Kidney adaptations in Dipodomys merriami
The earliest studies of the kangaroo rat kidney were histological, comparing the kidney to that of other small rodents. A few major differences were found. The first is a long papilla that extends into the ureter (Figure 1) (Vimtrup and Schmidt-Nielsen, 1952). Functionally, this allows the loops of Henle collecting ducts to be exceptionally long, increasing surface area and likely enhancing reabsorption.
Figure 1. The papilla of of the kangaroo rat extends into the ureter. This arrangement increases size and surface area of the loop of Henle and collecting ducts, increasing reabsorption. Adapted from Vimtrup and Schmidt-Nielsen 1952.
The most striking difference between the kangaroo rat kidney and that of non-desert animals is the structure of the collecting ducts. On almost every collecting duct, near the middle of the outer part of the papilla, the shape of the epithelium changes to flattened cells with rounded nuclei from the original cuboidal shape. The shape returns to cuboidal between the medium and distal third of the papilla. At this juncture, Vimtrup and Schmidt-Nielsen observed many transversely arranged nuclei that encircled some of the longitudinal channels, as if to coat them. Fibrils of a protoplasmic substance continue to encircle each nucleus. Vimtrup and Schmidt-Nielsen did not attempt to explain this phenomenon, but they assume that this arrangement may also increase reabsorption.
The final difference is the basement membrane; this membrane is much thicker in the white rat than in the kangaroo rat. Overall, it is clear that the major differences between a white rat kidney and a kangaroo rat kidney are found in the distal tubules and collecting ducts, where reabsorption occurs, while the glomeruli and proximal tubules are quite similar. The kangaroo rat has adapted highly efficient reabsorption which allows it to conserve water.
The kangaroo rat can also excrete very high amounts of sodium, chloride and other ions, even when urea concentration is high (Figure 2a & b) (Schmidt-Nielsen K et al., 1948). When kangaroo rats were fed a high salt diet, their urine was very concentrated, in terms of both electrolytes and urea. They observed a maximum concentration of chloride 50% higher than the maximum literature value reported for rats (Adolph, 1943). The maximum electrolyte concentration was more than double that of sea water. The kangaroo rats also tolerated the high salt diet without the diarrhea and dehydration observed in the control pocket mice. Clearly, the kangaroo rat can tolerate large amounts of salt without suffering a decrease in its kidney concentrating ability.
Figure 2a and b. Kangaroo rats can excrete urine with both high electrolyte and urea concentration. 2a. Plotted points represent the relationship between the concentration of electrolytes in plasma and urine. 2b. Plotted points represent the relationship between the concentration of urea in plasma and urine. Sample size is lower due to difficulties in obtaining samples large enough to test. Data from Schmidt-Nielsen K. et al. 1948.
The kangaroo rat may also use renal tubular excretion, a mechanism not found in other mammals, to excrete more urea without a loss of water. Schmidt-Nielsen used inulin to determine glomerular filtration rate and then compared rates of inulin and urea clearance. The rate of urea clearance was slightly higher than that of inulin clearance, suggesting that renal tubular excretion allows the kangaroo rat to excrete more urea (Schmidt-Nielsen, 1952).
The kangaroo rat kidney also shows adaptations at the protein level. AQP-4 is one of three aquaporins present in the kidney collecting ducts. While AQP-4 is present in the collecting ducts of non-desert animals, its expression is transcriptionally downregulated in the kangaroo rat kidney (Huang et al., 2001). Since close relatives of the kangaroo rat maintain AQP-4 expression in the kidney, its absence in the kangaroo rat may be key to the production of highly concentrated urine.
Ames and van Dyke examined the amount of ADH present in the kangaroo rat. When ADH is present, aquaporin-2 (AQP-2) is localized to the cell membranes of the cells lining the collecting duct, and water can be freely reabsorbed from the collecting duct (Figure 3) (Sadava et al., 2009). If ADH is not present, AQP-2 remains in the cytoplasm, and less water can be reabsorbed (Figure 3). Kangaroo rat urine contains up to 12 times as much ADH as that of dogs and cats, and six times that of white rats (Ames and van Dyke, 1950). High levels of ADH activity allow the kangaroo rat to reabsorb more water, concentrating its urine.
Figure 3. High levels of ADH localize AQP-2 to the cell membrane of cells lining the collecting duct, allowing reabsorption of water. Adapted from Sadava et al. 2009.
In addition, the kangaroo rat kidney is less sensitive to thyroxine. Thyroxine increases basal metabolic rate and water loss; kangaroo rats have lower than predicted free thyroxine concentrations and basal metabolic rates (Banta and Holcombe, 2002). Low thyroxine level may be an adaptation designed to conserve water. When kangaroo rats were injected with thyroxine, their thyroxine concentrations increased, but water loss did not. This result suggests kangaroo rats are highly adapted to conserve water even in the presence of diuretic hormones.