AMREICAN JOURNAL OF PHYSIOLOGY Vol. 228, No. 6, June 1975. Printed in U.S.A.
Comparative
metabolism
by macropodid
of tritiated
marsupials
M. J. S. DENNY AND TERENCE J. DAWSON School of Zoology, University of New South Wales, Kensington, Australia,
DENNY, M. J. S., AND TERENCE J. DAWSON. Comparative metabotism of tritiated water by macropodid marsupials. Am. J. Physiol. 228(6) : 1794-l 799. 1975.-The total body-water content (TBW) and rate of water turnover were measured using tritiated water in five species of macropodid marsupials (kangaroos), which ranged in weight from 1 to 50 kg. Animals fitted with rumen cannulas were used to estimate the time required for tritiated water to equilibrate within the body of large kangaroos. In hydrated kangaroos this was 6 h, during which time 2.7 y0 of the injected tritiated water was lost from the body. During dehydration, the equilibrium time was extended to 10 h. Values up to 78% of body weight were found for TBW in the larger species of kangaroo, and these values were similar to those found for other ruminantlike mammals, particularly those with a low body-fat content. The smaller macropodids had a TBW (about 607, of body weight) similar to that of most laboratory mammals. The rates of water turnover of the macropodids were related to body weights by the expression 1 /day = 0.09 kgO.80. Macropodid marsupials have a daily water usage which is about two-thirds of that found for eutherians and this may be related to the lower metabolic rate of marsupials. body-water kangaroos
content;
water
turnover
* equilibrium
9
times;
desert
IN MAMMAL HISTORY (possibly late Paleocene or early Eocene, i.e., about 50 million years ago) marsupials entered Australia, probably via Antarctica (13). Once in Australia, the marsupials spread widely in response to the different habitats available to them and nowadays are the most common type of native mammal within this country. Australia is regarded as being desertlike over 60 % of its surface, and water is at a premium within much of this area. If marsupials have evolved within a country of such aridity, is it possible that these animals have a water metabolism suited to such an environment? Studies of the water metabolism of marsupials are not common and only a limited number have been carried out on the kangaroo family (family Macropodidae). These marsupials appear to have good temperature-regulating abilities (28) and are known to have undergone speciation in a period when the Australian continent was becoming increasingly arid (9). Actual measurements of the water usage by kangaroos have been obtained for only a few species : the tammar wallaby Macro/ms eugenii (15), the quokka Setonix brachyurus (3), the red kangaroo Megaleia rufa (Zl), and the euro Macropus robustus (8). The results obtained from these studies all show that these macropodids required relatively small amounts of water. Unfortunately
EARLY
water
2033
it is difficult to satisfactorily compare the results of these studies because of the range of conditions under which the measurements were taken and the different techniques used to measure the water requirements. To obtain a more uniform estimate of water requirements, a group of macropodid marsupials was studied under similar conditions with use of the same method of measurement for all animals. The results obtained could then be compared with those obtained from other mammals for which similar methods were used, e.g., Richmond et al. (27). MATERIALS
AND
METHODS
Animals studied. Five species of the kangaroo family, Macropodidae, were studied. These are listed in Table 1,. along with their distribution and weights during the study. In most cases an equal sex ratio was maintained and females were not lactating. All larger species of kangaroo were weighed during the experimental period on a Wedderburn platform balance capable of weighing to 10 g, while the smaller animals were weighed on a Sauter pan balance, accurate to 2 g. Three grey kangaroos were fitted with rumen cannulas to facilitate the collection of rumen liquor. Because of the unusual shape and mode of locomotion of the kangaroo, the operation used to cannulate the rumen, although basically similar to that described for sheep by Jarrett (14) and using the same type of cannula (Jarrett rumen cannula, South Australian Rubber Mills S.A.) required modification. The operation was carried out in two stages: the first produced an adhesion between the rumen and the abdominal wall, the second stage involved insertion of the rumen cannula into a fistula made in the rumen and body wall. All operations were carried out under general anesthesia using Equithesin (chloral hydrate, 2.66 g, and magnesium sulfate, 1.32 g dissolved in 10 ml Nembutal solution containing 60 mg pentobarbitone per milliliter) at a dose rate of 0.28 ml/kg injected into the lateral tail vein. This dosage usually produced deep anesthesia for l-2 h. More Equithesin was given if required. The field of operation was on the left side of the animal where an 8- to IO-cm incision was made 10-l 2 cm from the transverse processes of the lumbar vertebras, and 5 cm posterior to the 12th rib. This placement of the cannulas was closer to the vertebras than that usual for sheep, because the hindlimbs of the kangaroo may rub against the cannula if it is placed lower. The muscles were retracted, the peritoneum was opened, and a cone-shaped pouch of rumen 1794
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WATER
TURNOVER
Common
Red
Name
kangaroo
OF
1795
KANGLIROOS
Scientific
Name
Distribution
Megaleia
rufa
Widely
distributed
over
Eastern grey kangaroo
1Macr0fms
giganteus
Mainly drier
in coastal areas
Wallaroo
MaCrOpUS
ro bustus
Eastern
coast
eugenii
Several tralian
islands and
Eastern
coast
Type
dry
regions,
areas but
of Australia
extending
Open into
of Australia
Forest
Hilly
Weight Range of Exptl Animals, kg
of Habitat
grassland and
14-35 woodlands
16-34
woodland
19-50
ro bustus Tammar wallaby
;‘Macro@us
Potoroo
Potorous tridactylus fridactylus
off, West
and small Australian
of New
was brought to the exterior with Allis forceps and fastened into position by a series of single stay sutures, placed at intervals around the base of the cone, fastening it to the body wall. The serosa of the body wall was scarified and the rumen was attached to the wall by sutures of no. 1 gut passing through the peritoneum and the transverse layer of the abdominal muscle. These sutures were placed at intervals of about 1 cm from each other and tied tightly to ensure as little leakage into the peritoneal cavity as possible. The top two layers of abdominal muscle were then sutured along the line of incision using no. 2 gut. The skin was sutured using fine, monofilament, stainless steel thread. The second part of the operation was performed 2-3 wk later. A 3-cm incision was made in the skin and underlying layers of muscle in the same area as before and the adhesion of the rumen to the body wall was checked before proceeding. If the adhesion was complete, the area of rumen inside the circle was pulled to the surface and a Z-cm incision was made, into which the cannula was inserted. Because of its soft nature the cannula could be rolled up and easily slipped into the small incision. This method of cannulation ensured a tight fit around the stem of the cannula and reduced leakage. The skin and muscles were then sutured tightly around the cannula using stainless steel thread and the animal left for 2 wk to allow for healing, All the animals cannulated survived the operation and lived for more than 6 mo. Estimation of equilibrium time of tritiuted water in large kangaroos. About 5 ml of tritiated water (“HTO, 200 $X/ml) were injected either into the peritoneum or via a vinyl cannula into the tail vein, Blood samples were taken every hour for 12 h from the lateral tail vein, and the plasma was separated immediately. Rumen liquor samples were taken from the three cannulated animals at the same time as the blood samples. During the experimental period, the kangaroos were placed in metabolism cages so that urine and feces could be collected. The animals were weighed both before and after the experiment to obtain an estimate of the insensible weight loss. The concentration of tritiated water in the plasma, rumen fluid, and urine was measured directly by liquid scintillation counting. Estimation of total body-water cord&. Total body water (TBW) was estimated from the dilution of a dose of tritiated water injected into the animal. A measured dose of 3Hz0 (about 25 &i/kg) was injected into the peritoneum of the red and grey kangaroos and the wallaroo, while about 150
South
areas on South coast WaIes
:Ius-
Dense thickets in sclerophyll forest Wet
sclerophyll
forest
dry
2%7.0
l-l-l.7
&i/kg were injected into the peritoneum of the tammar wallabies and the potoroos. After preinjection blood samples (2-5 ml) were taken the animals were injected with 3HQ0 and the time was noted. Blood samples were taken from the lateral tail vein except in the case of the potoroo, in which the method of Richmond et: al. (27) was used. Four hours later additional blood samples were taken from the tammar wallaby and the potoroo, while after 6 h blood samples were taken from the red and grey kangaroos and the wallaroo. The plasma was then separated from the blood and analyzed for tritium concentration. Estimation of water turnouer. After TBW was estimated the animals were released into yards measuring 470-530 m2. Blood samples were then taken from the kangaroos every 3 days for 15 days. During the experimental period, the animals were given ad libitum food and water. The larger macropodids were fed lucerne hay and commercial feed pellets, whereas fruit and hay were fed to the tammar wallabies and the potoroos. All experiments were carried out during mild autumn-winter months and the animals were well accustomed to their surroundings. Water turnover was calculated and tritium concentration estimated in the same manner as outlined by Denny and Dawson (7). RESWLTS
Equilibrium time. No difference was found in the time for the 3H20 to completely mix with the body water in the two species studied or between the two routes of injection (Table 2). The criterion for complete mixing was that the concentration of 3Hs0 in the rumen liquor was equal to that found in the plasma, within the limits of analytical error. In all hydrated animals the mixing time was between 4 and 6 h after injection. A typical set of results illustrating the rate of mixing of the injection of 3H20 with the body water of the animal is shown in Fig. 1. No regular urine samples were taken but three animals urinated frequently enough for it to be possible to estimate that the specific activity of urine cleared from the bladder reached the same 3Hz0 concentration as the plasma after 4 h. Both MacFarlane (18) and Siebert and MacFarlane (30) have pointed out that dehydration lengthens the time required for 3H20 to equilibrate with the body water. To find
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M.
1796 2. Time of equilibrium of tritiated water in body j’hids of k an g arous and an analysis of avenues of loss of injected 3H& during equilibrium time
TABLE
-
--
Kangaroo
Red Grey Grey Red Grey
---
I I II II III
-- -
--
Route of Injection
Weight, kg
IV IV IP IP IP
21.4 17.2 16.6 21.9 16.0
Mean IV, intravenous;
ip,
During Time, lost
9 24 42 34
9 5 14 10 7
91 86 62 48 59
22
9
69
TO of Dose Injected
Equilibrium Time, h
2.8 349 3.9 1.1 3.0
5 5.5 5 4 6
intraperitoneal.
intravenous
injection
intraperitoneaL
I
--
--
3H20 Excreted Equilibrium % of total
1
4
1
inject ion
1
8
I
I
12
time (hours) FIG.
garoo.
1. Equilibrium curves for tritiated water injected into 0, Plasma sample; x, rumen sample; 0, urine sample,
a kan-
the change in equilibrium time for kangaroos, four red kangaroos were dehydrated to 80 % of their body weight and “Hz0 injected into the peritoneum. From the hourly blood samples taken it was found that the concentration of 3Hs0 in the blood was constant between 8 and 10 h, thus a 10-h blood sample would give the best estimate of total body water. Losses of 3H& during equilibrium time. If a period of 6 h elapses before the injected 3Hz0 mixes fully with the body water, then during that time, a certain proportion of “Ha0 must be lost via the normal routes of body water loss. The amounts of 3H20 lost in urine were calculated from the amount of urine lost multiplied by the 3H20 concentration in the urine. The amount lost in the feces was calculated from the amount of fecal water lost multiplied by the 3Ha0 concentration in the plasma at 6 h, assuming that the fecal water would be in equilibrium with the plasma. Insensible water loss was taken as the weight loss that occurred during the equilibrium period less the weight of urine and feces
J. S. DENNY
AND
T. J.
DAWSON
lost and this multiplied by the 6-h plasma 3H20 concentration. The concentration of 3Hz0 in the water evaporated from the body is essentially the same as that in the body fluids, according to Pinson and Langham (26). However, this method would tend to overestimate the amount of 3H20 lost via evaporated water as the Oa-CO2 exchange contributes 20 % to insensible weight loss. Relative losses of 3Hg0 from the body during the equilibrium period are given in Table 2. Although the 3Hg0 concentration in the water leaving the body will not be at all times equal to the plasma 3Hz0 concentration, this would not overshadow the general trends shown. Comparison of extrapolated and 6-h values and repeatability of measurements. Another method used to estimate TBW is to extrapolate the biological decay curve of 3Hz0 to zero time and use the concentration of 3Hz0 at that time to calculate TBW. This method is useful when measuring water turnover, as a series of samples must be taken to obtain the slope of the decay curve. Ten red kangaroos were injected with 3H20, blood w as taken and analyzed for 3H~0 every 4 days for 16 days. The TBW was calculated from the extrapolated zero-time concentration and from the 6-h sample. The difference between the values obtained by these two methods was approximately 2 %; the values for TBW obtained from the 6-h sample and from the zero-time concentration were 71.7 =t 1.9 SE and 70.5 =t 2.0 SE, respectively. Accuracy of the method used to measure TBW was tested by comparing two successive measurements of TBW on individual animals. Five red kangaroos were placed in metabolism cages and weighed daily until all maintained a relatively stable weight. The TBW was measured on all animals and then measured again 1 wk later, the individual values of %TBW are shown in Table 3. The difference between the mean %TBW values was 3.4, which is slightly less than the 5 % variation Till and Downes (32) found in a similar study in sheep. Total body-water content and rate uf water turnover of fue species ofmacropodid marsupial. The values for total body-water content of five species of macropodid are given in Table 4; these are expressed as liters of water and as a percentage of the animal’s body weight. The relationship between the body-water content and total body solids for the five macropodid species as well as for cattle, sheep, and goats is shown plotted logarithmically in Fig. 2. Also included in Fig. 2 is the straight line used by Richmond et al. (27) to express an exponential relationship between body solids and body water of several mammalian species. The values for the daily water turnover rates of the five macropodid species TABLE 3. Repeatability of total body-water measurements in kangaroos
yO Change Between I and XT
Kangaroo
__
I 2 3 4 5 Mean Estimations
I and
81. -6 79.9 78.6 78.7 79.1
78.9 77.6 77.1 80.5 74.5
3.5 3.0 1.9 2.2 6.2
79.6
76.5
3.4
II were
made
1 wk
apart.
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WATER
TURNOVER
OF
KANGAROOS
1797’
4. Total body-water content in jva species during nonstress conditions
TABLE
of macropodid Species
Water
Sex Ratio
Weight,
Content
kg liters
M.
giganteus
2314
Q*
% body
17,17~1.07
22.1ztl.5
78.0xt2.50 (6) 77.6+2.67 (5) 72.5h2.25 (6)
16) M.
robusfus
4 d':l
Q
31.1zt5.2
rufu
2 $:4
3
23.4=l&6
3 $13
Q
6.5&0.2
3.92h0.14
60.8zt1.95
Q
(6) 1.4ztO.l
0.83ztO.04
(6) 58.8A2.33
Me.
23.96+3+66
(5) 16.98H.08
(6) M.
eugenii
P. tridactylus
38~3
(5)
Values theses.
wt
3 w 0 A
(5)
are means & SE; number * All females nonlactating.
of animals
is given
in paren-
LOG
BODYWEIGHT@)
FIG. 3. Interspecific correlation between and log body weight. Eutherian line taken Symbols same as in Fig. 2.
0.97). This regression method of least squares.
equation
log daily water turnover from Richmond et al. (27).
was
calculated
by
the
DTSCUSSTON
2 LOG
4
SOLIDS
(G)
2. Relationship between body water and body solids in kangaroos and other ruminants, Straight line is taken from Richmond et al. (27). H, potoroo; A, tammar wallaby; l , grey kangaroo; 0, red kangaroo; +, wallaroo; q , goat (value from Panaretto (25)) ; X, sheep (value from MacFarlane (19)) ; A, cattle (value from Springell (31)). FIG.
TABLE 5. plater turnover values in jve species of macropodid during nonstress conditions
Weight, ks
Species
l-----Wallaroo Red
kangaroo
Grey
kangaroo
Tammar Potoroo
are means
ml/kg-day
ml/kg’-‘-day
I-l
9.7zt1.13 (5) 8.6zt0.76 (6 > 13.3zt1.12 (6 > 8.3&l. 13 (5) 7.4~1.66 (4)
=I= SE; number
Turnover -
liters/day
l--l
3l.lh5.2 (5) 23.4ztl.6 (6) 22.1 zlzl.47 (6) 6.6ztO.20 (5) 1.5zt0.08 (4)
Values
Water
3HaO
Half-Time, days
1.86zt0.36 (5) 1.41&0.12 > 0.92dzO.06
(6
(6) 0.29ztO.01 (5 > 0. I5ztO.001 (4)
of animals
is given
59.7A9.74
117.9*17.24
(5) 61.1~1~5.74 (61 42.4zt3.35 > 44.7h3.57 (5 1 97. 8zt2.76 (4:
(5) 119.7zt10.92 (6) 78.5zJz5.75 (6) 65.2zt4.96 (5) 105.9zt3.96 (4)
(6
in parentheses,
are given in Table 5. Figure 3 shows the interspecific relationship between the daily water turnover and body weight. Water turnover in liters per day is exponentially related to body weight by the expression 1/day = 0.090 kg@ 80 (r =
Based on anatomical (23) and physiological (24) evidence, kangaroos are now regarded as 2uminantlike” mammals. Because of the high gut-to-body weight ratio, one can expect the equilibrium time for 3Hg0 to be similar to that of sheep and cattle. Studies of the equilibrium time in ruminants are limited to sheep (32) cattle (29, 31), and camels (30). All give equilibrium-time values that are longer than those of monogastric animals of comparable weight (26). In the kangaroo an equilibrium time of 6 h is similar to that of the sheep (32). Studies on ruminants have shown that 1 % of the injected dose of 3H20 in camels (30) and 2 % of the injected 3H20 in sheep (32) were lost during equilibrium time. In this study 2.7 % of the injected dose was lost, slightly more than that lost from sheep and camels. This difference may be due to the excitable nature of the kangaroos when placed in pens, thus increasing the amount of water lost by evaporation. The value obtained for the amount of injected “H20 lost during the equilibrium period can be checked against a water turnover value for red kangaroos during winter. The value is about 60 ml/kg*day, and with a TBW value of 72 % one can calculate that 8 % of the injected dose is turned over every 24 h, i.e., 2 % every 6 h, approximately the same as the value found in this experiment. In kangaroos dehydrated to 80 % of their hydrated body weight, the equilibrium time was extended from 6 to 10 h. This extension of time was also seen in camels in which the equilibrium time during dehydration was 18 h compared with 8 h when hydrated (30). This delay was probably caused by a fall in the rate of secretion of salivary and pancreatic fluids as well as a slower rate of turnover between the alimentary tract and the blood (19)* The method of obtaining the TBW which uses the extrapolated zero-time concentration value is not valid under these circumstances because this method depends on a constant body-water pool which does not occur in the case of a dehydrating animal. Thus for dehydrated kangaroos an estimate of TBW
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1798
M.
can only be obtained from an equilibrium-time blood sample taken 10 h after the 3Hz0 has been injected. It can be seen from Fig. 2 that the three species of large kangaroos have a high body-water content relative to their body solids. The high TBW found in the large kangaroos appears to be due to two factors: ~1) the ruminantlike gastrointestinal tract of the macropodids, and b) the lower proportion of body fat in “native” animals when compared with their domesticated counterparts. One characteristic of ruminantlike mammals is their relatively high ratio of gut-to-body weight. The ratio of stomach contents to body weight ,in red kangaroos is approximately 11 % (C. J, H arrop, personal communication). Consequently if the rumen is composed of about 80 % water (18), the amount of water in the body of a kangaroo will be higher than that found in nonruminants. This applies not only to the large kangaroos but also to cattle, sheep, and goats, as can be seen from Fig+ 2. The potoroo, however, differs in that it is omnivorous ( W and does not have a ruminantlike feeding behavior. Body-water content is not only infl uenced by the size of gut-water pool but also by the amount of fat contained in the body. Since fat cells have a water content of about 12 % (Z), animals with a hi gh fa t content will have a lower proportion of body water than leaner an imals. In a comparison among kangaroos, goats, and sheep, Tribe and Peel (33) found that two species of kangaroo had a lower fat content than that found in sheep (red kangaroo 0.4 %, grey kangaroo 0.08 Yc, and sheep 13.3 % body fat). Similar results have been found in other nondomesticated animals such as mule deer (17) and various East African antelopes (22). The animals used in this present study were nondomesticated species and all possibly had a low body-fat content. Consequently a high body-wa ter content could be expected in these animals. In the tammar wallaby, however, the percent TBW value was low, comparable with that of small laboratory animals (27). Th erc was, however, a tendency for these animals to accumulate body fat in captivity. Although the values for TBW of the macropodid marsupials appear similar to those found of eutherians, the water turnover rates appear to differ markedly in these two groups. An interspecific relationship between water turnover and body weight has been established for many years. Adolph (1) proposed that in eutherian mammals many functions of water, e.g., urine loss, insensible water loss, etc., were exponentially related to body weight. By use of tritiated water, Richmond et al. (27) related daily water use to the 0.8 power of body weight for a range of eutherian mammals. MacFarlane (19) found that tritiated water turnover in three species of ruminant was related to the 0.82 power of their body weight. A similar relationship exists between standard energy metabolism and body weight in eutherian mammals (16)
J*
S. DENNY
AND
T.
J.
DL~WSON
and marsupials (6). In both groups of animals standard energy metabolism is proportional to the 0.75 power of body weight, but in marsupials the actual level is approximately 30 ‘, lower than in eutherian mammals. Consequently it is of interest to find that, although the water turnover of macropodids is related to the 0.8 power of body weight, the actual level is 26 % lower than that given by Richmond et al. (27) for eutherians. That there is a relationship between oxygen consumption and water metabolism has been mentioned by several authors (12, 15), and recently MacFarlane et al. (20) ranked several species of ruminents, rodents, and Dasyurid marsupials on the basis of these criteria. MacFarlane et al. (20) pointed out that animals with a low metabolic rate also have a low water turnover, and it is this relationship that would explain the low water turnover found in macropodids. The various avenues of water loss from the body are all indirectly influenced by the animals’ metabolic rate. For example, fecal water loss is determined in part by the amount of food eaten, which has been found to be lower in some species of kangaroo, when compared with eutherians (4). Urine water loss is partly determined by glomerular filtration rate which is lower in kangaroos than in most other mammals studied- Insensible water loss via the skin would tend to be low because of the lower body temperatures in marsupials (6), and respiratory water loss would also tend to be reduced due to the lower oxygen metabolism in kangaroos. Dawson et al. (5) point out that the tammar wallaby had an evaporative water loss lower than that measured in eutherians of similar size. All the macropodids studied had a low water turnover and if Table 1 is studied, it can be seen that the red kangaroo, the wallaroo, and perhaps the grey kangaroo are from arid areas, whereas the other animals, particularly the potoroo, are found in more temperate regions. This lack of correlation between water turnover and aridity of habitat is particularly interesting since &lacFarlane (19) proposes that water turnover values obtained during ad libitum conditions can be used to separate “desert-hardy” species from any other, i-e., the animals with a high water turnover under “nonstress” conditions were those that were found in waterrich habitats. This is obviously not so in this present study. Therefore, any study of an animal’s ability to survive in an arid area should include work done on the animal under conditions similar to those of the arid zone. This study was supported in part by a grant from the Australian Research Grants Comrni ttee. M. J. S. Denny was in receipt of a Council for Scientific and Industrial Research Organization postgraduate studentship. We especially thank Professor E. D. P. Thompson and Dr. hl. J. K. Macey of the University of New South Wales for the use of their scintillation counters. Received
for
publication
5 July
1974.
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of mamconfiguIssekutz. an
ks-
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127 : l-10, nutrition. rohmtus. Thermal
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WATER
TURNOVER
OF
1799
KANGilROOS
balance Biochem.
10.
of the macropodid marsupial, &!acr@us eugenii. camp. Physiol. 3 1 : 6455653, 1969. DAWSON, T. J., AND A. J. HULBERT. Standard metabolism, body temperature, and surface areas of Australian marsupials. Am. J. Physiol. 2 18 : 1233-1238, 1970. DENNY, hf. J. S., AND T, J. DAWSON. 11 f-leld technique for studying water metabolism of large marsupials. J. Wildlife Management 37: 574-578, 1973. EALEY, E. H. M., P. J, BENTLEY, AND A. R. MAIN. Studies on water metabolism of the Hill kangaroo, Macropus robustus, in Northwest Australia. Ecology 46 : 473-479, 1965. GILL, E. D. The Australian “arid period”. Australian J, Sci. 17: 204-206, 1955. GUILER, E. R. Food of the potoroo (luarsupialia, Macropodidae).
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SHARPIZ. Hierarchy of water and energy turnover of Nature 234 : 483-484, 197 1. W. V., R. J. I-3. MORRIS, AND B. HOWARD. Turn-
M.
mammals.
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in desert 1963.
camels,
sheep,
cattle
and
Thermoregulation and antelopes: the hartebeest and PhysioZ. 38: 525-534, 1971. digestion and evolution. 111: Handbook of PhysioZogy. Alimentary Canal. Washington, D.C. : Am, Physiol. SOC., 1968, sect. 6, vol. v, chapt. 126, p. 2673-2694. MOIR, R. J., M. SOMERS, AND H. WARING. Studies on marsupial nutrition. I. Ruminant-like digestion in a herbivorous marsupia1 (Setonix brachyurus). Australian J. BioZ. Sci. 9: 293-304, 1956. PANARETTO, B. A. Body composition in vivo. III. The composition of living ruminants and its relation to the tritiated water spaces. Australian J. Agri. Res. 14 : 944-952, 1963. PINSON, E. A., AND LANGHAM, W. H. Physiology and toxicology of tritium in man. J. Appl. P/zysioZ. 10 : 108-126, 1957. RICHMOND, C. R., W* H. LANGHAM, AND T. T. TRUJILLO. Comparative metabolisrn of tritiated water by mammals. J. Cellular Camp. Physiol. 59 : 45-53, 1962. ROBINSON, K. W., AND P. R. MORRISON. The reaction to hot ate mospheres of various species of Australian marsupial and placental animals. J. Cellular Corn@. Physiol. 49 : 455-478, 19.57. SHUMWAY, R. P., T. T. TRUJILLO, J. A. BENNETT, D. J. MATHEWS, AND R. 0. ASPLUND. Fat determination in live steers using tritium Proc. West. Sect. Am. Sot. Anim. Prod. 7 : 1-4, 1956. injections. SIEBERT, B. D., AND W. V. MACFARLANE. Water turnover and renal function of dromedaries in the desert. Physiol. ZooZ. 44: 225240, 1971. SPRINGELL, P. H. Water content and water turnover in beef cattle. Australian J. Agri. Res. 19: 129-144, 1968. TILL, A. R., AND A. M. DOWNES. The measurement of total body water in the sheep. Australian .J. Agri. Res. 13 : 335-342, 1962. TRIBE, D. E,, AND L. PEEL. Body composition of the kangaroo (Macropus sp.) . A us t ra Zian J. Zool. I 1: 273-289, 1963. ~~ALOIY,
G.
M.
0,
water relations of two impala. Camp. Biochem, 23. MOIR, R, J, Ruminant
J. Physiol.
16. KLEIBER, M. The Fire of Life: An Introduction to Animal Energetics. New York: Wiley, 1961. 17. KNOX, K. L., J. G. NAGY, AND R. D. BROWN. Water turnover in mule deer. J. Wildlife 1Managemenf 33: 389-393, 1969. 18. MACFARLANE, W. V. Terrestrial animals in dry heat: unguXates, In : Handbook of Physiology. Adaptation to the Environment. Washington, D.C. : Am. Physiol. Sot., 1964, sect. 4, chapt. 33, p. 509-539. 19. MIACFARLANE, W. V. Water metabolism of desert ruminants. In: Studies in Physiology, edited by D. R. Curtis and A. K. M. McIntyre. Berlin : Springer-Verlag, 1965. 20. MACFARLANE, W, V., B. HOWARD, H. HAINES, P. M. KENNEDY,
C.
21. MACFARLANE, over and distribution of water kangaroos. Nature 197: 270-271,
25.
in farm
206: 1369-1372, 1964. 12. HUDSON, J. W. Water metabolism in desert mammals. In: Thirst, edited by RI. J, Wayner. London: Pergamon, 1964. 13. JARDINE, N., AND D. MCKENZIE. Continental drift and the dispersal and evolution of organisms. Nature 235: 20-24, 1972. 14. JARRETT, I. G. The production of rumen and abomasal fistulae in sheep, G.S.1.R. nes. Reu, 21: 311-315, 1948. 15. KINNEAR, J. E., K. G. PUROHIT, AND A. R. MAIN. The ability of the tammar wallaby (Macropus eugenii) to drink seawater. Camp. Biochem.
AND
desert
AND
D.
HOPCRAFI-.
East African
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Comparative
metabolism
by macropodid
of tritiated
marsupials
M. J. S. DENNY AND TERENCE J. DAWSON School of Zoology, University of New South Wales, Kensington, Australia,
DENNY, M. J. S., AND TERENCE J. DAWSON. Comparative metabotism of tritiated water by macropodid marsupials. Am. J. Physiol. 228(6) : 1794-l 799. 1975.-The total body-water content (TBW) and rate of water turnover were measured using tritiated water in five species of macropodid marsupials (kangaroos), which ranged in weight from 1 to 50 kg. Animals fitted with rumen cannulas were used to estimate the time required for tritiated water to equilibrate within the body of large kangaroos. In hydrated kangaroos this was 6 h, during which time 2.7 y0 of the injected tritiated water was lost from the body. During dehydration, the equilibrium time was extended to 10 h. Values up to 78% of body weight were found for TBW in the larger species of kangaroo, and these values were similar to those found for other ruminantlike mammals, particularly those with a low body-fat content. The smaller macropodids had a TBW (about 607, of body weight) similar to that of most laboratory mammals. The rates of water turnover of the macropodids were related to body weights by the expression 1 /day = 0.09 kgO.80. Macropodid marsupials have a daily water usage which is about two-thirds of that found for eutherians and this may be related to the lower metabolic rate of marsupials. body-water kangaroos
content;
water
turnover
* equilibrium
9
times;
desert
IN MAMMAL HISTORY (possibly late Paleocene or early Eocene, i.e., about 50 million years ago) marsupials entered Australia, probably via Antarctica (13). Once in Australia, the marsupials spread widely in response to the different habitats available to them and nowadays are the most common type of native mammal within this country. Australia is regarded as being desertlike over 60 % of its surface, and water is at a premium within much of this area. If marsupials have evolved within a country of such aridity, is it possible that these animals have a water metabolism suited to such an environment? Studies of the water metabolism of marsupials are not common and only a limited number have been carried out on the kangaroo family (family Macropodidae). These marsupials appear to have good temperature-regulating abilities (28) and are known to have undergone speciation in a period when the Australian continent was becoming increasingly arid (9). Actual measurements of the water usage by kangaroos have been obtained for only a few species : the tammar wallaby Macro/ms eugenii (15), the quokka Setonix brachyurus (3), the red kangaroo Megaleia rufa (Zl), and the euro Macropus robustus (8). The results obtained from these studies all show that these macropodids required relatively small amounts of water. Unfortunately
EARLY
water
2033
it is difficult to satisfactorily compare the results of these studies because of the range of conditions under which the measurements were taken and the different techniques used to measure the water requirements. To obtain a more uniform estimate of water requirements, a group of macropodid marsupials was studied under similar conditions with use of the same method of measurement for all animals. The results obtained could then be compared with those obtained from other mammals for which similar methods were used, e.g., Richmond et al. (27). MATERIALS
AND
METHODS
Animals studied. Five species of the kangaroo family, Macropodidae, were studied. These are listed in Table 1,. along with their distribution and weights during the study. In most cases an equal sex ratio was maintained and females were not lactating. All larger species of kangaroo were weighed during the experimental period on a Wedderburn platform balance capable of weighing to 10 g, while the smaller animals were weighed on a Sauter pan balance, accurate to 2 g. Three grey kangaroos were fitted with rumen cannulas to facilitate the collection of rumen liquor. Because of the unusual shape and mode of locomotion of the kangaroo, the operation used to cannulate the rumen, although basically similar to that described for sheep by Jarrett (14) and using the same type of cannula (Jarrett rumen cannula, South Australian Rubber Mills S.A.) required modification. The operation was carried out in two stages: the first produced an adhesion between the rumen and the abdominal wall, the second stage involved insertion of the rumen cannula into a fistula made in the rumen and body wall. All operations were carried out under general anesthesia using Equithesin (chloral hydrate, 2.66 g, and magnesium sulfate, 1.32 g dissolved in 10 ml Nembutal solution containing 60 mg pentobarbitone per milliliter) at a dose rate of 0.28 ml/kg injected into the lateral tail vein. This dosage usually produced deep anesthesia for l-2 h. More Equithesin was given if required. The field of operation was on the left side of the animal where an 8- to IO-cm incision was made 10-l 2 cm from the transverse processes of the lumbar vertebras, and 5 cm posterior to the 12th rib. This placement of the cannulas was closer to the vertebras than that usual for sheep, because the hindlimbs of the kangaroo may rub against the cannula if it is placed lower. The muscles were retracted, the peritoneum was opened, and a cone-shaped pouch of rumen 1794
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WATER
TURNOVER
Common
Red
Name
kangaroo
OF
1795
KANGLIROOS
Scientific
Name
Distribution
Megaleia
rufa
Widely
distributed
over
Eastern grey kangaroo
1Macr0fms
giganteus
Mainly drier
in coastal areas
Wallaroo
MaCrOpUS
ro bustus
Eastern
coast
eugenii
Several tralian
islands and
Eastern
coast
Type
dry
regions,
areas but
of Australia
extending
Open into
of Australia
Forest
Hilly
Weight Range of Exptl Animals, kg
of Habitat
grassland and
14-35 woodlands
16-34
woodland
19-50
ro bustus Tammar wallaby
;‘Macro@us
Potoroo
Potorous tridactylus fridactylus
off, West
and small Australian
of New
was brought to the exterior with Allis forceps and fastened into position by a series of single stay sutures, placed at intervals around the base of the cone, fastening it to the body wall. The serosa of the body wall was scarified and the rumen was attached to the wall by sutures of no. 1 gut passing through the peritoneum and the transverse layer of the abdominal muscle. These sutures were placed at intervals of about 1 cm from each other and tied tightly to ensure as little leakage into the peritoneal cavity as possible. The top two layers of abdominal muscle were then sutured along the line of incision using no. 2 gut. The skin was sutured using fine, monofilament, stainless steel thread. The second part of the operation was performed 2-3 wk later. A 3-cm incision was made in the skin and underlying layers of muscle in the same area as before and the adhesion of the rumen to the body wall was checked before proceeding. If the adhesion was complete, the area of rumen inside the circle was pulled to the surface and a Z-cm incision was made, into which the cannula was inserted. Because of its soft nature the cannula could be rolled up and easily slipped into the small incision. This method of cannulation ensured a tight fit around the stem of the cannula and reduced leakage. The skin and muscles were then sutured tightly around the cannula using stainless steel thread and the animal left for 2 wk to allow for healing, All the animals cannulated survived the operation and lived for more than 6 mo. Estimation of equilibrium time of tritiuted water in large kangaroos. About 5 ml of tritiated water (“HTO, 200 $X/ml) were injected either into the peritoneum or via a vinyl cannula into the tail vein, Blood samples were taken every hour for 12 h from the lateral tail vein, and the plasma was separated immediately. Rumen liquor samples were taken from the three cannulated animals at the same time as the blood samples. During the experimental period, the kangaroos were placed in metabolism cages so that urine and feces could be collected. The animals were weighed both before and after the experiment to obtain an estimate of the insensible weight loss. The concentration of tritiated water in the plasma, rumen fluid, and urine was measured directly by liquid scintillation counting. Estimation of total body-water cord&. Total body water (TBW) was estimated from the dilution of a dose of tritiated water injected into the animal. A measured dose of 3Hz0 (about 25 &i/kg) was injected into the peritoneum of the red and grey kangaroos and the wallaroo, while about 150
South
areas on South coast WaIes
:Ius-
Dense thickets in sclerophyll forest Wet
sclerophyll
forest
dry
2%7.0
l-l-l.7
&i/kg were injected into the peritoneum of the tammar wallabies and the potoroos. After preinjection blood samples (2-5 ml) were taken the animals were injected with 3HQ0 and the time was noted. Blood samples were taken from the lateral tail vein except in the case of the potoroo, in which the method of Richmond et: al. (27) was used. Four hours later additional blood samples were taken from the tammar wallaby and the potoroo, while after 6 h blood samples were taken from the red and grey kangaroos and the wallaroo. The plasma was then separated from the blood and analyzed for tritium concentration. Estimation of water turnouer. After TBW was estimated the animals were released into yards measuring 470-530 m2. Blood samples were then taken from the kangaroos every 3 days for 15 days. During the experimental period, the animals were given ad libitum food and water. The larger macropodids were fed lucerne hay and commercial feed pellets, whereas fruit and hay were fed to the tammar wallabies and the potoroos. All experiments were carried out during mild autumn-winter months and the animals were well accustomed to their surroundings. Water turnover was calculated and tritium concentration estimated in the same manner as outlined by Denny and Dawson (7). RESWLTS
Equilibrium time. No difference was found in the time for the 3H20 to completely mix with the body water in the two species studied or between the two routes of injection (Table 2). The criterion for complete mixing was that the concentration of 3Hs0 in the rumen liquor was equal to that found in the plasma, within the limits of analytical error. In all hydrated animals the mixing time was between 4 and 6 h after injection. A typical set of results illustrating the rate of mixing of the injection of 3H20 with the body water of the animal is shown in Fig. 1. No regular urine samples were taken but three animals urinated frequently enough for it to be possible to estimate that the specific activity of urine cleared from the bladder reached the same 3Hz0 concentration as the plasma after 4 h. Both MacFarlane (18) and Siebert and MacFarlane (30) have pointed out that dehydration lengthens the time required for 3H20 to equilibrate with the body water. To find
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M.
1796 2. Time of equilibrium of tritiated water in body j’hids of k an g arous and an analysis of avenues of loss of injected 3H& during equilibrium time
TABLE
-
--
Kangaroo
Red Grey Grey Red Grey
---
I I II II III
-- -
--
Route of Injection
Weight, kg
IV IV IP IP IP
21.4 17.2 16.6 21.9 16.0
Mean IV, intravenous;
ip,
During Time, lost
9 24 42 34
9 5 14 10 7
91 86 62 48 59
22
9
69
TO of Dose Injected
Equilibrium Time, h
2.8 349 3.9 1.1 3.0
5 5.5 5 4 6
intraperitoneal.
intravenous
injection
intraperitoneaL
I
--
--
3H20 Excreted Equilibrium % of total
1
4
1
inject ion
1
8
I
I
12
time (hours) FIG.
garoo.
1. Equilibrium curves for tritiated water injected into 0, Plasma sample; x, rumen sample; 0, urine sample,
a kan-
the change in equilibrium time for kangaroos, four red kangaroos were dehydrated to 80 % of their body weight and “Hz0 injected into the peritoneum. From the hourly blood samples taken it was found that the concentration of 3Hs0 in the blood was constant between 8 and 10 h, thus a 10-h blood sample would give the best estimate of total body water. Losses of 3H& during equilibrium time. If a period of 6 h elapses before the injected 3Hz0 mixes fully with the body water, then during that time, a certain proportion of “Ha0 must be lost via the normal routes of body water loss. The amounts of 3H20 lost in urine were calculated from the amount of urine lost multiplied by the 3H20 concentration in the urine. The amount lost in the feces was calculated from the amount of fecal water lost multiplied by the 3Ha0 concentration in the plasma at 6 h, assuming that the fecal water would be in equilibrium with the plasma. Insensible water loss was taken as the weight loss that occurred during the equilibrium period less the weight of urine and feces
J. S. DENNY
AND
T. J.
DAWSON
lost and this multiplied by the 6-h plasma 3H20 concentration. The concentration of 3Hz0 in the water evaporated from the body is essentially the same as that in the body fluids, according to Pinson and Langham (26). However, this method would tend to overestimate the amount of 3H20 lost via evaporated water as the Oa-CO2 exchange contributes 20 % to insensible weight loss. Relative losses of 3Hg0 from the body during the equilibrium period are given in Table 2. Although the 3Hg0 concentration in the water leaving the body will not be at all times equal to the plasma 3Hz0 concentration, this would not overshadow the general trends shown. Comparison of extrapolated and 6-h values and repeatability of measurements. Another method used to estimate TBW is to extrapolate the biological decay curve of 3Hz0 to zero time and use the concentration of 3Hz0 at that time to calculate TBW. This method is useful when measuring water turnover, as a series of samples must be taken to obtain the slope of the decay curve. Ten red kangaroos were injected with 3H20, blood w as taken and analyzed for 3H~0 every 4 days for 16 days. The TBW was calculated from the extrapolated zero-time concentration and from the 6-h sample. The difference between the values obtained by these two methods was approximately 2 %; the values for TBW obtained from the 6-h sample and from the zero-time concentration were 71.7 =t 1.9 SE and 70.5 =t 2.0 SE, respectively. Accuracy of the method used to measure TBW was tested by comparing two successive measurements of TBW on individual animals. Five red kangaroos were placed in metabolism cages and weighed daily until all maintained a relatively stable weight. The TBW was measured on all animals and then measured again 1 wk later, the individual values of %TBW are shown in Table 3. The difference between the mean %TBW values was 3.4, which is slightly less than the 5 % variation Till and Downes (32) found in a similar study in sheep. Total body-water content and rate uf water turnover of fue species ofmacropodid marsupial. The values for total body-water content of five species of macropodid are given in Table 4; these are expressed as liters of water and as a percentage of the animal’s body weight. The relationship between the body-water content and total body solids for the five macropodid species as well as for cattle, sheep, and goats is shown plotted logarithmically in Fig. 2. Also included in Fig. 2 is the straight line used by Richmond et al. (27) to express an exponential relationship between body solids and body water of several mammalian species. The values for the daily water turnover rates of the five macropodid species TABLE 3. Repeatability of total body-water measurements in kangaroos
yO Change Between I and XT
Kangaroo
__
I 2 3 4 5 Mean Estimations
I and
81. -6 79.9 78.6 78.7 79.1
78.9 77.6 77.1 80.5 74.5
3.5 3.0 1.9 2.2 6.2
79.6
76.5
3.4
II were
made
1 wk
apart.
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WATER
TURNOVER
OF
KANGAROOS
1797’
4. Total body-water content in jva species during nonstress conditions
TABLE
of macropodid Species
Water
Sex Ratio
Weight,
Content
kg liters
M.
giganteus
2314
Q*
% body
17,17~1.07
22.1ztl.5
78.0xt2.50 (6) 77.6+2.67 (5) 72.5h2.25 (6)
16) M.
robusfus
4 d':l
Q
31.1zt5.2
rufu
2 $:4
3
23.4=l&6
3 $13
Q
6.5&0.2
3.92h0.14
60.8zt1.95
Q
(6) 1.4ztO.l
0.83ztO.04
(6) 58.8A2.33
Me.
23.96+3+66
(5) 16.98H.08
(6) M.
eugenii
P. tridactylus
38~3
(5)
Values theses.
wt
3 w 0 A
(5)
are means & SE; number * All females nonlactating.
of animals
is given
in paren-
LOG
BODYWEIGHT@)
FIG. 3. Interspecific correlation between and log body weight. Eutherian line taken Symbols same as in Fig. 2.
0.97). This regression method of least squares.
equation
log daily water turnover from Richmond et al. (27).
was
calculated
by
the
DTSCUSSTON
2 LOG
4
SOLIDS
(G)
2. Relationship between body water and body solids in kangaroos and other ruminants, Straight line is taken from Richmond et al. (27). H, potoroo; A, tammar wallaby; l , grey kangaroo; 0, red kangaroo; +, wallaroo; q , goat (value from Panaretto (25)) ; X, sheep (value from MacFarlane (19)) ; A, cattle (value from Springell (31)). FIG.
TABLE 5. plater turnover values in jve species of macropodid during nonstress conditions
Weight, ks
Species
l-----Wallaroo Red
kangaroo
Grey
kangaroo
Tammar Potoroo
are means
ml/kg-day
ml/kg’-‘-day
I-l
9.7zt1.13 (5) 8.6zt0.76 (6 > 13.3zt1.12 (6 > 8.3&l. 13 (5) 7.4~1.66 (4)
=I= SE; number
Turnover -
liters/day
l--l
3l.lh5.2 (5) 23.4ztl.6 (6) 22.1 zlzl.47 (6) 6.6ztO.20 (5) 1.5zt0.08 (4)
Values
Water
3HaO
Half-Time, days
1.86zt0.36 (5) 1.41&0.12 > 0.92dzO.06
(6
(6) 0.29ztO.01 (5 > 0. I5ztO.001 (4)
of animals
is given
59.7A9.74
117.9*17.24
(5) 61.1~1~5.74 (61 42.4zt3.35 > 44.7h3.57 (5 1 97. 8zt2.76 (4:
(5) 119.7zt10.92 (6) 78.5zJz5.75 (6) 65.2zt4.96 (5) 105.9zt3.96 (4)
(6
in parentheses,
are given in Table 5. Figure 3 shows the interspecific relationship between the daily water turnover and body weight. Water turnover in liters per day is exponentially related to body weight by the expression 1/day = 0.090 kg@ 80 (r =
Based on anatomical (23) and physiological (24) evidence, kangaroos are now regarded as 2uminantlike” mammals. Because of the high gut-to-body weight ratio, one can expect the equilibrium time for 3Hg0 to be similar to that of sheep and cattle. Studies of the equilibrium time in ruminants are limited to sheep (32) cattle (29, 31), and camels (30). All give equilibrium-time values that are longer than those of monogastric animals of comparable weight (26). In the kangaroo an equilibrium time of 6 h is similar to that of the sheep (32). Studies on ruminants have shown that 1 % of the injected dose of 3H20 in camels (30) and 2 % of the injected 3H20 in sheep (32) were lost during equilibrium time. In this study 2.7 % of the injected dose was lost, slightly more than that lost from sheep and camels. This difference may be due to the excitable nature of the kangaroos when placed in pens, thus increasing the amount of water lost by evaporation. The value obtained for the amount of injected “H20 lost during the equilibrium period can be checked against a water turnover value for red kangaroos during winter. The value is about 60 ml/kg*day, and with a TBW value of 72 % one can calculate that 8 % of the injected dose is turned over every 24 h, i.e., 2 % every 6 h, approximately the same as the value found in this experiment. In kangaroos dehydrated to 80 % of their hydrated body weight, the equilibrium time was extended from 6 to 10 h. This extension of time was also seen in camels in which the equilibrium time during dehydration was 18 h compared with 8 h when hydrated (30). This delay was probably caused by a fall in the rate of secretion of salivary and pancreatic fluids as well as a slower rate of turnover between the alimentary tract and the blood (19)* The method of obtaining the TBW which uses the extrapolated zero-time concentration value is not valid under these circumstances because this method depends on a constant body-water pool which does not occur in the case of a dehydrating animal. Thus for dehydrated kangaroos an estimate of TBW
Downloaded from www.physiology.org/journal/ajplegacy by ${individualUser.givenNames} ${individualUser.surname} (129.237.035.237) on January 18, 2019.
1798
M.
can only be obtained from an equilibrium-time blood sample taken 10 h after the 3Hz0 has been injected. It can be seen from Fig. 2 that the three species of large kangaroos have a high body-water content relative to their body solids. The high TBW found in the large kangaroos appears to be due to two factors: ~1) the ruminantlike gastrointestinal tract of the macropodids, and b) the lower proportion of body fat in “native” animals when compared with their domesticated counterparts. One characteristic of ruminantlike mammals is their relatively high ratio of gut-to-body weight. The ratio of stomach contents to body weight ,in red kangaroos is approximately 11 % (C. J, H arrop, personal communication). Consequently if the rumen is composed of about 80 % water (18), the amount of water in the body of a kangaroo will be higher than that found in nonruminants. This applies not only to the large kangaroos but also to cattle, sheep, and goats, as can be seen from Fig+ 2. The potoroo, however, differs in that it is omnivorous ( W and does not have a ruminantlike feeding behavior. Body-water content is not only infl uenced by the size of gut-water pool but also by the amount of fat contained in the body. Since fat cells have a water content of about 12 % (Z), animals with a hi gh fa t content will have a lower proportion of body water than leaner an imals. In a comparison among kangaroos, goats, and sheep, Tribe and Peel (33) found that two species of kangaroo had a lower fat content than that found in sheep (red kangaroo 0.4 %, grey kangaroo 0.08 Yc, and sheep 13.3 % body fat). Similar results have been found in other nondomesticated animals such as mule deer (17) and various East African antelopes (22). The animals used in this present study were nondomesticated species and all possibly had a low body-fat content. Consequently a high body-wa ter content could be expected in these animals. In the tammar wallaby, however, the percent TBW value was low, comparable with that of small laboratory animals (27). Th erc was, however, a tendency for these animals to accumulate body fat in captivity. Although the values for TBW of the macropodid marsupials appear similar to those found of eutherians, the water turnover rates appear to differ markedly in these two groups. An interspecific relationship between water turnover and body weight has been established for many years. Adolph (1) proposed that in eutherian mammals many functions of water, e.g., urine loss, insensible water loss, etc., were exponentially related to body weight. By use of tritiated water, Richmond et al. (27) related daily water use to the 0.8 power of body weight for a range of eutherian mammals. MacFarlane (19) found that tritiated water turnover in three species of ruminant was related to the 0.82 power of their body weight. A similar relationship exists between standard energy metabolism and body weight in eutherian mammals (16)
J*
S. DENNY
AND
T.
J.
DL~WSON
and marsupials (6). In both groups of animals standard energy metabolism is proportional to the 0.75 power of body weight, but in marsupials the actual level is approximately 30 ‘, lower than in eutherian mammals. Consequently it is of interest to find that, although the water turnover of macropodids is related to the 0.8 power of body weight, the actual level is 26 % lower than that given by Richmond et al. (27) for eutherians. That there is a relationship between oxygen consumption and water metabolism has been mentioned by several authors (12, 15), and recently MacFarlane et al. (20) ranked several species of ruminents, rodents, and Dasyurid marsupials on the basis of these criteria. MacFarlane et al. (20) pointed out that animals with a low metabolic rate also have a low water turnover, and it is this relationship that would explain the low water turnover found in macropodids. The various avenues of water loss from the body are all indirectly influenced by the animals’ metabolic rate. For example, fecal water loss is determined in part by the amount of food eaten, which has been found to be lower in some species of kangaroo, when compared with eutherians (4). Urine water loss is partly determined by glomerular filtration rate which is lower in kangaroos than in most other mammals studied- Insensible water loss via the skin would tend to be low because of the lower body temperatures in marsupials (6), and respiratory water loss would also tend to be reduced due to the lower oxygen metabolism in kangaroos. Dawson et al. (5) point out that the tammar wallaby had an evaporative water loss lower than that measured in eutherians of similar size. All the macropodids studied had a low water turnover and if Table 1 is studied, it can be seen that the red kangaroo, the wallaroo, and perhaps the grey kangaroo are from arid areas, whereas the other animals, particularly the potoroo, are found in more temperate regions. This lack of correlation between water turnover and aridity of habitat is particularly interesting since &lacFarlane (19) proposes that water turnover values obtained during ad libitum conditions can be used to separate “desert-hardy” species from any other, i-e., the animals with a high water turnover under “nonstress” conditions were those that were found in waterrich habitats. This is obviously not so in this present study. Therefore, any study of an animal’s ability to survive in an arid area should include work done on the animal under conditions similar to those of the arid zone. This study was supported in part by a grant from the Australian Research Grants Comrni ttee. M. J. S. Denny was in receipt of a Council for Scientific and Industrial Research Organization postgraduate studentship. We especially thank Professor E. D. P. Thompson and Dr. hl. J. K. Macey of the University of New South Wales for the use of their scintillation counters. Received
for
publication
5 July
1974.
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