Differential catabolism of muscle protein in Garden Warblers ( Sylvia borin ): flight and leg muscle act as a protein source during long-distance migration

Abstract

Samples of flight and leg muscle tissue were taken from migratory garden warblers at three different stages of migration: (1) pre-flight: when birds face an extended flight phase within the next few days, (2) post-flight: when they have just completed an extended flight phase, and (3) recovery: when they are at the end of a stop-over period following an extended flight phase. The changes in body mass are closely related to the changes in flight (P<0.001) and leg muscle mass (P<0.001), suggesting that the skeletal muscles are involved in the protein metabolism associated with migratory flight. From pre- to post-flight, the flight and the leg muscle masses decrease by about 22%, but are restored to about 12% above the pre-flight masses during the recovery period. Biochemical analyses show that following flight a selective reduction occurred in the myofibrillar (contractile) component of the flight muscle (P<0.01). As this selective reduction accounts only for a minor part of the muscle mass changes, sarcoplasmic (non-contractile) and myofibrillar proteins of both the flight and leg muscle act as a protein source during long-distance migration. As a loss of leg muscle mass is additionally observed besides the loss in flight muscle mass, mass change seems not to be strictly associated with the mechanical power output requirements during flight. Whereas the specific content of sarcoplasmic proteins in the flight muscle is nearly twice as high as that in the leg muscle (P<0.001), the specific content of myofibrillar proteins differs only slightly (P < 0.05), being comparably low in both muscles. The ratio of non-contractile to contractile proteins in the flight muscle is one of the highest observed in muscles of a vertebrate.

Recent advances in understanding migration systems of New World land birds

“…Birds increase the size of flight muscles and accumulate fat and other nutrient stores in preparation for migration, and then refuel periodically along migration routes, presumably to protect much-needed muscle tissue (Piersma 1990, Butler and Bishop 2000, Bauchinger and Biebach 2001). Short-distance and long-distance migrants fatten to differing degrees.…”

“…Long-distance migrants that cross large barriers, e.g., the Blackpoll Warbler, are capable of almost doubling their mass (from an average of 11 g to 21 g) largely from deposited fat (Berthold 1975(Berthold , 1996. With the exception of soaring migrants including many raptors (Bildstein 2006), adipose fat, or lipids, is the primary metabolic fuel for migration with protein from muscle and digestive organs supplementing the energy reserves (Piersma and Jukema 1990, Ramenofsky 1990, Lindstro¨m and Piersma 1993, Battley et al 2000, Bauchinger and Biebach 2001, McWilliams and Karasov 2001. Recent work has shown that many shorebirds actually absorb much of the nutrient value from their intestines before long flights, such that stopover ecology involves rebuilding the intestinal tract before actually rebuilding fat loads (Piersma and Gill 1998, Karasov and Pinshow 2000, Guglielmo and Williams 2003.…”

Allocation of endogenous and dietary protein in the reconstitution of the gastrointestinal tract in migratory blackcaps at stopover sites

“…The different nutritional and locomotory requirements during periods of flight and stopover demand dynamic structural and functional changes in some organs, mainly flight muscles and digestive organs. As a result, migrating birds have evolved a high degree of phenotypic flexibility in organ size and function (Battley et al, 2000;Karasov and Pinshow, 1998;Hume and Biebach, 1996;Schwilch et al, 2002;Piersma, 1998;Bauchinger and Biebach, 2001;Biebach and Bauchinger, 2002;McWilliams and Karasov, 2005). The study of phenotypic flexibility of the different organs of birds during migration gains evolutionary and ecological significance when one considers that reduction in size and, consequently, function of organs is associated with reduced energy expenditure (Biebach and Bauchinger, 2002;Battley et al, 2000;Piersma and van Gils, 2011), but, at the same time, imposes constraints on food processing rates (van Gils et al, 2003;van Gils et al, 2006), and thus the overall pace of migration (McWilliams and Karasov, 2005).…”

“…Sources of protein are either recently ingested food or endogenous reserves (Bauchinger and Biebach, 2001). The most likely source of endogenous protein is flight muscle.…”

Stage-dependent survival in relation to timing of fledging in a migratory passerine, the Northern Wheatear (Oenanthe oenanthe)

“…In this period, juveniles must prepare for southbound migration by an energy-consuming post-juvenile moult and by strongly increasing fat reserves (Berthold 1996;Bauchinger and Biebach 2001) to be able to fly long distances and cross barriers such as the Mediterranean Sea, the Gulf of Mexico, the Great Lakes, the Sahara Desert or the deserts east of the Caspian Sea (Moreau 1972;Gauthreaux 1999;Deppe and Rotenberry 2005;Newton 2008;Holmes 2007). Thus, failure to prepare may carry-over to affect survival during migration (Berthold 1996;Bauchinger and Biebach 2001).…”