Shorebirds' seasonal adjustments in thermogenic capacity are reflected by changes in body mass: how preprogrammed and instantaneous acclimation work together

Phenotypic flexibility in shorebirds has been studied mainly in the context of adjustments to migration and to quality of food; little is known on how birds adjust their phenotype to harsh winter conditions. We showed earlier that red knot (Calidris canutus islandica) can acclimate to cold by elevating body mass. This goes together with larger pectoral muscles, i.e., greater shivering machinery, and thus, better thermogenic capacity. Here, we present results of a yearlong experiment with indoor captive knots to determine whether this strategy is part of their natural seasonal phenotypic cycle. We maintained birds under three thermal regimes: constant cold (5 °C), constant thermoneutrality (25 °C) and natural seasonal variation between these extremes (9-22 °C). Each month we measured variables related to the birds' endurance to cold and physiological maintenance [body mass, thickness of pectoral muscles, summit metabolic rate (M(sum)), food intake, gizzard size, basal metabolic rate (BMR)]. Birds from all treatments expressed synchronized and comparable variation in body mass in spite of thermal treatments, with a 17-18% increase between the warmest and coldest months of the year; which appeared regulated by an endogenous driver. In addition, birds living in the cold exhibited a 10% higher average body mass than did those maintained at thermoneutrality. Thickness of the pectoral muscle tracked changes in body mass in all treatments and likely contributed to greater capacity for shivering in heavier birds. Consequently, M(sum) was 13% higher in cold-acclimated birds compared to those experiencing no thermoregulation costs. However, our data also suggest that part of maximal heat production comes from nonshivering processes. Birds facing cold conditions ate up to 25% more food than did birds under thermoneutral conditions, yet did not develop larger gizzards. Seasonal variation in BMR followed changes in body mass, probably reflecting changes in mass of metabolically active tissues. Just as cold-exposed birds, red knots in the variable treatment increased body mass in winter, thereby improving cold endurance. During summer, however, they maintained a lower body mass and thermogenic capacity compared to cold-exposed birds, similar to individuals kept at thermoneutrality. We conclude that red knots acclimate to seasonal variations in ambient temperature by modulating body mass, combining a preprogrammed increase in mass during winter with a capacity for fine-tuning body mass and thermogenic capacity to temperature variations.     

Phenotypic flexibility of a southern African duck Alopochen aegyptiaca during moult: do northern hemisphere paradigms apply?

Phenotypic flexibility during moult has never been explored in austral nomadic ducks. We investigated whether the body condition, organ (pectoral muscle, gizzard, liver and heart) mass and flight‐feather growth Egyptian geese Alopochen aegyptiaca in southern Africa show phenotypic flexibility over their 53‐day period of flightless moult. Changes in body mass and condition were examined in Egyptian geese caught at Barberspan and Strandfontein in South Africa. Mean daily change in primary feather length was calculated for moulting geese and birds were dissected for pectoral muscle and internal organ assessment. Mean body mass and condition varied significantly during moult. Body mass and condition started to decrease soon after flight feathers were dropped and continued to do so until the new feathers were at least two‐thirds grown, after which birds started to regain body mass and condition. Non‐moulting geese had large pectoral muscles, accounting for at least 26% of total body mass. Once moult started, pectoral muscle mass decreased and continued to do so until the flight feathers were at least one‐third grown, after which pectoral muscle mass started to increase. The regeneration of pectoral muscles during moult started before birds started to gain overall body mass. Gizzard mass started to increase soon after the onset of moult, reaching a maximum when the flight feathers were two‐thirds grown, after which gizzard mass again decreased. Liver mass increased significantly as moult progressed, but heart mass remained constant throughout moult. Flight feather growth was initially rapid, but slowed towards the completion of moult. Our results show that Egyptian geese exhibit a significant level of phenotypic flexibility when they moult. We interpret the phenotypic changes that we observed as an adaptive strategy to minimize the duration of the flightless period. Moulting Egyptian geese in South Africa undergo more substantial phenotypic changes than those reported for ducks in the northern hemisphere.     

REPTILIAN PHYSIOLOGY AND THE FLIGHT CAPACITY OF ARCHAEOPTERYX

Current scenarios frequently interpret the Late Jurassic bird Archaeopteryx as having had an avian-type physiology and as having been capable of flapping flight, but only from “the trees downward.” It putatively lacked capacity for takeoff and powered flight from the ground upward. Data from extant reptiles indicate that if Archaeopteryx were physiologically reptilian, it would have been capable of ground upward takeoff from a standstill, as well as “trees downward” powered flight. This conclusion is based largely on a previously unrecognized attribute of locomotory (skeletal) muscle in a variety of extant reptiles: During “burst-level” activity, major locomotory muscles of a number of active terrestrial taxa generate at least twice the power (watts kg^?1 muscle tissue) as those of birds and mammals. Reptilian physiological status also helps resolve the apparently uneven development of various flight support structures in Archaeopteryx (e.g., well-developed flight features but relatively unspecialized pectoral girdle, supracoracoideus muscles, etc.). Endothermy and capacity for longer-distance powered flight probably evolved only in Early Cretaceous birds, which were the first birds to have a keeled sternum, strap-like coracoid, and hypocleidium-bearing furcula.     

Changes in body mass and organ size during wing moult in non-breeding greylag geese Anser anser

The "cost-benefit" hypothesis states that specific body organs show mass changes consistent with a trade-off between the importance of their function and cost of their maintenance. We tested four predictions from this hypothesis using data on non-breeding greylag geese Anser anser during the course of remigial moult: namely that (i) pectoral muscles and heart would atrophy followed by hypertrophy, (ii) leg muscles would hypertrophy followed by atrophy, (iii) that digestive organs and liver would atrophy followed by hypertrophy and (iv) fat depots be depleted. Dissection of geese captured on three different dates during wing moult on the Danish island of Saltholm provided data on locomotory muscles and digestive organ size that confirmed these predictions. Locomotory organs associated with flight showed initial atrophy (a maximum loss of 23% of the initial pectoral muscle mass and 37% heart tissue) followed by hypertrophy as birds regained the powers of flight. Locomotory organs associated with running (leg muscles, since geese habitually run to the safety of water from predator-type stimuli) showed initial hypertrophy (a maximum gain of 37% over initial mass) followed by atrophy. The intestines and liver showed initial atrophy (41% and 37% respectively), consistent with observed reductions in daily time spent feeding during moult, followed by hypertrophy. The majority of the 22% loss in overall body mass (mean 760 g) during the flightless period involved fat utilisation, apparently consumed to meet shortfalls between daily energetic needs and observed rates of exogenous intake. The results support the hypothesis that such phenotypic plasticity in size of fat stores, locomotor and digestive organs can be interpreted as an evolutionary adaptation to meet the conflicting needs of the wing moult.     

Rapid changes in the size of different functional organ and muscle groups during refueling in a long-distance migrating shorebird.

The adaptive value of size changes in different organ and muscle groups was studied in red knots (Calidris canutus islandica) in relation to their migration. Birds were sampled on five occasions: at arrival in Iceland in May 1994, two times during subsequent refueling, at departure toward, and on return from, the high arctic breeding grounds. During their 24-d stopover in May, body mass increased from 144.3 to 214.5 g. Mass gains were lowest over the first week (0.85 g/d, only fat-free tissue deposited). Over the subsequent 10 d, average mass increased by 5.0 g/d (fat contributing 78%), and over the last week before takeoff, it increased by 2.0 g/d (fat contributing over 100% because of loss of lean components). There were no sex differences in body and fat mass gains. Over the first interval, lean masses of heart, stomach, and liver increased. During the middle 10 d, sizes of leg muscle, intestine, liver, and kidneys increased. Stomach mass decreased over the same interval. In the last interval before takeoff, the stomach atrophied further and the intestine, leg muscles, and liver became smaller too, but pectoral muscles and heart increased in size. Sizes of "exercise organs" such as pectoral muscle and heart were best correlated with body mass, whereas sizes of organs used during foraging (leg muscles) and nutrient extraction (intestine, liver) were best correlated with rate of mass gain. Kidneys changed little before takeoff, which suggests that they are needed as much during flight as during refueling.     

Wild geese do not increase flight behaviour prior to migration

Hypertrophy of the flight muscles is regularly observed in birds prior to long-distance migrations. We tested the hypothesis that a large migratory bird would increase flight behaviour prior to migration, in order to cause hypertrophy of the flight muscles, and upregulate key components of the aerobic metabolic pathways. Implantable data loggers were used to record year-round heart rate in six wild barnacle geese (Branta leucopsis), and the amount of time spent in flight each day was identified. Time in flight per day did not significantly increase prior to either the spring or the autumn migration, both between time periods prior to migration (5, 10 and 15 days), or when compared with a control period of low activity during winter. The lack of significant increase in flight prior to migration suggests that approximately 22 min per day is sufficient to maintain the flight muscles in condition for prolonged long-distance flight. This apparent lack of a requirement for increased flight activity prior to migration may be attributable to pre-migratory mass gains in the geese increasing workload during short flights, potentially prompting hypertrophy of the flight muscles.     

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

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.     

Move that fatty acid: fuel selection and transport in migratory birds and bats

The metaphor of marathon running is inadequate to fully capture the magnitude of long-distance migratory flight of birds. In some respects a journey to the moon seems more appropriate. Birds have no access to supplementary water or nutrition during a multi-day flight, and they must carefully budget their body fat and protein stores to provide both fuel and life support. Fatty acid transport is crucial to successful non-stop migratory flight in birds. Although fat is the most energy-dense metabolic fuel, the insolubility of its component fatty acids makes them difficult to transport to working muscles fast enough to support the highly aerobic exercise required to fly. Recent evidence indicates that migratory birds compensate for this by expressing large amounts of fatty acid transport proteins on the membranes of the muscles (FAT/CD36 and FABPpm) and in the cytosol (H-FABP). Through endogenous mechanisms and/or diet, migratory birds may alter the fatty acid composition of the fat stores and muscle membranes to improve endurance during flight. Fatty acid chain length, degree of unsaturation, and placement of double bonds can affect the rate of mobilization of fatty acids from adipose tissue, utilization of fatty acids by muscles, and whole-animal performance. However, there is great uncertainty about how important fatty acid composition is to the success of migration or whether particular types of fatty acids (e.g., omega-3 or omega-6) are most beneficial. Migratory bats provide an interesting example of evolutionary convergence with birds, which may provide evidence for the generality of the bird model to the evolution of migration by flight in vertebrates. Yet only recently have attempts been made to study bat migration physiology. Many aspects of their fuel metabolism are predicted to be more similar to those of migrant birds than to those of non-flying mammals. Bats may be distinct from most birds in their potential to conserve energy by using torpor between flights, and in the behavioral and physiological trade-offs they may make between migration and reproduction, which often overlap.     

Transition between moult and migration in a long-distance migratory passerine: organ flexibility in the African wintering area

Phenotypic flexibility of organs in migratory birds has been documented for a variety of species of different genera during the migratory period. However, very little is known about phenotypic mass changes of organs with respect to other events within the annual cycle. This seems particularly interesting when birds face different physiological challenges in quick succession. We investigated mass changes of 13 organs from garden warblers (Sylvia borin) during the transition from moult to migration. These long-distance migratory birds perform a complete moult within their wintering area just shortly before the onset of spring migration. Birds were sampled in three successive stages according to their moult status: group I consisted of birds with growing primary or secondary wing feathers, group II consisted of birds with completed wing moult but with still moulting body feathers, and group III consisted of birds that had completed wing moult and body moult. Size-corrected flight muscle, kidney mass, and pancreas mass differed significantly among the three groups. Flight muscle was heaviest in birds that were about to leave their wintering area (group III) compared with birds still in body moult (group II). Kidney and pancreas showed a pattern similar to each other, with the heaviest mass occurring in birds with moulting wing feathers (group I) and significantly reduced mass in birds that had completed wing moult (group II) or both wing and body moult (group III). Mass reductions of kidney and pancreas during the transition from moult to migration are considered to be related to the demands of moult, while increased flight muscle may be due to moult, migration, or both. Phenotypic mass changes of organs in birds occur during their migration, but they also occur during the transition between other phases of the annual cycle such as moult and migration and are not restricted to the flight muscle.     

Seasonal variation in body composition in an Afrotropical passerine bird: increases in pectoral muscle mass are,unexpectedly, associated with lower thermogenic capacity

Phenotypic flexibility in avian metabolic rates and body composition have been well-studied in high-latitude species, which typically increase basal metabolic rate (BMR) and summit metabolism (M_sum) when acclimatized to winter conditions. Patterns of seasonal metabolic acclimatization are more variable in lower-latitude birds that experience milder winters, with fewer studies investigating adjustments in avian organ and muscle masses in the context of metabolic flexibility in these regions. We quantified seasonal variation (summer vs winter) in the masses of organs and muscles frequently associated with changes in BMR (gizzard, intestines and liver) and M_sum (heart and pectoral muscles), in white-browed sparrow-weavers (Plocepasser mahali). We also measured pectoral muscle thickness using a portable ultrasound system to determine whether we could non-lethally estimate muscle size. A concurrent study measured seasonal changes in BMR and M_sum in the same population of sparrow-weavers, but different individuals. There was no seasonal variation in the dry masses of the gizzard, intestines or liver of sparrow-weavers, and during the same period, BMR did not vary seasonally. We found significantly higher heart (~ 18% higher) and pectoral muscle (~ 9% higher) dry mass during winter, although ultrasound measurements did not detect seasonal changes in pectoral muscle size. Despite winter increases in pectoral muscle mass, M_sum was ~ 26% lower in winter compared to summer. To the best of our knowledge, this is the first study to report an increase in avian pectoral muscle mass but a concomitant decrease in thermogenic capacity.

     

Phenotypic flexibility of body composition in relation to migratory state,age, and sex in the western sandpiper (Calidris mauri)

We investigated the flexibility of body composition in relation to seasonally variable demands for endurance flight capacity and hyperphagia in a migratory shorebird. Migrating western sandpipers were sampled in spring and fall while refueling at a north temperate stopover and were compared with nonmigrating birds captured at a tropical wintering area in Panama. Sandpipers weighed 25% more at stopover, and nearly 40% of migratory mass increase consisted of lean body components. Most organs and flight muscles were 10%-100% larger during migration, and the greatest relative size increases occurred in the digestive system (including liver). Birds preparing to initiate spring migration from Panama deposited only fat, suggesting that changes in lean body components take place after migration has begun, possibly through training effects. Sex did not influence body composition. Juveniles making their first southward migration were similar to adults in structural size and body mass but had substantially enlarged alimentary tracts. Sandpipers appeared to deposit lean mass during stopover in fall but not in spring. The dramatic enlargement of the digestive system in this small species that makes short flights and fuels frequently contrasts with the reduction of digestive components in larger species that fuel only once or twice by making one or two very long flights to their destination.     

Impact of hand-rearing on morphology and physiology of the capercaillie (Tetrao urogallus)

Morphological and physiological disparities between 20 captive and 11 wild capercaillies were determined. Birds, their pectoral and leg muscles, hearts, livers and gizzards were weighed. The length of small intestines and caeca were measured. Haemoglobin, haematocrit, glucose, triglycerides, total protein, uric acid and thyroid hormones as well as the cytochrome c-oxidase activity of the pectoral muscle and heart were determined. The glycogen and protein contents of pectoral and leg muscles and liver were analysed. Chemical composition (water, fat, protein, ash) of muscles and liver was determined. Captive males had heavier pectoral muscles than wild ones. The result was opposite in females. Wild birds had heavier hearts, livers, and gizzards, and also longer small intestines and caeca than captive birds. The cytochrome c-oxidase activity of pectoral muscle and heart was higher in wild than in hand-reared birds. The chemical composition of livers of wild birds differed significantly from that of hand-reared capercaillies. Plasma uric acid and T(4) concentrations were higher in captive than in wild birds. The observed differences in digestive system and liver can result in diminished ability of captive birds to utilise natural food nutrients. Decreased cytochrome c-oxidase activity of hand-reared birds can affect their takeoff and flying capacity and increase their vulnerability to predation. These facts may contribute to the low survival of hand-reared birds after release.     

An improved technique for estimating pectoral muscle protein condition from body measurements of live gulls

Body measurements, which could be taken from live birds, were used to estimate total pectoral muscle protein in Lesser Black-backed Gulls Larus fuscus. The maximum cross-sectional area of the flight muscles was measured from the profile of the muscle surface over the keel, and this was used in conjunction with the length of the flight muscle to estimate muscle volume. The estimate of muscle volume was then used with fresh body weight to estimate total flight muscle protein. A highly significant correlation was found between the estimated values and actual pectoral muscle protein mass determined by carcass analysis. The model developed from the source group was then validated using a second independent sample, in which flight muscle protein was estimated from the model. Carcass analysis again demonstrated a good correlation between estimated and actual total protein. Different methods of controlling for body-size to calculate protein condition from measures of total protein were considered. The technique described here provides a simple and reliable method of estimating pectoral muscle protein condition in live gulls which could be applied to studies of body condition in other species.     

Alterations in tissue aerobic capacity may play a role in premigratory fattening in shorebirds

Migratory shorebirds show regulated seasonal increases in body mass (BM) even in captivity, consisting primarily, but not exclusively, of fat. We examined whether captive red knot (Calidris canutus) exhibited seasonal alterations in mitochondrial volume (liver, pectoral muscle) and/or succinate dehydrogenase (SDH) activity (liver, pectoral muscle, heart, small intestine) during three distinct life-cycle stages: stable BM, spring peak in BM, and as BM rapidly declined after the spring peak. Mitochondrial volume in liver and pectoral muscle and SDH activity in liver and heart did not alter with life-cycle stage. However, red knot undergoing premigratory fattening exhibited significantly lower pectoral muscle SDH activity in concert with significantly elevated activity in the small intestine compared with the other two time-points, suggesting that tissue metabolic rate alters with life-cycle stage. The increased intestinal SDH activity may indicate an elevation in energy assimilation at a time when intestine hypertrophy occurs, thus maximizing BM increase prior to putative migration. The concomitant decrease in pectoral muscle activity may act to reduce overall metabolic rate, or at least help counter the elevation in intestinal mass-specific metabolic rate. Both tissues hypertrophy prior to migration in wild red knot, but hypertrophy of the intestine precedes that of pectoral muscle. Indeed, it appears that the intestinal mass undergoes atrophy by the time pectoral muscle hypertrophy occurs in wild red knot. Thus, physiological adjustments in tissue metabolism may be an important factor in the life-history strategies of migrating shorebirds.     

Regulation of protein breakdown and adrenocortical response to stress in birds during migratory flight

During long-term fasting at rest, protein utilization is maintained at low levels until it increases at a threshold adiposity. This study examines 1) whether such a shift in energy substrate use also occurs during endurance exercise while fasting, 2) the role of corticosterone, and 3) the adrenocortical response to an acute stressor. Ten species of migrating birds caught after an endurance flight over at least 500 km were examined. Plasma uric acid and corticosterone levels were low in birds with fat stores >5% of body mass and high in birds with smaller fat stores. Corticosterone levels were very high in birds with no visible fat stores and emaciated breast muscles. Corticosterone levels increased with handling time only in birds with large fat stores. These findings suggest that 1) migrating birds with appreciable fat stores are not stressed by endurance flight, 2) a metabolic shift (increased protein breakdown), regulated by an endocrine shift (medium corticosterone levels), occurs at a threshold adiposity, as observed in birds at rest, 3) adrenocortical response to an acute stressor is inhibited after this shift, and 4) an adrenocortical response typical for an emergency situation (high corticosterone levels) is only reached when muscle protein is dangerously low.     

Catabolic capacity of the muscles of shorebird chicks: maturation of function in relation to body size

Newly hatched precocial chicks of arctic shorebirds are able to walk and regulate their body temperatures to a limited extent. Yet, they must also grow rapidly to achieve independence before the end of the short arctic growing season. A rapid growth rate may conflict with development of mature function, and because of the allometric scaling of thermal relationships, this trade-off might be resolved differently in large and small species. We assessed growth (mass) and functional maturity (catabolic enzyme activity) in leg and pectoral muscles of chicks aged 1-16 d and adults of two scolopacid shorebirds, the smaller dunlin (Calidris alpina: neonate mass 8 g, adult mass 50 g) and larger whimbrel (Numenius phaeopus; neonate mass 34 g, adult mass 380 g). Enzyme activity indicates maximum catabolic capacity, which is one aspect of the development of functional maturity of muscle. The growth rate-maturity hypothesis predicts that the development of catabolic capacity should be delayed in faster-growing muscle masses. Leg muscles of both species were a larger proportion of adult size at hatching and grew faster than pectoral muscles. Pectoral muscles grew more rapidly in the dunlin than in the whimbrel, whereas leg muscles grew more rapidly in the whimbrel. In both species and in both leg and pectoral muscles, enzyme activities generally increased with age, suggesting increasing functional maturity. Levels of citrate synthase activity were similar to those reported for other species, but l-3-hydroxyacyl-CoA-dehydrogenase and pyruvate kinase (PK) activities were comparatively high. Catabolic capacities of leg muscles were initially high compared to those of pectoral muscles, but with the exception of glycolytic (PK) capacities, these subsequently increased only modestly or even decreased as chicks grew. The earlier functional maturity of the more rapidly growing leg muscles, as well as the generally higher functional maturity in muscles of the more rapidly growing dunlin chicks, contradicts the growth rate-maturity function trade-off and suggests that birds have considerable latitude to modify this relationship. Whimbrel chicks, apparently, can rely on allometric scaling of power requirements for locomotion and the thermal inertia of their larger mass to reduce demands on their muscles, whereas dunlin chicks require muscles with higher metabolic capacity from an earlier age. Thus, larger and smaller species may adopt different strategies of growth and tissue maturation.     

Catabolic enzyme activities in relation to premigratory fattening and muscle hypertrophy in the gray catbird (Dumetella carolinensis)

Summary The flight muscles of the gray catbird (Dumetella carolinensis) were examined to determine if short term adjustments occur in the activity of key catabolic enzymes during preparation for long distance migration. The aerobic capacity of the pectoralis muscle as indicated by citrate synthase activity (CS) is among the highest reported for skeletal muscle (200 moles [min·g fresh mass]^–1 at 25°C). The mass specific aerobic capacity as indicated by CS activity or cytochromec concentration does not change during premigratory fattening (Fig. 2) or in relation to the muscle hypertrophy that occurs concomitantly. The maintenance of mass specific aerobic capacity indicates that the total aerobic capacity increases in proportion to the increase in muscle size. The augmented potential for total aerobic power output is considered an adaptation to meet the increased power requirements of flight due to the increased body mass. Additionally, the capacity to oxidize fatty acids, as indicated by -hydroxyacyl-CoA dehydrogenase activity, approximately doubles during premigratory fattening (from 35 to 70 moles [min·g fresh mass]^–1 at 25°C; Fig. 1A). This adaptation should favor fatty acid oxidation, thereby sparing carbohydrate and prolonging endurance. The activity of phosphofructokinase, a key glycolytic enzyme, does not change before migration.Abbreviations CPT carnitine palmitoyl transferase - CS citrate synthase - HOAD -hydroxyacyl-CoA-dehydrogenase - PFK phosphofructokinase     

Flight responses by a migratory soaring raptor to changing meteorological conditions

Soaring birds that undertake long-distance migration should develop strategies to minimize the energetic costs of endurance flight. This is relevant because condition upon completion of migration has direct consequences for fecundity, fitness and thus, demography. Therefore, strong evolutionary pressures are expected for energy minimization tactics linked to weather and topography. Importantly, the minute-by-minute mechanisms birds use to subsidize migration in variable weather are largely unknown, in large part because of the technological limitations in studying detailed long-distance bird flight. Here, we show golden eagle (Aquila chrysaetos) migratory response to changing meteorological conditions as monitored by high-resolution telemetry. In contrast to expectations, responses to meteorological variability were stereotyped across the 10 individuals studied. Eagles reacted to increased wind speed by using more orographic lift and less thermal lift. Concomitantly, as use of thermals decreased, variation in flight speed and altitude also decreased. These results demonstrate how soaring migrant birds can minimize energetic expenditures, they show the context for avian decisions and choices of specific instantaneous flight mechanisms and they have important implications for design of bird-friendly wind energy.     

During stopover, migrating blackcaps adjust behavior and intake of food depending on the content of protein in their diets

During migration, birds undergo alternating periods of fasting and re-feeding that are associated with dynamic changes in body mass (m(b)) and in organ size, including that of the digestive tract. After arrival at a migratory stopover site, following a long flight, a bird must restore the tissues of its digestive tract before it can refuel. In the present study we examined how the availability of dietary protein influences refueling of migrating blackcaps (Sylvia atricapilla) during a migratory stopover. We tested the following predictions in blackcaps deprived of food and water for 1-2 days to induce stopover behavior: (1) birds provided with a low-protein diet will gain m(b), lean mass and fat mass, and increase in pectoral muscle size slower than do birds fed a high-protein diet; (2) since stopover time is shorter in spring, birds will gain m(b) and build up fat tissue and lean tissue faster than in autumn; and (3) if low dietary protein limits a bird's ability to gain m(b) and fat reserves, then birds that do not obtain enough protein will initiate migratory restlessness (Zugunruhe) earlier than will birds with adequate dietary protein. These predictions were tested by providing captured migrating blackcaps with semisynthetic isocaloric diets differing only in their protein content. Each day, we measured m(b), and food intake; also lean mass and fat mass were measured using dual energy X-ray absorptiometry. In addition, we monitored nocturnal activity with a video recording system. In both spring and autumn, birds fed diets containing either 3 or 20% protein increased in m(b), lean mass and fat mass at similar rates during the experiment. However, the group receiving 3% protein ate more than did the group receiving 20% protein. In support of our predictions, m(b), lean mass, fat mass, and intake of food all were higher in spring than in autumn. We also found that in spring all birds had higher levels of migratory restlessness, but birds fed 3% protein were less active at night than were birds fed 20% protein, possibly an adaptation conserving energy and protein. We conclude that protein requirements of migrating blackcaps during stopover are lower than expected, and that birds can compensate for low dietary protein by behavioral responses, i.e. hyperphagia and decreased migratory restlessness, that ensure rapid refueling.     

Increased oxidative capacity in skeletal muscles from cold-acclimated ducklings: a comparison with rats

1. The effects of prolonged cold exposure on cytochrome oxidase activity were investigated in skeletal muscles, liver and adipose tissues from cold-acclimated (CA) and control (TN) ducklings and rats. 2. Cold acclimation increased the oxidative capacity of skeletal muscles (+33% in gastrocnemius and +195% in pectoral) and liver (+47%) from CA ducklings, but decreased the oxidative capacity of gastrocnemius muscle (-22%) from CA rats. On the other hand, in these CA rats it increased the oxidative capacity of liver by 88% and, above all, brown adipose tissue by 544%. 3. The significance of these changes due to acclimation to cold in ducklings and rats is discussed. Such an increase in oxidative capacity of CA duckling muscles may explain the non-shivering thermogenesis observed in these birds.