On fuel choice and water balance during migratory bird flights

Abstract

It has been proposed that water loss during flight in migratory birds under high evaporative conditions can be offset by the production of water through increased protein catabolism. Indeed, oxidation of protein may supply 7-times more water/kJ than fat. However, the lack of a relative increase in protein catabolism over that of fat during long flights indicates that processes other than water balance may be the primary drivers of protein catabolism during long and strenuous flights. These processes include the release of stress hormones (which increase both protein and fat catabolism) and protein catabolism triggered by increased oxidative damage to muscle proteins from reactive oxygen species produced by mitochondria. Protein catabolism is an important source of water for birds during migratory flight, but it remains to be determined if this process is directly regulated by hydration status.

Introduction

Preventing dehydration is a major challenge for birds that migrate long distances without stopping to consume water. It has been reported that the water loss during flight in migratory birds under high evaporative conditions (HEWL) is offset by the production of water through increased protein catabolism, as demonstrated by higher post-flight plasma uric acid levels (20). Essentially this indicates that when faced with a negative water balance, these birds increase protein oxidation to provide both energy and water since protein catabolism produces 5 to 6 times more water than fat catabolism. The purpose of this brief review is to provide an overview of water formation associated with substrate catabolism and discuss how shifts in substrate oxidation can influence water formation.

Water Formation During Substrate Oxidation

For pedagogical purposes, it is important to clarify the origin of the water produced during tissue catabolism. To illustrate this issue, we have calculated the water contribution from various substrates (Table I). Total water is the sum of water released by oxidation of a particular substrate, also called metabolic water (Table I, A & C), and that released by the hydration shell associated with substrates and electrolytes that occurs primarily as a consequence of the loss of lean tissue mass (Table I, D & F).

TABLE I.

Water formation by oxidation of storage substrates

	A	B	C	D	E	F	G
Substrates	Metabolic H2O in g/kJ of oxidized substratea	Energy in kJ/g substrate wet wt	Metabolic H2O in g/g fuel (A × B)	H2O content in g/g dry wt substrated	Energy in kJ/g dry wt	H2O content in g/kJ (D/E)	Total H2O in g/kJ (A + F)
Fat	0.0272	39.6e	1.08	0.20	39.6	0.005	0.032
Protein	0.0220	3.7b	0.08	3.65	18.4	0.198	0.220
Carbohydrate	0.0318	5.6c	0.18	2.10	17	0.124	5.632

^aValues for calculating metabolic water production from indirect respiration calorimetry (35).

^bAssuming that lean tissue contains approximately 73% water (12, 51).

^cAssuming that 2/3 of glycogen wet weight is water.

^dWater associated with electrolytes and hydration shells.

^eAssuming that fatty acids can be mobilized from adipose tissue without loss of tissue water.

In the case of birds, it is crucial to consider the energy density of the substrate (kJ/g substrate wet weight) since body weight may compromise flight performance. Given that fat produces 7–10 times higher energy/g than lean tissue (Table, I B), it is not surprising that flight (as a high ATP-demanding process) under all humidity conditions, is sustained primarily by fatty acid oxidation (>90%; (36, 50)). In regard to metabolic water production, fat produces 6 and 13.5 times more metabolic water/g than hydrated glycogen or lean mass, respectively (Table I, C). However, if total water generation (metabolic water plus substrate-associated water) were the prime factor determining fuel storage, glycogen would be the preferred substrate yielding 180- and 26-times more water/kJ compared to fat and protein, respectively (Table I, G). Reliance on glycogen, nonetheless, is not a viable option for birds undergoing sustained exercise since there is a limited amount of glycogen that can be stored in the body without affecting significantly body weight. The next best option for migrating birds would be to breakdown lean tissue, which yields 7-times more water/kJ than fat (Table I, G).

To meet the intense metabolic demands of migration, birds rely on the ability of adipose tissue (i) to store high amount of fat in a relatively short period (about 10-fold fat increase in a week) and (ii) to catabolize it in 2–3 days during nonstop migratory flights (36). Respiration and evaporative cooling primarily account for water losses in migratory birds (1, 21). While most energy will be provided by fat during long flights, the total water produced by fat oxidation is almost equal to that produced by the much smaller amount of lean mass catabolized:

$${[0.032\mathrm{g}\text{water}/\text{kJ}\times 0.9]}_{\text{fat}}+{[0.220\mathrm{g}\text{water}/\text{kJ}\times 0.1]}_{\text{lean}\text{mass}}=0.029+0.022$$

Gaining enough fat would minimize the frequency and duration of stopovers (which increases the risk of predatorial activity) and provide better chances of breeding at the final destination (14). However, some loss of lean mass (second sum term in the above equation) seems the only option that birds on long flights have for generating more water (after glycogen is depleted) if they encounter HEWL conditions. The success of this strategy will depend on how much lean mass can be gained prior to migration and how much lean mass can be lost before exercise performance is compromised. Protein catabolism from flight muscles and other organs has the concomitant advantage that flight muscle mass can be continuously adapted to the decreasing body mass (37) and the body mass to be carried is reduced (39). Pectoral muscle thickness decreases, as expected, during long flights (27, 33). However, the energetic demands of long flight produce changes in both lean and fat tissue mass. High residual body mass loss occurs in parallel with high plasma levels of both protein and lipid catabolites in migrating birds (27), indicating that rates of both protein and lipid metabolism increase in concert with no major change in the proportion of substrates used for energy. Furthermore, during 10 h flights, residual energy expenditure was positively correlated with both lipid catabolite levels and body mass loss (30). Although protein catabolism is an important contributor to water production during migratory flight, it is not clear if water status is a factor regulating substrate utilization by the animal.

Alternative hypotheses

Does negative water balance influencing the mix of substrates oxidized for energy during migratory flight? This is the central question in determining if protein catabolism during long flights is a regulated process for supplying birds with water. Alternative hypotheses to this regulated protein catabolism for water generation concept include water generation simply as a useful byproduct of increased protein catabolism driven by the release of stress hormones and/or increased oxidative damage to muscle proteins during strenuous, long flights.

Catecholamines and glucocorticoids (such as corticosterone) have been reported to play a role in stimulating flight, regulating fuel utilization during flight and optimizing flight performance in birds (4, 6–8, 13, 15–17, 19, 23, 24, 40, 44, 48). However, there is not uniform agreement regarding the effect of long flights on these hormones with some studies reporting that levels are not increased from baseline, possibly indicating an adaptation to long flights to minimize both lean mass protein loss which can compromise flight performance (26, 31). The stress-related hormones increase lipid and protein catabolism to provide energy, sustain gluconeogenesis (glucogenic amino acids, glycerol) and (25, 27) compensate for water losses. Additional work is needed, however, to determine if stress-related hormones are the primary stimulus for protein catabolism and generation of water during migratory flight.

Oxidative damage to lipids, nucleic acids and proteins during long flights (or sustained exercise; (9–11, 28, 32)) could also contribute to protein catabolism and production of water. This damage, mediated by reactive oxygen species leaking from mitochondria (2, 5, 22, 29, 34, 38, 41, 45, 47, 49), could induce protein catabolism to clear the oxidatively modified targets (3, 18, 46). This activation of catabolic pathways functions to ensure the removal of dysfunctional proteins (42, 43), does not seem to be triggered by a putative negative water balance. It remains to be determined if an appreciable amount of water is generated secondary to protein catabolism in response to flight-related oxidative stress.

Conclusions

Catabolism of both fats and proteins generate water, which helps mitigate water loss during long migratory flights. Although protein catabolism is often a relatively minor contributor to energy supply during migration, the large amount of water generated during breakdown of lean versus fat tissue makes protein catabolism an important source of water during flight. While the protein-for-water strategy should work in all animals (not only uricotelic), the sustained, intense exercise that occurs in migratory birds (especially those flying over oceans with 40–60 h for > 1,000 km) without the consumption of drinking water makes this process much more important in birds than terrestrial animals which undergo less intense levels of sustained exercise. It remains to be determined if water status plays an important role in regulating protein catabolism in migrating birds or if water is simply a fortunate byproduct of protein catabolism induced by intense exercise.