Water and electrolyte homeostasis and kidney function of desert-dwelling marsupial wallabies in Western Australia
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J Comp Physiol B (2001) 171: 23±32 Ó Springer-Verlag 2001
ORIGINAL PAPER
S. D. Bradshaw á K. D. Morris á F. J. Bradshaw
Water and electrolyte homeostasis and kidney function
of desert-dwelling marsupial wallabies in Western Australia
Accepted: 24 August 2000
Abstract Prolonged drought, necessitating conservation although the hare-wallaby is superior to the rock-
of water, is one of the major environmental challenges wallaby in this respect. Rock-wallabies appear to rely
faced by many Australian marsupials. Radioactive iso- primarily on behavioural rather than physiological
topes of water and sodium were used to assess the ability responses for their survival in the Pilbara and appear to
of two species of marsupial wallabies to maintain water be more vulnerable to extinction in the event of signi®-
and electrolyte balance during periods of extreme water cant habitat modi®cation. The secure nature of their
deprivation in the arid Pilbara region of Western Aus- rock habitat, however, means that they have suered less
tralia. The spectacled hare-wallaby, Lagorchestes than hare-wallabies in the recent past.
conspicillatus, has the lowest mass-speci®c rate of water
turnover at 27.5 ml á kg)0.82 á day)1 yet reported for any Key words Marsupial á Kidney function á Wallaby á
mammal and was two to three orders of magnitude Desert á Water
lower than that of the Rothschild's rock-wallaby, Pet-
rogale rothschildi. Studies of renal function show that Abbreviations ADH anti-diuretic hormone á CH2 O free-
the hare-wallaby conserves water by producing a highly water clearance á CI condition index á COSM osmolar
concentrated urine under the in¯uence of lysine vaso- clearance á CPAH clearance of 3H-para-amino hippuric
pressin (LVP), the anti-diuretic hormone (ADH) in acid á ECFV extracellular ¯uid volume á FF ®ltration
macropodid marsupials. In contrast, rock-wallabies fraction á FRH2 O fractional reabsorption of the
show unusual renal responses to water deprivation, with ®ltrate á LVP lysine vasopressin á PAH 3H-para-amino
no change in LVP levels and a limited response to water hippuric acid á RH relative humidity á TBW total body
deprivation involving a reduction in renal plasma ¯ow water content á U/POSM urine-to-plasma ratio of
and glomerular ®ltration rate, with no signi®cant change osmolytes
in tubular function. Both species are able to maintain
water and electrolyte homeostasis during periods of
drought, highlighting the ecacy of their diering
adaptive solutions to the problem of water scarcity, Introduction
Seventy percent of the Australian environment is classi-
®ed as arid or desert and water is a major limiting
Communicated by I. D. Hume resource for animals inhabiting these regions. Measure-
ments of rates of water turnover of free-ranging indi-
Preliminary communications of some of these data have been made viduals, using isotopes of hydrogen (Nagy and Costa
at the 13th International Congress of Comparative Endocrinology
in Yokohama in 1997 and at the Australian Mammal Society 1980; Nagy and Peterson 1988; Green 1997), provide a
meeting in Perth in December 1998 means of assessing the extent to which dierent species
are buered from the eects of long-term drought by the
S. D. Bradshaw (&) á F. J. Bradshaw ecacy of their homeostatic regulatory systems (Brad-
Department of Zoology and Centre for Native Animal Research, shaw 1997). Studies of renal function also enable us to
The University of Western Australia, Perth, WA 6009, Australia
e-mail: Don.Bradshaw@uwa.edu.au gauge the extent to which pituitary and adrenal hormones
are responsible for maintaining ¯uid and electrolyte ho-
K. D. Morris
Science Information Division, meostasis of desert-dwelling marsupials that are routinely
Department of Conservation & Land Management, exposed to long periods of water deprivation that may
Woodvale, WA, 6026, Australia involve stress responses de®ned as: ``the physiological24
resultant of demands that exceed an organism's regula-
tory capacities'' (Bradshaw 1986, 1992). Materials and methods
Bakker and Bradshaw (1983) studied renal function
Study areas
in the spectacled hare-wallaby, Lagorchestes conspicill-
atus, from Barrow Island and suggested that its ex- Field studies were carried out on Enderby Island (Latitude:
tremely ecient water economy was linked to its ability 20°36¢33¢¢S, Longitude: 116°31¢12¢¢E)and Barrow Island (Latitude:
to recycle nitrogen in the form of urea to its digestive 20°47¢57¢¢S Longitude: 115°24¢18¢¢E) in the arid Pilbara region of
tract. They also proposed a mechanism for urea recy- Western Australia, some 1500 km north of Perth. Field trips to
Barrow Island were carried out in November 1990, April 1991 and
cling based on a signi®cant positive correlation that they April 1992; trips to Enderby Island were in March and November
observed between urea clearance and rates of urine 1986, December 1987 and February 1989. Barrow Island is ap-
production ± suggesting that urea recycling was initiated proximately 80 km from the coast whereas Enderby Island forms
by elevated levels of anti-diuretic hormone (ADH). part of the Dampier Archipelago and lies 5 km o the coast. The
islands are exposed to a summer rainfall reÂgime, derived from pe-
Their study was limited, however, by the lack of a riodic cyclones, which deposit extremely variable amounts of rain
suitable assay for marsupial ADH. This was subse- from year to year. The ocial ``average'' rainfall on Barrow Island
quently identi®ed as lysine vasopressin (LVP), rather is, for example, 330 mm (1968±1988) but may vary from 122 mm
than arginine vasopressin in the macropodid marsupials (in 1990) to 750 mm in 1974 following a large cyclone which de-
posited over 250 mm in 24 h. Monthly mean rainfall data for
by Chauvet et al. (1983). The development of an heter- Barrow Island are shown in Fig. 1.
ologous radio-immunoassay for LVP paved the way for
further studies of the role of this hormone in controlling
the water economy of a variety of marsupial species, Microclimatic data
including those from desert habitats (Bradshaw 1990,
1997; Jones et al. 1990). Temperature and humidity data collected during each of the ®eld
trips to Barrow and Enderby Islands are summarised in Tables 1
The present study focused on two desert-dwelling and 2, along with the amount of rainfall that had fallen in the
macropodid wallabies found living on islands o the 1 month prior to each trip. Temperature and relative humidity
arid north-west coast of Western Australia. One, the were recorded continuously with Thiess hygrothermographs that
spectacled hare-wallaby L. conspicillatus, is now only were calibrated with a Schlutheis mercury thermometer and a sling
found in abundance in spinifex grasslands on Barrow psychrometer before use.
Island, some 1500 km north of the capital, Perth, and
its ability to maintain thermal balance in this hot, dry Animals and turnover measurements
habitat has been previously studied by Dawson and
Bennett (1978). Rothschild's rock-wallaby, Petrogale Rock-wallabies (P. rothschildi) were collected on Enderby Island in
rothschildi, is a species endemic to the Pilbara region of Bromilow traps (Kinnear et al. 1988), baited with apple. Traps
WA and found associated with large rock piles oering were set at dusk and cleared throughout the night at 3-h intervals.
Wallabies were taken to a ®eld laboratory set up on the Island
caves and caverns suitable for refuge during the day. where blood (ca. 10 ml) for hormone measurements was immedi-
The two species thus dier in the extent of their ex-
posure to the aridity of their habitat ± the hare-wallaby
shelters during the day within large spinifex clumps
where temperatures rise to over 40 °C. The rock-wal-
laby, on the other hand, avoids the heat of the day by
sheltering in cool, humid caves where the air temper-
ature rarely exceeds 30 °C and one would expect its
water economy to bene®t as a result of this. The two
species thus oer an unique opportunity to compare
the water and electrolyte balance and ecacy of the
hormonal control systems of two macropodid marsu-
pials occupying an arid habitat but possibly diering in
the extent to which they rely on physiological adapta- Fig. 1 Average monthly rainfall for the period 1968±1998 on Barrow
tions for their ultimate survival. Island o the arid Pilbara coast of Western Australia
Table 1 Microclimatic data for Barrow Island ®eld trips 1990±1992. (NS not signi®cant, RH relative humidity)
Trip no. No. of Rainfall 1 month Mean max Mean min Mean max Mean min
and date records prior to trip (mm) temp (°C) temp (°C) RH (%) RH (%)
1 Nov 1990 17 0 34.8 1.3 21.2 0.4 96.9 1.0* 41.2 3.9
2 April 1991 12 0 35.8 0.6 24.3 0.8* 89.4 3.3 39.8 2.7
4 April 1992 6 112 30.2 0.8* 20.2 1.2 88.7 3.6 47.8 7.2
Statistical F2,32 = 4.26 F2,32 = 9.88 F2,32 = 3.95 F2,32 = 0.64
signi®cance P = 0.02 P = 0.0005 P = 0.02 NS
* Indicates which trips are the source of the signi®cant dierences25
Table 2 Microclimatic data for Enderby Island ®eld trips 1986±1989
Trip no. No. of Rainfall 1 month Mean max Mean min Mean max Mean min
and date records prior to trip (mm) temp (°C) temp (°C) RH (%) RH (%)
6 Mar 1986 9 118 31.8 0.6 28.0 0.3* 92.7 2.1* 66.7 2.9*
7 Nov 1986 9 0 31.0 0.5 25.3 0.3 73.7 1.5 44.4 2.2
8 Dec 1987 6 0 31.9 0.3 25.7 0.8 19.2 1.7 56.2 0.4
10 Feb 1989 7 211 33.2 1.2 28.3 0.8* 91.0 3.3* 68.3 5.4*
Statistical F3,27 = 1.61 F3,27 = 8.65 F3,27 = 18.25 F3,27 = 12.70
signi®cance NS P = 0.0003 P = 0.0001 P = 0.0001
* Indicates which trips are the source of the signi®cant dierences
ately taken by cardiac puncture, with approval from the Animal Renal parameters
Ethics Committee of the University of Western Australia. The
blood sample was centrifuged at 3000 rpm, the plasma separated Renal parameters were measured on selected wallabies after their
and then frozen in liquid nitrogen for subsequent analysis. The removal from the metabolism cages, and prior to their release in the
wallabies were then weighed (to 0.01 kg, Salter), measured with late afternoon. Glomerular ®ltration rate (GFR) and renal plasma
vernier calipers (short-leg and pes length in mm used to calculate ¯ow were measured using a clearance technique based on that of
the Condition Index ± see Bakker and Main 1980), marked with ear Sapirstein et al. (1955) and Reid (1969) and modi®ed for use with
tags and injected intramuscularly with 1.0 ml solution containing the hare-wallaby by Bakker and Bradshaw (1983). The wallabies
tritium (3HHO, 16.6MBq/ml, 450 lCi) and sodium-22 (22NaCl, were held in a Hessian bag during the procedure with their tail
0.19 MBq/ml, 5 lCi). The animals were then placed in individual exteriorised and remained very quiet throughout the whole proce-
metabolism cages and held for 12 h in the dark for the collection of dure. A lateral tail vein was cannulated with a Bardicath which was
voided faeces and urine. The animals were not provided with water extended up the vein until it entered the vena cava and then taped
and ambient temperature varied between 15 °C and 28 °C over the securely in place. A bolus injection of 1 ml sterile saline containing
14
12-h period. Twelve hours was chosen as the most suitable time C-inulin (0.18 MBq) and 3H-Para-amino hippuric acid (PAH;
from which a 24-h rate of urine production could be estimated and 3.7 MBq) was given by the cannula and washed in rapidly with
dilution of the tritium isotope by metabolic eater production during 5 ml 2% Heparin in sterile saline. Successive 0.5-ml blood samples
this period was calculated to be minimal. On removal from the at 5, 10, 20, 40, 60, 80 and 120 min were then taken via the cannula,
metabolism cages, the rock-wallabies were bled a second time from centrifuged, and the plasma processed for 3H/14C double isotope
the lateral tail vein (ca. 1 ml) for an equilibration sample from counting. The decline in activity of the two isotopes over time was
which the volume of distribution of the injected isotopes was cal- plotted and curve ®tting, as shown in Fig. 2, enabled the calcula-
culated. The rock-wallabies were released, at their site of capture, tion of the clearances of both inulin and PAH. The extracellular
late in the afternoon on the next day, once ambient temperatures ¯uid volume (ECFV) of each wallaby was estimated from the cal-
had fallen below 30 °C. The rock-wallabies were left undisturbed culated dilution volume at time zero of the injected 14C-inulin ±
for 7±10 days before attempting any recaptures where the proce- estimated by linear regression from the last four points on the
dure was much simpler ± a small blood sample (ca. 1 ml, the disappearance curve (40, 60, 80 and 120 min) according to the
recapture sample) was taken from the tail vein contra-lateral to that procedure of Sapirstein et al. (1955) which is detailed in Bakker
bled initially and the body weight of the animal was recorded. The and Bradshaw (1983). Clearances of electrolytes and osmolytes
wallabies were then released at their site of capture. The procedure were calculated knowing their respective concentrations in plasma
used for processing spectacled hare-wallabies on Barrow Island (P) and urine (U) samples and the rate of urine production (V)
diered only in that the wallabies were captured by hand from a from: Cx Ux/Px á V, where x is the osmolyte concerned. This was
moving vehicle using long-handled nets, rather than being trapped estimated from the urine voided over the 12-h period that the
(Bakker and Bradshaw 1989). Hormone blood samples were taken
within 5 min of capture of the hare-wallaby and they were then
transported to the ®eld laboratory (some 5 km distant) for pro-
cessing as described for rock-wallabies. Metabolism cages were
maintained in an air-conditioned room with an average overnight
temperature of 23 °C.
The decline in the speci®c activity of the injected isotopes was
measured by liquid scintillation spectrometry (Packard Tri-Carb
300CD) in 100 ll plasma samples diluted in 5 ml Pico-Fluor 15
scintillant (Packard). All samples were counted to less than 1%
error and quenching was estimated and corrected for by automatic
external standardisation. Rates of turnover of water were calcu-
lated using the equations of Nagy and Costa (1980) and sodium
turnover was calculated after measuring the sodium-23 concen-
trations of the equilibration and recapture samples in a Varian
(Model 475) atomic absorption (AA) spectrophotomer.
Electrolyte concentrations and osmolality
Plasma sodium and potassium concentrations in the hormone
sample and urine samples were measured in 5-ll aliquots by AA.
Chloride concentrations were measured by amperometric titration
in a Buchler-Cotlove chloridometer on 10-ll aliquots. The osmotic Fig. 2 Representative disappearance curves for intravenously injected
14
pressure of plasma and urine samples was measured on 10-ll sam- C-inluin and 3H-para-amino hippuric acid (PAH) used to estimate
ples in a Wescor model 5100B vapor pressure osmometer, with urine simultaneously renal plasma ¯ow and glomerular ®ltration rate
samples being appropriately diluted with triple distilled water. (GFR) in wallabies26
wallabies had been held in the metabolism cages. The metabolism corresponding with the wet season, and this was also
cages were calibrated individually for losses by adding known re¯ected in mean minimum values for RH.
volumes of distilled water onto the silicone-treated, stainless steel
collecting funnels (0.5±50 ml) and then measuring the volume
collected. A linear regression of y mx + c was calculated where
y volume of ¯uid collected and x volume of ¯uid added. Water and electrolyte homeostasis
Separate equations were derived for the dierent metabolism cages
used for hare-wallabies and rock-wallabies and the equations
were y 1.0262x + 0.1322 (r2 0.98 ) and y 1.93x + 0.796
Data are available for three successive ®eld trips to
(r2 0.99) respectively. All urine samples were corrected using Barrow Island for the hare-wallaby and four to Enderby
these equations and then converted to ml (kg á day))1 to calculate Island for the rock-wallaby. The trips were timed to
rates of V. Free-water clearance (CH2O) was calculated from compare the condition of the rock-wallabies during the
V CH2O + COSM. driest part of the year (November±December) with that
seen following cyclonic rain in late summer and early
Assay of LVP autumn (February±April). Turnover data and informa-
tion on plasma composition for hare-wallabies are
Lys8-vasopressin (LVP) was assayed by RIA using the method shown in Table 3 and compared with similar informa-
originally developed for arginine vasotocin by Rice (1982) and
modi®ed for the measurement of LVP in marsupial plasma by Jones tion for rock-wallabies in Table 4.
et al. (1990). Synthetic [Lys8]-Vasopressin (Sigma V-6879) was Trip 1 in November 1990 coincided with the driest
iodinated (125I) using the chloramine-T oxidation method year yet recorded on Barrow Island with a total of only
of Greenwood et al. (1963) and a high-speci®c activity fraction 122 mm of rain recorded (see Fig. 1 for average precip-
isolated on a Sephadex G25 column. The antibody used (courtesy
of Dr G.E. Rice) was originally raised to Arg8-vasotocin (AVT) but itation data). Despite this drought, the condition of the
also showed high cross-reactivities with Arg8-vasopressin (AVP), hare-wallabies appeared excellent, with condition indices
LVP and phenypressin (Phe3-Arg8-vasopressin). LVP in 1-ml (CI) ranging from 4.3 to 4.9. ANOVA shows that the CI
plasma samples was extracted by absorption of plasma proteins on was just signi®cantly higher in trip 4 (after rain) than on
octadecasilyl silica followed by subsequent elution with acetonitrile
(Bennett et al. 1977) using C-18 Sep-Paks (Waters No. 51910). Free
trip 2 (dry) with F2,101 3.29 and P 0.04. Body mass
and protein-bound LVP were separated by precipitation with an showed a similar trend, with trip 4 animals being sig-
anti-rabbit globulin (IDS Tyne and Wear, UK) and all samples ni®cantly heavier than those collected on dry trips, but
were counted to less than 1% error in a Packard Prias PGD the total body water content (TBW) did not vary sig-
autogamma scintillation counter. Intra- and inter-assay variabili- ni®cantly. Changes in water in¯ux and eux between
ties were 9.8% and 6.4%, respectively.
trips were however dramatic, increasing signi®cantly
from 27.5 ml (kg0.82 á day))1 on trip 1 to 139.1 ml á
Statistical analyses (kg0.82 á day))1 on trip 4. Paired t-tests of in¯ux versus
out¯ux show that the wallabies were in hygric balance on
The distribution of all data was assessed for normality by con-
structing probability plots (Gnanadesikan 1977) and, where trips 2 and 4 but water eux was signi®cantly greater
appropriate, variables were logarithmically transformed prior than in¯ux on trip 1 with paired t13 6.93 and
to statistical analysis. Patterns of variation in the data set were P < 0.001. Given that the rock-wallabies collected on
explored initially through analysis of variance (ANOVA) coupled the next trip in April 1991 showed no decrease in either
with either a Student-Neuman Keuls Test (SNK), a Bonferroni
Test or Tukey HSD post hoc multiple comparisons. The signi®- body mass or condition, it would appear that this im-
cance of dierences between selected group means was also balance was only transitory and perhaps re¯ected the
assessed, where appropriate, by Student's t-test. additional stress brought about by capture and handling.
Sodium in¯ux and eux also varied between trips,
falling signi®cantly after rain, presumably as a result of
Results the extremely high water intake and reduced sodium
content of the vegetation. The sodium pool was
Environmental conditions and microclimatic data low at 42.6 1.0 mmol á kg)1 on trip 1 but increased
signi®cantly to 73.3 1.5 mmol á kg)1 and 72.6
Both Barrow and Enderby Islands are located in the arid 1.2 á mmol á kg)1 on trips 2 and 4 respectively (F2,88
Pilbara region of Western Australia and subjected to the 231.1, P < 0.001).
same summer rainfall reÂgime. Maximum ambient tem- Plasma sodium concentrations varied slightly be-
peratures ranged from 30.2 °C to 35.8 °C on Barrow tween the three trips, ranging from 155.3
Island, being signi®cantly lower in April 1992 than in 1.1 mmol l)1 in the dry seasons to 146.7 0.7 mmol l)1
April 1991, along with the mean minimum temperature after rain (F2,101 17.85 P < 0.001). Plasma potassium
of 20.2 °C (see Table 1). Levels of dew formation are concentrations remained constant however, as did the
always high on Barrow Island and this is re¯ected in the plasma osmolality, indicating that the dry season ani-
elevated measurements for relative humidity (RH) on all mals were not suering from any dehydration which
the trips. Mean maximum temperatures did not dier would elevate their plasma solute concentrations.
signi®cantly over the four ®eld trips to Enderby Island In contrast to the values for the hare-wallabies, data
(see Table 2) but trips 6 and 10 had signi®cantly higher from the four rock-wallaby trips shown in Table 4 were
mean minimum temperatures. Mean maximum humid- much more variable. Much of this variation in the var-
ity levels were high in March 1986 and February 1989, ious parameters recorded is due to trip 6 in March 1986Table 3 Water and electrolyte turnover and homeostasis of spectacled hare-wallabies on Barrow Island (Mean SE with n in parentheses)
Trip no. Body mass Condition Total body Water in¯ux Water Eux Na In¯ux Na Eux [Na+]p [K+]p [OP]p
and date (kg) Index (CI) water (%) ml á (kg0.82 á day))1 ml á (kg0.82 á day))1 mM á (kg á day))1 mM á (kg á day))1 mmol á l)1 mmol á l)1 mosmol á kg)1
1 Nov 1990 2.31 0.06 4.56 0.18 76.4 1.60 27.5 2.0 36.3* 2.5 2.66 0.29 3.07 0.31 151.9 1.1 5.6 0.2 287.3 2.1
(36) (36) (36) (14) (14) (14) (14) (36) (36) (22)
2 April 1991 2.31 0.07 4.29 0.19 79.5 1.20 35.3 2.0 35.9 2.3 3.47 0.32 3.52 0.22 155.3 1.3 5.2 0.1 280.1 2.2
(24) (24) (23) (12) (12) (12) (12) (24) (23) (23)
4 April 1992 2.8 0.04 4.92 0.14 79.7 0.74 139.1 5.9 138.8 5.6 2.21 0.23 2.18 0.34 146.7 0.7 5.6 0.1 285.8 3.3
(43) (42) (29) (13) (13) (13) (13) (42) (42) (41)
Signi®cance F2,102 = 22.6 F2,101 = 3.18 F2,87 = 2.1 F2,38 = 273.1 F2,38 = 246.9 F2,38 = 8.46 F2,38 = 12.95 F2,101 = 17.85 F2,100 = 1.35 F2,99 = 1.61
P < 0.001 P = 0.04 NS P 0.001 P 0.001 P = 0.014 P < 0.001 P < 0.001 NS NS
* In¯ux and out¯ux dier signi®cantly with paired t13 = 6.93 and P < 0.001
Table 4 Water and electrolyte turnover and homeostasis of rock-wallabies on Enderby Island (Mean SE with n in parentheses)
Trip no. Body mass Condition Total body Water in¯ux Water Eux Na In¯ux Na Eux [Na+]p [K+]p [OP]p
and date (kg) Index (CI) water (%) ml á (kg0.82 day))1 ml á (kg0.82 day))1 mM á (kg day))1 mM á (kg day))1 mmol á l)1 mmol á l)1 mosmol á kg)1
6 Mar 1986 2.53 0.11 5.28 0.16 81.3 1.46 160.1 15.6 157.9 14.6 4.91 1.35 4.79 1.30 146.9 1.13 5.17 0.20 283.9 2.57
(32) (32) (12) (4) (4) (4) (4) (15) (15) (15)
7 Nov 1986 3.11 0.13 6.77 0.14 73.0 1.42 60.0 3.3 63.9 4.2 2.27 0.38 2.57 0.36 134.8 4.0 4.6 0.15 293.7 2.7
(39) (39) (26) (18) (18) (17) (17) (33) (32) (33)
8 Dec 1987 3.07 0.14 6.59 0.19 70.3 1.69 65.6 6.8 77.2* 6.8 5.74 0.61 6.31 0.59 137.6 1.12 3.8 0.12 275.8 2.8
(36) (36) (30) (13) (13) (13) (13) (32) (32) (32)
10 Feb 1989 3.32 0.12 6.33 0.14 78.2 1.69 68.9 5.2 81.1* 5.0 2.88 0.37 3.49 0.32 145.9 0.86 3.9 0.12 291.3 2.5
(32) (31) (24) (14) (14) (14) (14) (28) (28) (28)
Signi®cance F4,139 = 5.13 F4,138 = 12.54 F4,92 = 6.57 F4,48 = 20.5 F4,48 = 16.3 F4,47 = 7.75 F4,47 = 9.1 F4,108 = 3.8 F4,107 = 11.98 F4,109 = 7.5
P = 0.001 P < 0.001 P < 0.001 P 0.001 P < 0.001 P < 0.001 P < 0.001 P = 0.006 P < 0.001 P < 0.001
* In¯ux and out¯ux dier signi®cantly with paired t13 = 4.47 and t12 = 6.3 for trips 8 and 10 respectively, P < 0.001
2728
which followed a cyclone and heavy rainfall on Enderby
3.7 0.4
3.4 0.3
Table 5 Renal parameters in spectacled hare-wallabies on Barrow Island compared in dry and wet seasons (Mean SE, n = 6). (CH2 O free-water clearance, CIN clearance of inulin,
COSM osmolar clearance, CPAH clearance of para-amino hippuric acid, ECFV extracellular ¯uid volume, FF ®ltration fraction, FRH2 O fractional reabsorption of ®ltrate, LVP lysine
16.0 2.6
8.8 0.9
pg á ml)1
P = 0.02
pg á ml)1
Island, with 69 mm of rain recorded in the month pre-
LVP
vious to the ®eld trip. The rock-wallabies were in poor
NS
LVP
condition, with a mean body mass of 2.5 0.1 kg and
CI of 5.3 0.2 ± both variables being signi®cantly
ECFV (%)
12.2 0.5
18.8 1.1
P < 0.001
18.3 0.8 lower than on the other three trips (F4,139 5.13,
18.2 1.4 P < 0.001). The TBW of trip 6 animals was also sig-
ECFV
ni®cantly elevated which also re¯ects their poor body
ml á (kg min))1 (%)
NS
condition with a replacement of solids in the body by
ml á (kg min))1
water. The rates of water in¯ux and eux were over
7.94 0.46
twice as high in animals collected on trip 6 than those
6.05 0.43
9.04 1.32
5.80 0.1
P = 0.004
measured during the three other trips, averaging
160.1 15.6 ml (kg0.82 day))1 and 157.9 14.6 ml
CPAH
CPAH
(kg0.82 day))1 respectively. Trip 6 animals were in hygric
NS
balance, however, (i.e. in¯ux eux) in contrast to the
rock-wallabies on trips 8 and 10 when euxes were
signi®cantly greater than in¯uxes over the period of
5.4 0.4
4.2 0.5
8.0 0.4
1.26 0.2
P < 0.001
U/POSM
measurement (Paired t12 4.467 P < 0.001 and paired
U/POSM
t13 6.30 P < 0.001 for trips 8 and 10, respectively).
NS
The sodium pool of trip 6 animals, at 79.3
Table 6 Renal parameters in rock-wallabies on Enderby Island compared in dry and wet seasons (Mean SE, n = 7)
13.3 mmol kg)1, was very signi®cantly higher than
ml á (kg day))1
ml á (kg day))1
measured on the other three trips, which ranged from
99.4 0.12
99.2 0.09
99.6 0.06
46.5 mmol kg)1 to 49.7 mmol kg)1, and plasma sodium
97.8 0.3
P = 0.002
FRH2O
concentrations were also higher in trips 6 and 10 than in
FRH2O
trips 7 and 8 (see Table 4). Plasma potassium concen-
NS
trations showed less variation but were signi®cantly
elevated in trip 6 animals at 5.2 0.20 mmol l)1 com-
ml á (kg day))1 ml á (kg day))1
ml á (kg day))1 ml á (kg day))1
)29.4 3.3
)42.5 4.4
pared with means closer to 4 mmol l)1 on the other
)51.7 5.2
)26.6 9.3
three trips. Plasma osmolality was signi®cantly reduced
P = 0.02
on trip 8 at 275.8 2.8 mosmol kg)1, falling otherwise
CH2O
CH2O
NS
within the normal mammalian range of 285±295
vasopressin, U/POSM urine to plasma ratio of osmolytes, V = rate of urine production)
mosmol kg)1.
107.0 13.3
37.4 4.3
59.2 6.8
58.6 5.7
P = 0.003
Renal function
COSM
COSM
NS
Detailed analysis of renal function in both hare-walla-
bies and rock-wallabies was not possible on all trips, due
14.4 0.96
16.9 2.43
24.3 0.4
31.3 2.5
to logistic limitations and the occasional intervention of
P = 0.01
FF (%)
FF (%)
cyclones which necessitated speedy evacuation from the
®eld, but data from the two species in both wet and dry
NS
seasons are compared in Tables 5 and 6. Clearance data
ml á (kg min))1 ml á (kg day))1
ml á (kg min))1 ml á (kg day))1
are only available from six or seven individuals on each
trip but more extensive data on other related renal pa-
6.9 0.6
50.2 4.6
6.7 1.4
14.3 5.5
P < 0.001
P = 0.01
rameters from more individuals are reported in the text
for comparison.
Rates of urine production were low at 6.9
V
V
0.63 ml kg)1 day)1 in hare-wallabies on the very dry
trip 1 in November 1990 and the urine was highly con-
1.45 0.09
2.69 0.23
0.82 0.05
1.28 0.12
P = 0.001
P = 0.005
centrated with a urine-to-plasma ratio of osmolytes
(U/Posm) of 8.0 0.4 and a mean osmolality of
2357 109 mosmol kg)1. The GFR, measured by the
CIN
CIN
clearance of inulin, was low at 1.45 0.09 ml
kg)1 min)1 and urine plasma ¯ow, measured as the
4, April 1992 wet
10, Feb 1989 wet
1, Nov 1990 dry
8, Dec 1987 dry
clearance of PAH, was also quite low at 6.05
0.43 ml kg)1 min)1, giving a ®ltration fraction (FF) of
Signi®cance
Signi®cance
date season
date season
24.3 0.42%. Fractional reabsorption of the ®ltrate
Trip no.
Trip no.
(FRH2 O ) was thus exceptionally high at 99.58 0.06%.
Osmolar clearance (CH2 O ) was also low at 58.6 ml kg)129
)1 )1
day and CH2 O highly negative at )51.7 5.2 ml 3.4 0.3 pg ml were not dierent from those mea-
kg)1 day)1 as would be anticipated from the elaboration sured during the dry season.
of highly concentrated urine. Plasma LVP levels were
elevated at 16.0 2.6 pg ml)1 and the mean value of a
more extensive sample of hare-wallabies from trip 1 Discussion
which were not part of the kidney function study was
even higher at 39.8 8.8 pg ml)1 (n 18). Maintenance of water and electrolyte homeostasis
Trip 4 in April 1992 followed a cyclone that depos-
ited considerable rain on Barrow Island and renal The widespread use of tritium to estimate rates of water
parameters from the six hare-wallabies studied show turnover of free-ranging vertebrates (Green 1989, 1997;
signi®cant changes when compared with the animals Nagy and Costa 1980; Nagy 1982, 1987b; Hume 1999),
collected in the drought year of 1990. Renal plasma ¯ow as well as the use of doubly labelled water to measure
was not signi®cantly higher, but the GFR had increased ®eld metabolic rates (Nagy 1987a; Nagy and Peterson
to 2.69 0.23 ml kg)1 min)1 as a result of a signi®cant 1988; Nagy 1994) facilitates comparisons between spe-
increase in the FF to 31.3 2.5%. Rates of urine cies as a function of habitat. A priori, one expects desert-
production were dramatically increased almost nine-fold dwelling animals to display an enhanced water economy
to a mean of 50.2 4.6 ml kg)1 day)1 and the urinary when compared with related species occupying more
concentration, as measured by the U/Posm ratio had mesic or humid habitats, with lower rates of water
fallen signi®cantly from 8.0 to 1.26 0.18, with a sig- turnover and utilisation.
ni®cant decrease in FRH2 O from 99.6% to 97.8 0.3% Rates of water turnover of the spectacled hare-wal-
(P 0.0001). Cosm was signi®cantly higher, as would be laby on Barrow Island were ®rst measured by Bakker
anticipated from the increased urinary volumes, and and Bradshaw (1989), who reported a value of
CH2 O was less negative at )26.6 9.3 ml kg)1 day)1. 43.5 ml kg)0.82 day)1 for the dry part of the year. This
There was no change in ECFV between the two trips, contrasts with the mean value of 27.5 2.0 ml
remaining at approximately 18%, but plasma LVP kg)0.82 day)1 reported here for November 1990 but this
levels fell signi®cantly to 8.8 0.9 pg ml)1. As was the driest year ever recorded on Barrow Island and
with trip 1, LVP levels were measured in other indi- one can anticipate an extremely low value. Nagy and
viduals not destined for the study of kidney function, Bradshaw (2000) again measured rates of turnover of
and the overall mean plasma concentration was 9.3 hare-wallabies on Barrow Island in December 1993 and
1.2 pg ml)1 (n 39). reported a mean value of 29.4 ml kg)0.82 day)1 con-
Renal function in the Enderby Island rock-wallabies ®rming that this species of wallaby indeed has the lowest
contrasts signi®cantly with the picture seen in hare- rate of water turnover of any mammal yet studied
wallabies. During the dry season rates of urine produc- world-wide. Nagy and Bradshaw (2000) also reported
tion were as low as in hare-wallabies, at 6.7 the Water Economy Index (WEI) of this species, calcu-
1.4 ml kg)1 day)1 but the concentration of the urine, as lated as the ratio of the water in¯ux to daily energy
measured by the U/Posm ratio was lower at 5.4 0.4. consumption (ml water per kJ FMR), as 0.104 which is
Renal plasma ¯ow (CPAH) was similar at 5.8 also low and re¯ects on this species' level of adaptation
0.1 ml kg)1 min)1 but the FF of the rock-wallabies was to its arid habitat.
some 10% lower at 14.4 1.0, giving a substantially Nagy and Bradshaw (2000) further compared allo-
reduced GFR of 0.82 0.05 ml kg)1 min)1. The metric relations of rates of water turnover of arid versus
FRH2 O was high at 99.4 0.1%, slightly lower than non-arid marsupials and derived two signi®cantly
that of the hare-wallabies in the dry season. Circulating dierent regressions. That for non-arid marsupials was
levels of LVP were quite low, however, at 3.7 1.87g0.64 ml day)1 (r2 0.939) compared with 0.777g0.69
0.4 pg ml)1 and the ECFV was also low at 12.2 ml day)1 (r2 0.848) for nine arid-living species. This
0.5%. LVP concentrations from a larger sample of second equation predicts a daily water in¯ux of 81.0 ml
rock-wallabies collected on trip 8 averaged 3.49 (kg0.82 day))1 for a 3 kg wallaby which falls within the
0.37 pg ml)1 con®rming the low levels measured in the range reported here for both hare- and rock-wallabies.
seven renal animals. As may be seen, the water turnover measured with
Following cyclonic rain in February 1989, renal tritium is not an invariant feature of the species, but
parameters were little changed in the rock-wallabies. depends very much on the actual weather conditions
Rates of urine production doubled to a mean of 14.3 during the period of measurement. Following rain, for
5.5 ml kg)1 day)1 but the U/Posm of the urine produced example, rates of water in¯ux in the spectacled hare-
did not change signi®cantly and neither did the Cosm nor wallaby rose to 139 ml kg)0.82 day)1, and turnover was
the CH2 O . There was a signi®cant increase in CPAH to thus markedly increased over that measured during
7.94 0.46 ml kg)1 min)1 which appeared primarily periods of chronic water deprivation.
responsible for the small but signi®cant increase in the The water economy of a number of other arid
GFR to 1.28 0.12 ml kg)1 min)1, as the FF remained marsupial species occurring on Barrow Island was also
unchanged. ECFV increased after rain to a more usual studied by Nagy and Bradshaw (2000) in December
mean of 18.8 1.1% but plasma LVP levels at 1993, including the burrowing bettong, Bettongia30
Table 7 Body composition
homeostasis in desert wallabies Species Body Condition Total body Plasma Plasma Plasma
± maximum percentage mass index water content Na+ K+ osmolality
variation (%) in parameters
recorded over all ®eld trips Hare-wallaby 21.2 14.7 4.3 5.9 7.7 2.9
Rock-wallaby 31.2 28.2 15.7 9.0 36.9 5.6
lesueur (85.7 ml kg)0.82 day)1), the black-footed and shows clearly that the rock-wallaby experiences
rock-wallaby, Petrogale lateralis lateralis variations in TBW as well as plasma electrolyte con-
(70.6 ml kg)0.82 day)1), the golden bandicoot Isoodon centrations and osmolality that are two-to-three-times
auratus barrowensis (127 ml kg)0.82 day)1), the northern greater than those experienced by hare-wallabies. These
brushtail possum, Trichosurus vulpecula arnhemensis data highlight the extent to which the hare-wallaby is
(164.3 ml kg)0.82 day)1), and the dwarf Barrow Island able to minimise the impact of daily high thermal loads
euro kangaroo, Macropus robustus isabellinus on its overall water economy. Figure 3 shows tempera-
(67.1 ml kg)0.82 day)1), and all are clearly low when ture records from a data logger recording environmental
compared with other values in the literature. temperature and humidity records on Barrow Island in
A primary determinant of water economy in mam- November±December 1993. The temperature within a
mals is the renal-concentrating capacity, which is in turn large spinifex tussock (Triodia angusta), used as a daily
determined to a large extent by the renal anatomy, and refuge site by hare-wallabies, is only marginally lower
the relative dimensions of the renal medulla. Sperber's than the ambient air temperature and reaches as high as
(1944) index of medullary thickness has been calculated 45 °C on some days. The very much lower and more
for a number of species of marsupials and the hare- stable temperature recorded over the same period from a
wallaby is high at 8.7 (Purohit 1974). The mean osmol- burrow of the burrowing bettong, is similar to records
ality of voided urine of hare-wallabies from Barrow taken from cave sites used by rock-wallabies on Enderby
Island was signi®cantly higher than that of Enderby Island and shows the extent to which these privileged
Island rock-wallabies (1397 106 versus 1207 sites enable this species to conserve body water. Taken
72 mosmol kg)1 respectively, P < 0.001), although the together, the data on body composition homeostasis and
maximum recorded values for each species were similar perceived environmental heat loads for the two species
at 3,600 mosmol kg)1. (Dawson and Bennett 1978), suggest that the hare-
The data presented in this study enable one to assess wallaby is far better adapted physiologically than the
the extent to which the two desert wallabies are able to rock-wallaby to cope with extended periods of water
maintain water and electrolyte homeostasis in the face deprivation.
of chronic water deprivation. Clearly, the hare-wallaby ±
despite its greater environmental exposure ± is more
eective at regulating its milieu inteÂrieur. The percent Comparisons of renal function between
change in body composition variables listed in Tables 3 the two species
and 4 for the two species over all trips is listed in Table 7
Although the renal data presented in Table 6 give the
impression that the rock-wallabies are unable to vary
Fig. 3 Temperature records taken by datalogger on Barrow Island in
November/December 1993. The solid line records from an under-
ground warren, built and inhabited by burrowing bettongs (Bettongia Fig. 4 Variation in urinary-concentrating activity of the kidneys of
lesueur), the dotted line records from the middle of a spinifex clump hare-wallabies and rock-wallabies (U/Posm) as a function of rate of
used as a refuge by hare-wallabies and the dashed line is the ambient urine production. The power curve is ®tted to the data for hare-
temperature wallabies but does not dier signi®cantly for that for rock-wallabies31
pial. The Rottnest Island quokka (Setonix brachyurus)
inhabiting areas where brackish water was available
during mid-summer had circulating levels of LVP of
35.6 15.8 pg ml)1. This compared with a mean of
89.2 19.6 pg ml)1 measured in animals with no
access to free water (Jones et al. 1990). Plasma levels of
LVP in the Tammar wallaby (Macropus eugenii)
reported by Wilkes and Jannsens) 1986 averaged
21.5 4.4 pg ml)1, con®rming earlier measurements of
circulating levels of ADH in this species reported by
Bakker et al. (1982) using a toad bioassay (Bakker and
Bradshaw 1978). Wilkes and Jannsens (1986) also
demonstrated that LVP functions as an eective ADH in
the developing tammar wallaby.
Given the unusual nature of the renal responses to
water deprivation in the rock-wallaby, it may well be
Fig. 5 Variation in circulating levels of lysine vasopressin (LVP) in that this species lacks an hormonally mediated response.
hare-wallabies and rock-wallabies as a function of the concentrating
activity of the kidney (U/Posm) Acknowledgements Wallabies on Barrow and Enderby Islands
were collected under permit from the Department of Conservation
signi®cantly the concentration of their urine, Fig. 4 and Land Management (CALM) and all experimental procedures
were approved by the Animal Ethics Committee (then the Animal
suggests that this is not the case by plotting U/Posm ra- Welfare Committee) of The University of Western Australia.
tios versus rate of urine production (V) for the complete Grateful acknowledgement is made to Brian Clay, Darren Murphy,
data set. Rates of urine production in rock-wallabies do Chris Dickman, Phil Withers and Bob McNeice for assistance in
not exceed 55 ml kg)1 day)1 ± whereas they almost the ®eld, and to Zorica Kostadinovic for help with laboratory
analyses. The work was funded by the Australian Research Council
reach 100 ml kg)1 day)1 in hare-wallabies ± but U/Posm (ARC) and was greatly assisted by material support from WA
ratios reach levels of 10 in some individuals of both Petroleum (WAPET) which provided transport to and accommo-
species. The power curve ®tted to the data is for hare- dation on Barrow Island.
wallabies only, but data for the rock-wallaby do not
dier signi®cantly from this line.
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