Preparing for long-distance migration: Effects of dietary fatty acids on metabolism of semipalmated sandpipers

Abstract

At the end of every summer, the semipalmated sandpiper (Calidris pusilla) stops in the Bay of Fundy (east coast of Canada) to build large fat reserves before its non-stop flight to wintering grounds in South America. During this two-week stopover, body mass is doubled by feeding on a burrowing amphipod, Corophium volutator, containing extremely high levels of n-3 polyunsaturated fatty acids (n-3 PUFA), most notably 31% eicosapentaenoic acid (EPA). Several lines of evidence link high n-3 PUFA content in membranes with elevated muscle and exercise performance. Furthermore, high PUFA content in muscle phospholipids have been shown to increase membrane fluidity, thereby accelerating cellular lipid uptake and, possibly, improving endurance. In mammals, dietary n-3 PUFA are known to increase mitochondrial and peroxisomal content, as well as the activities of oxidative enzymes. I hypothesized that dietary EPA could be used by semipalmated sandpipers as a natural "performance enhancing" substance to prime their flight muscles for migration. Birds were collected at various stages of fat loading throughout the stopover to measure changes in percent fat and fatty acid composition of muscle and lipid reserves (in both neutral lipids and phospholipids). Activities of several enzymes were also measured in flight muscle: namely citrate synthase (CS, Krebs cycle enzyme used as a marker for mitochondrial density), carnitine palmitoyl transferase, 3-hydroxyacyl dehydrogenase (respectively CPT and HOAD, markers for beta-oxidation) and lactate dehydrogenase (LDH, index of glycolytic metabolism). Results show that EPA and docosahexaenoic acid (DHA) were rapidly incorporated in muscle phospholipids and lipid reserve neutral lipids. Over the course of the stopover, the fatty acid profiles of these tissues converged with that of the birds' diet. However, data indicate that a significant proportion of dietary EPA and DHA are converted before storage (particularly into 18:1). Stored oleate (18:1) may offer a compromise between high energy density and ease of mobilization/oxidation of lipid reserves. In addition, CS and HOAD activities in pectoral muscle increased during the stopover. Unexpectedly, LDH activity was strongly related to n-3 PUFA content in the sandpipers' tissues. LDH may be used to convert lactate into pyruvate, which may serve as an important fuel for aerobic metabolism. Observed physiological changes prior to migration in the semipalmated sandpiper are consistent with the stimulatory effects of n-3 PUFA on endurance capacity previously observed in other vertebrates. Dietary PUFAs may therefore be used as pharmacological agents to prepare the flight muscles of long-distance migrant shorebirds for extreme endurance exercise.