GENERAL AND COMPARATIVE

ENDOCRINOLOGY

General and Comparative Endocrinology 133 (2003) 273–278

www.elsevier.com/locate/ygcen

The effects of age, season, and gender on serum cortisol levelsin the tammar wallaby, Macropus eugenii

Sarah McKenzie and Elizabeth M. Deane*

Division of Environmental and Life Sciences, Macquarie University, North Ryde, NSW, 2109, Australia

Accepted 24 April 2003

Abstract

Serum cortisol levels were measured in a total of 73 tammar wallabies maintained in a captive population at Macquarie Uni-

versity, NSW, Australia. Previous studies of corticosteroids in marsupials have generally involved low sample numbers, a diverse

array of analytical techniques, and a variety of sampling conditions. We have conducted a substantive, longitudinal study of serum

cortisol levels using a radioimmunoassay protocol, and data have been analysed with respect to age, sex, and seasonality. There were

no apparent effects of age or sex on serum cortisol levels, although an inverse but non-significant relationship was observed between

males and females. However a significant difference in serum cortisol levels was observed between seasons, with mean serum cortisol

significantly higher in summer than in autumn. These data will serve as a reference for �normal� ranges of serum cortisol levels,

particularly in the female tammar wallaby. As deviations from these values can indicate compromised animal health and well-being,

this information will assist wildlife managers in assessing and monitoring the health status of individuals in captive and free-ranging

populations.

� 2003 Elsevier Science (USA). All rights reserved.

1. Introduction

Successful maintenance and breeding of captive

wildlife populations requires knowledge of their basicbiology and behaviour, as well as the tools to monitor

their well-being. In eutherian mammals, an important

biological measure of this well-being is the level of cir-

culating glucocorticoids. Glucocorticoids are released

from the adrenal gland as a result of a cascade of events

initiated by a disturbance to homeostasis (Moberg,

1987). The hypothalamus releases corticotrophin-re-

leasing hormone (CRH), which in turn stimulates therelease of adrenocorticotrophin (ACTH) from the pi-

tuitary gland. ACTH subsequently acts on the adrenal

gland, resulting in the release of glucocorticoids (Matteri

et al., 2000). These glucocorticoids, primarily cortisol

and corticosterone, are important mediators of the

metabolic response to stress. An increase in glucocorti-

coid concentration results in a diversion of energy away

from non-essential activities, and the increased produc-

* Corresponding author. Fax: +61-2-9850-9671.

E-mail address: edeane@els.mq.edu.au (E.M. Deane).

0016-6480/$ - see front matter � 2003 Elsevier Science (USA). All rights res

doi:10.1016/S0016-6480(03)00185-0

tion of readily usable energy, in the form of increased

plasma glucose concentration. In the short-term, chan-

ges mediated by glucocorticoids are adaptive, and assist

in coping with and surviving a stressor (Matteri et al.,2000; Munck et al., 1984). However, chronic activation

of this response has numerous deleterious effects, par-

ticularly on immune and reproductive function (Sapol-

sky, 1992; Wingfield et al., 1998).

Cortisol has been identified as the major glucocorti-

coid in the blood of the majority of marsupial species

studied to date (Table 1). However some researchers

have identified corticosterone and 11-deoxycortisol insignificantly higher amounts in the koala (Oddie et al.,

1976; Scoggins 1978) and wombat (Oddie et al., 1976)

respectively, whilst 21- and 11-deoxycortisol have been

identified as minor components in a number of species

(Weiss, 1968; Weiss and McDonald, 1967; Weiss and

Richards, 1970).

Similarly, documented responses to ACTH vary. In

some marsupials, including the tammar wallaby (Cooleyand Janssens, 1977; Janssens and Hinds, 1981; Janssens

and Tyndale-Biscoe, 1982) the brushtail possum

(Than and McDonald, 1973; Than and McDonald,

erved.

Table 1

Summary of reported methods used to measure cortisol in marsupials and associated results

Species Concentration (number of animals in study) Primary method of analysis Reference

Brushtail possum 144lg dL�1 (n ¼ 6)� Chromatography Chester Jones et al., 1964��

Wombat 1.1–1.4lg dL�1 (n ¼ 2F) Chromatography Weiss and McDonald, 1966

3.1lg dL�1 (n ¼ 1M)

Grey kangaroo 2.0–8.1lg dL�1 (n ¼ 6) Chromatography Weiss and McDonald, 1967��

1.8� 1.1lg dL�1 (n ¼ 7) Double isotope derivation Oddie et al., 1976

Koala 6.3lg dL�1 (n ¼ 1) Chromatography Weiss and Richards, 1970��

10–36nmol/L (n ¼ n=a) (Charcoal separation) McDonald et al., 1990

Tasmanian devil 2.8–7.5lg dL�1 (n ¼ 3) Chromatography Weiss and Richards, 1971��

(Thin layer)

Eastern quoll 3.2–7.0lg dL�1 (n ¼ 3) Chromatography Weiss and Richards, 1971��

(Thin layer)

Tammar wallaby 2.8� 0.4 ng dL�1 (n ¼ 3) Chromatography, competitive Catling and Vinson, 1976

protein-binding assay

Black-tailed wallaby 1.1� 0.2lg dL�1 (n ¼ 3) Double isotope derivation Oddie et al., 1976

Bennett�s wallaby 1.7� 0.6lg dL�1 (n ¼ 4) Double isotope derivation Oddie et al., 1976

Chuditch 2.9lg dL�1 (n ¼ 1) Double isotope derivation Oddie et al., 1976

Quokka 1.2� 0.5lg dL�1 (n ¼ 7) Double isotope derivation Oddie et al., 1976

0.75� 0.10lg dL�1 (n ¼ 17F) Radioligand assay McDonald and Bradshaw, 1977

0.93� 0.14lg dL�1 (n ¼ 9 M)

Sugar glider 4.4� 0.3mmol/L (n ¼ 5) Extraction and RIA Bradley and Stoddart, 1990

*Adrenal venous blood only.**Animals under anaesthetic.

274 S. McKenzie, E.M. Deane / General and Comparative Endocrinology 133 (2003) 273–278

1974a,b), the dusky antechinus (McDonald et al., 1981),

and the sugar glider (Bradley and Stoddart, 1990), ex-

posure to ACTH resulted in increased plasma glucose,

glycosuria, increased liver glycogen, and weight loss due

to protein mobilisation. In contrast, however, in the red

kangaroo (Griffiths et al., 1969), red-bellied pademelon

(Martin and McDonald, 1986) and the quokka (Mc-

Donald and Bradshaw, 1981), the diabetogenic effect ofglucocorticoids (i.e., increased plasma glucose and de-

creased insulin sensitivity) was absent.

These studies used variable capture and sampling

conditions that may have affected the levels of stress

being experienced by the test animal as well as a variety

of analytical techniques and very low sample sizes (Ta-

ble 1). All of these factors make direct comparisons

difficult. This study has made use of the recent refine-ments in immunoassay protocols and access to a captive

breeding population of the tammar wallaby, Macropus

eugenii (Marsupialia: Macropodidae) to undertake a

systematic study of serum cortisol levels in these ani-

mals, and reports the normal range of serum cortisol

and the effect of variables, including age, sex, and season

on these levels.

2. Methods

2.1. Animals and sample collection

The animals used in this study were part of a captive

breeding colony maintained at the Macquarie Univer-

sity Fauna Park, Sydney, Australia. The colony ishoused in enclosures ranging in size from 150–225m2,

and fed a diet of commercially available pellets, with

water ad libitum. A total of 83 blood samples were

collected from 73 individuals during the sampling pe-

riod, in summer (October–December 2001) and autumn

(March–April 2002). In summer, 22 females and 6 males

were sampled, with 13 animals in the 1- to 2-year-old

group, 16 in the 2- to 3-year-old group, and 9 animals

older than 3 years of age. In autumn, 34 females and 11males were sampled, with 7 animals in the 0- to 1-year-

old age group, 18 in the 1- to 2-year-old group, 10 in the

2- to 3-year-old group, and 10 animals older than 3

years of age. Eighteen males and 18 females were sam-

pled twice and a number of animals moved from a

younger to older age group during the study period.

Low numbers of males were available for the study

due to the husbandry practice of removing surplus malesas pouch young. In addition, blood samples for serum

cortisol analysis were taken opportunistically from ani-

mals in the 0- to 1-year old age group, and were not

available in the summer 2001 sampling period. Animals

suffering from injury, recent ill health, or recovering

from surgery or other procedures were excluded from

the study.

Standard capture protocols used in the MacquarieUniversity Fauna Park were observed. These involved

quietly herding animals to a corner of their enclosure

and capturing the animals using large hand held nets.

Immediately on capture animals were transferred to a

hessian sack and placed in the shade. This immediately

calms the animals. After capture, animals were weighed

and approximately 3ml of blood was taken from the

caudal vein at the base of the tail. This was transferredinto a vacuette serum tube (Interpath Services, Caring-

S. McKenzie, E.M. Deane / General and Comparative Endocrinology 133 (2003) 273–278 275

bah, NSW), and the tube was gently inverted repeatedlyfor one minute, then placed in an insulated container.

All blood samples were taken within 30min of capture.

Capture and sampling occurred between 7.30 and 9.30

a.m. in order to minimize the possibility of heat stress,

and to avoid the possible effects of diurnal variation in

serum cortisol levels.

All blood samples were coagulated for 2 h and then

centrifuged at 450g for 15min at 4 �C, the serumtransferred into 1.5ml microtubes (Sarstedt, Germany)

and stored at )20 �C until analysis.

This project was carried out with the approval of the

Macquarie University Animal Ethics Committee, ap-

proval number 2001/006.

2.2. Cortisol radioimmunoassay

All serum samples were analysed by radioimmuno-

assay (RIA) using an Active Cortisol RIA Kit (DSL-

2000, Diagnostic Systems Laboratories, Texas, USA),

according to the manufacturer�s instructions. This RIA

uses a specific rabbit anti-cortisol antibody, and is based

on competitive-binding principles. The Active Cortisol

RIA has a sensitivity of 0.3 lg dL�1, and cross-reactiv-

ities were as follows: cortisol 100%, prednisolone33.33%, corticosterone 9.3%, 11-deoxycortisol 3.8%,

cortisone 2.22%, prednisone 1.42%, 17a-hydroxypro-gesterone 1%, 11-deoxycorticosterone 0.61%, dexa-

methasone 0.38%, testosterone 0.14%, progesterone

0.12%, epiandrosterone 0.04%, dehydroepiandrosterone

0.02%, and estradiol 0.02%.

Radioactivity was counted in a gamma counter

(LKB-Wallac CliniGamma 1272) for one minute andresults were expressed as counts per minute (cpm) and

use to generate a standard curve to convert results to

lg dL�1. Intra-assay variation was calculated by fol-

lowing the assay results of six replicates each of two

samples and the calculated maximum was 10%. Inter-

assay variation was calculated by following the assay

results of two duplicate samples during each radioim-

munoassay procedure. It was calculated to be 16%.

2.3. Statistical analysis

Standard curves were generated using GraphPad

Prism 3.02 (GraphPad Software) and GenTerm V2.B

Table 2

Serum cortisol levels in different age groups of the tammar wallaby

Age group

0–1 y.o. 1–2 y.o.

Summer N/A 24.01� 1.52 (n ¼ 13)

Autumn 24.50� 2.68 (n ¼ 7) 18.65� 1.70 (n ¼ 18)

Data is expressed as means� SEM; cortisol in lg dL�1.

Summer: not significant, p ¼ 0:7

Autumn: not significant, p ¼ 0:4.

(Wallac). Data are expressed as mean� SE, and wereanalysed using SPSS for Windows. Following Levene�stest for homogeneity of variance, comparisons between

age groups were made using one-way ANOVA, between

sexes using independent t tests and between seasons by

using paired samples t tests (p < 0:05). When seasonal

comparisons were made, only those animals that had

been sampled in both summer and autumn were in-

cluded in the analysis. Outliers, identified by GenTermV2.B (Wallac), were not included in any of the analyses.

Significance level was p < 0:05.

3. Results

Table 2 shows serum cortisol levels in tammar wal-

labies in age groups 0–1 years (autumn only), 1–2 years,2–3 years, and older than 3 years in summer (October–

December 2001) and autumn (March–April 2002). Se-

rum cortisol concentration did not differ significantly

between age groups, although variation in the range of

concentrations was observed. In summer, serum cortisol

concentration in animals in the 1- to 2-year old (y.o.) age

group (n ¼ 13) ranged from 11.89 to 31.01 lg dL�1, in

the 2–3 y.o. age group (n ¼ 16) from 12.99 to30.97 lg dL�1, and in the >3 y.o. age group (n ¼ 9) from

1.71 to 38.30 lg dL�1. In autumn, this variability was

again observed, with serum cortisol concentration in the

0–1 y.o. age group (n ¼ 7) ranging from 17.19 to

38.03 lg dL�1, in the 1- to 2-year old (y.o.) age group

(n ¼ 18), from 7.34 to 36.71 lg dL�1, in the 2–3 y.o. age

group (n ¼ 10) from 10.09 to 31.79 lg dL�1, and in the

>3 y.o. age group (n ¼ 10) from 10.46 to 41.35 lg dL�1.When data were combined, the mean serum cortisol le-

vel for the tammar wallaby was 22.75� 1.60 lg dL�1

(n ¼ 28) in the summer sampling period, and

20.48� 1.16 lg dL�1 (n ¼ 45) in the autumn sampling

period.

Serum cortisol levels of female and male tammar

wallabies are presented in Table 3. No significant dif-

ference was observed between the sexes. In the summer,males (n ¼ 6) had an average serum cortisol concentra-

tion of 23.04� 2.67 lg dL�1, which was higher than the

average level of 22.67� 1.93 lg dL�1 in females (n ¼ 22).

In autumn, this pattern was reversed, with the average

serum cortisol concentration of females (20.95

2–3 y.o. >3 y.o.

22.89� 2.57 (n ¼ 6) 20.82� 4.27 (n ¼ 9)

19.61� 2.33 (n ¼ 10) 21.83� 2.99 (n ¼ 10)

Table 3

Serum cortisol level in female and male tammar wallabies

Sex

Female Male

Summer 21.79� 2.12 (n ¼ 19) 24.76� 2.22 (n ¼ 6)

Autumn 20.95� 1.43 (n ¼ 34) 19.03� 1.81 (n ¼ 11)

Data is expressed as means�SEM; cortisol in lg dL�1.

Summer: not significant, p ¼ 0:4.

Autumn: not significant, p ¼ 0:5.

Table 4

Seasonal change in serum cortisol level in the tammar wallaby

Season

Summer Autumn

Cortisol 24.63� 1.62 (n ¼ 18)� 18.12� 1.51 (n ¼ 18)�

Data is expressed as means�SEM; cortisol in lg dL�1.* Indicates a significant difference between seasons, p < 0:01.

276 S. McKenzie, E.M. Deane / General and Comparative Endocrinology 133 (2003) 273–278

� 1.43 lg dL�1, n ¼ 34) being higher than that of males

(19.03� 1.81 lg dL�1, n ¼ 11). During the autumn

sampling period, 26 of 37 females were carrying pouch

young. However, when the serum cortisol concentra-tions of these females were compared with males, the

difference was not significant.

Significant seasonal variation in serum cortisol levels

was apparent in this study. Levels of cortisol in indi-

viduals that had been sampled in both summer and

autumn were analysed by a paired t test, which revealed

that the mean serum cortisol concentration in summer

(24.63� 1.62 lg dL�1) was significantly higher (p < 0:01)than the mean concentration in autumn (18.12�1.51 lg dL�1) (Table 4).

There was a high level of variation in serum cortisol

concentration between individuals within the popula-

tion. This was reflected in the range of serum cortisol

concentrations, from 1.71 to 41.35 lg dL�1. This vari-

ability was evident between individuals within age

groups and sexes.

4. Discussion

This longitudinal study of a captive population of the

tammar wallaby has allowed us to document the normal

range of serum cortisol levels and to examine the effect

of age, sex, and season on these levels. In contrast toprevious studies, in which sample sizes were low, sam-

pling conditions were highly variable and a variety of

methods employed, we have tested a larger population

of animals over two seasons and in some instances, were

able to sample from the same animal during the study

period. This, in combination with the use of a consistent

and reliable RIA protocol, has provided the information

to establish a database of serum cortisol for the tammar

wallaby. The tammar wallaby has been positioned as a�model� for marsupial research (Tyndale-Biscoe and

Janssens, 1988), and as such, it is essential the funda-

mental biological parameters be documented. Such data

not only provide a basis for monitoring well-being in

captive populations but may also be valuable for com-

parisons with different species.

Age-related changes in serum cortisol concentration

were not evident in the tammar wallaby, and the dif-ferences in concentration between each age group were

not significant. Similarly, there was no significant dif-

ference between the sexes in serum cortisol concentra-

tion. However, males had apparently higher levels than

females in summer, although this relationship was not

significant and the numbers of male samples available

were limited. For all animals there was a significant

difference in mean serum cortisol concentration betweenseasons. Serum cortisol concentration was significantly

higher in summer than in autumn. The variability in

serum cortisol concentration between the sexes, and

significantly between the seasons, may be reflective of

the reproductive cycle of the tammar wallaby. Mating

occurs in the summer, when the males had higher serum

concentrations, while females are carrying growing

pouch young in autumn, during which time the serumcortisol concentration of females was higher than that of

males.

The mean serum cortisol concentration in the tam-

mar wallaby reported in this study is higher than that

reported by Cooley and Janssens (1977), who found an

average of 15.6� 0.64 lg dL�1 (n ¼ 3), using a radioli-

gand assay, which involved extraction and dilution of

samples. However, in addition to methodological dif-ferences, the season in which this study was conducted

was not given, and may be responsible for the discrep-

ancy, as the average value reported approaches that

found in this study in autumn, of 18.12� 1.51 lg dL�1

(n ¼ 38). In the quokka, only traces of cortisol

(0.42� 0.09 lg dL�1) and corticosterone (0.37� 0.05

lg dL�1) were detected in serum (McDonald and

Bradshaw, 1977), using a radioligand assay and extrac-tion and dilution of samples. In the koala, corticoste-

rone was measured at 0.07� 0.06 lg dL�1 while cortisol

was not detected, although the method of analysis was

not reported (Scoggins, 1978). Methodological differ-

ences could account for the large difference in quantities

of cortisol detected, given that with new techniques

samples no longer require extraction and that the sen-

sitivity of radioimmunoassays (0.3 lg dL�1) exceeds thatof earlier methods. Additionally, measurements re-

ported for the red and eastern grey kangaroos under

anaesthesia (Weiss and McDonald, 1967) and eastern

grey kangaroos immediately after they had been shot

(Coghlan and Scoggins, 1967), may not be reflective of

baseline cortisol levels. These early studies had low

sample sizes and used chromatographic mobility for

S. McKenzie, E.M. Deane / General and Comparative Endocrinology 133 (2003) 273–278 277

quantification, reporting concentrations in nmol/L,further complicating comparisons.

A number of studies have investigated the variation of

serum cortisol concentration between the sexes. Cortisol

secretion rate was found to be greater in female thanmale

brushtail possums (Than and McDonald, 1973), wom-

bats (Weiss andMcDonald, 1966), and in eastern and red

kangaroos (Weiss and McDonald, 1967). Additionally,

females were found to have higher serum cortisol levelsthan males of the Tasmanian devil and tiger quoll (Weiss

and Richards, 1971), eastern grey kangaroo (Coghlan

and Scoggins, 1967), and quokka (McDonald and

Bradshaw, 1981). No significant difference between the

sexes was found in the echidna (Weiss and McDonald,

1965). However, apart from the study of the quokka, in

which 17males and 9 females were compared, sample size

for each of these studies of other species was very low,ranging from one female to 3 females, and hence the re-

ported results are not statistically robust. Comparisons

are also made difficult where studies did not include de-

tails as to whether sampled females were carrying pouch

young. Additionally, many studies report large variation

between individuals within the study population (e.g.,

McDonald and Bradshaw, 1977), and where sample sizes

are small, this variability may be responsible for reporteddifferences, rather than a real dimorphism.

Age is not a variable that has been considered in most

studies, although Catling and Vinson (1976) found that

plasma cortisol concentration did not change with age in

pouch young of the tammar wallaby. Age has been

found to be a factor influencing haematological and

serum biochemical values in the tammar wallaby

(McKenzie et al., 2002), but this does not appear toaffect serum cortisol levels.

Seasonal variation in corticosteroid levels has been

reported for the koala (McDonald et al., 1990), while no

difference between seasons was observed in the quokka

(Miller and Bradshaw, 1979). However, it was reported

that cortisol levels were higher at the end of summer

than in the spring. Levels reported in this study were

also greater in the summer, although these were relativeto autumn. As discussed earlier with respect to repro-

ductive status, the cortisol levels of males may have been

greater in the summer due to breeding activity, and that

of females greater in autumn due to the energetic de-

mands of the growing pouch young. However, the dif-

ference between the sexes was not significant in either

season, implying that reproductive status is not the un-

derlying cause of seasonal variation in serum cortisolconcentration in the tammar wallaby.

We have conducted a longitudinal study into the se-

rum cortisol concentrations of the tammar wallaby.

Analysis of variables revealed that serum cortisol is not

affected by the age or sex of an animal, but does vary

seasonally. These factors must be taken into account

when using serum cortisol as a measure of animal

health. The large variation between individuals mustalso be considered, and emphasises the importance of

baseline values for each individual animal being as-

sessed. It is the individual animal�s response to stress

which is meaningful, therefore, a profile must include

both unstressed (baseline) and stressed measurements

for each individual being monitored.

Acknowledgments

Thank you to the staff and volunteers at the Mac-

quarie University Fauna Park, as well as members of the

Marsupial CRC, for assistance with animal capture and

blood sampling. Dr Sinan Ali and Dr Rita Holland

provided invaluable assistance, advice and lab space, aswell as access to a gamma counter. SM was supported

by an ARC Linkage grant with Perth Zoo.

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