Understanding how birds rebuild fat stores during migration: insights from an experimental study

Pedro M. Araújo,Liliana Mendonça,John G. Jones,José A. Alves,Auxiliadora Villegas,Afonso D. Rocha,Jaime A. Ramos,José A. Masero,Ivan Viegas

doi:10.1038/s41598-019-46487-z

Abstract

Mechanisms underlying fat accumulation for long-distance migration are not fully understood. This is especially relevant in the context of global change, as many migrants are dealing with changes in natural habitats and associated food sources and energy stores. The continental Black-tailed godwit Limosa limosa limosa is a long-distance migratory bird that has undergone a considerable dietary shift over the past few decades. Historically, godwits fed on an animal-based diet, but currently, during the non-breeding period godwits feed almost exclusively on rice seeds. The latter diet may allow building up of their fuel stores for migration by significantly increasing de novo lipogenesis (DNL) activity. Here, we performed an experiment to investigate lipid flux and the abundance of key enzymes involved in DNL in godwits, during fasting and refueling periods at the staging site, while feeding on rice seeds or fly larvae. Despite no significant differences found in enzymatic abundance (FASN, ME1, ACC and LPL) in stored fat, experimental godwits feeding on rice seeds presented high rates of DNL when compared to fly-larvae fed birds (~35 times more) and fasted godwits (no DNL activity). The increase of fractional DNL in godwits feeding on a carbohydrate-rich diet can potentially be enhanced by the fasting period that stimulates lipogenesis. Although requiring further testing, these recent findings provide new insights into the mechanisms of avian fat accumulation during a fasting and refueling cycle and associated responses to habitat and dietary changes in a migratory species.

Highlights

Migratory animals need to adjust their physiology to accumulate high amounts of fat in preparation for migratory journeys[1]
The acetyl-CoA carboxylase (ACC) and fatty acid synthetase (FASN) are the main enzyme complexes involved in lipogenesis[10]
Using deuterated water (2H2O) as a tracer for de novo lipogenesis (DNL), a recent study demonstrated the synthesis of fatty acids (FA) from non-lipid precursors, showing that godwits are able to increase their DNL rate when they feed on a poor lipidic dietary during the winter period[34]

Summary

Introduction

Migratory animals need to adjust their physiology to accumulate high amounts of fat in preparation for migratory journeys[1]. Some studies assumed that malic enzyme (ME1) is not involved in FA synthesis[24], but Shah et al.[25] found that ME1 activity increased in the liver during the pre-migratory phase These enzymes may play a significant role in lipogenesis during migration, and assessing their expression patterns can help understand the metabolic pathways at play during fuelling and fasting cycles, which might differ according to dietary sources. Most shorebirds, those that undertake long migrations by continuous powered flight, present a high capacity to store and rapidly use adipose fat on a strict annual schedule[26,27,28], with many using stopover or staging sites to refuel between flights along their routes[29]. We measured the mRNA abundance in order to understand whether the godwits used different metabolic pathways during the re-fuelling phase, given the two different diets sources

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