The Chinese soft-shelled turtle,Pelodiscus sinensis, excretes urea mainly through the mouth instead of the kidney

Abstract

SUMMARY The Chinese soft-shelled turtle, Pelodiscus sinensis, is well adapted to aquatic environments, including brackish swamps and marshes. It is ureotelic, and occasionally submerges its head into puddles of water during emersion, presumably for buccopharyngeal respiration. This study was undertaken to test the hypothesis that the buccophyaryngeal cavity constitutes an important excretory route for urea in P. sinensis. Results indicate that a major portion of urea was excreted through the mouth instead of the kidney during immersion. When restrained on land, P. sinensis occasionally submerged their head into water (20–100 min), during which urea excretion and oxygen extraction occurred simultaneously. These results indicate for the first time that buccopharyngeal villiform processes (BVP) and rhythmic pharyngeal movements were involved in urea excretion in P. sinensis. Urea excretion through the mouth was sensitive to phloretin inhibition, indicating the involvement of urea transporters (UTs). In addition, saliva samples collected from the buccopharyngeal surfaces of P. sinensis injected intraperitoneally with saline contained ~36 mmol N l−1 urea, significantly higher than that (~2.4 mmol N l−1) in the plasma. After intraperitoneal injection with 20 μmol urea g−1 turtle, the concentration of urea in the saliva collected from the BVP increased to an extraordinarily high level of ~614 μmol N ml−1, but the urea concentration (~45 μmol N ml−1) in the plasma was much lower, indicating that the buccopharyngeal epithelium of P. sinensis was capable of active urea transport. Subsequently, we obtained from the buccopharyngeal epithelium of P. sinensis the full cDNA sequence of a putative UT, whose deduced amino acid sequence had ~70% similarity with human and mouse UT-A2. This UT was not expressed in the kidney, corroborating the proposition that the kidney had only a minor role in urea excretion in P. sinensis. As UT-A2 is known to be a facilitative urea transporter, it is logical to deduce that it was localized in the basolateral membrane of the buccopharyngeal epithelium, and that another type of primary or secondary active urea transporter yet to be identified was present in the apical membrane. The ability to excrete urea through the mouth instead of the kidney might have facilitated the ability of P. sinensis and other soft-shelled turtles to successfully invade the brackish and/or marine environment.

Effect of Salinity on the Survival, Ions and Urea Modulation in Red-eared Slider (Trachemys scripta elegans)

“…Lee et al (2006) studied that increases in urea contents in tissues of P. sinensis on days 3, 4 and 6 indicated an increase in the rate of urea synthesis, and the overall rate of urea synthesis increased 1.4 fold during the 6 d. Also, the capacity of P. sinensis to retain urea is apparently limited, and the urea excretion rate returned back to the control level as the plasma urea concentration increased, which is coincident with our results. However, the recent study on an important excretory route for urea in P. sinensis has shown that it is well adapted to aquatic environments, including brackish swamps and marshes, can excrete urea mainly through the buccophyaryngeal cavity of mouth instead of the kidney during immersion (Ip et al, 2012). Indeed, ureogenesis allows the transfer from fresh water to seawater in the diamondback terrapin; moreover, in a dehydrated desert tortoise, Gopherus agassizii, the increase in the osmolarity of the blood is principally due to an increase in urea concentration (Dantzler and Schmidt-Nielsen, 1966).…”

The Chinese soft-shelled turtle, Pelodiscus sinensis, decreases nitrogenous excretion, reduces urea synthesis and suppresses ammonia production during emersion

“…It is primarily ureotelic, excreting the majority (71%) of the waste nitrogen (N) as urea-N in freshwater. Unlike other reptiles, it excretes urea predominantly through the mouth instead of the kidney during immersion (Ip et al, 2012). When restrained on land, P. sinensis occasionally submerges its head in water, during which urea excretion and O 2 uptake occur simultaneously.…”

“…When restrained on land, P. sinensis occasionally submerges its head in water, during which urea excretion and O 2 uptake occur simultaneously. Its buccopharyngeal epithelium is capable of active urea excretion, and expresses a putative urea transporter (UT-A2), which is absent from the kidney (Ip et al, 2012).…”

“…Buccopharyngeal urea excretion might have facilitated P. sinensis (Ip et al, 2012) and other members of Trionychidae (Minnich, 1979) to invade the brackish or marine environment. When exposed to brackish water (salinity 15), significant increases in plasma osmolality, [Na + ], [Cl -] and [urea], which presumably decrease the osmotic loss of water, occur in P. sinensis (Lee et al, 2006).…”

“…We hypothesized that the normal ammonia excretion rate would be maintained during emersion because ammonia could be excreted through the highly vascularized ventral carapace, which was in constant contact with a film of water during emersion. Because P. sinensis excreted urea mainly through the buccopharyngeal cavity (Ip et al, 2012), and as no water was available to rinse the mouth during emersion, we further hypothesized that emersion would lead to a greater reduction in urea excretion than in ammonia excretion.…”