Calculated from data in Odum (1960) and Odum et al. (1961).

Calculated from data in Odum (1960) and Odum et al. (1961).

migrants apparently travel with reserves no greater than this. However, most regular passerine migrants depart with fuel loads amounting to 10-30% of their lean body mass, and those making especially long flights accumulate fuel loads between 40 and 70% of their lean mass, approaching 100% in a few species (Fry et al. 1970, Moreau & Dolp 1970, Alerstam & Lindstrom 1990). Similarly, some shorebirds attain very large fuel loads, as high as 50-90% of lean body mass, but with a maximum of around 100% in those embarking on the longest non-stop flights. They may then lose up to half their body mass during their flights over the next few days.

The amount of fuel deposited by migratory birds thus varies according to the length of their non-stop flights. This variation is evident even between different populations of the same species. For example, three races of Quelea quelea, inhabiting eastern, western and southern Africa respectively, each migrate at the start of the wet season, but for greatly differing distances. The amount of pre-migratory fat and protein accumulated differs significantly between the three populations, and correlates with the lengths of their respective journeys (Ward & Jones 1977). Similarly, among Barn Swallows Hirundo rustica studied at different localities in the Mediterranean region, the pre-migratory fuel stores matched the distances to be covered across the sea and the Sahara Desert (Rubolini et al. 2002). Among the Northern Wheatears Oenanthe oenanthe that pause in spring on Heligoland Island, birds of the nominate race, which breed over much of Europe, mostly stop and feed for up to a day before moving on, whereas birds of the larger Greenland race usually stop for 10-17 days, building up larger reserves for their long oversea journey (Delingat & Dierschke 2000). In contrast to individuals in migratory populations, those in resident populations show no obvious extra fat deposition in either autumn or spring, except perhaps in females in association with egg-laying.

Pre-migratory weight increase involves not only the deposition of fat, but also of body protein. Fuel should therefore be regarded as a combination of the two, but not necessarily in consistent proportions. In the most extreme species, protein contents increase prior to migration by less than two-fold, whereas fat contents may increase by more than 10-fold. Nevertheless, the protein and fat levels usually increase in step with one another during migratory fuelling, so appear to be closely correlated (e.g. Johnson et al. 1989). Some species, such as Sandhill Crane Grus canadensis, add protein and fat at migration times in the approximate ratio of 1:10 (Krapu et al. 1985), whereas other migratory birds lay down approximately equal weights of protein and fat in the ratio of 1:1 (see later). This difference may result simply from differences in the diets of different species, or in their metabolism, but it may also represent an adaptation to the different types of journey they undertake. Populations that are obliged to make long non-stop flights are presumably under greatest pressure to maximise dependence on fat, rather than carbohydrate or protein.

The ratio of fat to protein deposited as body reserve can also depend on the needs of the time, and the same species can alter this ratio between seasons. For example, the 40-50-g mass gain by 200-g European Golden Plovers Pluvialis apri-caria during autumn stopovers consists almost entirely of fat, but a similar mass gain in spring consists of proteinaceous tissue (mainly muscle). This difference may be because Golden Plovers face different needs at the two seasons. They face energy deficits on autumn migration and in winter when they eat mainly protein-rich earthworms, but in spring they risk protein deficits, when after arrival in arctic breeding areas they eat mainly berries but must soon produce eggs (Piersma & Jukema 2002). Another indication that birds can adjust their body reserves to oncoming needs comes from King Penguins Aptenodytes patagonicus, which double their body mass before long fasts on land, but with reserves consisting of about 14% protein before incubation, and 29% protein before feather moult (Cherel 1995).

At least 5-10% of the total energy released during a migratory flight must come from protein, in order to satisfy requirements in the breakdown of fat (Jenni & Jenni-Eiermann 1998). Hence, the amount of protein consumed depends partly on the amount of fat consumed. The protein is derived not only from the flight muscles, but also from other organs, including the gut, body and leg muscles (Piersma & Gill 1998). However, because the fat fraction contributes so much of the total energy needs, it has more influence than protein on the overall flight range.

Although protein breakdown is essential for fat metabolism, there are at least two reasons why birds should minimise the use of protein as fuel. First, as mentioned above, wet protein holds only about one-seventh as much energy as the same weight of adipose tissue (Table 5.1; Jenni & Jenni-Eiermann 1999), so per unit weight it is a much less efficient fuel. This is clearly a more important consideration in birds migrating by long non-stop flights than in those migrating by short flights. Second, the metabolism of protein is more complex and inefficient than that of fat and carbohydrate, and also results in toxic by-products. If protein is deposited as a major fuel, therefore, there must presumably be some other reason. Among other things, it supplies important precursors and intermediates for other physiological processes (McWilliams et al. 2004), but particularly in spring it contributes to egg formation in some species (see later). The breakdown of wet protein also yields about five times as much water as an equivalent weight of fat.

Carbohydrate is present in the form of glycogen in the liver and muscle tissue, but occurs in such small quantities at migration times that it is of relatively minor importance as an energy source. The highest glycogen values reported from birds amount to no more than about 3.0% of liver mass and about 0.5% of total body mass (Marsh 1983, Blem 1990). As they begin to prepare for migration, some small passerines change from a metabolism based mainly on carbohydrate (glycogen) to a metabolism based mainly on fat (Dolnik & Blyumental 1967, Jenni-Eierman & Jenni 1996). The weight of the liver then diminishes, because of the reduction in glycogen reserves, and shows less diurnal fluctuation in size. It becomes increasingly involved in lipogenesis, lipids being obtained directly from food or synthesised in the liver from carbohydrates. They are then transported as lipoproteins in the bloodstream to the adipose tissue. The lipid is hydrolysed and stored 'dry'. This is in contrast to carbohydrate and protein, the storage of each gram of which requires 3-5 g of extra water (Table 5.1; Blem 1990). This is a substantial weight burden, but because the water is released when carbohydrate or protein is metabolised, it may help to counter dehydration on long journeys through hot regions. So while prior to migration, glycogen is a major source of stored energy, as departure approaches, fat becomes by far the main source.

Because very little of the necessary fuel can be stored within the working muscles, their metabolic needs are met chiefly by continuous input of fuel materials via the blood system from the adipose tissues and elsewhere. Of the three fuel types, carbohydrate (glycogen) is the most readily mobilised. Based on evidence from pigeons, the three types of fuel are not used in similar ratio throughout a flight. Carbohydrates are mainly used at the start for the initial take-off and climb, while fatty acids from adipose tissues reach their steady state contribution after 1-2 hours of flight, and amino acids from tissue protein after 4-5 hours (Nachtigall 1990, Jenni-Eiermann & Jenni 2003). In birds with a fat content of more than 25%, only about 5% of the energy is derived from protein, but this proportion increases during a journey as fuel is consumed, and once the fat content falls below 5%, about 20% of flight energy derives from protein. This trend has been observed within species, as well as in comparisons between species (Jenni & Jenni-Eiermann 1998). Eventually, as the fat reserves dwindle, the bird switches even more to protein, and starvation sets in (Schwilch et al. 2002a).

The use of different types of fuel by birds has other consequences. Use of adipose tissue has little adverse effect other than to reduce energy stores and, to a small extent, body protein. But the use of too much protein could result in some functional or structural loss, because protein has no special storage form. For example, a reduction in the digestive organs (consisting mainly of muscle protein) could result in reduced ability to process food rapidly and in a lower refuelling rate during the first days of stopover (Biebach 1998, Piersma 1998). The complete loss of glycogen stores would render sudden fast flights during stopover impossible, making the bird vulnerable to predator attack or unable to chase mobile prey. To cope with emergencies, the migrant would therefore benefit from conserving some glycogen stores, or from reconstituting them soon after landing (Jenni-Eiermann & Jenni 2001, 2003).

The notion that species differ in the proportions of different fuel types used during migration is supported by findings from blood analyses of passerine birds caught directly on migratory flight, as at the high mountain pass of Col de Bretolet in Switzerland (Jenni-Eiermann & Jenni 2003). The presence of uric acid in blood plasma was taken as indicating protein metabolism, and triglycerides as indicating fat metabolism. In the blood plasma of migrants, uric acid levels were lower in five highly frugivorous species than in 13 other species that feed mainly on arthropods. Conversely, the frugivorous species showed very high levels of plasma triglycerides, indicating a heavy dependence on fat metabolism. Similarly, in birds arriving in spring at an Italian island (Ventotene) after crossing the Mediterranean Sea from North Africa (a non-stop flight of at least 500 km), plasma uric acid levels of two frugivorous and nectarivorous species were significantly lower than in seven insectivorous species (Jenni et al. 2000). Similar results were obtained for birds migrating through Israel (Gannes 2001). The implication is that different species use different ratios of fat and protein during migration, and because this is related to their diets, it gives further indication that they accumulate fat and protein as fuel in different ratios.

Unanswered questions, however, concern the extent to which migratory birds, with extremely rapid energy deposition, can influence the composition of their stores irrespective of food composition, and how much the composition of stores is controlled by metabolic or nutritional constraints. The composition of migratory fat varies to some extent with diet, but some fatty acids can apparently be synthesised, or absorbed and stored selectively (Egeler et al. 2003). Another important question is how birds 'know' they have accumulated sufficient body reserve for a migratory flight. They can clearly assess their own body condition, as can mammals, but the mechanism is unknown.

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