Role of urinary and cloacal bladders in chelonian water economy: historical and comparative perspectives

Abstract

The Parisian comparative anatomist Claude Perrault, dissecting an Indian giant tortoise in 1676, was the first to observe that the urinary bladder is of an extraordinary size in terrestrial tortoises. In 1799, the English comparative physiologist Robert Townson suggested that the bladder functioned as a water reservoir, as he had shown previously for frogs and toads. However, these observations went unnoticed in subsequent reports on tortoise water economy that were made by travellers and naturalists visiting the Galapagos Archipelago and marvelling over the huge numbers of giant tortoises that inhabited these desert-like islands. The first such report was by an American naval officer, David Porter, who was a privateer in the 1812–15 war with England. In his journal he referred to the constant supply of water which the Galapagos tortoises carried with them. References to the location in the body, as well as the amounts and quality of the water stored, were, however, contradictory.

The confusion concerning the anatomical identity of the water reservoir in the Galapagos tortoise, Geochelone elephantopus, persisted throughout the nineteenth century, and continued when studies of tortoise water economy and drinking behaviour in arid environments were taken up independently in the desert tortoise, Gopherus agassizii, which inhabits the desert regions in the south-western United States. In 1881 Cox found large sacs filled with clear water under the carapace, but it was half a century later that these sacs were identified as the large bilobed bladder; references to specific water sacs continued to appear in the literature until the 1960s.

Since 1970, information on the water economy of desert tortoises has been obtained from extensive field studies. Rates of disappearance of tritiated water injected into the body have shown that during the drought periods of the summer, water turnover (intake) rates do not differ from the rates of metabolic water production. Under these conditions urine is not voided, but is stored in the large bladder. During a drought period the bladder urine increases from initially low osmolality finally to reach isosmolality with the blood plasma. Soluble K⁺ is the major cation of the urine, but large amounts of K⁺ are also present as precipitated urates. During a drought period the body is in negative water balance, but despite substantial losses of total body water, the plasma concentrations of Na⁺ and Cl⁻ can remain constant for many months, indicating regulation of the extracellular fluid and water content of the body tissues by reabsorption of water from the urinary bladder. The bladder thus acts both as a store for nitrogenous waste and K⁺ and as a water reservoir during droughts. Following rain showers, there is a sharp decline in tritium activity correlated with copious drinking from temporary pools of rain water. The old bladder urine is voided and most of the water drunk is stored as a highly dilute urine.

In 1676 Perrault observed that in a freshwater turtle, Emys orbicularis, but not in the giant tortoise, two other bladders opened into the cloaca. By the mid-twentieth century it had been established that these cloacal bladders typically were restricted to species of chelonians that led a semi-terrestrial or semi-aquatic life. The function of the bladders has been debated since Townson observed in 1799 that dehydrated freshwater turtles took up water by anal drinking, suggesting that anal drinking served in the water economy of semi-terrestrial turtles. Since then, the bladders have been ascribed hydrostatic and respiratory functions, but the recent literature mostly argues for a respiratory function. The possible role of the cloacal bladders as a water reservoir in amphibious turtles is still open.

Terrestrial amphibians and tortoises are unique among vertebrates in possessing large urinary bladders that may function as water reservoirs in dry environments. This function depends upon copious water intake when water becomes available combined with discontinued voiding of urine in the absence of water. Adaptation to terrestrial habitats in ureotelic amphibians is correlated with tolerance of high urea concentrations in the body fluids. In arid-zone tortoises and uricotelic tree frogs, nitrogenous waste products are precipitated in the bladder, which functions as the main sink. Renewed contact with water releases drinking behaviour and voiding of the bladder urine until the accumulated excretory products are eliminated from the body and/or bladder, preparing the organism for re-exposure to arid conditions.