Ecophysiology of Australian Arid-Zone Marsupials

Abstract

Studies of the ecophysiology of Australia's marsupials are still in their infancy but recent work has focused on the question of stress in species inhabiting arid and semi-arid environments. An operational definition of stress as ‘the physiological resultant of demands that exceed an animal’s homeostatic capacities’ has been used here to search for instances of stress in arid-zone marsupials due to high temperatures and lack of water. Significant perturbations of water and electrolyte balance in arid-zone marsupials were found to be rare, and, even in the driest year ever recorded on Barrow Island, only one species, the Barrow Island euro, showed signs of an increased allostatic load, but not ‘allostatic overload’, or stress. The Spectacled hare-wallaby, serves as an exemplar of the level of adaptation by some arid-zone marsupials, having the lowest rate of water loss yet recorded for any mammal worldwide. This contrasts with the Rothschild’s rock wallaby, which lacks hormonal control over water loss by the kidney but survives in a similar habitat to that of the hare wallaby by its reliance during daylight hours on cool and humid caves and rockpile shelters to conserve water. Arid-zone marsupials thus appear physiologically and behaviourally well buffered to withstand the rigours of their habitat, but the environmental changes wrought by European colonisation of the continent increasingly put these adaptations to the test.

Glossary

CWR

The critical weight range of 35 g–5.5 kg for which Australian marsupials have been found most vulnerable to extinction.

Stress

An unfavourable body condition originally defined by Hans Selye as ‘a state of non-specific tension in living matter’.

Stressor

An environmental factor that will provoke stress if sustained.

Allostasis

Originally conceived as ‘maintaining stability through change’ and introduced into the medical literature to deal with situations, such as fever, where the body changes to a new regulated state, with a change in the set point for body temperature. The concept has been developed by biologists who have introduced the concept of ‘allostatic load’, which can be monitored through changes in circulating levels of adrenal corticosteroids.

Glucocorticoids

Steroid hormones secreted by the adrenal glands in vertebrates that are released under stressful conditions and act to mobilise glucose reserves in the body.

Allostatic overload

A condition equivalent to chronic stress.

‘milieu intérieur’

The ‘internal environment’ of animals identified by the French physiologist, Claude Bernard in 1878, as the closely regulated condition common to all vertebrate animals and on which their independence from the external environment depends.

Homeostasis (also homoiostasis)

The term introduced by the American physiologist, Walter Cannon in 1929, to describe the process by which the ‘internal environment’ of vertebrates is protected from change.

ADH

Antidiuretic hormone, which is secreted by the posterior lobe of the pituitary gland and, when released into the blood, stimulates reabsorption of water from the kidney of vertebrates, reducing urine production and assisting in coping with water deprivation and dehydration.

Heterothermy

Significant variation throughout the day in body temperature – as opposed to homeothermy in which body temperature is maintained between narrow limits.

Adaptive heterothermy

The process originally described in desert camels whereby they contend with excessive heat by allowing their body temperature to rise, thus storing heat that may then be lost at night by radiation.

Carotid rete

A group of specialised blood vessels in the base of the brain of some mammals that operates to cool warmed blood flowing to the brain by countercurrent exchange.

Crepuscular

Animals that commence their activity at dawn and dusk.

Torpor

A condition in which an animal ceases activity for a period of time and is associated with a significant fall in both body temperature and metabolic rate. Torpor may last for hours or days and is truncated by spontaneous arousal of the animal with a rapid rise in its body temperature back to normal levels.

Leptin

Often known as the ‘satiety hormone’, is a hormone produced by fat cells that helps to regulate energy balance by inhibiting hunger.

Ghrelin

Also called the ‘hunger hormone’ is a peptide hormone, made up of a small number of amino acids, that is produced by cells in the intestinal tract and acts on the central nervous system to increase appetite.

Arcuate nucleus

A group of nerve cell bodies in the hypothalamus of the brain that contain important neurotransmitters involved in controlling hormone release from the pituitary gland.

Neuropeptide Y

Neurones (NPY) are also located in the arcuate nucleus and are important in the regulation of appetite.

Tanycytes

Special cells found in the brain and on the floor of the fourth ventricle, which have processes extending deep into the hypothalamus. It is thought that their function is to transfer chemical signals from the cerebrospinal fluid to the central nervous system.

Thyroidectomy

Removal of the thyroid gland.

Deiodinase

Specific enzymes that break down the hormone thyroxin (T₄) by successively removing iodine molecules.

Iodothyronine (T₃)

The active form of the hormone thyroxin, which has three molecules of iodine instead of four.

Pars tuberalis

A group of cells located around the stalk of the pituitary gland that contain hormone-secreting cells.

Brown fat

Highly metabolically active tissue found in eutherian mammals that produces heat to restore the normal body temperature of torpid mammals. Brown fat is not found in marsupials, which recover from torpor by shivering.

ADH (anti-diuretic hormone)

A hormone secreted by the posterior lobe of the pituitary gland, which acts on the kidney to enhance reabsorption of water from the urine when animals are dehydrated or water deprived.

HPA axis (hypothalamo-pituitary-adrenal axis)

Many of the hormones secreted by the pituitary gland (e.g. growth hormone, thyroid-stimulating hormone, adrenocorticotropic hormone (ACTH), etc.) are controlled by small molecule ‘releasing factors’ elaborated in the hypothalamus of the brain and transported to the pituitary gland by a dedicated portal blood supply. Stressors act via the HPA to activate secretion of hormones, firstly from the pituitary gland, which then go on to stimulate other glands in the body, such as the adrenals.

Doubly-labelled water

This is water where the heavy isotope of oxygen (¹⁸O) replaces normal oxygen (¹⁶O) and hydrogen is replaced by either deuterium (²H) or radioactive tritium (³H). When injected into animals, the differential turnover of the two isotopes enables one to measure the rate of carbon dioxide production in free-ranging animals and hence their field metabolic rate (FMR).

Macropodids

Marsupial species belonging to the family Macropodidae (large foot) which includes the kangaroos and wallabies.

Osmolality

The osmotic pressure of a liquid that is a function the number of molecular components dissolved in the fluid (e.g. plasma or urine).

Water economy index (WEI)

The ratio of water influx to FMR and a measure of animal’s adaptation to low water regimes.

Eosinophil

One type of white-blood cell and one of the immune system’s components responsible for combating multicellular parasites and certain infections in vertebrates. Their numbers are often used as a measure of the competence of the animal’s immune system.

Anaemia

A reduction in the number of red cells in the blood, and its haemoglobin content, resulting in a lowering of the oxygen-carrying capacity of the blood.

U/P_OSM

The ratio of the osmotic pressure of the urine relative to the plasma is a measure of the concentrating capacity of the kidney and increases when animals are water deprived.

Renal plasma flow (RPF)

The rate at which blood flows through the kidneys.

Glomerular filtration rate (GFR)

The rate at which blood is filtered in the kidney to produce urine. GFR is usually measured by the rate of clearance of inulin, a plant polysaccharide, and expressed as C_IN.

C_OSM/C_IN

Relative osmolar clearance.

Dry sheep equivalent (DSE)

The amount of energy that a marsupial requires per day compared with a similar-sized sheep. The figure of 0.7 is usually quoted and reflects the fact that the basal metabolic rate (BMR) of marsupials is approximately 30% lower than that of eutherian mammals.

‘Diabetogenic’ effect of steroid hormones

So-called because steroids such as cortisol and corticosterone increase blood sugar levels when injected.

C_UREA/C_IN

Relative urea clearance and the amount of urea cleared from the blood relative to the rate of glomerular filtration.