Osmosis and solute-solvent drag: fluid transport and fluid exchange in animals and plants.

In 1903, George Hulett explained how solute alters water in an aqueous solution to lower the vapor pressure of its water. Hulett also explained how the same altered water causes osmosis and osmotic pressure when the solution is separated from liquid water by a membrane permeable to the water only. Hulett recognized that the solute molecules diffuse toward all boundaries of the solution containing the solute. Solute diffusion is stopped at all boundaries, at an open-unopposed surface of the solution, at a semipermeable membrane, at a container wall, or at the boundary of a solid or gaseous inclusion surrounded by solution but not dissolved in it. At each boundary of the solution, the solute molecules are reflected, they change momentum, and the change of momentum of all reflected molecules is a pressure, a solute pressure (i.e., a force on a unit area of reflecting boundary). When a boundary of the solution is open and unopposed, the solute pressure alters the internal tension in the force bonding the water in its liquid phase, namely, the hydrogen bond. All altered properties of the water in the solution are explained by the altered internal tension of the water in the solution. We acclaim Hulett's explanation of osmosis, osmotic pressure, and lowering of the vapor pressure of water in an aqueous solution. His explanation is self-evident. It is the necessary, sufficient, and inescapable explanation of all altered properties of the water in the solution relative to the same property of pure liquid water at the same externally applied pressure and the same temperature. We extend Hulett's explanation of osmosis to include the osmotic effects of solute diffusing through solvent and dragging on the solvent through which it diffuses. Therein lies the explanations of (1) the extravasation from and return of interstitial fluid to capillaries, (2) the return of luminal fluid in the proximal and distal convoluted tubules of a kidney nephron to their peritubular capillaries, (3) the return of interstitial fluid to the vasa recta, (4) return of aqueous humor to the episcleral veins, and (5) flow of phloem from source to sink in higher plants and many more examples of fluid transport and fluid exchange in animal and plant physiology. When a membrane is permeable to water only and when it separates differing aqueous solutions, the flow of water is from the solution with the lower osmotic pressure to the solution with the higher osmotic pressure.

Evolving ideas about osmosis and capillary fluid exchange.

When a solute is dissolved in water at (T, pel), the temperature and external pressure applied to the solution, the water in the solution is altered as is pure liquid water at (T, pel - piH2Ol). The liquid water and the water in the solution are in equilibrium when piH2Ol is the osmotic pressure of the water in the solution. Every partial molar property of the water in the solution at (T, pel), including its vapor pressure, chemical potential, volume, internal energy, enthalpy and entropy, is identical with the same molar property of pure liquid water at (T, pel - piH2Ol). This elementary fact was deduced by Hulett in 1903 from a thought experiment; he concluded that the internal tension in the force bonding the water is the same in both solution and pure liquid water, in equilibrium, at these differing applied pressures. Hulett's understanding of osmosis and the means by which the water was altered by the solute were neglected and abandoned. Competing ideas included the notions that the solute attracts the water into the solution and that the solute lowers the activity (or concentration) of the water in the solution. These ideas imply that the solute acts on the solvent at the semipermeable membrane separating the solution and water. Hulett's theory of osmosis requires that the solute alter the water at the free surface of the solution where the solute exerts an internal pressure on the boundary of the solution retaining the solute. Fluid exchange across the capillary endothelium is influenced, in part, by colloidal proteins in the plasma. The role of the proteins in capillary fluid exchange must be reinterpreted based on Hulett's view, the only valid view of osmosis.

Roles of colloidal molecules in Starling's hypothesis and in returning interstitial fluid to the vasa recta.

To begin to understand the role of colloidal molecules, a simple question requires an answer: How do the solutes alter water in an aqueous solution? Hulett's answer deserves attention, namely, the water in the solution at temperature and external pressure applied to solution (T,pe1) is altered in the same way that pure water is altered by reducing the pressure applied to it by the osmotic pressure of the water at a free surface of the solution. It is nonsense to relate the lower chemical potential of water in a solution to a lower fugacity or to a lower activity of the water in the solution, since these terms have no physical meaning. It is also incorrect to attribute the lower chemical potential of the water to a lower concentration of water in the solution. Both claims are derived from the teachings of G. N. Lewis and are erroneous. Textbook accounts of the flux of fluid to and from capillaries in the kidney and other tissues are inadequate, if not in error, as they are based on these bogus claims. An understanding of the process by which colloidal proteins in plasma affect the flux of nearly protein-free fluid across the capillary endothelium must start with insights derived from the teachings of G. Hulett and H. Dixon. The main points are 1) colloidal molecules can exert a pressure against a membrane that reflects them and, thereby, displace a distensible membrane; 2) they can alter the internal tension of the fluid through which they diffuse when there is a concentration gradient of the molecules; and 3) only by these means can they influence the flux of plasma fluid across the capillary endothelium. However, the process is complex, since both the hydrostatic pressure and protein concentrations of fluids inside and outside the capillary vary with both position and time as plasma flows through the capillary.

The shivering response during cross-circulation in the common eider duck (Somateria mollissima).

The possible role of humoral factors in the control of shivering in the common eider duck (Somateria mollissima) was investigated using a cross-circulation technique. Pairs of animals were coupled so that the arterial system of one animal was connected to the venous system of the other. The rate of blood transferral was 12.8 ml min-1. By adequate heparinization of the extracorporeal blood supply, cross-circulation could be maintained for periods of up to 12 h. The temperature of blood entering each animal Tinlet) was controlled by heat exchangers. During control experiments Tinlet was maintained at a temperature close to normal body temperature. During cooling experiments Tinlet was maintained at c. 20 degrees C. Changes in metabolic heat production and oesophageal temperature in response to blood cooling were measured in cross-circulated pairs of animals cooled simultaneously or individually. Based on analysis of the metabolic responses under the different experimental situations, no evidence was found to indicate that blood-borne substances are involved in the shivering response in these animals.

Total calorimetry and temperature regulation in the nine-banded armadillo.

Cold exposure in the nine-banded armadillo causes vigorous shivering and a rise in core temperature (Tc). The increase in metabolic rate and Tc depends upon exposure temperature, but may be as much as six times and 3 degrees C respectively (Johansen 1961). These findings might indicate an insensitivity to Tc, which is puzzling since internal temperature is thought to be the primary and regulated variable. It is suggested that positive feedback may play a role in temperature regulation in these animals. To investigate this problem two series of experiments were performed in the same species. Series 1. Measurements of changes in heat loss (direct calorimetry) and heat production (indirect calorimetry) following transferral from a thermoneutral to a cold environment. The difference between these measurements determines whether heat storage is positive due to the increased core temperature or negative due to reduction in the size of the core with the increased temperature. Series 2. Investigation of core thermosensitivity (body core cooling using colonic thermode) under different environmental conditions. The results of the first series showed that the rise in Tc was accompanied by positive heat storage in the body. The second series demonstrated core thermosensitivities similar to those previously reported for a variety of other homeothermic mammals.

Autoradiographic localization and characterization of circumventricular angiotensin II receptors in duck brain.

Binding of [125I-5Val]angiotensin II and [125I-1Sar, 8Ile]angiotensin II to target sites in the hypothalamus of the Pekin duck was determined by quantitative receptor autoradiography and conventional membrane binding techniques. Circumventricular areas involved in body fluid homeostasis like the subfornical organ (SFO), median eminence and the anterior-ventral region of the third ventricle showed highest labeling density. Binding sites for angiotensin II were also found in the paraventricular and supraoptic nuclei. The physiological relevance of the labeled SFO angiotensin II receptor is indicated by similarities between rank orders of potency of angiotensin II analogues in displacing radiolabeled ligands and their physiological osmoregulatory potencies. Receptor density in the SFO of saltwater-acclimated ducks was increased 3-fold compared to non-acclimated freshwater ducks, indicating an up-regulation of the angiotensinergic system in ducks under conditions of dehydration or high salt intake.

Body temperature and rate of O2 consumption in Chinese pangolins.

Body temperatures and rates of O2 consumption and CO2 production were measured in four Chinese pangolins (Manis pentadactyla) during short-term exposures (2-4 h) to ambient temperatures (Ta) of 10-34 degrees C. At Ta less than 27 degrees C the pangolins curled into a sphere. At Ta greater than 28 degrees C the animals laid on their backs with their soft abdominal skin exposed. Rectal temperatures between 33.4 and 35.5 degrees C were recorded from animals exposed to Ta of 10-32 degrees C. At Ta greater than or equal to 32 degrees C the animals appeared to be markedly heat stressed, rate of breathing was elevated, and core temperature rose somewhat. Resting metabolic rates averaged 3.06 ml O2 X kg-1 X min-1. This is significantly lower than would be predicted from the relationship between body mass and metabolic rate established by Kleiber (The Fire of Life: an Introduction to Animal Energetics. New York: Wiley, 1975) for other eutherian mammals. The magnitude of the metabolic response to Ta below the lower critical temperature was inversely correlated to the mass of the pangolin, the slope being greatest for the smallest animals. Respiratory quotients of 0.85-1.0 were observed.

Total calorimetric measurements in the rat: influences of the sleep-wakefulness cycle and of the environmental temperature.

Rates of production as well as dry and evaporative heat loss during the sleep-wakefulness cycle were studied in 11 male, adult albino rats with chronically implanted electrodes and thermocouple re-entrant tubes. Two groups of animals chronically acclimated to 6 or 23 degrees C were acutely studied at 15, 20, 25, 30 and 35 degrees C. Statistical analysis of the data shows that rates of heat production and dry heat loss differ with respect to acclimation and acute environmental temperatures, and show significant differences depending on the states of the sleep-wakefulness cycle. Rate of heat production was highest during wakefulness, intermediate during synchronized sleep and lowest during paradoxical sleep. Rate of dry heat loss of 15 degrees C was maximal during paradoxical sleep. Rate of evaporative heat loss apparently did not change with the states of the sleep-wakefulness cycle. Heat storage estimated from difference in rates of heat production and heat loss was positive during wakefulness, slightly negative during synchronized sleep and markedly negative during paradoxical sleep. The data presented suggest a clear although partial suppression of thermoregulatory mechanisms during paradoxical sleep in the white rat.

Respiratory water loss in camels.

Rates of oxygen consumption and respiratory water loss were studied in camels that were exposed to desert heat and water deprivation. We found that changes in body temperature are accompanied by considerable changes in respiratory water loss. Body temperature fluctuations are greatest in dehydrated camels (up to 7 degrees C), and in these the respiratory water loss might vary from abut 0.06 to 1.2 g/min. The respiratory frequency varied from about 4 to 28 min-1, while the metabolic rate varied less than twofold. The lowest values for respiratory water loss can be explained by the exhalation of air at temperatures far below body temperature, and, in addition, removal of water vapour from the exhaled air, resulting in exhalation of air at less than 100% relative humidity.

Properties of body fluids influencing salt gland secretion in Pekin ducks.

Pekin ducks were reared and maintained on 620 mosmol NaCl/kg H2O to enhance the secretory capability of their salt glands. When a control solution of 1,000 mosmol NaCl/kg H2O was infused intravenously at 0.2, 0.4, or 0.6 ml/min for 60-90 min, the infused loads were secreted in approximately equal quantities, indicating that the amount of NaCl in the extracellular fluid (ECF) before and after each infusion did not change. Salt and water secreted in response to experimental infusions of hyposmotic saline or blood were less than the solute and water infused. Thus, ECF volume increased and the Na+ concentration decreased. Infusions of control solution followed these experimental infusions. The salt and water secreted again equaled the amounts infused, indicating that the threshold concentration of Na+ ([Na+]th) for salt gland secretion was decreased by the increase in ECF volume. When the colloid dextran was added to the control solution, its infusion increased the colloid osmotic pressure of the blood and decreased nasal secretion. Because dextran increased the intravascular volume while the interstitial fluid volume (ISFV) decreased, we conclude that the [Na+]th was inversely correlated with ISFV.

Sickle-cell hemoglobin: fall in osmotic pressure upon deoxygenation.

Macromolecules such as hemoglobin exert both kinetic and matrix effects on osmotic pressure. The kinetic osmotic pressure of sickle-cell hemoglobin is lost upon deoxygenation at physiological erythrocyte concentrations. The non-kinetic or matrix component of osmotic pressure remains relatively unchanged. Loss of thermal-osmotic activity during deoxygenation occurs throughout a hemoglobin concentration range between 2.5 and 35 g/100 ml. Deoxygenation of sickle-cell hemoglobin causes aggregation such that the matrix effect is unchanged but the kinetic (van't Hoff) effect nearly vanishes. A loss of intracellular osmotic pressure during deoxygenation could dehydrate the erythrocyte sufficiently to promote more rapid sickle-cell hemoglobin aggregation. Subsequently, complete gelation of these aggregates could cause additional water loss and thrust the sickled cell into an irreversible cycle. The osmotic pressure of normal hemoglobin does not change appreciably during deoxygenation and is essentially the same as the osmotic pressure of oxygenated sickle-cell hemoglobin.

Energy balance in ovariectomized rats with and without estrogen replacement.

The effect of estrogen replacement on several parameters of energy balance was investigated in ovariectomized rats tested during the dark phase of their diurnal cycle. Estrogen replacement, either as 17 beta-estradiol or beta-estradiol-3-benzoate via subcutaneous Silastic capsules, was associated with elevated rates of heat production and dry heat loss relative to untreated ovariectomized controls. Estrogen treatment reduced body mass and retarded fur growth. The effects of estrogen replacement on heat production and dry heat loss could not be attributed to these differences in body mass and fur growth or locomotor activity. Estrogen replacement had no effect on rate of evaporative heat loss. If estrogen replacement was delayed 75 days following ovariectomy, the increase in heat production and dry heat loss was not observed. There was no effect of the hormone treatment on rectal temperature. It was concluded that either heat production was elevated, with dry heat loss increased to compensate for the additional thermal load, or dry heat loss was accelerated with heat production elevated in compensation.

Dehydration elevates osmotic threshold for salt gland secretion in the duck.

Acute salt and water balance measurements were made in two conscious salt water-acclimated Pekin ducks at and above their osmotic threshold for salt gland secretion. Intravneous infusion of 1,000 mosmol/kg H2O NaCl at 0.350 ml/min increased plasma tonicity less than 0.5% and increased secretion from nearly zero to a rate matching the infusion. Continuous secretion at a similar submaximal rate was driven by 5,600 mosmol/kg H2O NaCl infused at 0.070 ml/min. Osmolality of secreted fluid was constant for any secretion rate, so that net water loss occurred when the concentration of infusate exceeded that of secreted fluid. Threshold plasma osmolality increased by 9 mosmol/kg H2O after the loss of 77 g water (3% body wt). Solutes were always secreted at the infusion rate, even when body fluid osmolality increased while body water decreased. We conclude that the salt gland controller is sensitive to more than just extracellular fluid (ECF) tonicity, and we suggest that elevation of the osmotic threshold may occur in response to decreased ECF volume.

Hypothalamic temperature and osmoregulation in the Pekin duck.

The temperature of the anterior and middle hypothalamus of conscious Pekin ducks was altered with chronically implanted thermodes. Both urine formation and salt secretion by the supraorbital glands were influenced by hypothalamic cooling. When osmotic diuresis was induced by continuous intravenous infusion of 1.2 ml . min-1 of 293 mosm . kg-1 mannitol in H2O solution, hypothalamic cooling increased urine flow rate at reduced urine osmolality and unchanged osmolal excretion rate. The degree of this cold induced diuresis increased with cooling intensity. Additional ADH administration by continuous infusion at a supramaximal dose abolished the diuretic effect of hypothalamic cooling. When water diuresis was induced by intragastric continuous infusion of 1.2 ml . min-1 of distilled water, hypothalamic cooling enhanced the diuresis, but hypothalamic warming had equivocal effects. The diuretic effects of hypothalamic cooling suggest an inhibition of endogeneous ADH release by lowering hypothalamic temperature. When the salt glands of salt adapted ducks were stimulated by continuous intravenous infusion of 0.2 ml . min-1 of 800 mosm . kg-1 NaCl in H2O solution, hypothalamic cooling reduced the salt gland secretion rate to an extent depending on cooling intensity. It is concluded that the activities of those integrative and/or efferent hypothalamic neurons, which mediate the hormonal control of renal water absorption and the nervous control of salt secretion by the supraorbital gland, depend on their own temperature.

Hypothalamic thermosensitivity in conscious Pekin ducks.

Conscious Pekin ducks with chronically implanted hypothalamic thermodes were submitted to thermoneutral (Ta 25 degrees C), cold (Ta 5 degrees C), and warm (Ta 33 degrees C) ambient temperatures. Hypothalamic temperature (Thy) was varied in nine steps between 27.9 and 43.5 degrees C in repeated experiments. Cooling of the hypothalamus induced a fall of core temperature (Tc) that was linearly related to Thy and amounted to 1.1--1.3 degrees C at highest cooling intensity. The decrease of Tc was caused by inhibition of metabolic heat production and/or vasodilatation in the skin at cold and thermoneutral Ta and by activation of panting at warm Ta. After the end of cooling a temporary overshoot of heat production occurred, the degree of which depended on the degree of cooling and on Ta, and led to a rapid normalization of Tc. Warming of the hypothalamus induced a slight fall of Tc due to a reduction of metabolic heat production at cold and thermoneutral Ta and to an activation of panting at warm Ta. It is concluded that no specific cold reception and a weak specific warm reception exist in the duck's hypothalamus. A "nonsensory" temperature susceptibility of hypothalamic control functions is responsible for those reactions of thermoregulatory effector activities which do not fall into the categories of adequate thermoregulatory responses to a central thermal stimulus.