Lamprey parasitism of sharks and teleosts: high capacity urea excretion in an extant vertebrate relic

Abstract

We observed 10 sea lampreys ( Petromyzon marinus) parasitizing basking sharks ( Cetorhinus maximus), the world's second largest fish, in the Bay of Fundy. Due to the high concentrations of urea in the blood and tissues of ureosmotic elasmobranchs, we hypothesized that sea lampreys would have mechanisms to eliminate co-ingested urea while feeding on basking sharks. Post-removal urea excretion rates ( J Urea) in two lampreys, removed from separate sharks by divers, were initially 450 (≈9000 μmol N kg −1 h −1) and 75 times (≈1500 μmol N kg −1 h −1) greater than basal (non-feeding) rates (≈20 μmol N kg −1 h −1). In contrast, J Urea increased by 15-fold after parasitic lampreys were removed from non-ureosmotic rainbow trout ( Oncorhynchus mykiss). Since activities of the ornithine urea cycle (OUC) enzymes, carbamoyl phosphate synthetase III (CPSase III) and ornithine carbamoyl transferase (OCT) were relatively low in liver and below detection in intestine and muscle, it is unlikely that the excreted urea arose from de novo urea synthesis. Measurements of arginase activity suggested that hydrolysis of dietary arginine made a minor contribution to J Urea.. Post-feeding ammonia excretion rates ( J Amm) were 15- to 25-fold greater than basal rates in lampreys removed from both basking sharks and rainbow trout, suggesting that parasitic lampreys have a high capacity to deaminate amino acids. We conclude that the sea lamprey's ability to penetrate the dermal denticle armor of sharks, to rapidly excrete large volumes of urea and a high capacity to deaminate amino acids, represent adaptations that have contributed to the evolutionary success of these phylogenetically ancient vertebrates.