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First published online June 15, 2006
Journal of Experimental Biology 209, 2495-2508 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02294
Metabolic organization of freshwater, euryhaline, and marine elasmobranchs: implications for the evolution of energy metabolism in sharks and rays
1 Department of Integrative Biology, University of Guelph, Guelph, Ontario,
NIG 2W1, Canada
2 Department of Biological Science, National University of Singapore, Kent
Ridge, Singapore 117543, Republic of Singapore
* Author for correspondence (e-mail: jballant{at}uoguelph.ca)
Accepted 24 April 2006
To test the hypothesis that the preference for ketone bodies rather than
lipids as oxidative fuel in elasmobranchs evolved in response to the
appearance of urea-based osmoregulation, we measured total non-esterified
fatty acids (NEFA) in plasma as well as maximal activities of enzymes of
intermediary metabolism in tissues from marine and freshwater elasmobranchs,
including: the river stingray Potamotrygon motoro (<1 mmol
l–1 plasma urea); the marine stingray Taeniura
lymma, and the marine shark Chiloscyllium punctatum (>300
mmol l–1 plasma urea); and the euryhaline freshwater stingray
Himantura signifer, which possesses intermediate levels of urea.
H. signifer also were acclimated to half-strength seawater
(15
) for 2 weeks to ascertain the metabolic effects of the higher urea
level that results from salinity acclimation. Our results do not support the
urea hypothesis. Enzyme activities and plasma NEFA in salinity-challenged
H. signifer were largely unchanged from the freshwater controls, and
the freshwater elasmobranchs did not show an enhanced capacity for
extrahepatic lipid oxidation relative to the marine species. Importantly, and
contrary to previous studies, extrahepatic lipid oxidation does occur in
elasmobranchs, based on high carnitine palmitoyl transferase (CPT) activities
in kidney and rectal gland. Heart CPT in the stingrays was detectable but low,
indicating some capacity for lipid oxidation. CPT was undetectable in red
muscle, and almost undetectable in heart, from C. punctatum as well
as in white muscle from T. lymma. We propose a revised model of
tissue-specific lipid oxidation in elasmobranchs, with high levels in liver,
kidney and rectal gland, low or undetectable levels in heart, and none in red
or white muscle. Plasma NEFA levels were low in all species, as previously
noted in elasmobranchs. D-ß-hydroxybutyrate dehydrogenase
(D-ß-HBDH) was high in most tissues confirming the importance
of ketone bodies in elasmobranchs. However, very low D-ß-HBDH
in kidney from T. lymma indicates that interspecific variability in
ketone body utilization occurs. A negative relationship was observed across
species between liver glutamate dehydrogenase activity and tissue or plasma
urea levels, suggesting that glutamate is preferentially deaminated in
freshwater elasmobranchs because it does not need to be shunted to urea
production as in marine elasmobranchs.
Key words: elasmobranch, freshwater, marine, salinity, intermediary metabolism, enzyme, ketone body, lipid, non-esterified fatty acid, urea, evolution, Potamotrygon motoro, Himantura signifer, Taeniura lymma, Chiloscyllium punctatum
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