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The effect of water deprivation and hypertonic salt injection on several rodent species compared with the albino rat
Camp. B&hem. Physiol., 1973, Vol. 44A, pp. 473 to 485. Pergamon Press. printed in Great Britain
THE EFFECT OF WATER DEPRIVATION AND HYPERTONIC SALT INJECTION ON SEVERAL RODENT SPECIES COMPARED WITH THE ALBINO RAT URI KATZ Department of Zoology, The Hebrew University of Jerusalem, Jerusalem (Received
3 May
1972)
Abstract-A comparison was made of the response of six rodent species from Israel, to water deprivation at room temperature (moderate) and 37°C (acute conditions). 1. The rodents were separated into two groups according to their response to water deprivation: The albino rat, spiny mouse and golden hamster were defined as mesophifc, whereas the jerboa, fat jird and little jird were defined as xeric species. 2. The xeric species were found to maintain weight without drinking water at room temperature, 3. The mesophilic species tolerated a greater loss of their initial body weight than the xeric species at 37°C during the same time limit. 4. Eighty per cent mortality occurred among the albino rat, fat and little jird upon intraperitoneal injection of 6% NaCl; only 20 and 30 per cent mortality were found among the spiny mice and albino mice. 5. Water content of the gastrointestinal tract was markedly reduced under water deprivation at 37”C, among the xeric species only. 6. The significance of these findings is discussed in connection to the problem of adaptation in its relation to the ecological background and the systematic origin of the species.
INTRODUCTION
EXTENSIVEstudies on the effects of arid conditions on small rodents have been carried out during the past 25 years; the monograph of K. Schmidt-Nielsen (1964) summarizing most of the results on this subject from a comparative point of view. The main conclusion to be drawn from these studies is that physiological adaptation of small rodents to arid conditions is achieved mainly by their osmoregulatory organs, namely the kidneys. In addition, physiological adaptations such as reduced evaporative water loss, reduced water content of the faeces and other such mechanisms contribute to their ability to survive in a hot and dry environment. We have studied the response of several species of rodents from different ecological backgrounds to water deprivation at various ambient conditions. We were concerned mainly with the effect on the milieu intthkur, looking for possible adaptations of organs other than those concerned with osmoregulation. Two different groups were distinguished, with the most xeric animals not proving 473
474
URI
KATZ
necessarily the most resistant to water deprivation at high temperatures. The gastrointestinal tract was found to play an important role in water balance of the xeric species under the above-mentioned conditions. Our results contribute to the general physiological distinction which is established between two different ecological groups with respect to their response to ambient environmental conditions. MATERIALS AND METHODS The species studied were as follows: 1. Albino rat (Rattus norwegicus) of the Tzabar strain, bred at the Hebrew University Hadassah Medical School of Jerusalem (family-Muridae). 2. Albino mouse (Mus musculus), bred at the Hebrew University Hadassah Medical School of Jerusalem (family-Muridae). 3. Common spiny mouse (Acomys cuhirinus) trapped near Jerusalem (family-Muridae). 4. Golden hamster (Mesocricetus aurutus) bred at the Hebrew University Hadassah Medical School of Jerusalem (family-Cricetidae). 5. Jerboa (_%rcuZus juculus) caught in the arid zone of southern Israel in a sandy habitat near Khumob (family-Dipodidae). 6. Little jird (GerbiZZus dusyurus) trapped near Jerusalem (family-Gerbillidae). 7. Fat jird (Meriones crassus) trapped in the arid zone of southern Israel near Hatxeva (family-Gerbillidae). The duration of the study was approximately 4 years; no significance was attached to season of capture, but animals were kept at least 4 weeks under laboratory conditions before being subjected to experimental treatment. Males were used throughout. The animals were kept at 21-25°C (room temperature) and 70-78% relative humidity (r.h.) in the laboratory. Rats were fed laboratory Purina chow and had free access to tap water. The other species were fed wheat seeds containing about 10 per cent water; the spiny mice and the Jerboa were given fresh carrots two or three times a week. Little and fat jirds maintained and even gained weight without drinking water at 25 and 30°C under laboratory conditions. Experimental
treatment
1. Water and food deprivation at room temperature (25°C; 70% r.h.). 2. Water and food deprivation at 37* 1°C and 15% r.h. Food deprivation only under the above-mentioned conditions served as control. 3. Sodium chloride injection of 3 and 6% (at 35”C), intraperitoneally, in amounts of about 3 ml/100 g body weight. Body weight was followed to the nearest 0.5 g. Blood was collected in heparinized F’yrex capillaries, (10,000 U/ml) from the cut end of the tail, and centrifuged. The hematocrit was measured, cells discarded and the plasma kept for further analysis. Chloride was titrated according to the modification by Brown of S&ales & Schales (1941). BY&e body and tissue analysis. Animals were killed by a stream of CO*, and immediately dissected. Whole tissue of skeletal muscle (gastrocnemius), heart and gastrointestinal tract (intestine and stomach from sphincter to the end of colon) were removed, as well as a sample from the liver. Tissues were blotted on Whatman No. 2 filter paper, and weighed to the nearest 0.1 mg; the gastrointestinal tract and the carcass were weighed to the nearest 0.01 g. All samples were dried to a constant weight in a 100°C oven. Water content was calculated from the difference between fresh and dry weight. Fat was extracted from the dry carcass by ether, according to Gradwhol (1948). Duplicates did not differ by more than l-2.5 per cent. Body water is given for lean body mass. Ether extracted fat in muscles did not yield more than 3 per cent of the fresh weight for which no correction has therefore been made.
WATER DEPRIVATION
475
IN SMALL RODENTS
Faeces were collected under parafhn oil, blotted, weighed and dried to constant weight in a 100°C oven. Digestability is calculated as the ratio of dry faeces secreted per dry food consumed per body weight during a given time. RESULTS
Weight loss Two distinct groups of curves are apparent in Figs. 1 and 2; the species to whom these curves are related have a common ecological background. The ecologically xeric animals are less resistant to weight loss at high temperature, and usually reach a lethal level on losing 10-15 per cent of their initial body weight.
I
I
I
I
I
2
I
I
4
I
I
6
I
I
S
IO
days
time,
FIG. 1. Time course of weight change at 25°C and 70% r.h. for the species studied. Mean of four to six animals in each species. 1. Albino rat. 2. Spiny mouse. 3. Golden hamster. 4. Jerboa. 5. Little jird. 6. Fat jird.
L
(1
4
11
8
11
12 Time,
11
16
11
20
11
24
11
hr
FIG. 2. Time course of weight change at 37°C and 15% r.h. for the species studied. Mean of four to six animals in each species. The sign (t) indicates the time at which animals began to die.
42.5 + 4.1 (3) 35.9 +_2.7 (4)
65.8 f 3.6 (4) 60.2 +_3.5 (4)
29.1 + 3.2 (3) 20.9 f 0.7 (6)
85.5 f 9.7 (5) 70.3 +_12.6 (6)
Spiny mouse Water and food ad lib. at room temperature Water deprivation at 37°C
Jerboa Water and food ad Zib. at room temperature Water deprivation at 37°C
Little jird Water and food ad lib. at room temperature Water deprivation at 37°C
Fat jird Water and food ad lib. at room temperature Water deprivation at 37°C
-
10 hr
-
4 days
-
30 hr
(4)
6.0 f 2.3 (6)
-
13.7 zkl-5 (6)
-
11*4*zo
18.7 f 0.7 (4)
-
17.8 +_1.2 (11)
24 hr
10 hr
Weight loss (%)
66.8 f 1.1 (5) 60.8 zk6-l (6)
64.7 Z!I1.8 (3) 55.6 + 1.4 (6)
62.2 + 1 a9 (4) 60-7 zk3.3 (4)
63.3 f 2.0 (3) 57.8 +_1.6 (4)
68.0 * 0.5 (13) 64.6 +_0.9 (11)
Water content in the whole body (%)
72.0 + 0.9 (5) 70.4 f 3.1 (6)
71.0 + 1.4 (3) 68.2 f 1.9 (6)
70.3 f O-8 (4) 67.4f 1.3 (4)
69.7 f 1-l (3) 65-5 -I O-5 (4)
71.5 z!?0.3 (13) 68.5 f 0.6 (11)
Water content in fat free body weight (%)
79.6
-
89
-
93.7
-
88.5
-
89
-
Calculated amount of water in the total weight loss (%)
ON WRIGHT LOSS AND THE WATER CONTENT OF THE WHOLE BODY IN 5 OF
THE SPECIES STUDIED
37°C
Duration of water deprivation
AT
* The weight at time of sacrifice. Mean values f S.E. Number of animals in parentheses.
183 f 10.8 (13) 149 f 9.4 (11)
Weight of animals * (g)
EFFECT OF WATER DEPRIVATION
Albino rat Water and food ad lib. at room temperature Water deprivation at 37°C
TABLE I-THE
g
WATER
DEPRIVATION
IN
SMALL
477
RODENTS
The weight is lost, however, during a much longer period of time ; at room temperature these animals could maintain their weight even without drinking water. The little jird was most striking in this respect, for this animal could live more than 4 days at 37°C and 15% r.h., loosing only 20 per cent of its initial body weight (a proportion lost by the albino rat in less than 24 hr under the same conditions). This ability is due, at least in part, to the fact that this species did not become hyperthermic at this temperature (Katz, 1966). Water balance
The water content of the whole body does not differ much among the species studied, under normal conditions (fully hydrated); when calculated for lean body mass this value is more or less 70 per cent of the fresh body weight (Table 1). Only at high temperature and low humidity could the weight lost be accounted for by water loss; under other conditions of water deprivation, even for a long period, water and solids are presumably lost at similar rates. Plasma electrolytes
The chloride concentration in the plasma of four of the species was analyzed under conditions of water deprivation at 35 f 1°C (Table 2). A greater increase was found in the albino rat and spiny mouse. Table 2 also summarizes the results of an experiment which was designed to examine the maximal plasma chloride concentration which is tolerated by four species. The second injection, with 6% NaCl, TABLE SPECIES
2--CHLORIDE AFTER
CONCENTRATION
WATER
DEPRIVATION
IN
AT 35”C, OF 3 AND
THE AND
6%
PLASMA UPON
(m-equiv./l.)
INTRAPERITONRAL
OF
FOUR
INJECTION
NaCl
NaCl injection Species Albino rat Spiny mouse Fat jird Little jird
Control 111.3 109.2 110.8 106.8
k6.9 (6) + 7.1 (6) f 12.6 (6) f 3.1 (6)
Water deprivation * 118.4 + 5.8 (5) 128.3 f 9.4 (5) 111*2f9.6 (5) 110-l zk10.7 (4)
3%t 143.1 147.0 149.7 149.7
+_7.4 (4) + 6.0 (3) f 13.2 (3) f 17.5 (4)
6%: 170.1 162.7 179.2 181.0
* 4.7 (4) -I 27.6 (4) + 16.3 (4) (1)
* The albino rats lost about 17 per cent of their initial body weight in 2 days, whereas the spiny mice, the fat and little jird lost about 9.5 per cent each, in 3 days. t 3 ml/100 g body weight. $ 4.2 ml/100 g body weight. Mean + S.E. Number of animals in parentheses.
caused 80 per cent mortality within l-6 hr among the albino rats, fat and little jirds (five deaths out of six) ; only 20 and 30 per cent mortality were found among the spiny mice and the albino mice respectively (one and two deaths out of six). Chloride concentration increased quite similarly in the different species.
478
URI
TABLE 3-THR THE WHOLE
KATZ
RRRRCT OF WATERDEPRIVATION AT 37°C ON THE
TISSUE
IN THR HEART,
GASTROCNRMIUS
WATER CONTENT
OF
MUSCLE AND THE LIVER IN THR
SPECIES STUDIED
Albino rat Water and food ad lib. at room temperature Water deprivation at 37°C
P Spiny mouse Water and food ad lib. at room temperature Water deprivation at 37°C
P Golden hamster Water and food ad lib. at room temperature Water deprivation at 37°C
P Jerboa Water and food ad lib at room temperature Water deprivation at 37°C
P Little jird Water and food ad lib. at room temperature Water deprivation at 37°C
P Fat jird Water and food ad lib. at room temperature Water deprivation at 37%
Heart
Liver
77.4 ?z0.8 (15)
76.6 f 1.7 (30)
72.1 rl1.9 (15)
-
75.6 f0.0 (14) 0.005
74.7f
71-O+ 1.9 (14) 0.10
17.8f3.9
74.5 + 0.1 (2)
76.7 f 0.7 (4)
72.0 _+1.5 (2)
72.7 k 2.2 (6) 0.05
74.2 + 1.7 (12) 0.001
70.4f
76.2 z!z0.3 (4)
74.8 f 0.3 (4)
72.0 f 0.4 (4)
75.6 + 0.3 (4)
o-10
73.0 + 1.1 (4) 0.025
71.6 f 0.4 (4) 0.20
76.2 + 1.2 (4)
75.4 + 0.8 (8)
71.5 f 2.9 (4)
-
75.3 f O-4 (5) 0.01
74.8 f 1.7 (10) 0.01
69.8 + 2.1 (5) 0.30
143 f 4.3 (5)
76.3 f 4.7 (4)
76.2 + 1.2 (4)
70.9 f 0.7 (4)
-
75.6 f 2.7 (8) 0.10
71.3 f 2.1 (8) 0.001
66.2 f 5.5 (8) 0.10
16.4 f 5.6 (8)
79.3 f 0.3 (2)
76.8 k 0.2 (4)
71.5 f 1.5 (2)
-
75.9 f 1.2 (4)
74.9 f 1.0 (8) 0.005
60.2 f 3.2 (4) 0.01
O-005
P Mean f S.E.
body weight) Total weight lost (% of initial
Skeletal muscle (gastrocnemius)
1.6 (28) 0.001
Number of determinations in parentheses.
2.5 (6) 0.025
(14)
17.4 f 2-l (6)
15.7 i4.5
(4)
9.4 f 3.1 (4)
WATER DEPRIVATION
IN SMALL RODENTS
479
Water content of the tissues Table 3 gives the percentage of water in three tissues for the six species studied. The water content of each tissue under normal (hydrated) conditions is quite similar for the different species studied. The various tissues, however, contain different proportions of water which are differentially affected when the animals are deprived of exogenous water. It is also possible on this basis to distinguish between the two ecological groups mentioned. It seems that in the xeric species the gastrocnemius and the liver, but not the heart, lost a greater proportion of water during water deprivation, than in the mesophilic species. The gastrointestinal tract The water content of the gastrointestinal tract is close to that of other organs (Table 4), and amounts to about 75 per cent of its fresh weight. This value is, however, greatly reduced in the xeric species under water deprivation at 37°C; it is only a little affected in the albino rat and remains unchanged in the spiny mouse. Table 5 gives the percentage of water content in the faeces for five of the species studied when deprived of water. It should be noted that for the xeric species this was examined only at 37°C because they maintain water balance at 25 and 30°C on dry barley only, without having free drinking water. Digestive coefficients were derived from the ratio of the dry faeces secreted to the amount of dry food consumed per 24 hr. This value is 0.20 f 0.05 (four samples) for the rat at 23°C with water ad lib. and is reduced to 0.12 f 0.04 (eight samples) during water deprivation; food utilization is therefore improved. No such reduction was found in the xeric species. DISCUSSION
Looking at the mechanisms activated when small rodents are deprived of water, water distribution and its proportionate loss should be focused upon. Only the total water content of several organs and the whole animal was measured in this study. The water content of skeletal (gastrocnemius) muscle, liver and gastrointestinal tract, is reduced under water deprivation in all the species studied; a greater reduction, however, was observed in the xeric species (Table 3). This observation points to the possible existence of a special mechanism by which the gastrointestinal tract and, to a lesser extent, skeletal muscle and liver may contribute to the total water loss. The water content of the gastrointestinal tract is regulated mainly by the ratio of the food and water intake and varies little (Lepkovsky et al., 1957). Moreover, we found less than a 20 per cent decrease in the amount of water which is stored in this system in the rats during water deprivation (Table 5); but almost a 50 per cent reduction in the xeric species under similar conditions. An important function has been attributed similarly to the gut and the alimentary canal in the camel under conditions of water deprivation (Macfarlane, 1964).
37°C SPBCIRS STUDIED
10.5 f 1.6 (3)
89.8 + 13.4 (3)
21.2 Ik2.2 (4)
21.4 AZ 2.3 (4)
52.1 f 2.0 (2)
-
13.4 Ik0.4 (3)
57.5 zk3.0 (3)
21.3 zk1.3 (3)
-
17.4 f 0.8 (7)
36.7 + 1.7 (7)
69.1 k4.5 (3)
-
17.8 f 1.2 (11)
137.1+ 15.2 (11)
44.5 f 1.8 (2)
-
28
68.1 f 2.5 (3)
76.8 I!Y0.6 (2)
65.4 + 2-O (4)
100
-
80.3 _+4.4 (3)
70.8 * 25 (3)
30
-
78.5 f 2.0 (3)
73.4 f 1.0 (7)
-
18
73.9 + l-6 (2)
73.12 0.6 (11)
15
-
76.6 + 0.4 (14)
-
0.05
0.01
0.05
0.80
0.001
P
TRACT
8.6 _+1.5 (3)
13.0 + 4.4 (2)
9.2 * 1.1 (4)
18.0 f 4.3 (3)
5.6 + 0.7 (3)
11*7f 1.3 (2)
10.2 zk1.0 (7)
10.9 + o-5 (2)
12.7 + 0.5 (11)
15.3 _+0.6 (14)
P
0.30
0.05
0.01
0.70
o*oos
IN 5 OF THE
Water content in the gastrointestinal tract as percentage of the whole body water content (%I
OF THE GASTROINTESTINAL
Water content of the gastrointestinal tract with its content (% of wet weight)
ON THE WATER CONTENT
181.9 f 10.0 (14)
Mean + S.E. Number of animals in parentheses.
Fat jird Water and food ad lib. at room temperature Water deprivation at 37°C
Little jird Water and food ad lib. at room temperature Water deprivation at 37°C
Jerboa Water and food ad lib. at room temperature Water deprivation at 37°C
Spiny mouse Water and food ad lib. at room temperature Water deprivation at 37°C
AT
Duration of exposure to Weight lost experimental Weight of the environment animals (% of body weight) (hr) (g)
OF WATER DEPRIVATION
Albino rat Water and food sd lib. at room temperature Water deprivation at 37°C
TABLE ‘i-----EFFECT
f
2
$ 0
WATRRDEPRIVATION
IN SMALL RODENTS
481
TABLE S-EFFECT OF WATRR DR~RIVATI~N AT ~00~ TEMPERATURE (FOR 1OOhr) 37°C (FOR 48hr) ON THE WATER CONTENT OF THE FARCES IN FIVE SPECIEG
AND
Water content in the faeces (%) 25°C; 70% r.h.
37°C; 15% r.h.
Albino rat Water and food ad lib. Water deprivation
74.3 + 1.3 (4) 47.8 + 5.3 (4)
69.8 f 3.2 (4) 52.4 + 3.0 (4)
Golden hamster Water and food ad lib. Water deprivation
63.6 k 0.3 (3) 53.5 * 5.3 (3)
74.4 + 2.6 (3) 36.5 k 1.4 (3)
Jerboa* Water and food ad lib. Water deprivation
-
44.4 f 2.7 (3) 35.6 + 2.9 (3)
Little jird * Water and food ad lib. Water deprivation
-
63.9 f 7.5 (8) 38.3 zk 12.0 (8)
Fat jird* Water and food ad lib. Water deprivation
-
51.5 f. 3.4 (3) 21.3 k 3.7 (3)
* The desert species: fat and little jird and the jerboa lived permanently on dry diet at room temperature without drinking water. Mean f S.E. Number of animals in parentheses.
The water content of the faeces in the xeric species is lower than for the mesophilic species under normal conditions; they can also extract even more water when deprived of drinking water at high temperature (Table 5). It would be interesting to investigate whether it is the length of the colon (Lang 8z Staaland, 1970) which is responsible for this effect and whether it is also controlled by hormones (Edmonds & Marriott, 1969). The rat and most of the other mesophilic species lose their appetite and reduce their food intake about a day or two after onset of water deprivation. Strominger (1967) has pointed out the interdependency of water and food intake in rats. It is therefore a great advantage for the xeric species that they can maintain normal feeding without drinking water which is usually inaccessible to them. The appetite center in the brain of the different species might be controlled differently. Plasma osmolarity was found to control food and water intake in rats (Gutman & Krausz, 1969); if the same mechanism applies also to the xeric species they should have stopped, or at least decreased, their food consumption when their plasma osmolarity increases. The fact that these species keep their plasma osmolarity within a very narrow range raises the possibility that their central control system might be more sensitive to such changes.
482
URI
&AZ
There is no need to stress the well-established differences in kidney function between the xeric and mesophilic species (B. Schmidt-Nielsen, 1964; Dantzler, 1970). It is worth noting, however, that all the species in this study, except for the albino rat, possess a relatively long renal papilla and are able to produce a highly concentrated urine. “Dehydration” is rather a poor definition, as it gives only a general description of various conditions which are attained in several different ways. Desert animal physiologists usually dehydrate by depriving them of drinking water (K. SchmidtNielsen, 1964), whereas others (Darrow & Yannet, 1935 ; Moyer & Nissan, 1961) do so by injection of hypertonic solutions (either of salt or impermeant molecules). In both cases this is referred to as “dehydration”, although the results are quite different from one another. “The only similarity between the different conditions” says Nadal et aZ. (1941) “is that implied by the term ‘dehydration’.” A decrease in the extracellular fluid volume is the main change which characterizes dehydration caused by water deprivation; on the other hand, there is only cellular dehydration when hypertonic solutions are injected, which might or might not be accompanied by an increase of NaCl concentration in the plasma, depending on whether salt or impermeant molecule was used. The molal concentration of the water (which is inversely related to the concentration of the solid constituents in the cell) is obviously an important factor for normal physiological function. Hayward (1965) h as stressed the basic need for a dependable reference criterion for comparisons; he also pointed out the interindividual constancy of body water content which makes it useful for this purpose. Two general phenomena are apparent from the present and numerous other studies: Firstly, the water content of the whole body, in rodents, and mammals in general, is only a little affected by water deprivation at different temperatures. When the amount of water lost under the different conditions of water deprivation is calculated as a percentage of total weight lost (Table 1, last row) it may be seen that only under acute conditions, 90 per cent of the weight lost by rats was water, whereas only 75 per cent water accounted for the weight lost when animals were deprived of exogenous water at room temperature. Similar proportions were found for the other species. It appears that in rodents, only water deprivation at high temperature during a short time period (Lewis et al., 1961) can be considered as a “real” dehydration (Adolph et al., 1947). It would be worth mentioning here that the mammals which are known to be the most resistant to water deprivation (the camel and donkey, K. Schmidt-Nielsen, 1964) drink at a single session almost all that they have lost in weight, when previously deprived of water. Only in this latter case could the weight loss be considered “real” dehydration. The second phenomenon is the distinction which could be made for two different groups with regard to their response to water deprivation (Figs. 1 and 2, and Tables 2). These two groups have different ecological backgrounds: Of the wild species, the common spiny mouse and the little jird, inhabit both the northern (moist) part and the southern (dry) part of Israel. The rat jird and the jerboa
WATER DEPRIVATION
IN SMALL RODENTS
483
inhabit the southern part of the country where the average rainfall does not exceed 100 mm a year. The golden hamster is a breed of a couple which were originally trapped in the Syrian desert. The species have therefore been differentiated as arid or xeric as opposed to the mesophilic group. (They are called “dry” and “moist” rodents by K. Schmidt-Nielsen, 1964, p. 179). Surprisingly, the mesophilic group could tolerate a greater degree of weight and water loss when deprived of water at 37°C than the xeric group during approximately the same time limit. Similarly, in the experiment of 6% NaCl injection, the xeric species were found to be more sensitive to elevation in plasma NaCl concentration (Table 2). From these observations it may be surmised that although the xeric group have better mechanisms for water conservation under the same environmental conditions (SchmidtNielsen et al., 1948), they do not possess a better resistance to actual changes in their internal environment. Albino rats are far more vulnerable than the other species in respect to their weight change and probably also other physiological parameters (Horowitz & Borut, 1970), whereas the spiny mouse may represent a special case in which the kidney is highly developed and able to secrete a very concentrated urine (Shkolnik & Borut, 1969), but at the same time the animal is still exposed to fluctuating environmental conditions and can therefore tolerate considerable changes in plasma electrolytes. Shkolnik (1960), who studied seven different Israeli species in respect to their resistance to heat during water deprivation, concluded that they behaved in a systematic order in their tolerance to arid conditions. The Gerbillidae are the most tolerant, then come the Dipodidae, whereas the Muridae are the least resistant in this respect. The observations reported in the present study are in accord with the systematic order mentioned above (in fact three species were the same in both studies). Lang & Staaland (1970) studied the function of the caecum-colon structure in salt and water conservation. They correlated the higher efficiency of sodium and water reabsorption in the caecum-colon structure of the Norway lemming compared with that of the Norway rat with the anatomy of this structure ; this was found to be related to the systematic origin of the family (i.e. all Cricetidae examined possess a post-caecal spiral which is absent in the Muridae, and they also have a longer colon). Caste1 & Abraham (1969) found that the hypothalamic neurohypophyseal system of four species, all from the family Muridae responded differently to water deprivation; this was in correlation with their weight loss so that in the albino rat the hormones were almost completely diminished, whereas in the other species (white mice and spiny mice) partial depletion was followed by repletion. Horowitz & Borut (1970) found 32 and 18 per cent reduction in the extracellular fluid of water deprived rats and fat jirds respectively, but no change in this compartment in the spiny mice. Similar reduction was found in the blood volume. These three species (rat, spiny mouse and fat jird) cannot therefore be classified simply by their ecological background according to this parameter. We find then, some physiological and anatomical adaptations that could be classified according to systematic order (Shkolnik, 1960; Lang & Staaland, 1970; present study), whereas the development of other mechanisms is not bound to hereditary
484
URI KAn
options (Caste1 & Abraham, 1969 ; Horowitz & Borut, 1969 ; and others). It is pertinent in this connection that Bogert (1949) found that reptiles belonging to the same genus tend to have similar, although not necessarily identical, mean body temperature preferences, even though they live in different habitats and climatic regions. It should be interesting to find out to what extent this approach could be used, as it implies that certain families or genotypes got some options, on which further adaptation could be developed (Hudson, 1964). In 1932 Barcroft reviewed the fixity of the “millieu interieur”, he concluded that as far as investigations show anything, the fixity of the internal environment is controlled by the upper part of the central nervous system. It should now be worth comparing the effect of water deprivation on the activity of the central nervous system in different species. SUMMARY
AND CONCLUSIONS
Six rodent species were studied under conditions of water deprivation and have been compared for their response in weight change, whole body and tissues water content and plasma chloride concentration. Two distinct groups were distinguished, mainly according to their ecological background. Unexpectedly, it was found that the xeric species were less resistant to water loss at high temperature and to hypertonic salt injection. Adaptation is discussed in relation to the ecological background (environmental) and to the systematic origin of the species. It is concluded that physiological adaptation to water deprivation (dehydration), does not necessarily concern all physiological mechanisms, but rather those related to the fixity of the internal milliue. Acknowledgement-I would like to thank Drs. Mona Caste1 and Michal Horowitz for their critical reading of the manuscript. REFERENCES E. F. (1947) Tolerance to heat and dehydration in several species of mammals. Am.9. Physiol. 151, 564475. BARCROFT J. (1932) La fixt6 du milieu interieur est la condition de la vie libre (Claude Bernard). Biol. Rev 7, 24-87. BOGERT C. M. (1949) Thermoregulation in reptiles, a factor in evolution. Ewolution 3, 195-211. CASTELM. & ABRAHAM M. (1969) Effects of dry diet on the hypothalamic neurohypophysical neurosecretory system in spiny mice as compared to the albino rat and mouse. Gen. & compar. Endocr. 12, 231-241. DANTZLERW. H. (1970) Kidney function in desert vertebrates. In Hormones and En&onment (Edited by BENSONG. K. & PHILLIPS J. G.), 18, 157-189. Mem. Sot. Endocr. DARROWD. C. & YANNET H. (1935) The changes in the distribution of body water accompanying increase and decrease in extracellular electrolyte. J. clin. Invest. 14,266-275. EDMONDSC. J. & MARRIOTTJ. C. (1969) The effect of aldosterone on the electrical activity of rat colon. J. Endocr. 363-377. GRADWHOL R. B. H. (1948) Clinical Laboratory Methods and Diagnosis. Kimpton, London. GUTMANY. & KRAUSZM. (1969) Regulation of food and water intake in rats as related to plasma osmolarity and volume. Physiol. & Behuu. 4, 311-313. ADOLPH
WATERDEPRIVATION IN SMALLRODENTS
485
HAYWARDJ. S. (1965) The gross body composition of six geographic races of Peromysicus. Can.J. Zool. 43, 297-308. HOROWITZM. & BORUTA. (1970) Effect of acute dehydration on body fluid compartments in three rodent species: Rattus norvegicus, Acomys cahirinus and Meriones w~ssus. Camp. Biochem. Physiol. 35, 283-290. HUDSONJ. W. (1964) Water metabolism in desert mammals. In Thirst, pp. 211-233. Proc. of 1st Int. Symp. Pergamon Press, Oxford. KATZ U. (1969) Studies on the mechanism of dehydration and muscle activity in small rodents. M.Sc. thesis, the Hebrew University, Jerusalem. (In Hebrew with English summary.) LANG R. & STAALANDH. (1970) Adaptations of the caecum colon structure of rodents. Comp. Biochem. Physiol. 35, 905-919. LEWIS A. C., RUBIN M. E. & BEISEL W. R. (1960) A method for rapid dehydration of rats. J. appl. Physiol. 15, 525-527. LEPKOVSKYS., LYMAN R., FLEMINGD., NAGUMOM. & DIMICK M. (1957) Gastrointestinal regulation of water and its effect on food intake and rate of digestion. Am. J. Physiol. 188, 327-331. MACFARLANE W. V. (1964) Terrestrial animals in dry heat: Ungulates. In HQTI&OO~ of Physiology-Environment, pp. 509-539. American Physiological Sot., Washington, D.C. MOYER C. A. & NISSAN S. (1961) Alterations in the basal oxygen consumption of rats attendant upon three types of dehydration. Ann. Surg. 154, Suppl. 51-64. NADALJ. W., PEDERSENS. & MADDOCKW. G. (1949) A comparison between dehydration from salt loss and from water deprivation. 3. clin. Invest. 20,691-703. SCHALES0. & SCHALESS. (1941) A simple and accurate method for the determination of chloride in biological fluids. J. biol. Chem. 140, 879-884. SCHMIDT-NIELSEN B. (1964) Organ system in adaptation: the excretory system. In fkndbook of Physiology-Environment, pp. 879-884. American Physiological Society, Washington, D.C. SCHMIDT-NIELSENB., SCHMIDT-NIELSENK., BROKAWA. & SCHNEIDERMAN H. (1948) Water conservation in desert rodents. Am. J. Physiol. 32, 331-360. SCHMIDT-NIELSENK. (1964) Desert Animals. Oxford. SHKOLNIKA. (1960) Tolerance of desert mice living on dry food only, to different ambient conditions. M.Sc. thesis, The Hebrew University of Jerusalem. (In Hebrew.) SHKOLNIKA. & BORUTA. (1969) Temperature and water relations in two species of spiny mice (Acomys) J. Mammal. 50, 245-255. STROMINGER J. L. (1947) The relation between water intake and food intake in normal rats and rats with hypothalamic hyperphagia. YaleJ. biol. Med. 19, 279-287. WALLACEW. M., GODSTEINK., TAYLORA. & TEREE T., (1970) Thermal dehydration of the rat: distribution of losses among tissues. Am. J. Physiol. 219, 1544-1548. Key Word Index-Desert rodents; water deprivation; hypertonic salt injection; plasma chloride; body water content; Rattus norvegicus; Acomys cahirinus; Mus musculus; MesoMeriones crassus. cricetus auratus; &rboa jaculus; Gerbillus ahyu~us;
THE EFFECT OF WATER DEPRIVATION AND HYPERTONIC SALT INJECTION ON SEVERAL RODENT SPECIES COMPARED WITH THE ALBINO RAT URI KATZ Department of Zoology, The Hebrew University of Jerusalem, Jerusalem (Received
3 May
1972)
Abstract-A comparison was made of the response of six rodent species from Israel, to water deprivation at room temperature (moderate) and 37°C (acute conditions). 1. The rodents were separated into two groups according to their response to water deprivation: The albino rat, spiny mouse and golden hamster were defined as mesophifc, whereas the jerboa, fat jird and little jird were defined as xeric species. 2. The xeric species were found to maintain weight without drinking water at room temperature, 3. The mesophilic species tolerated a greater loss of their initial body weight than the xeric species at 37°C during the same time limit. 4. Eighty per cent mortality occurred among the albino rat, fat and little jird upon intraperitoneal injection of 6% NaCl; only 20 and 30 per cent mortality were found among the spiny mice and albino mice. 5. Water content of the gastrointestinal tract was markedly reduced under water deprivation at 37”C, among the xeric species only. 6. The significance of these findings is discussed in connection to the problem of adaptation in its relation to the ecological background and the systematic origin of the species.
INTRODUCTION
EXTENSIVEstudies on the effects of arid conditions on small rodents have been carried out during the past 25 years; the monograph of K. Schmidt-Nielsen (1964) summarizing most of the results on this subject from a comparative point of view. The main conclusion to be drawn from these studies is that physiological adaptation of small rodents to arid conditions is achieved mainly by their osmoregulatory organs, namely the kidneys. In addition, physiological adaptations such as reduced evaporative water loss, reduced water content of the faeces and other such mechanisms contribute to their ability to survive in a hot and dry environment. We have studied the response of several species of rodents from different ecological backgrounds to water deprivation at various ambient conditions. We were concerned mainly with the effect on the milieu intthkur, looking for possible adaptations of organs other than those concerned with osmoregulation. Two different groups were distinguished, with the most xeric animals not proving 473
474
URI
KATZ
necessarily the most resistant to water deprivation at high temperatures. The gastrointestinal tract was found to play an important role in water balance of the xeric species under the above-mentioned conditions. Our results contribute to the general physiological distinction which is established between two different ecological groups with respect to their response to ambient environmental conditions. MATERIALS AND METHODS The species studied were as follows: 1. Albino rat (Rattus norwegicus) of the Tzabar strain, bred at the Hebrew University Hadassah Medical School of Jerusalem (family-Muridae). 2. Albino mouse (Mus musculus), bred at the Hebrew University Hadassah Medical School of Jerusalem (family-Muridae). 3. Common spiny mouse (Acomys cuhirinus) trapped near Jerusalem (family-Muridae). 4. Golden hamster (Mesocricetus aurutus) bred at the Hebrew University Hadassah Medical School of Jerusalem (family-Cricetidae). 5. Jerboa (_%rcuZus juculus) caught in the arid zone of southern Israel in a sandy habitat near Khumob (family-Dipodidae). 6. Little jird (GerbiZZus dusyurus) trapped near Jerusalem (family-Gerbillidae). 7. Fat jird (Meriones crassus) trapped in the arid zone of southern Israel near Hatxeva (family-Gerbillidae). The duration of the study was approximately 4 years; no significance was attached to season of capture, but animals were kept at least 4 weeks under laboratory conditions before being subjected to experimental treatment. Males were used throughout. The animals were kept at 21-25°C (room temperature) and 70-78% relative humidity (r.h.) in the laboratory. Rats were fed laboratory Purina chow and had free access to tap water. The other species were fed wheat seeds containing about 10 per cent water; the spiny mice and the Jerboa were given fresh carrots two or three times a week. Little and fat jirds maintained and even gained weight without drinking water at 25 and 30°C under laboratory conditions. Experimental
treatment
1. Water and food deprivation at room temperature (25°C; 70% r.h.). 2. Water and food deprivation at 37* 1°C and 15% r.h. Food deprivation only under the above-mentioned conditions served as control. 3. Sodium chloride injection of 3 and 6% (at 35”C), intraperitoneally, in amounts of about 3 ml/100 g body weight. Body weight was followed to the nearest 0.5 g. Blood was collected in heparinized F’yrex capillaries, (10,000 U/ml) from the cut end of the tail, and centrifuged. The hematocrit was measured, cells discarded and the plasma kept for further analysis. Chloride was titrated according to the modification by Brown of S&ales & Schales (1941). BY&e body and tissue analysis. Animals were killed by a stream of CO*, and immediately dissected. Whole tissue of skeletal muscle (gastrocnemius), heart and gastrointestinal tract (intestine and stomach from sphincter to the end of colon) were removed, as well as a sample from the liver. Tissues were blotted on Whatman No. 2 filter paper, and weighed to the nearest 0.1 mg; the gastrointestinal tract and the carcass were weighed to the nearest 0.01 g. All samples were dried to a constant weight in a 100°C oven. Water content was calculated from the difference between fresh and dry weight. Fat was extracted from the dry carcass by ether, according to Gradwhol (1948). Duplicates did not differ by more than l-2.5 per cent. Body water is given for lean body mass. Ether extracted fat in muscles did not yield more than 3 per cent of the fresh weight for which no correction has therefore been made.
WATER DEPRIVATION
475
IN SMALL RODENTS
Faeces were collected under parafhn oil, blotted, weighed and dried to constant weight in a 100°C oven. Digestability is calculated as the ratio of dry faeces secreted per dry food consumed per body weight during a given time. RESULTS
Weight loss Two distinct groups of curves are apparent in Figs. 1 and 2; the species to whom these curves are related have a common ecological background. The ecologically xeric animals are less resistant to weight loss at high temperature, and usually reach a lethal level on losing 10-15 per cent of their initial body weight.
I
I
I
I
I
2
I
I
4
I
I
6
I
I
S
IO
days
time,
FIG. 1. Time course of weight change at 25°C and 70% r.h. for the species studied. Mean of four to six animals in each species. 1. Albino rat. 2. Spiny mouse. 3. Golden hamster. 4. Jerboa. 5. Little jird. 6. Fat jird.
L
(1
4
11
8
11
12 Time,
11
16
11
20
11
24
11
hr
FIG. 2. Time course of weight change at 37°C and 15% r.h. for the species studied. Mean of four to six animals in each species. The sign (t) indicates the time at which animals began to die.
42.5 + 4.1 (3) 35.9 +_2.7 (4)
65.8 f 3.6 (4) 60.2 +_3.5 (4)
29.1 + 3.2 (3) 20.9 f 0.7 (6)
85.5 f 9.7 (5) 70.3 +_12.6 (6)
Spiny mouse Water and food ad lib. at room temperature Water deprivation at 37°C
Jerboa Water and food ad Zib. at room temperature Water deprivation at 37°C
Little jird Water and food ad lib. at room temperature Water deprivation at 37°C
Fat jird Water and food ad lib. at room temperature Water deprivation at 37°C
-
10 hr
-
4 days
-
30 hr
(4)
6.0 f 2.3 (6)
-
13.7 zkl-5 (6)
-
11*4*zo
18.7 f 0.7 (4)
-
17.8 +_1.2 (11)
24 hr
10 hr
Weight loss (%)
66.8 f 1.1 (5) 60.8 zk6-l (6)
64.7 Z!I1.8 (3) 55.6 + 1.4 (6)
62.2 + 1 a9 (4) 60-7 zk3.3 (4)
63.3 f 2.0 (3) 57.8 +_1.6 (4)
68.0 * 0.5 (13) 64.6 +_0.9 (11)
Water content in the whole body (%)
72.0 + 0.9 (5) 70.4 f 3.1 (6)
71.0 + 1.4 (3) 68.2 f 1.9 (6)
70.3 f O-8 (4) 67.4f 1.3 (4)
69.7 f 1-l (3) 65-5 -I O-5 (4)
71.5 z!?0.3 (13) 68.5 f 0.6 (11)
Water content in fat free body weight (%)
79.6
-
89
-
93.7
-
88.5
-
89
-
Calculated amount of water in the total weight loss (%)
ON WRIGHT LOSS AND THE WATER CONTENT OF THE WHOLE BODY IN 5 OF
THE SPECIES STUDIED
37°C
Duration of water deprivation
AT
* The weight at time of sacrifice. Mean values f S.E. Number of animals in parentheses.
183 f 10.8 (13) 149 f 9.4 (11)
Weight of animals * (g)
EFFECT OF WATER DEPRIVATION
Albino rat Water and food ad lib. at room temperature Water deprivation at 37°C
TABLE I-THE
g
WATER
DEPRIVATION
IN
SMALL
477
RODENTS
The weight is lost, however, during a much longer period of time ; at room temperature these animals could maintain their weight even without drinking water. The little jird was most striking in this respect, for this animal could live more than 4 days at 37°C and 15% r.h., loosing only 20 per cent of its initial body weight (a proportion lost by the albino rat in less than 24 hr under the same conditions). This ability is due, at least in part, to the fact that this species did not become hyperthermic at this temperature (Katz, 1966). Water balance
The water content of the whole body does not differ much among the species studied, under normal conditions (fully hydrated); when calculated for lean body mass this value is more or less 70 per cent of the fresh body weight (Table 1). Only at high temperature and low humidity could the weight lost be accounted for by water loss; under other conditions of water deprivation, even for a long period, water and solids are presumably lost at similar rates. Plasma electrolytes
The chloride concentration in the plasma of four of the species was analyzed under conditions of water deprivation at 35 f 1°C (Table 2). A greater increase was found in the albino rat and spiny mouse. Table 2 also summarizes the results of an experiment which was designed to examine the maximal plasma chloride concentration which is tolerated by four species. The second injection, with 6% NaCl, TABLE SPECIES
2--CHLORIDE AFTER
CONCENTRATION
WATER
DEPRIVATION
IN
AT 35”C, OF 3 AND
THE AND
6%
PLASMA UPON
(m-equiv./l.)
INTRAPERITONRAL
OF
FOUR
INJECTION
NaCl
NaCl injection Species Albino rat Spiny mouse Fat jird Little jird
Control 111.3 109.2 110.8 106.8
k6.9 (6) + 7.1 (6) f 12.6 (6) f 3.1 (6)
Water deprivation * 118.4 + 5.8 (5) 128.3 f 9.4 (5) 111*2f9.6 (5) 110-l zk10.7 (4)
3%t 143.1 147.0 149.7 149.7
+_7.4 (4) + 6.0 (3) f 13.2 (3) f 17.5 (4)
6%: 170.1 162.7 179.2 181.0
* 4.7 (4) -I 27.6 (4) + 16.3 (4) (1)
* The albino rats lost about 17 per cent of their initial body weight in 2 days, whereas the spiny mice, the fat and little jird lost about 9.5 per cent each, in 3 days. t 3 ml/100 g body weight. $ 4.2 ml/100 g body weight. Mean + S.E. Number of animals in parentheses.
caused 80 per cent mortality within l-6 hr among the albino rats, fat and little jirds (five deaths out of six) ; only 20 and 30 per cent mortality were found among the spiny mice and the albino mice respectively (one and two deaths out of six). Chloride concentration increased quite similarly in the different species.
478
URI
TABLE 3-THR THE WHOLE
KATZ
RRRRCT OF WATERDEPRIVATION AT 37°C ON THE
TISSUE
IN THR HEART,
GASTROCNRMIUS
WATER CONTENT
OF
MUSCLE AND THE LIVER IN THR
SPECIES STUDIED
Albino rat Water and food ad lib. at room temperature Water deprivation at 37°C
P Spiny mouse Water and food ad lib. at room temperature Water deprivation at 37°C
P Golden hamster Water and food ad lib. at room temperature Water deprivation at 37°C
P Jerboa Water and food ad lib at room temperature Water deprivation at 37°C
P Little jird Water and food ad lib. at room temperature Water deprivation at 37°C
P Fat jird Water and food ad lib. at room temperature Water deprivation at 37%
Heart
Liver
77.4 ?z0.8 (15)
76.6 f 1.7 (30)
72.1 rl1.9 (15)
-
75.6 f0.0 (14) 0.005
74.7f
71-O+ 1.9 (14) 0.10
17.8f3.9
74.5 + 0.1 (2)
76.7 f 0.7 (4)
72.0 _+1.5 (2)
72.7 k 2.2 (6) 0.05
74.2 + 1.7 (12) 0.001
70.4f
76.2 z!z0.3 (4)
74.8 f 0.3 (4)
72.0 f 0.4 (4)
75.6 + 0.3 (4)
o-10
73.0 + 1.1 (4) 0.025
71.6 f 0.4 (4) 0.20
76.2 + 1.2 (4)
75.4 + 0.8 (8)
71.5 f 2.9 (4)
-
75.3 f O-4 (5) 0.01
74.8 f 1.7 (10) 0.01
69.8 + 2.1 (5) 0.30
143 f 4.3 (5)
76.3 f 4.7 (4)
76.2 + 1.2 (4)
70.9 f 0.7 (4)
-
75.6 f 2.7 (8) 0.10
71.3 f 2.1 (8) 0.001
66.2 f 5.5 (8) 0.10
16.4 f 5.6 (8)
79.3 f 0.3 (2)
76.8 k 0.2 (4)
71.5 f 1.5 (2)
-
75.9 f 1.2 (4)
74.9 f 1.0 (8) 0.005
60.2 f 3.2 (4) 0.01
O-005
P Mean f S.E.
body weight) Total weight lost (% of initial
Skeletal muscle (gastrocnemius)
1.6 (28) 0.001
Number of determinations in parentheses.
2.5 (6) 0.025
(14)
17.4 f 2-l (6)
15.7 i4.5
(4)
9.4 f 3.1 (4)
WATER DEPRIVATION
IN SMALL RODENTS
479
Water content of the tissues Table 3 gives the percentage of water in three tissues for the six species studied. The water content of each tissue under normal (hydrated) conditions is quite similar for the different species studied. The various tissues, however, contain different proportions of water which are differentially affected when the animals are deprived of exogenous water. It is also possible on this basis to distinguish between the two ecological groups mentioned. It seems that in the xeric species the gastrocnemius and the liver, but not the heart, lost a greater proportion of water during water deprivation, than in the mesophilic species. The gastrointestinal tract The water content of the gastrointestinal tract is close to that of other organs (Table 4), and amounts to about 75 per cent of its fresh weight. This value is, however, greatly reduced in the xeric species under water deprivation at 37°C; it is only a little affected in the albino rat and remains unchanged in the spiny mouse. Table 5 gives the percentage of water content in the faeces for five of the species studied when deprived of water. It should be noted that for the xeric species this was examined only at 37°C because they maintain water balance at 25 and 30°C on dry barley only, without having free drinking water. Digestive coefficients were derived from the ratio of the dry faeces secreted to the amount of dry food consumed per 24 hr. This value is 0.20 f 0.05 (four samples) for the rat at 23°C with water ad lib. and is reduced to 0.12 f 0.04 (eight samples) during water deprivation; food utilization is therefore improved. No such reduction was found in the xeric species. DISCUSSION
Looking at the mechanisms activated when small rodents are deprived of water, water distribution and its proportionate loss should be focused upon. Only the total water content of several organs and the whole animal was measured in this study. The water content of skeletal (gastrocnemius) muscle, liver and gastrointestinal tract, is reduced under water deprivation in all the species studied; a greater reduction, however, was observed in the xeric species (Table 3). This observation points to the possible existence of a special mechanism by which the gastrointestinal tract and, to a lesser extent, skeletal muscle and liver may contribute to the total water loss. The water content of the gastrointestinal tract is regulated mainly by the ratio of the food and water intake and varies little (Lepkovsky et al., 1957). Moreover, we found less than a 20 per cent decrease in the amount of water which is stored in this system in the rats during water deprivation (Table 5); but almost a 50 per cent reduction in the xeric species under similar conditions. An important function has been attributed similarly to the gut and the alimentary canal in the camel under conditions of water deprivation (Macfarlane, 1964).
37°C SPBCIRS STUDIED
10.5 f 1.6 (3)
89.8 + 13.4 (3)
21.2 Ik2.2 (4)
21.4 AZ 2.3 (4)
52.1 f 2.0 (2)
-
13.4 Ik0.4 (3)
57.5 zk3.0 (3)
21.3 zk1.3 (3)
-
17.4 f 0.8 (7)
36.7 + 1.7 (7)
69.1 k4.5 (3)
-
17.8 f 1.2 (11)
137.1+ 15.2 (11)
44.5 f 1.8 (2)
-
28
68.1 f 2.5 (3)
76.8 I!Y0.6 (2)
65.4 + 2-O (4)
100
-
80.3 _+4.4 (3)
70.8 * 25 (3)
30
-
78.5 f 2.0 (3)
73.4 f 1.0 (7)
-
18
73.9 + l-6 (2)
73.12 0.6 (11)
15
-
76.6 + 0.4 (14)
-
0.05
0.01
0.05
0.80
0.001
P
TRACT
8.6 _+1.5 (3)
13.0 + 4.4 (2)
9.2 * 1.1 (4)
18.0 f 4.3 (3)
5.6 + 0.7 (3)
11*7f 1.3 (2)
10.2 zk1.0 (7)
10.9 + o-5 (2)
12.7 + 0.5 (11)
15.3 _+0.6 (14)
P
0.30
0.05
0.01
0.70
o*oos
IN 5 OF THE
Water content in the gastrointestinal tract as percentage of the whole body water content (%I
OF THE GASTROINTESTINAL
Water content of the gastrointestinal tract with its content (% of wet weight)
ON THE WATER CONTENT
181.9 f 10.0 (14)
Mean + S.E. Number of animals in parentheses.
Fat jird Water and food ad lib. at room temperature Water deprivation at 37°C
Little jird Water and food ad lib. at room temperature Water deprivation at 37°C
Jerboa Water and food ad lib. at room temperature Water deprivation at 37°C
Spiny mouse Water and food ad lib. at room temperature Water deprivation at 37°C
AT
Duration of exposure to Weight lost experimental Weight of the environment animals (% of body weight) (hr) (g)
OF WATER DEPRIVATION
Albino rat Water and food sd lib. at room temperature Water deprivation at 37°C
TABLE ‘i-----EFFECT
f
2
$ 0
WATRRDEPRIVATION
IN SMALL RODENTS
481
TABLE S-EFFECT OF WATRR DR~RIVATI~N AT ~00~ TEMPERATURE (FOR 1OOhr) 37°C (FOR 48hr) ON THE WATER CONTENT OF THE FARCES IN FIVE SPECIEG
AND
Water content in the faeces (%) 25°C; 70% r.h.
37°C; 15% r.h.
Albino rat Water and food ad lib. Water deprivation
74.3 + 1.3 (4) 47.8 + 5.3 (4)
69.8 f 3.2 (4) 52.4 + 3.0 (4)
Golden hamster Water and food ad lib. Water deprivation
63.6 k 0.3 (3) 53.5 * 5.3 (3)
74.4 + 2.6 (3) 36.5 k 1.4 (3)
Jerboa* Water and food ad lib. Water deprivation
-
44.4 f 2.7 (3) 35.6 + 2.9 (3)
Little jird * Water and food ad lib. Water deprivation
-
63.9 f 7.5 (8) 38.3 zk 12.0 (8)
Fat jird* Water and food ad lib. Water deprivation
-
51.5 f. 3.4 (3) 21.3 k 3.7 (3)
* The desert species: fat and little jird and the jerboa lived permanently on dry diet at room temperature without drinking water. Mean f S.E. Number of animals in parentheses.
The water content of the faeces in the xeric species is lower than for the mesophilic species under normal conditions; they can also extract even more water when deprived of drinking water at high temperature (Table 5). It would be interesting to investigate whether it is the length of the colon (Lang 8z Staaland, 1970) which is responsible for this effect and whether it is also controlled by hormones (Edmonds & Marriott, 1969). The rat and most of the other mesophilic species lose their appetite and reduce their food intake about a day or two after onset of water deprivation. Strominger (1967) has pointed out the interdependency of water and food intake in rats. It is therefore a great advantage for the xeric species that they can maintain normal feeding without drinking water which is usually inaccessible to them. The appetite center in the brain of the different species might be controlled differently. Plasma osmolarity was found to control food and water intake in rats (Gutman & Krausz, 1969); if the same mechanism applies also to the xeric species they should have stopped, or at least decreased, their food consumption when their plasma osmolarity increases. The fact that these species keep their plasma osmolarity within a very narrow range raises the possibility that their central control system might be more sensitive to such changes.
482
URI
&AZ
There is no need to stress the well-established differences in kidney function between the xeric and mesophilic species (B. Schmidt-Nielsen, 1964; Dantzler, 1970). It is worth noting, however, that all the species in this study, except for the albino rat, possess a relatively long renal papilla and are able to produce a highly concentrated urine. “Dehydration” is rather a poor definition, as it gives only a general description of various conditions which are attained in several different ways. Desert animal physiologists usually dehydrate by depriving them of drinking water (K. SchmidtNielsen, 1964), whereas others (Darrow & Yannet, 1935 ; Moyer & Nissan, 1961) do so by injection of hypertonic solutions (either of salt or impermeant molecules). In both cases this is referred to as “dehydration”, although the results are quite different from one another. “The only similarity between the different conditions” says Nadal et aZ. (1941) “is that implied by the term ‘dehydration’.” A decrease in the extracellular fluid volume is the main change which characterizes dehydration caused by water deprivation; on the other hand, there is only cellular dehydration when hypertonic solutions are injected, which might or might not be accompanied by an increase of NaCl concentration in the plasma, depending on whether salt or impermeant molecule was used. The molal concentration of the water (which is inversely related to the concentration of the solid constituents in the cell) is obviously an important factor for normal physiological function. Hayward (1965) h as stressed the basic need for a dependable reference criterion for comparisons; he also pointed out the interindividual constancy of body water content which makes it useful for this purpose. Two general phenomena are apparent from the present and numerous other studies: Firstly, the water content of the whole body, in rodents, and mammals in general, is only a little affected by water deprivation at different temperatures. When the amount of water lost under the different conditions of water deprivation is calculated as a percentage of total weight lost (Table 1, last row) it may be seen that only under acute conditions, 90 per cent of the weight lost by rats was water, whereas only 75 per cent water accounted for the weight lost when animals were deprived of exogenous water at room temperature. Similar proportions were found for the other species. It appears that in rodents, only water deprivation at high temperature during a short time period (Lewis et al., 1961) can be considered as a “real” dehydration (Adolph et al., 1947). It would be worth mentioning here that the mammals which are known to be the most resistant to water deprivation (the camel and donkey, K. Schmidt-Nielsen, 1964) drink at a single session almost all that they have lost in weight, when previously deprived of water. Only in this latter case could the weight loss be considered “real” dehydration. The second phenomenon is the distinction which could be made for two different groups with regard to their response to water deprivation (Figs. 1 and 2, and Tables 2). These two groups have different ecological backgrounds: Of the wild species, the common spiny mouse and the little jird, inhabit both the northern (moist) part and the southern (dry) part of Israel. The rat jird and the jerboa
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inhabit the southern part of the country where the average rainfall does not exceed 100 mm a year. The golden hamster is a breed of a couple which were originally trapped in the Syrian desert. The species have therefore been differentiated as arid or xeric as opposed to the mesophilic group. (They are called “dry” and “moist” rodents by K. Schmidt-Nielsen, 1964, p. 179). Surprisingly, the mesophilic group could tolerate a greater degree of weight and water loss when deprived of water at 37°C than the xeric group during approximately the same time limit. Similarly, in the experiment of 6% NaCl injection, the xeric species were found to be more sensitive to elevation in plasma NaCl concentration (Table 2). From these observations it may be surmised that although the xeric group have better mechanisms for water conservation under the same environmental conditions (SchmidtNielsen et al., 1948), they do not possess a better resistance to actual changes in their internal environment. Albino rats are far more vulnerable than the other species in respect to their weight change and probably also other physiological parameters (Horowitz & Borut, 1970), whereas the spiny mouse may represent a special case in which the kidney is highly developed and able to secrete a very concentrated urine (Shkolnik & Borut, 1969), but at the same time the animal is still exposed to fluctuating environmental conditions and can therefore tolerate considerable changes in plasma electrolytes. Shkolnik (1960), who studied seven different Israeli species in respect to their resistance to heat during water deprivation, concluded that they behaved in a systematic order in their tolerance to arid conditions. The Gerbillidae are the most tolerant, then come the Dipodidae, whereas the Muridae are the least resistant in this respect. The observations reported in the present study are in accord with the systematic order mentioned above (in fact three species were the same in both studies). Lang & Staaland (1970) studied the function of the caecum-colon structure in salt and water conservation. They correlated the higher efficiency of sodium and water reabsorption in the caecum-colon structure of the Norway lemming compared with that of the Norway rat with the anatomy of this structure ; this was found to be related to the systematic origin of the family (i.e. all Cricetidae examined possess a post-caecal spiral which is absent in the Muridae, and they also have a longer colon). Caste1 & Abraham (1969) found that the hypothalamic neurohypophyseal system of four species, all from the family Muridae responded differently to water deprivation; this was in correlation with their weight loss so that in the albino rat the hormones were almost completely diminished, whereas in the other species (white mice and spiny mice) partial depletion was followed by repletion. Horowitz & Borut (1970) found 32 and 18 per cent reduction in the extracellular fluid of water deprived rats and fat jirds respectively, but no change in this compartment in the spiny mice. Similar reduction was found in the blood volume. These three species (rat, spiny mouse and fat jird) cannot therefore be classified simply by their ecological background according to this parameter. We find then, some physiological and anatomical adaptations that could be classified according to systematic order (Shkolnik, 1960; Lang & Staaland, 1970; present study), whereas the development of other mechanisms is not bound to hereditary
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options (Caste1 & Abraham, 1969 ; Horowitz & Borut, 1969 ; and others). It is pertinent in this connection that Bogert (1949) found that reptiles belonging to the same genus tend to have similar, although not necessarily identical, mean body temperature preferences, even though they live in different habitats and climatic regions. It should be interesting to find out to what extent this approach could be used, as it implies that certain families or genotypes got some options, on which further adaptation could be developed (Hudson, 1964). In 1932 Barcroft reviewed the fixity of the “millieu interieur”, he concluded that as far as investigations show anything, the fixity of the internal environment is controlled by the upper part of the central nervous system. It should now be worth comparing the effect of water deprivation on the activity of the central nervous system in different species. SUMMARY
AND CONCLUSIONS
Six rodent species were studied under conditions of water deprivation and have been compared for their response in weight change, whole body and tissues water content and plasma chloride concentration. Two distinct groups were distinguished, mainly according to their ecological background. Unexpectedly, it was found that the xeric species were less resistant to water loss at high temperature and to hypertonic salt injection. Adaptation is discussed in relation to the ecological background (environmental) and to the systematic origin of the species. It is concluded that physiological adaptation to water deprivation (dehydration), does not necessarily concern all physiological mechanisms, but rather those related to the fixity of the internal milliue. Acknowledgement-I would like to thank Drs. Mona Caste1 and Michal Horowitz for their critical reading of the manuscript. REFERENCES E. F. (1947) Tolerance to heat and dehydration in several species of mammals. Am.9. Physiol. 151, 564475. BARCROFT J. (1932) La fixt6 du milieu interieur est la condition de la vie libre (Claude Bernard). Biol. Rev 7, 24-87. BOGERT C. M. (1949) Thermoregulation in reptiles, a factor in evolution. Ewolution 3, 195-211. CASTELM. & ABRAHAM M. (1969) Effects of dry diet on the hypothalamic neurohypophysical neurosecretory system in spiny mice as compared to the albino rat and mouse. Gen. & compar. Endocr. 12, 231-241. DANTZLERW. H. (1970) Kidney function in desert vertebrates. In Hormones and En&onment (Edited by BENSONG. K. & PHILLIPS J. G.), 18, 157-189. Mem. Sot. Endocr. DARROWD. C. & YANNET H. (1935) The changes in the distribution of body water accompanying increase and decrease in extracellular electrolyte. J. clin. Invest. 14,266-275. EDMONDSC. J. & MARRIOTTJ. C. (1969) The effect of aldosterone on the electrical activity of rat colon. J. Endocr. 363-377. GRADWHOL R. B. H. (1948) Clinical Laboratory Methods and Diagnosis. Kimpton, London. GUTMANY. & KRAUSZM. (1969) Regulation of food and water intake in rats as related to plasma osmolarity and volume. Physiol. & Behuu. 4, 311-313. ADOLPH
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HAYWARDJ. S. (1965) The gross body composition of six geographic races of Peromysicus. Can.J. Zool. 43, 297-308. HOROWITZM. & BORUTA. (1970) Effect of acute dehydration on body fluid compartments in three rodent species: Rattus norvegicus, Acomys cahirinus and Meriones w~ssus. Camp. Biochem. Physiol. 35, 283-290. HUDSONJ. W. (1964) Water metabolism in desert mammals. In Thirst, pp. 211-233. Proc. of 1st Int. Symp. Pergamon Press, Oxford. KATZ U. (1969) Studies on the mechanism of dehydration and muscle activity in small rodents. M.Sc. thesis, the Hebrew University, Jerusalem. (In Hebrew with English summary.) LANG R. & STAALANDH. (1970) Adaptations of the caecum colon structure of rodents. Comp. Biochem. Physiol. 35, 905-919. LEWIS A. C., RUBIN M. E. & BEISEL W. R. (1960) A method for rapid dehydration of rats. J. appl. Physiol. 15, 525-527. LEPKOVSKYS., LYMAN R., FLEMINGD., NAGUMOM. & DIMICK M. (1957) Gastrointestinal regulation of water and its effect on food intake and rate of digestion. Am. J. Physiol. 188, 327-331. MACFARLANE W. V. (1964) Terrestrial animals in dry heat: Ungulates. In HQTI&OO~ of Physiology-Environment, pp. 509-539. American Physiological Sot., Washington, D.C. MOYER C. A. & NISSAN S. (1961) Alterations in the basal oxygen consumption of rats attendant upon three types of dehydration. Ann. Surg. 154, Suppl. 51-64. NADALJ. W., PEDERSENS. & MADDOCKW. G. (1949) A comparison between dehydration from salt loss and from water deprivation. 3. clin. Invest. 20,691-703. SCHALES0. & SCHALESS. (1941) A simple and accurate method for the determination of chloride in biological fluids. J. biol. Chem. 140, 879-884. SCHMIDT-NIELSEN B. (1964) Organ system in adaptation: the excretory system. In fkndbook of Physiology-Environment, pp. 879-884. American Physiological Society, Washington, D.C. SCHMIDT-NIELSENB., SCHMIDT-NIELSENK., BROKAWA. & SCHNEIDERMAN H. (1948) Water conservation in desert rodents. Am. J. Physiol. 32, 331-360. SCHMIDT-NIELSENK. (1964) Desert Animals. Oxford. SHKOLNIKA. (1960) Tolerance of desert mice living on dry food only, to different ambient conditions. M.Sc. thesis, The Hebrew University of Jerusalem. (In Hebrew.) SHKOLNIKA. & BORUTA. (1969) Temperature and water relations in two species of spiny mice (Acomys) J. Mammal. 50, 245-255. STROMINGER J. L. (1947) The relation between water intake and food intake in normal rats and rats with hypothalamic hyperphagia. YaleJ. biol. Med. 19, 279-287. WALLACEW. M., GODSTEINK., TAYLORA. & TEREE T., (1970) Thermal dehydration of the rat: distribution of losses among tissues. Am. J. Physiol. 219, 1544-1548. Key Word Index-Desert rodents; water deprivation; hypertonic salt injection; plasma chloride; body water content; Rattus norvegicus; Acomys cahirinus; Mus musculus; MesoMeriones crassus. cricetus auratus; &rboa jaculus; Gerbillus ahyu~us;