Physiology&Behavior,Vol. 50, pp. 1221-1226. ©Pergamon Press plc, 1991. Printed in the U.S.A.

0031-9384/91 $3.00 + .00

The Economics of Water and Salt Balance G E O R G E C O L L I E R , D E A N N E F. J O H N S O N A N D C L A U D I O S T A N Z I O L A

Department of Psychology, Busch Campus, Rutgers, The State University of New Jersey, New Brunswick, NJ 08903 R e c e i v e d 4 February 1991 COLLIER, G., D. F. JOHNSON AND C. STANZIOLA. The economics of water and salt balance. PHYSIOL BEHAV 50(6) 1221-1226, 1991.--Two environmental features often associated are a shortage of water and an excess of electrolytes. We explored the economics of this situation by jointly manipulating the instrumental cost of consuming water and the amount of salt in the diet of rats. As the dietary salt increased, water intake increased; and as water cost increased, water intake fell. Food intake also declined as water cost increased, and the rats maintained a minimum ratio of water:salt consumed across all conditions. For all diets, as water intake fell, food intake and body weight also declined, perhaps defending the ratio of body water to lean body mass. There was no evidence that the slope of the demand curve for water changed as a function of dietary salt. Water balance

Sodium balance

Water intake

Salt intake

THE regulation of water and electrolyte balance is accomplished by a complex system of intake, conservation, and excretion. The mechanisms of this regulation are sufficiently well understood that the ideal consumption of water for a given species can be specified as a function of a number of factors (7). Rats generally consume water in excess of their requirements when it is freely available. The excess intake has been called facultative, to distinguish it from the water requirement, or obligatory intake (20). If water intake is constrained below the obligatory level, there is a voluntary reduction of food intake in an amount such that body weight falls in proportion to the constraint and the ratio of body water to lean body mass is conserved (5, 15, 20). On the other hand, if sensible or insensible water output is increased, there is an increase in water intake, again conserving the ratio of body water to lean body mass (20). Because water is required for urine production, intake increases when excretion products (wastes, electrolytes, etc.) increase. For example, if the protein or salt content of the diet are increased above requirements, water intake and excretion of urine increase, in the first case to eliminate the nitrogen resulting from the deamination of the excess protein (6,8) and in the second case to excrete the excess sodium. We have found that increases in the concentration of sodium chloride (NaC1) in the food from 0 to 3% lead to increases in rat's daily ad lib water consumption from 20 to 42 ml [cf. (17,19)]. Additionally, the abundance, availability, and distribution of water and electrolytes vary from habitat to habitat for a given niche (1, 7, 16). These factors influence the " c o s t s " of these items, i.e., the time and energy required of animals to locate, gain access to, and consume them. Although the effect of economic variables on food intake has received much attention (2,18), there has been little investigation of the economic constraints on water and electrolyte intake. In what way do environmental costs and benefits influence the amount or pattern of intake? Field reports indicate that when water sources axe widely spaced in the habitat, making the time and energy required to gain access to water relatively high, animals drink in fewer bouts per day than when water is more densely distributed and abun-

Water cost

dant (1, 14, 16). This phenomenon has been explored in a laboratory environment (3,12) where a cost was placed on initiating a drinking bout by imposing a bar-press price on access to water. As the access price was increased, rats decreased the number and increased the size of drinking bouts. Total intake declined somewhat, but never below obligatory levels, as determined by body weight maintenance. The decrease in bout frequency has been interpreted as an economic response to increasing access cost because the daily bar-press output is reduced compared to that required if bout frequency were to remain high (2). The effects on intake of a second class of costs has also been examined. These are costs incurred during a bout of consumption, and a different pattern of behavioral change occurs as a function of consumption costs. For example, food consumption cost has been increased by imposing a bar-press price on small (45 mg) food pellets. Increases in the pellet price produce only small changes in bout size and frequency, but result in a reliable increase in the rate of instrumental responding. The rate increase does not compensate completely for the increase in price, however, so the rate of pellet intake (pellets per min during meals) falls and the time spent feeding increases (4,9). The rate change is still interpreted as economic, however, because the actual changes in feeding rate and feeding time are not as great as they would be if there were no change in response rate with increasing consumption cost. We have found the same pattern of change in response rate, intake rate, and consumption time when we have manipulated the consumption cost of water by imposing a bar-press price on small amounts of water using either a 0.15 ml dipper (12) or short presentations of a water spout (13). Another effect of increasing consumption cost is a decline in daily intake, especially at higher costs (4, 10, 12, 13). This has been interpreted as an example of the demand law, an economic principle relating the consumption of a commodity to its price. Economists have used the slopes of demand curves (amount consumed plotted as a function of price) to compare the "elasticity of demand" for different commodities. Generally, intake declines more slowly with price (demand is less elastic) for commodities that are essential and for which there is no substitute (10,I 1).

1221

1222

COLLIER, .IOHNSON AN[) SIANZIOI,-k

In the present study, we examined the interaction of water cost and water requirement as they affect the amount and pattern of water consumption. Cost was manipulated by imposing a bar-press price on small sips of water, and requirement was manipulated by varying the concentration of salt in the food. We predicted that water consumption would decline as a function of water price, but that the slope of the demand function would decrease (demand would he less elastic) as the saltiness of the food increased. METHOD

Subjects and Apparatus Four male, 50-day-old, Sprague-Dawley-derived rats (Camm Research Institute, Wayne, N J) were housed individually in double-sized (41 x 23 x 19 cm) cages located in a temperaturecontrolled room with the lights on from 0800 to 2000 daily. The rats lived in these cages continuously except for a daily maintenance period of approximately 40 min during which they were weighed, the food and water were replenished, and the apparatus was cleaned and tested. Each cage was fitted with a cam-operated, 100-ml drinking tube and a feeder tunnel giving access to a cam-operated food cup containing approximately 50 g of food. A T-shaped bar requiring 35 N to activate (BCS, Inc., South Plainfield, N J) was located next to the drinking tube, and a second bar was placed next to the feeder tunnel. A lickometer (Gerbrands) detected contact with the drinking tube and a photocell monitored the rat's presence in the food tunnel. The drinking tube and food cup were normally positioned out of the rat's reach. When a number of bar presses (the "sip price") were made on the bar nearest the water, the drinking tube would move into the rat's reach until 20 licks were made or 5 s elapsed, whichever occurred first, and then withdrawn. Each drinking-tube presentation was called a " s i p . " A drinking bout was defined as a group of sips separated from other sips by at least l0 consecutive minutes. The completion of 10 bar presses on the bar nearest the food resulted in the food cup moving up to the tunnel mouth. The food cup remained available until the rat remained out of the tunnel for 10 consecutive minutes, and then the cup was lowered. A feeding bout, or meal, was defined as one presentation of the food cup. The equipment was controlled and the data were recorded by microprocessors (PET 4032, Commodore) located in another room.

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(rat 4) lost approximately 20% of its body weight by the end of the sip-price-30 condition with the 2% and 3% diets, and it was not tested at a sip price of 40 with those diets. Finally, the three rats that had completed all prior conditions received the 4% NaCI diet and sip prices of 5, 10, 20, and 30. Each condition was in effect for at least 1 1 days.

Data Analysis The values reported here are means over the last 10 days of each condition. The data were analyzed with two-factor (sip price x dietary NaC1) ANOVA with repeated measures; the alpha level was 0.05. Two analyses were performed. One used the data from all four rats for the 0, 2, and 3% diets, estimating the missing cell values for rat 4 for the 2 and 3% diets at sip price 40. The second analysis was of the data for the three rats exposed to all four diets with sip prices of 5, 10, 20 and 30. In all cases, the two analyses yielded identical conclusions as to significant and nonsignificant effects, and so only the F values from the latter analysis are reported here. The data presented in the figures are means for all 4 rats except for the conditions which rat 4 did not complete, where means for 3 rats are shown. RESULTS

Diets Four purified, isocaloric diets containing 0.5, 2.0, 3.0, or 4.0% NaC1 (w/w) were prepared. NaC1 was substituted for fiber; other minerals and nutrients were equivalent among the diets (Table 1).

Procedure The rats were trained to use the apparatus over several days during which the food available was rat chow meal (Purina 5001). The food bar was installed first and the price of food access was gradually increased from 1 to 10 bar presses. The water bar was then installed and the sip price was gradually increased from 1 to 5 bar presses. Sip prices of 10, 20, 30, and 40 were then imposed for 10 days each. During the experiment, three diets: 0, 2, and 3% NaCI, were combined factorially with five sip prices: 5, 10, 20, 30, and 40. Each rat received all three diets in a random order; within each diet the sip prices were presented in ascending order. One rat

The Cost of Water The actual cost of water (in bar presses per ml) was not only a function of the sip price we imposed, but also was determined by the volume of water consumed in each sip. Because the sip volume (calculated for each rat by dividing the total daily water intake by the total number of sips earned) differed among the rats, the range of water costs experienced by each rat was somewhat different (Table 2). Sip volumes were not significantly affected by sip price, F(3,6)=0.58, or dietary NaCI, F(3,6)= 1.70. Water cost increased with sip price, F(3,6)= 14.00, but was unaffected by dietary NaC1, F(3,6)=0.86.

Daily Intake and Bout Patterns Water intake (Fig. 1) increased 300% as a function of dietary salt concentration, F(3,6)---5.86, and decreased 20% as a function of sip price, F(3,6)=5.36. There was no interaction. Both the frequency and the size of drinking bouts (Fig. 1) in-

WATER AND SALT BALANCE

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1223

TABLE 2

24

THE AMOUNT OF WATER TAKEN PER SIP BY EACH RAT AND THE COST OF WATER AT EACH SIP PRICE

22

Water Cost (bar presses/ml) Sip Price

Sip Volume (ml)

1

0.19

2 3 4

0.08 0.13 0.12

5

10

20

30

40

31 62 37 43

52 122 74 74

99 262 146 180

151 371 243 266

201 450 303 313

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creased with dietary NaC1 [ F ( 3 , 6 ) = 5 . 1 8 and F ( 3 , 6 ) = 5.77, respectively]. Sip price, however, affected only bout size, which decreased as sip price increased, F ( 3 , 6 ) = 5.02; bout frequency did not change significantly with sip price, F ( 3 , 6 ) = 0.14. Food intake and body weight (Fig. 2) declined as a function of sip price [F(3,6)= 17.81 and F ( 3 , 6 ) = 31.62, respectively] but

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were not significantly affected by dietary NaC1 [ F ( 3 , 6 ) = 3 . 5 0 and F ( 3 , 6 ) = 2.46, respectively]. Changes in food intake with sip price resulted from changes in both meal frequency, F ( 3 , 6 ) = 10.4, and meal size, F ( 3 , 6 ) = 4 . 8 0 (Fig. 3).

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FIG. 3. Mean ( - s . e . ) daily meals and meal size (g) as a function of the dietary NaC1 and the cost of water.

1224

COLLIER. JOHNSON AND S[ANZIOLA 300

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FIG. 5. Mean (___s.c.) daily water intake per gram food intake (top) and water intake per gram NaCI intake (bottom) as a function of the dietary NaCI and the cost of water.

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FIG. 4. Mean (___s.c.) daily time spent drinking, response rate while earning water, and rate of water intake as a function of the dietary NaC1 and the cost of water.

Drinking Time and Consumption Rate The time spent earning and drinking water each day (Fig. 4) increased with dietary salt because the amount consumed increased, and also increased with sip price because the number of bar presses emitted increased. The magnitude of these effects was moderated by changes in the rats' bar-pressing behavior, however (Fig. 4). As the sip price increased, the rate of barpressing for water increased, F(3,6)= 23.38. The change was not sufficient to conserve the rate of earning sips, however, and thus water was consumed more slowly as sip price increased, F(3,6) = 85.97. Dietary NaC1 appeared to influence the response rate also, but the differences were only significant at high sip prices when the rats responded faster (and drank faster) when eating saltier food.

Regulation The changes in water intake with dietary salt resulted in differences in the ratio of water consumed to food consumed, ml/g (Fig. 5). For the 0.5% NaC1 diet, the ratio was about 1:1, but

this increased significantly with NaCI concentration, F(3,6)= 13.18. Because both water and food intake declined with sip price, there was no effect of sip price on the water:food ratio, F(3,6)=2.61. Consider now the ratio of water consumed to NaC1 consumed (Fig. 5). This ratio decreased significantly as a function of dietary NaC1, F(3,6)= 23.89, falling from about 170 ml/g for the 0.5% diet to about 50 ml/g for the 2.0% diet. There was no further decrease as dietary NaC1 increased to 3 and 4%.

Demand for Water The demand for water did decrease with water cost; however, the elasticity of demand was not affected by the NaC1 concentration in the food. Because the cost of water differed among rats, we plotted demand curves for individual animals (Fig. 6); there is no consistent relationship between the slope of the demand curve and the dietary NaC1 content (Table 3).

DISCUSSION

Four basic findings emerged from this study: 1) Increases in the salt in the diet resulted in no change in food intake, but proportional increases in water intake. 2) Increases in the consumption cost of water resulted in a reduction in water intake, the degree of which was unaffected by the concentration of salt in the food. 3) The voluntary decreases in total water intake as a function of cost were accompanied by proportional reductions in food intake such that the ratio of water:food intake (and water: salt intake) remained constant for each diet. A proportional reduction in body weight accompanied the reductions in water and food intake. 4) Increases in consumption cost resulted in increases in the instrumental rate (responses/min) that, however,

WATER AND SALT BALANCE

1225

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TABLE 3 THE SLOPES OF THE INDIVIDUAL RAT'S WATER-DEMAND CURVES DURING EACH DIET

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60

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Diet Rat

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2.0%

3.0%

4.0%

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1 2 3 4

-0.02 -0.01 - 0.04 -0.05

-0.01 -0.01 - 0.03 -0.08

-0.04 0.00 - 0.04 -0.07

-0.04 0.00 - 0.02

10

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~

80 Rat2

100

60 40

were not sufficient to maintain the rate of water intake (sips/min) during a bout of drinking. Both the instrumental rate and the intake rate increased with dietary salt concentration. Of these four findings, we believe the first and third are due to physiological, regulatory processes, and the second and fourth, to economic processes. As the dietary NaC1 content and the cost of water were varied, the rats adjusted both water and food intake in apparent defense of a lower limit on the ratio of water intake to salt intake (approximately 50 ml water per g NaC1). The increase in water intake with increasing salt in the diet is a regulatory response allowing the excretion of excess sodium (20). Only at the lowest concentration of dietary salt was the facultative intake of water high enough to result in a ratio of water:NaC1 consumed higher than 50 ml/g. Within each diet, the water:NaC1 ratio was constant across water costs because, although water intake fell as the price of water increased, food intake was also reduced. Note that this change in food intake accompanied a voluntary reduction in water intake. In a previous study (5), when water intake was restricted by the experimenter, food intake declined in a similar fashion. In that study, the reduced food intake resulted in the loss of lean body mass and a constant ratio of body water to lean body mass. Thus, although we did not measure body composition, we speculate that the reduction in food intake and loss of body weight seen in the present study again resulted in the defense of the water:lean mass ratio. The decrease in water intake as a function of consumption cost is an economic response conserving total consumption effort (and/or time). That is, although the number of water responses made each day increased with water cost, the response effort would have increased even more if intake had remained constant as cost increased. The imposition of an instrumental consumption cost on water at its lowest value reduces water intake to the obligatory level, i.e., that required to just maintain cost-free body weight (5, 12, 20). (In the training phase of this study the rats ate standard chow and drank 46_+ 2 ml when water was cost-free, but reduced their intake to 3 2 - 1 ml, with no change in chow intake or body weight, when each sip cost only 1 or 2 bar presses.) When the cost is raised, water intake falls below the obligatory level, as indicated by the decline in food intake and body weight. We would note that during each cost condition, weight did not decrease continuously, but stabilized at the new, lower value. Despite their opposing effects on the amount of water consumed, both experimental manipulations increased the time spent drinking each day; dietary salt because more water was consumed, and sip price because more bar presses had to be made to earn the daily water ration. Both manipulations produced increases in the rate of bar pressing for water, although the diet

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FIG. 6. Mean daily water intake at the water costs experienced by each rat while eating each food. The best-fit lines are drawn illustrating water demand during each diet condition. effect was not as strong. We interpret the increases in response rate and the decreases in intake as economic adjustments which serve to limit the increase in time and effort spent drinking as cost increases (4). The question raised in this experiment was whether these physiological and economic processes would interact, that is, whether the animal would pay a higher price for water when consuming a high-salt diet. We had predicted that the elasticity of demand for water, measured by the rate of change in intake with price, would decrease with increasing salt content of the diet. This was not the case, however. The regulatory and economic responses appear to be independent. ACKNOWLEDGEMENTS The research was supported by NIH grant DK 31016 and by a grant from the Campbell's Soup Company to the fast author.

1226

COLLIER, JOHNSON AND STANZIOLA

REFERENCES I. Chew, R. M. Water metabolism of mammals. In: Mayer, W, V.; Van Gelder. R. G., eds. Physiological mammalogy. Ne~ York: Academic Press; 1965. 2. Collier, G.; Johnson, D. F. The time window of feeding. Physiol. Behav. 48:771-777; 1990. 3. Collier, G. H.; Johnson, D. F.; CyBulski, K. A.; McHale, C. A. Activity patterns in rats (Rattus norvegicus) as a function of the cost of access to four resources. J. Comp. Psychol. 104:53-65; 1989. 4. Collier, G. H.; Johnson, D. F.; Hill, W. L.; Kaufman, L. W. The economics of the law of effect. J. Exp. Anal. Behav. 46:113-136; 1986. 5. Collier, G.: Levitsky, D. Defense of water balance in rats: Behavioral and physiological responses to depletion. J. Comp. Physiol. Psychol. 64:59-67; 1967. 6. Collier, G. H.; Squibb, R. L. Diet and activity. J. Comp. Physiol. Psychol. 64:409-413:1967. 7. Denton, D. The hunger for salt. Berlin: Springer-Verlag; 1982. 8. Fitzsimons, J. T.; LeMagnen, J. Eating as a regulatory control of drinking. J. Comp. Physiol. Psychol. 67:273-283; 1969. 9. Hursh, S. R. Economic concepts for the analysis of behavior. J. Exp. Anal. Behav. 34:219-238; 1980. 10. Hursh, S. R. Behavioral economics. J. Exp. Anal. Behav. 42:435452; 1984. 11. Lea, S. E. G. The psychology and economics of demand. Psychol. Bull. 85:441-446; 1978.

12. Marwine, A.; Collier, G. The rat at the waterhole..t ('~*mp. Physiol. Psychol. 93:391-402: 1979. 113. Mathis, C.; Johnson, D. F.; Collier, G. H. "Time budgets m It)r-. aging rats." Paper presented to the Eastern Psychological Association; Philadelphia; (April) 1990. 14. Oatley, K. Simulation and theory of thirst. In: Epstein, A. N.: Kis~ sileff. H. R.; Stellar, E., eds. The neurophysiology of thirst: New findings and advances in concepts. Washington, DC: V H. Winston; 1973:199-224. 15. Richter, C. P.; Brailey, M. E. Water-intake and its relation to the surface area of the body. Proc. Natl. Acad. Sci. USA 15:570-578; 1929. 16. Schmidt-Nielsen, K. Desert animals: Physiological problems of heat and water. London: Oxford University Press; 1964. 17. Stellar, E.; Hyman, R.; Samet, S. Gastric factors controlling waterand salt-solution-drinking. J. Comp. Physiol. Psychol. 47:220-226; 1954. 18. Stephens, D. W.; Krebs, J. R. Foraging theory. Princeton: Princeton University Press; 1987. 19. Toril, K. Salt intake and hypertension in rats. In: Kare, M. R.; Fregly, M. J.; Bernard, R. A., eds. Biological and behavioral aspects of salt intake. New York: Academic Press; 1980:345-366. 20. Wotf, A. V. Thirst: Physiology of the urge to drink and problems of water lack. Springfield, IL: Charles C. Thomas: 1958.