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First published online July 23, 2003
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The Journal of Experimental Biology 206, 2931-2940 (2003)
doi: 10.1242/jeb.00510

The osmotic response of the Asian freshwater stingray (Himantura signifer) to increased salinity: a comparison with marine (Taeniura lymma) and Amazonian freshwater (Potamotrygon motoro) stingrays

Wai L. Tam1, Wai P. Wong1, Ai M. Loong1, Kum C. Hiong1, Shit F. Chew2, James S. Ballantyne3 and Yuen K. Ip1,*

1 Department of Biological Science, National University of Singapore, Kent Ridge, Singapore 117543, Republic of Singapore
2 Natural Sciences, National Institute of Education, Nanyang Technological University, 1 Nanyang Walk, Singapore 637616, Republic of Singapore
3 Department of Zoology, University of Guelph, Guelph, Ontario, Canada, NIG 2W1

* Author for correspondence (e-mail: dbsipyk{at}nus.edu.sg)

Accepted 19 May 2003

The white-edge freshwater whip ray Himantura signifer can survive in freshwater (0.7{per thousand}) indefinitely or in brackish water (20{per thousand}) for at least two weeks in the laboratory. In freshwater, the blood plasma was maintained hyperosmotic to that of the external medium. There was approximately 44 mmol l-1 of urea in the plasma, with the rest of the osmolality made up mainly by Na+ and Cl-. In freshwater, it was not completely ureotelic, excreting up to 45% of its nitrogenous waste as urea. Unlike the South American freshwater stingray Potamotrygon motoro, H. signifer has a functional ornithine-urea cycle (OUC) in the liver, with hepatic carbamoylphosphate synthetase III (CPS III) and glutamine synthetase (GS) activities lower than those of the marine blue-spotted fan tail ray Taeniura lymma. More importantly, the stomach of H. signifer also possesses a functional OUC, the capacity (based on CPS III activity) of which was approximately 70% that in the liver. When H. signifer was exposed to a progressive increase in salinity through an 8-day period, there was a continuous decrease in the rate of ammonia excretion. In 20{per thousand} water, urea levels in the muscle, brain and plasma increased significantly. In the plasma, osmolality increased to 571 mosmol kg-1, in which urea contributed 83 mmol l-1. Approximately 59% of the excess urea accumulated in the tissues of the specimens exposed to 20{per thousand} water was equivalent to the deficit in ammonia excretion through the 8-day period, indicating that an increase in the rate of urea synthesis de novo at higher salinities would have occurred. Indeed, there was an induction in the activity of CPS III in both the liver and stomach, and activities of GS, ornithine transcarbamoylase and arginase in the liver. Furthermore, there was a significant decrease in the rate of urea excretion during passage through 5{per thousand}, 10{per thousand} and 15{per thousand} water. Although the local T. lymma in full-strength sea water (30{per thousand}) had a much greater plasma urea concentration (380 mmol l-1), its urea excretion rate (4.7 µmol day-1 g-1) was comparable with that of H. signifier in 20{per thousand} water. Therefore, H. signifer appears to have reduced its capacity to retain urea in order to survive in the freshwater environment and, consequently, it could not survive well in full-strength seawater.

Key words: ammonia, amino acid, elasmobranch, freshwater stingray, Himantura signifer, ornithine-urea cycle, osmoregulation, Potamotrygon motoro, stingray, Taeniura lymma, urea, urea transporter


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