovulation. The slower development of the CL in some species is linked with delays in the development of the embryo during its unattached phase and results in relatively long gestation periods. A common feature of these, in monovular species, is a short pulse of P4 from the newly-luteinised CL, which is all that is needed for the subsequent development of the embryo to term. Maternal recognition of pregnancy occurs soon after the formation of the blastocyst, with embryo-induced changes in ovarian production of P4 and the uterine endometrium. The embryo, similar to the eutherian, determines the length of the gestation period and initiates its own birth, but in direct contrast, the embryo of some marsupial species shortens the life-span of the CL. The evidence points to a different strategy; one of a reduction, rather than an expansion of the potential ovarian and placental support available during pregnancy. The marsupial mode of reproduction, where all species produce highly altricial young, receiving complex and extensive maternal care, has facilitated the adaptive radiation of this group and avoided the need for precociality.

Monitoring reproduction in the critically endangered marsupial, Gilbert's potoroo (Potorous gilbertii): preliminary analysis of faecal oestradiol-17beta, cortisol and progestagens.

Gilbert's potoroo (Potorous gilbertii) was rediscovered in 1994 after having been presumed extinct for 120 years. Estimates indicate fewer than 40 individuals remain at Two Peoples Bay Nature Reserve on the south coast of Western Australia although a translocated population of approximately 20 animals has recently been established on nearby Bald Island. A captive breeding facility has been established adjacent to the mainland population but few young have been produced (8 since 1995). Faecal levels of oestradiol-17beta (E(2)) were monitored over a 2-year period in an effort to determine cyclic reproductive activity, and faecal cortisol levels were also monitored to gauge whether chronic stress may be a factor limiting breeding in captivity. Faecal steroids were monitored in six captive females, and four captive male potoroos, and four wild females. The only captive births recorded after 1998 were one in August 1999 and one in February 2001, both to the same female. Peaks in E(2) concentration, up to 10 ng g(-1) of dried faecal mass were measured and results to date suggest the main breeding period to be November-December based on elevated E(2) levels at this time. Clear patterns of reproductive activity in the captive females, however, were not evident. Analysis of epithelial cell counts from urinogenital swabs and faecal E(2) and progestagen (PM) levels from a single female kept at the Perth Zoo, suggest that Gilbert's potoroo has an oestrous cycle of approximately 39 days. Faecal cortisol levels in captive females were significantly lower than those in wild-caught individuals and thus there is no indication that elevated cortisol levels per se inhibited reproduction in captive females.

Environmental endocrinology.

The rapidly evolving discipline of environmental endocrinology is briefly reviewed from the 'heroic era' to the present. Environmental endocrinology has developed in response to the need to understand how hormones modulate and control physiological processes in animals exposed to the exigencies of their particular, natural, environment. This has only been made possible through spectacular developments in hormone assay techniques which now make feasible hormone measurements on microlitre volumes of body fluids. The results of some recent research programmes working on animals in the field are reviewed. These include the reproductive responses of migratory birds in the Arctic, the role of antidiuretic hormone in the survival of desert rodents and marsupial wallabies, some interesting behavioural effects of glucocorticoids in reptiles, and the dynamic interplay between hormones and social status in primates.

Effect of hypernatraemia and the neurohypophysial peptide, arginine vasotocin (AVT) on behavioural thermoregulation in the agamid lizard, Ctenophorus ornatus.

Hypernatraemia induced by chronic injections of sodium chloride provokes thermal depression in the agamid lizard, Ctenophorus (formerly Amphibolurus) ornatus, with a fall of two degrees Celsius in the mean body temperature selected behaviourally in a photo-thermal gradient. The placement of an electrolytic lesion in the base of the hypothalamus, designed to eliminate secretion of the neuropeptide arginine vasotocin (AVT), did not affect the lizards' thermoregulatory behaviour and their Preferred Body Temperature (PBT) was not significantly different from that of unoperated controls. Saline loading, however, did not induce thermal depression in these tract-operated individuals and their PBT was significantly higher than that of salt-loaded intact individuals. When AVT was injected into operated, salt-loaded, animals, however, thermal depression was observed, supporting the hypothesis that thermal depression brought about by hypernatraemia is mediated through the action of AVT. AVT similarly significantly depressed the PBT of injected intact individuals by 3.2 degrees C when compared with hydrated controls. Immunostaining for AVT confirmed that the lesions placed in the region of the median eminence virtually eliminated AVT located in the neurohypophysial tract, and the pars nervosa. This is the first report of an effect of this peptide on behavioural thermoregulation in a lizard.

Physiological and hormonal control of thermal depression in the tiger snake, Notechis scutatus.

Plasma sodium concentrations in field-caught Western tiger snakes, Notechis scutatus, from semi-arid Carnac Island (CI) varied seasonally, with snakes exhibiting significant hypernatraemia during summer and normal concentrations following autumn rain. In contrast, field-caught tiger snakes from a perennial fresh-water swamp (Herdsman Lake, HL) exhibited no significant increase in plasma sodium concentrations during summer. Laboratory-induced hypernatraemia caused thermal depression in both populations; there was a weak negative relationship between plasma sodium concentration and temperature selection that was significant for CI snakes. Hypernatraemia significantly elevated circulating concentrations of the neuropeptide arginine vasotocin (AVT) in both CI and HL snakes. CI snakes injected with a physiological dosage of AVT also evidenced thermal depression. Despite the positive correlation between AVT and both plasma sodium concentration and osmolality for laboratory snakes, field samples from CI snakes indicate that circulating levels of AVT may be influenced more by plasma osmolality than sodium levels. The data suggest that, in CI snakes, chronic dehydration in the field leads to hypernatraemia which may lead to elevated levels of AVT if plasma osmolality also increases. This will in turn invoke a depression in thermal behaviour that may improve the water economy and survival of snakes on semi-arid CI. Although HL snakes do not experience seasonal dehydration, physiological changes away from the stable homeostatic state appear to prompt the same behavioural shifts, illustrating the intrinsic nature of the thermal behaviour in different populations of the same species of snake.

Hormonal control of salt and water balance in vertebrates.

The endocrine system mediates many of the physiological responses to the homeostatic and acclimation demands of salt and water transport. Many of the hormones involved in the control of salt and water transport are common to all vertebrates, although their precise function and target tissues have changed during evolution. Arginine vasopressin (vasotocin), angiotensin II, natriuretic peptides, vasoactive intestinal peptide, urotensin II, insulin and non-genomic actions of corticosteroids are involved in acute (minutes and hours) alterations in ion and water transport. This rapid alteration in transport is primarily the result changes in behavior, blood flow to osmoregulatory organs, and membrane insertion or activation (e.g., phosphorylation) of existing transport proteins, ion and water channels, contransporters and pumps. Corticosteroids (through genomic actions), prolactin, growth hormone, and insulin-like growth factor I primarily control long-term (several hours to days) changes in transport capacity that are the result of synthesis of new transport proteins, cell proliferation, and differentiation. In addition to the important task of establishing broad evolutionary patterns in hormones involved in ion regulation, comparative endocrinology can determine species and population level differences in signaling pathways that may be critical for adaptation to extreme or rapidly changing environments.

Gestation, thermoregulation, and metabolism in a viviparous snake, Vipera aspis: evidence for fecundity-independent costs.

Oxygen consumption of gestating Aspic vipers, Vipera aspis (L.), was strongly dependent on body temperature and mass. Temperature-controlled, mass-independent oxygen consumption did not differ between pregnant and nonpregnant females. Maternal metabolism was not influenced during early gestation by the number of embryos carried but was weakly influenced during late gestation. These results differ from previous investigations that show an increase in mass-independent oxygen consumption in reproductive females relative to nonreproductive females and a positive relationship between metabolism and litter size. These data also conflict with published field data on V. aspis that show a strong metabolic cost associated with reproduction. We propose that, under controlled conditions (i.e., females exposed to precise ambient temperatures), following the mobilisation of resources to create follicles (i.e., vitellogenesis), early gestation per se may not be an energetically expensive period in reproduction. However, under natural conditions, the metabolic rate of reproductive females is strongly increased by a shift in thermal ecology (higher body temperature and longer basking periods), enabling pregnant females to accelerate the process of gestation. Combining both laboratory and field investigation in a viviparous snake, we suggest that reproduction entails discrete changes in the thermal ecology of females to provide optimal temperatures to the embryos, whatever their number. This results in the counterintuitive notion that metabolism may well be largely independent of fecundity during gestation, at least in an ectothermic reptile.