Total fat mass
Figure 5.7 Comparison of different components of body mass in different samples of Great Knots Calidris tenuirostris caught just before and just after a 5420 km flight between northwest Australia and Chongming Island near Shanghai in China. From Battley et al. (2001).
on their northbound journey. The higher flight-range estimate for the Alaskan birds was not due mainly to their higher fat mass (only 5% higher), but to the higher proportion that fat formed of total body mass, which they had achieved in autumn by reducing the mass of other organs before departure. The 'fat fraction' was more important than the fat mass in influencing flight range (Pennycuick & Battley 2003).
Turning to another shorebird, samples of Great Knots Calidris tenuirostris were collected before and after a 5420 km flight from northwest Australia to Chongming Island near Shanghai in China (believed to be flown non-stop), again in order to determine the mass of fat consumed and also of protein withdrawn from flight muscles and other organs. This journey takes four days (Pennycuick & Battley 2003). Not only did these birds show reduction in fat content (but not to zero), they also showed loss of lean tissue mass, with statistically significant reductions in six organs (pectoral muscle, skin, salt glands, intestine, liver, kidney), and non-significant reductions in several others (Figure 5.7). The reduction in functional components between the start and the end of the flight was reflected in a lowering of BMR by 42%, one of the fastest rates of BMR change recorded in birds. Only the brain and lungs had not changed over this journey (Battley et al. 2000). Other Great Knots caught in northwest Australia were flown to the Netherlands, and kept without food until their body mass had declined to the level found in arriving birds on Chongming Island. Organ reductions were broadly similar but, compared with the fasted birds, those that had migrated had conserved more protein (Battley et al. 2001).
Another well-documented example of seasonal change in body composition concerns the Eared Grebe Podiceps nigricollis in North America (Jehl 1997, Jehl et al. 2003). Incapable of flight for months at a time, this species has the longest non-flying period of any northern hemisphere bird, totalling 9-10 months over the course of a year. In practical terms, the bird flies only to migrate and spends the rest of its life on water, in association with which it undergoes several cycles per year of expansion and contraction of particular body parts. Yet its existence depends on its ability to fly as much as 6000 km each year to reach high-yield seasonal environments that are exploitable by very few other species. After breeding mainly on prairie wetlands, the species migrates to assemble in huge numbers on a small number of hypersaline lakes, especially the Great Salt Lake in Utah and Mono Lake in California, each of which can hold more than a million grebes in autumn. The birds feed on the huge numbers of brine shrimps Artemia and alkali flies Ephydra available at this time.
The grebes arrive mainly in September (but from mid-July to early November), moult their feathers and remain until food supplies have dwindled (usually late November-December). They then migrate to wintering areas in the Gulf of California. They begin the return journey from January, travelling via the Salton Sea (in south California) where they remain for at least two months, again becoming flightless, and then in late March-April they continue to the Great Salt Lake, and thence to the prairies in April-June.
When birds leave their prairie nesting ponds in late summer they weigh about 420-450 g, but on arrival on the moulting sites after 2-3 nights of flight, they weigh as little as 250 g. Their moult leaves them flightless for 35 days, but they gradually increase in body mass to reach more than 600 g by mid-October. During this period they have accumulated massive fat stores, and their body organs have undergone large changes, involving increases in the size of the digestive organs and leg muscles, and a reduction of 50% or more in breast muscle, to below the size needed for flight. However, at the end of this autumn staging period, when the flight feathers have been replaced, the body changes are reversed. In the 2-3 weeks before leaving southward, the birds lose as much as one-third of their fat reserves, and reduce the size of nutritional organs by up to 75% while building their pectoral muscles and heart (Jehl 1997). These huge changes in body structure result in a net one-third loss of body mass to 420-450 g. In this way the grebes optimise flight efficiency by reducing weight and wing loading, and increasing flight range. No other bird species is known to reach migratory condition by losing so much mass before departure (but for nestlings of some species, see later). Most of the remaining fat reserves are used during the flight to wintering areas. Juveniles undergo similar but less extreme changes.
Additional cycles that involve less marked fattening are repeated at breeding and wintering areas and in some birds also at spring staging areas, so that body weight and composition are in continual flux. The extreme reductions in leg muscle mass that occur before every migration reduce flight costs. If the bird maintained the body structure best suited for swimming and feeding, it would need far greater energy reserves for its long-distance migrations. This continual modification of behaviour and body structure as the bird shifts between swimming and flight modes, sedentary and migratory phases, with minimal waste of resources, may have helped the Eared Grebe to become the most abundant grebe on earth.
It is clear from these various examples that a bird refuelling for long-distance migration is not like a plane landing, refuelling and taking off again. Unlike the plane, the bodies of long-distance migrant birds have to be partly reconstructed at each stopover and modified again before take-off. We can envisage that the sizes of organs carried at take-off by different populations represent evolutionary compromises between their functions during the pre-departure, flight and post-arrival phases of migration (Piersma 1998). In all populations, other tissue is invariably deposited along with fat, but in proportions that vary greatly between species, and between different populations of the same species, according to the journeys they make (Table 5.5). Before departure on long journeys, exercise organs (pectoral muscle and heart) tend to enlarge and nutritional organs (stomach, intestine and liver) tend to shrink. This makes sense on long flights where weight reduction is at a premium. In other species, the digestive tract is apparently reduced during the flight itself, rather than beforehand, contributing to the fuel and water needs of the migrant on its journey. Prior reductions in nutritional organs appear most pronounced in populations about to over-fly oceans that offer few or no opportunities for emergency landings, let alone feeding.
The adaptive role of muscle growth and shrinkage is not entirely clear, as it may serve more than one function. As explained already, muscle breakdown is necessary for efficient fat metabolism, providing intermediates for the citric acid cycle. It may also provide metabolites such as glucose for proper functioning of the nervous system, and uric acid which is an antioxidant that can de-toxify the free radicals produced when tissues consume oxygen (Dohn 1986, Klaassen 1996). At the same time, as muscles provide the power needed for migratory flights, their shrinkage during a flight may be an adaptation to the reducing weight (and hence reducing power needs) of the bird during its journey (Pennycuick 1975). On sustained long flights, loss of protein is thus unavoidable; but it also happens to be strategically convenient (Jenni & Jenni-Eierman 1998, Battley et al. 2000). However, populations differ in the ratio of fat to protein they accumulate as reserves, as do the same populations at different seasons. These facts cast further doubt on the idea that shrinking muscle size during flight serves primarily to reduce power output as the bird loses weight. This may be one function, but as flight muscle mass is not consistently related to overall body mass, it cannot be the whole story (Bauchinger & Biebach 2005).
Because protein catabolism results in a higher metabolic water yield per unit energy than lipid, it is of additional value on long, non-stop flights (Table 5.1; Klaassen 1996). Net water availability during continuous flight could therefore be altered by changes in the relative proportions of the different fuel types used. In Bar-tailed Godwits Limosa lapponica and other shorebirds on spring migration, fat and protein are deposited in almost equal amounts (fresh mass basis), but because of its greater energy content, fat provides about 90% of the energy required for the flight. The same ratio (roughly half and half) may apply to a much wider taxonomic array of birds, including Chaffinch Fringilla coelebs and Garden Warbler Sylvia borin, as well as various waders. This is far removed from an earlier assumption that all weight increase in migrant birds was due to fat, although the fat-to-protein ratio may differ greatly between species, and also between autumn and spring in the same species, as mentioned above. In some shorebirds, about two-thirds of the increase in flight muscle mass resulted from increases in myofibril mass, and about one-quarter from additional mitochondrial mass, while sarcoplasm increased very little (Evans & Davidson 1990). Most data refer to the autumn migration, and the situation may differ in spring when different routes are often taken, and when birds must ideally arrive on breeding areas with a surplus of fat and protein reserves left over for breeding (see later).
The fact that nutritional organs are not fully functional on arrival after a long flight may explain why some migrants, on reaching a stopping site, do not appear to feed. They simply rest, and depart later in the day or at night (e.g. Rappole & Warner 1976). Typically, they are less specific in their habitat needs than feeding birds, and individuals of normally territorial species make no attempt to establish a territory but sit around in groups. They are in flight mode rather than in feeding mode, and it may be more energy-efficient to move on while reserves last rather than reconstruct digestive machinery and start to feed again before this becomes necessary. An example of stopover periods recorded at a desert oasis are given in Figure 5.8. Most of the birds were recorded on only one day, and may have passed on without feeding, but others stayed for more than 10 days, replenishing their body reserves (for other records from another site, giving generally longer periods, see Table 5.4).
In most species that have been studied, individuals were found to arrive in breeding or wintering areas with residual body reserves not totally used on the journey (e.g. Sandberg 1996, Fransson & Jakobsson 1998, Farmer & Wiens 1999, Widmer & Biebach 2001, Morrison 2006, Krapu et al. 2006). For example, American Redstarts Setophaga ruticilla arrived in Michigan breeding areas with enough body fat for at least another 1000 km of further flight, while Bar-tailed Godwits Limosa lapponica from Alaska arrived in New Zealand with enough fat for another 5000-6000 km of flight (Pennycuick & Battley 2003). However, remaining fuel levels varied greatly between individuals, and from year to year in the same population.
Considering the energy cost of transporting such reserves, the question arises why birds carry so much more than they need? Extra reserves might act as insurance against food shortage or bad weather en route; they might enable migrants to fly faster than the maximum range speed on flights where they are likely to encounter unfavourable weather; or they may help to ensure survival after arrival in new areas, especially in spring when local food supplies are still scarce. In spring, they might also enable newly arrived males to concentrate on fighting and territory acquisition, or females to produce eggs earlier than they might otherwise do (Chapter 27). Clearly, these various possibilities are not mutually exclusive.
If the main function of surplus reserves is to promote survival, the first arriving sex (in most species the males) would be expected to arrive with the largest reserves; and if the main function is to aid egg production, the females should arrive with the largest reserves. In the sub-arctic environment of Swedish Lapland, long-distance passerine migrants arrived with enough fat to fly an estimated further 242-500 km, depending on species, while short-distance migrants arrived with lesser amounts (Sandberg 1996). Fat reserves on arrival were thus related to migration distance. They were also related to feeding habits which were assumed to influence the amount of reserve needed during the transition period between arrival and breeding. However, in seven out of nine species in which both sexes arrived together, females had significantly larger reserves than males, favouring the egg production hypothesis. In the two species in which the sexes had significantly different mean arrival dates, males and females showed
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