A. J. Bradley

Stress and mortality in a small marsupial (Antechinus stuartii, Macleay)

An investigation was made into the role of increased adrenocortical activity in the causation of the total postmating mortality of male Antechinus stuartii—a small shrew-like marsupial. A progressive rise in plasma androgen concentration of the males up to the time of mating was associated with increasingly aggressive behaviour and a progressive fall in plasma CBG concentration. During the mating period, the rate of fall in plasma CBG concentration increased markedly and plasma total corticosteroid concentration rose above the MCBC, so that there was a sharp rise in plasma free corticosteroid concentration just before the males all died. Although the plasma CBG concentration of females also fell during the mating period, with a moderate increase in plasma total glucocorticoid concentration, there was only a slight increase in plasma-free corticosteroid concentration at that time and it did not change significantly during the postmating, lactation period. Castration of captive males caused a marked increase in their plasma CBG concentration, and injection of testosterone or ACTH depressed it. There was a marked reduction in immunological competence and serum immunoglobulin concentration of the males just before their death. Postmortem examination revealed evidence of increased invasiveness of parasites and microorganisms, as well as severe haemorrhagic ulceration of the digestive tract. These effects could all be reproduced in captive animals by injection of cortisol acetate. It is concluded that a state of stress, induced by aggressive interactions at the time of mating and exacerbated by the fall in plasma CBG, results in suppression of the immune and inflammatory systems of the males, causing their death from gastrointestinal haemorrhage as well as invasion by parasites and microorganisms.

Endocrine changes in dasyurid marsupials with differing mortality patterns.

A comparison was made between the breeding-related endocrine changes in two species of dasyurid marsupial (Antechinus swainsonii and A. flavipes), which exhibit a catastrophic male mortality after a brief mating period; and those of another dasyurid species (Sminthopsis crassicaudata), the males of which survive an extended breeding period. In the males of both Antechinus species, the mating period was preceded by a rapid rinse in plasma androgen concentration and accompanied by a marked fall in plasma corticosteroid-binding globulin (CBG) concentration, to less than the total glucocorticoid concentration, which itself rose. As a consequence plasma free glucocorticoid concentration rose approximately 10-fold just before the males disappeared from the populations. Severe hemorrhagic ulceration of the upper digestive tract was consistently found soon after capture near the time of mating. In females, CBG concentration was always well in excess of total glucocorticoid concentration and free glucocorticoid concentration remained low. There was a significant negative correlation between plasma androgen and CBG concentrations in male Antechinus species from the natural populations. In laboratory-held castrate male A. swainsonii, injection of either testosterone or dihydrotestosterone caused a dose-related fall in CBG. In contrast to the above, the CBG concentration was always well in excess of total glucocorticoid concentration in the plasma of male S. crassicaudata and there was no evidence of interaction between plasma androgen and CBG concentration. These findings support the hypothesis that, in those species with a breeding-related mortality of males, an androgen-dependent fall in plasma CBG concentration and a stressful mating period result in death from adrenocortical suppression of the immune and inflammatory responses.

Stress and mortality in the red-tailed phascogale, Phascogale calura (Marsupialia: Dasyuridae).

An investigation was made of endocrine changes occurring during the life history of Phascogale calura, a small, arboreal, squirrel-like insectivorous marsupial. Following a 3-week mating period in July each year, all males disappear from the population and it is presumed that they die. During the mating period the plasma cortisol concentration in males increased to a greater extent than did the plasma corticosterone. During this period the plasma concentration of CBG decreased in the males but not in the females, which resulted in competition between the two glucocorticoids for binding sites and a 25-fold sex difference in free cortisol concentration. The plasma testosterone concentration in males reached its maximum value about the time of disappearance of the males and the plasma lacked high-affinity binding for androgens. The depression in CBG concentration was androgen dependent since castration of captive males caused a marked increase in plasma CBG concentration which could be reversed with androgen administration. Postmorten examination of moribund males revealed evidence of hemorrhage from gastric ulcers and some evidence of immune suppression and disease. It is considered that a state of stress in males triggered by aggressive interactions following an elevation in plasma testosterone concentration during mating and antagonized by an androgen-dependent decrease in CBG concentration results in suppression of both immune and inflammatory reactions. This is the first detailed description of endocrine changes which accompany a stress-related total male mortality in a dasyurid marsupial species which does not belong to genus Antechinus.

Wildlife disease prevalence in human-modified landscapes

Human‐induced landscape change associated with habitat loss and fragmentation places wildlife populations at risk. One issue in these landscapes is a change in the prevalence of disease which may result in increased mortality and reduced fecundity. Our understanding of the influence of habitat loss and fragmentation on the prevalence of wildlife diseases is still in its infancy. What is evident is that changes in disease prevalence as a result of human‐induced landscape modification are highly variable. The importance of infectious diseases for the conservation of wildlife will increase as the amount and quality of suitable habitat decreases due to human land‐use pressures. We review the experimental and observational literature of the influence of human‐induced landscape change on wildlife disease prevalence, and discuss disease transmission types and host responses as mechanisms that are likely to determine the extent of change in disease prevalence. It is likely that transmission dynamics will be the key process in determining a pathogens impact on a host population, while the host response may ultimately determine the extent of disease prevalence. Finally, we conceptualize mechanisms and identify future research directions to increase our understanding of the relationship between human‐modified landscapes and wildlife disease prevalence. This review highlights that there are rarely consistent relationships between wildlife diseases and human‐modified landscapes. In addition, variation is evident between transmission types and landscape types, with the greatest positive influence on disease prevalence being in urban landscapes and directly transmitted disease systems. While we have a limited understanding of the potential influence of habitat loss and fragmentation on wildlife disease, there are a number of important areas to address in future research, particularly to account for the variability in increased and decreased disease prevalence. Previous studies have been based on a one‐dimensional comparison between unmodified and modified sites. What is lacking are spatially and temporally explicit quantitative approaches which are required to enable an understanding of the range of key causal mechanisms and the reasons for variability. This is particularly important for replicated studies across different host‐pathogen systems. Furthermore, there are few studies that have attempted to separate the independent effects of habitat loss and fragmentation on wildlife disease, which are the major determinants of wildlife population dynamics in human‐modified landscapes. There is an urgent need to understand better the potential causal links between the processes of human‐induced landscape change and the associated influences of habitat fragmentation, matrix hostility and loss of connectivity on an animals physiological stress, immune response and disease susceptibility. This review identified no study that had assessed the influence of human‐induced landscape change on the prevalence of a wildlife sexually transmitted disease. A better understanding of the various mechanisms linking human‐induced landscape change and the prevalence of wildlife disease will lead to more successful conservation management outcomes.

Semelparity in a large marsupial

Complete mortality of males after mating is known in several small dasyurid and didelphid species (up to 300 g) and has previously been suggested to be a consequence of their small size and their inability to sequester sufficient fat reserves for an intense rut in the winter. Males of these species use increased corticosteroid levels to allow protein catabolism, enabling them to support their mating effort with other body reserves. However, increased corticosteroid levels have negative consequences such as anaemia, gastrointestinal ulceration, immune suppression and disease. The Australian dasyurid Dasyurus hallucatus shows complete male die off after mating in tropical savannah, yet males of this species may weigh as much as 1120 g and continue to eat during the rut. Die off in D. hallucatus shows many similarities to that in the smaller species including weight loss, fur loss, parasite infestation, increased testosterone levels and anaemia. However, in contrast to smaller species, there is no evidence of elevated corticosteroid levels or gastrointestinal ulceration. Consequently, the phenomenon of male die off after mating lacks a universal explanation.

Drought-driven change in wildlife distribution and numbers: a case study of koalas in south west Queensland

Context Global climate change will lead to increased climate variability, including more frequent drought and heatwaves, in many areas of the world. This will affect the distribution and numbers of wildlife populations. In south-west Queensland, anecdotal reports indicated that a low density but significant koala population had been impacted by drought from 2001–2009, in accord with the predicted effects of climate change. Aims The study aimed to compare koala distribution and numbers in south-west Queensland in 2009 with pre-drought estimates from 1995–1997. Methods Community surveys and faecal pellet surveys were used to assess koala distribution. Population densities were estimated using the Faecal Standing Crop Method. From these densities, koala abundance in 10 habitat units was interpolated across the study region. Bootstrapping was used to estimate standard error. Climate data and land clearing were examined as possible explanations for changes in koala distribution and numbers between the two time periods. Key results Although there was only a minor change in distribution, there was an 80% decline in koala numbers across the study region, from a mean population of 59 000 in 1995 to 11 600 in 2009. Most summers between 2002 and 2007 were hotter and drier than average. Vegetation clearance was greatest in the eastern third of the study region, with the majority of clearing being in mixed eucalypt/acacia ecosystems and vegetation on elevated residuals. Conclusions Changes in the area of occupancy and numbers of koalas allowed us to conclude that drought significantly reduced koala populations and that they contracted to critical riparian habitats. Land clearing in the eastern part of the region may reduce the ability of koalas to move between habitats. Implications The increase in hotter and drier conditions expected with climate change will adversely affect koala populations in south-west Queensland and may be similar in other wildlife species in arid and semiarid regions. The effect of climate change on trailing edge populations may interact with habitat loss and fragmentation to increase extinction risks. Monitoring wildlife population dynamics at the margins of their geographic ranges will help to manage the impacts of climate change.

Plasma DHEA levels in wild, territorial red squirrels : Seasonal variation and effect of ACTH

In many species, territorial behavior is limited to the breeding season and is tightly coupled to circulating gonadal steroid levels. In contrast, both male and female red squirrels (Tamiasciurus hudsonicus) are highly aggressive in both the breeding and non-breeding seasons in defense of food stores on their individual territories throughout the boreal and northern forests of North America. Dehydroepiandrosterone (DHEA), an androgen precursor, is secreted from the adrenal cortex in some mammals, and DHEA has been linked to aggression in non-breeding songbirds. Here, we examined plasma DHEA levels in a natural population of red squirrels in the Yukon, Canada. Plasma DHEA levels in both males and females reached high concentrations (up to 16.952 ng/ml in males and 14.602 ng/ml in females), markedly exceeding plasma DHEA concentrations in laboratory rats and mice and similar to plasma DHEA concentrations in some primates. Circulating DHEA levels showed both seasonal and yearly variation. Seasonal variation in male plasma DHEA levels was negatively correlated with testes mass. Yearly variation in male DHEA levels was positively correlated with population density. In both males and females, circulating DHEA rapidly increased after ACTH treatment, implying an adrenal origin. This is the first examination of plasma DHEA concentrations in a wild rodent and the first field experiment on the regulation of plasma DHEA in any wild mammal. These data lay the foundation for future studies on the role of DHEA in non-breeding territoriality in this species and other mammals.

Failure of glucocorticoid feedback during breeding in the male red-tailed phascogale Phascogale calura (Marsupialia: Dasyuridae).

An investigation was made into the factors which lead to an elevation in plasma free cortisol concentration during the last weeks of life of males in natural populations of the red-tailed phascogale Phascogale calura. The dexamethasone suppression-test was employed to examine the glucocorticoid feedback control of plasma cortisol both before and during the breeding season. In both sexes ACTH alone or in combination with dexamethasone caused an elevation in the plasma concentration of cortisol, corticosterone and free cortisol. Dexamethasone administration in both males and females resulted in significant decreases in the plasma concentration of each of the glucocorticoid groups both before and during the first week of the breeding season (June and early July), however during the last week of breeding (late July) dexamethasone decreased the plasma glucocorticoid concentration of females but not of males. Administration of ACTH caused a significant elevation in the plasma cortisol concentration in all groups. However, the magnitude of this response diminished with time in both sexes. Dexamethasone treatment resulted in a decrease in the plasma testosterone concentration in males before and early in the breeding season however toward the end of breeding this effect was abolished. It is apparent that towards the end of the breeding season and during the last week of life of the males, glucocorticoid feedback control of ACTH is almost abolished. These changes, which occur only in the males late in the breeding season and near the time of their disappearance from the population, are consistent with a condition known as end organ resistance to steroid hormones.

Behavioral and endocrinological correlates of social status in the male sugar glider (Petaurus breviceps Marsupialia: Petauridae)

Socially dominant male sugar gliders are heavier than socially subordinate males, have higher plasma testosterone and lower cortisol concentrations, win more social encounters, scan the arena more, scent-mark more, and are more active and move more quickly, even though they spend more time in the colony nesting box. When they are transferred into a foreign stable colony there is an impressive reversal of behavioral measures and a concomitant decrease in concentration of plasma testosterone and rise in cortisol that is apparent over the first 3 weeks of observation.

Influence of urban edges on stress in an arboreal mammal: a case study of squirrel gliders in southeast Queensland, Australia

There is growing recognition that ecological research must expand its focus beyond inference based on pattern-process relationships to the direct measurement of ecological and physiological processes. Physiological assessment is important because vertebrates cope with unpredictable and noxious stimuli by initiating a stress response. However, an over-activation of the acute stress response by numerous novel and potentially stressful anthropogenic pressures, including those associated with urban edges, has the potential to generate chronic stress and a greater susceptibility to disease, reduce fecundity and survivorship. An individual’s physiological response to edge habitats with varying degrees of contrast to the adjacent disturbed urban matrix (e.g. major vs. minor roads), may provide insight into their survival likelihood in fragmented urban landscapes. Although demographic changes in wildlife resulting from urbanization have been documented, only recently have physiological consequences been examined. We addressed this problem using a case study of the squirrel glider (Petaurus norfolcensis) in the fragmented urban landscape of southeast Queensland, Australia. Hair samples were used to enable a comparison of hair cortisol levels in individual squirrel gliders, providing an indication of potential stress. We applied a linear mixed-effect modeling approach clustered by patch to quantify the influence of site-level habitat factors and relative abundance comparative to edge contrast on hair cortisol levels. We found that edge type had a strong positive effect on hair cortisol levels; but this depended on the availability of abundant nest hollows at a site. We conclude that individual hair cortisol concentration, providing an index of stress, was lowest in interior habitats and highest in edge habitats adjacent to major roads. Furthermore, gliders occupying low edge contrast habitats adjacent to residential areas and minor roads, and containing abundant tree nest hollows, had low-moderate hair cortisol levels. This highlights the potential importance of these habitats for the conservation of arboreal mammals such as the squirrel glider in urban landscapes.