Metabolic profile of long-distance migratory flight and stopover in a shorebird

Migrating birds often complete long non-stop flights during which body energy stores exclusively support energetic demands. The metabolic correlates of such long-distance travel in free-living migrants are as yet poorly studied. Bar-tailed godwits, Limosa lapponica taymyrensis, undertake a 4500 km flight to their single spring stopover site and thus provide an excellent model in which to determine the energy fuels associated with endurance travel. To this end, we evaluated plasma concentrations of six key metabolites in arriving godwits caught immediately upon landing near their stopover site. Initial metabolite levels were compared with levels after 5 h of inactive rest to determine how flight per se affects energy metabolism. Birds refuelling on the stopover site were also examined. Arriving godwits displayed elevated plasma free fatty acids, glycerol and butyrate, confirming the importance of lipid fuel in the support of extended migratory activity. Further-more, elevated plasma triglycerides in these birds suggest that fatty acid provisioning is facilitated through hepatic synthesis and release of neutral lipids, as previously hypothesized for small migrants with high mass-specific metabolic rates. Finally, elevations in plasma uric acid suggest that protein breakdown contributes to the support of long-distance movement, to possibly maintain citric acid cycle intermediates, gluconeogenesis and/or water balance.     

Sex promotes spatial and dietary segregation in a migratory shorebird during the non-breeding season

Several expressions of sexual segregation have been described in animals, especially in those exhibiting conspicuous dimorphism. Outside the breeding season, segregation has been mostly attributed to size or age-mediated dominance or to trophic niche divergence. Regardless of the recognized implications for population dynamics, the ecological causes and consequences of sexual segregation are still poorly understood. We investigate the foraging habits of a shorebird showing reversed sexual dimorphism, the black-tailed godwit Limosa limosa, during the winter season, and found extensive segregation between sexes in spatial distribution, microhabitat use and dietary composition. Males and females exhibited high site-fidelity but differed in their distributions at estuary-scale. Male godwits (shorter-billed) foraged more frequently in exposed mudflats than in patches with higher water levels, and consumed more bivalves and gastropods and fewer polychaetes than females. Females tended to be more frequently involved and to win more aggressive interactions than males. However, the number of aggressions recorded was low, suggesting that sexual dominance plays a lesser role in segregation, although its importance cannot be ruled out. Dimorphism in the feeding apparatus has been used to explain sex differences in foraging ecology and behaviour of many avian species, but few studies confirmed that morphologic characteristics drive individual differences within each sex. We found a relationship between resource use and bill size when pooling data from males and females. However, this relationship did not hold for either sex separately, suggesting that differences in foraging habits of godwits are primarily a function of sex, rather than bill size. Hence, the exact mechanisms through which this segregation operates are still unknown. The recorded differences in spatial distribution and resource use might expose male and female to distinct threats, thus affecting population dynamics through differential mortality. Therefore, population models and effective conservation strategies should increasingly take sex-specific requirements into consideration.     

Pay-offs and penalties of competing migratory schedules

We relate variation in the timing of arrival by migrating birds breeding at northerly latitudes to individual differences in the prior accumulation of energy stores. Balancing starvation risks early in the season against the almost universal declining trend in reproductive prospects with advancing date is seen as an individual decision with fitness consequences. We review three studies implicating events at the staging sites or in winter in setting the individual migratory schedule. Climate change influences the timetable of a pied flycatcher (Ficedula hypoleuca) population breeding in The Netherlands and wintering in West Africa, followed since 1960. Mean air temperature in the period mid April‐mid May (arrival and laying) increased and laying date advanced by 10 days. Still, in recent years most birds did not lay early enough to maximise fitness (determined by recruitment and parental survival) whereas many parents achieved this goal in 1980–1985. As the flycatchers have not started to arrive earlier, some ecological constraint further upstream is postulated (possibly the hurdle of the crossing of Sahara and Mediterranean). The ability to follow individual migrants provides a second avenue to assess the fitness implications of migratory schedules. Thus, brightly coloured male bar‐tailed godwits (Limosa lapponica) captured in the Dutch Wadden Sea (the intermediate staging site linking a West African wintering area with breeding sites in arctic Russia) and traced with miniature radio‐transmitters did not depart early. The ‘best’ males (with bright breeding plumage) were picked up by the listening stations in Sweden 650 km further along the migratory route ten days later than the paler individuals. If early arrival confers the competitive advantage of prior occupancy but increases mortality, the ‘best’ males may be able to afford arriving later and thus avoid some of the survival costs. Return rate of the ‘bright’ males to the staging site in later seasons was indeed higher than for the ‘pale’, early males. Intensive observation of pink‐footed geese (Anser brachyrhynchus) fitted with coded neck‐collars substantiate the tight relationship between energy stores (fat) accumulated up to final departure from the final staging site (Vesterålen, N. Norway) en route to the nesting grounds (Spitsbergen) and subsequent success. The breeding outcome of individual parents (accompanied by juveniles or not) could be related to observations of body condition before departure (visual ‘abdominal profile index’). Recently, perceived conflicts with agriculture have resulted in widespread harassment by humans. The geese have: drastically shortened their stay on the Vesterålen, fail to achieve the body condition usual a decade ago and reproductive output has fallen. Although the geese are currently pioneering new staging sites, an adequate alternative has not materialised, underlining the critical role of the final take‐off site.     

Seasonal dynamics of flight muscle fatty acid binding protein and catabolic enzymes in a migratory shorebird

We developed an ELISA to measure heart-type fatty acid binding protein (H-FABP) in muscles of the western sandpiper (Calidris mauri), a long-distance migrant shorebird. H-FABP accounted for almost 11% of cytosolic protein in the heart. Pectoralis H-FABP levels were highest during migration (10%) and declined to 6% in tropically wintering female sandpipers. Premigratory birds increased body fat, but not pectoralis H-FABP, indicating that endurance flight training may be required to stimulate H-FABP expression. Juveniles making their first migration had lower pectoralis H-FABP than adults, further supporting a role for flight training. Aerobic capacity, measured by citrate synthase activity, and fatty acid oxidation capacity, measured by 3-hydroxyacyl-CoA-dehydrogenase and carnitine palmitoyl transferase activities, did not change during premigration but increased during migration by 6, 12, and 13%, respectively. The greater relative induction of H-FABP (+70%) with migration than of catabolic enzymes suggests that elevated H-FABP is related to the enhancement of uptake of fatty acids from the circulation. Citrate synthase, 3-hydroxyacyl-CoA-dehydrogenase, and carnitine palmitoyl transferase were positively correlated within individuals, suggesting coexpression, but enzyme activities were unrelated to H-FABP levels.     

Consistent avoidance of human disturbance over large geographical distances by a migratory bird

Recent work on animal personalities has demonstrated that individuals may show consistent behaviour across situations and contexts. These studies were often carried out in one location and/or during short time intervals. Many animals, however, migrate and spend their life in several geographically distinct locations, and they may either adopt behaviours specific to the local environment or keep consistent behaviours over ecologically distinct locations. Long-distance migratory species offer excellent opportunities to test whether the animals maintain their personalities over large geographical scale, although the practical difficulties associated with these studies have hampered such tests. Here, we demonstrate for the first time consistency in disturbance tolerance behaviour in a long-distance migratory bird, using the common crane Grus grus as an ecological model species. Cranes that hatched in undisturbed habitats in Finland choose undisturbed migratory stop-over sites in Hungary, 1300-2000 km away from their breeding ground. This is remarkable, because these sites are not only separated by large distances, they also differ ecologically: the breeding sites are wooded bogs and subarctic tundra, whereas the migratory stop-over sites are temperate zone alkaline grasslands. The significance of our study goes beyond evolutionary biology and behavioural ecology: local effects on behaviour may carry over large distances, and this hitherto hidden implication of habitat selection needs to be incorporated into conservation planning.     

Highly pathogenic avian influenza virus H5N1 infection in a long-distance migrant shorebird under migratory and non-migratory states

Corticosterone regulates physiological changes preparing wild birds for migration. It also modulates the immune system and may lead to increased susceptibility to infection, with implications for the spread of pathogens, including highly pathogenic avian influenza virus (HPAIV) H5N1. The red knot (Calidris canutus islandica) displays migratory changes in captivity and was used as a model to assess the effect of high plasma concentration of corticosterone on HPAIV H5N1 infection. We inoculated knots during pre-migration (N = 6), fueling (N = 5), migration (N = 9) and post-migration periods (N = 6). Knots from all groups shed similar viral titers for up to 5 days post-inoculation (dpi), peaking at 1 to 3 dpi. Lesions of acute encephalitis, associated with virus replication in neurons, were seen in 1 to 2 knots per group, leading to neurological disease and death at 5 to 11 dpi. Therefore, the risk of HPAIV H5N1 infection in wild birds and of potential transmission between wild birds and poultry may be similar at different times of the year, irrespective of wild birds'' migratory status. However, in knots inoculated during the migration period, viral shedding levels positively correlated with pre-inoculation plasma concentration of corticosterone. Of these, knots that did not become productively infected had lower plasma concentration of corticosterone. Conversely, elevated plasma concentration of corticosterone did not result in an increased probability to develop clinical disease. These results suggest that birds with elevated plasma concentration of corticosterone at the time of migration (ready to migrate) may be more susceptible to acquisition of infection and shed higher viral titers—before the onset of clinical disease—than birds with low concentration of corticosterone (not ready for take-off). Yet, they may not be more prone to the development of clinical disease. Therefore, assuming no effect of sub-clinical infection on the likelihood of migratory take-off, this may favor the spread of HPAIV H5N1 by migratory birds over long distances.     

Adjustment of the annual cycle to climatic change in a long-lived migratory bird species

Climate change has advanced the phenology of many organisms. Migratory animals face particular problems because climate change in the breeding and the wintering range may be asynchronous, preventing rapid response to changing conditions. Advancement in timing of spring migration may have carry-over effects to other parts of the annual cycle, simply because advancement of one event in the annual cycle also advances subsequent events, gradually causing a general shift in the timing of the entire annual cycle. Such a phenotypic shift could generate accumulating effects over the years for individuals, but also across generations. Here we test this novel hypothesis of phenotypic response to climate change by using long-term data on the Arctic tern Sterna paradisaea. Mean breeding date advanced by almost three weeks during the last 70 years. Annual arrival date at the breeding grounds during a period of 47 years was predicted by environmental conditions in the winter quarters in the Southern Ocean near the Antarctic and by mean breeding date the previous year. Annual mean breeding date was only marginally determined by timing of arrival the current year, but to a larger extent by arrival date and breeding date the previous year. Learning affected arrival date as shown by a positive correlation between arrival date in year (i+1) relative to breeding date in year (i) and the selective advantage of early breeding in year (i). This provides a mechanism for changes in arrival date being adjusted to changing environmental conditions. This study suggests that adaptation to changing climatic conditions can be achieved through learning from year to year[Current Zoology 55(2):92-101,2009].     

Permanent female mimics in a lekking shorebird

Female mimics are known from many species, but permanent, non-conditional, alternative mating strategies are only known from an isopod, a fish, a lizard and a bird. The single bird example refers to lek-breeding ruffs Philomachus pugnax, a shorebird for which two strategies (independent and satellite) have been known for over 50 years. Ruffs also provided the single case of an animal with two, rather than three, permanent alternative mating strategies. Here, we describe a rare female-like morph of ruffs: the 'missing' third alternative mating strategy, which we have called 'faeder'. Faeders are slightly larger than females and in late April have testes 2.5 time the size of testes of normal males. On leks in aviaries and in the wild they appear to combine feminine and masculine behaviours. Faeders may represent the ancestral, care-giving, male strategy, but their relatively large testes suggest that currently they behave as sneakers.     

Differential annual movement patterns in a migratory species: effects of experience and sexual maturation

Some animals migrate long distances to exploit important seasonal food resources in the northern regions of the northern hemisphere, whilst avoiding winter starvation. Changes in the individual's age and navigational skills are likely to affect migration, which in turn influences the geographic distribution of individuals. Processes such as sexual maturation and navigational abilities are affected by age, and age is thus a key factor in understanding migration patterns and differences in distribution ranges. In the present study, we investigated the effects of age on the geographic distribution of a population of Lesser Black-backed Gulls Larus fuscus throughout its annual cycle, by analyzing a dataset of 19,096 records from 10,000 color-ringed gulls. In contrast to previous assumptions, the results showed that gulls were geographically segregated by age throughout the entire annual cycle, rather than showing a geographic age-related cline only in the wintering areas. This asymmetric distribution results from a reduction in the annual range of sexually mature gulls, and the differential distribution of mature and immature individuals (mature birds remained in more northern areas, compared to immature birds, throughout the annual cycle). Furthermore, although immature gulls travelled longer distances than adults, they initiated their fall migration with short movements, in contrast to adults that migrated using longer movements. The effects identified in this study explain the non-homogenous distribution of populations throughout the annual cycle, with wide implications for the development of effective human health policies and/or wildlife management strategies.     

Test of a digestion optimization model: effect of variable-reward feeding schedules on digestive performance of a migratory bird

Birds on migration often alternate between feeding and nonfeeding periods, in part because food resources may be patchily distributed and in part because birds on migration may adopt a risk-prone foraging strategy characterized by selection of variable rather than constant food rewards. Optimal digestion models predict that increases in intermeal interval like those encountered by some migratory birds should result in longer retention time of digesta and higher digestive efficiency if birds are maximizing their rate of energy intake. We tested these predictions by comparing residence time of digesta and extraction efficiency of lipid for captive yellow-rumped warblers (Dendroica coronata) feeding adlibitum and when we added intervals of time when the birds received no food. We increased the likelihood that the warblers were maximizing their rate of energy intake by increasing light levels during spring to induce hyperphagia (treatment birds (16L:8D light: dark cycle) ate 2.13 ± 0.14 g dry food day⁻¹ (n = 8) while control birds (10L:14D) ate 1.25 ± 0.03 g dry food day⁻¹ (n = 6)). Treatment birds offered food only every other 2–3 h ate 50% more during the 4-h test period than when they were always feeding adlibitum. Despite these differences in food intake, extraction efficiency of glycerol trioleate remained high and constant (93%), and mouth-to-anus total mean retention time (TMRT) did not change (overall mean: 54.8 ± 6.0 min). Residence time of lipid in the stomach increased whereas residence time of lipid in the intestine decreased when birds fed only every other 2–3 h compared to when birds always fed ad libitum. None of the results were consistent with the predictions of the optimal digestion model unless we assume that birds were minimizing their feeding time rather than maximizing their rate of energy gain. Furthermore, the ability of yellow-rumped warblers to maintain high extraction efficiency with no change in TMRT suggests some spare digestive capacity when food intake increases by as much as 50%. Received: 14 June 1997 / Accepted: 20 November 1997     

The role of the Ghana coast in the annual cycle of migratory terns

Ntiamoa-Baidu, Y. & Nuoh, A. A. 2000. The role of the Ghana coast in the annual cycle of migratory terns. Ostrich 71 (1 & 2): 183.

Data are presented on counts of migratory terns on the Ghana coast over a ten-year period, 1986–1996. Fourteen species of terns were recorded during the period. Influx of terns begins in late August, peaking in September/October, with the highest likelihood of tern occurrence on the Ghana coast recorded in August-November and April-May. Terns fed mostly offshore and used the coastal lagoons as roosting sites, although a few species e.g. Black Tern Chlidonias niger and Little Tern Sterna albifrons, foraged also on the lagoons. Two sites, Songor Lagoon and Densu Delta, regularly held over 50 % of the total count recorded for all sites. A comparison of the day-time counts with dusk roost counts indicate that the day time counts under-represent the total numbers of terns using the Ghana coast. Trends in the populations of the four most abundant tern species: Black Tern, Common Tern Sterna hirundo, Sandwich Tern S. sandvicensis and Royal Tern S. maxima, are analysed; and the implications for conservation of the species are discussed.     

Lower annual fecundity in long-distance migrants than in less migratory birds of temperate Europe

We use widely supported handbook data on annual fecundity (clutch size × annual number of normal broods) to obtain indications related to the relative costs of long-distance migration compared to lower levels of migratoriness. Our examples show that the yearly production of eggs in congeneric passerines of similar size from temperate Europe is lower in long-distance migrants than in their less migratory relatives. The same tendency shows up in a more heterogeneous sample of non-passerines. In most passerines and in one among five pairs of non-passerines, this is due to longer breeding periods allowing a higher number of clutches in the less migratory species in spite of a tendency towards larger clutches in the passerine long-distance migrants. If both migratory types have only one clutch (as in one species pair of the passerines and in four non-passerine pairs) the trend towards larger clutches was reversed between the two types. The higher fecundity of the less migratory species suggests that wintering under harsh conditions may be more expensive than trans-Sahara migration among similar species. In keeping with this result, Ortolan and Rock Buntings (Emberiza hortulana and E. cia) breeding syntopically (and, in the 1980s, still in relatively stable populations) in an inner Alpine valley provide a well-studied example illustrating the high longevity of the migrants compared to the relatively short life span of the residents.     

Metabolic consequences of overlapping food restriction and cell‐mediated immune response in a long‐distance migratory shorebird,the little ringed plover Charadrius dubius

Investment in immunity is commonly viewed as an energetically costly activity in birds. Although several studies have focused on the energy cost of mounting an immune response and its concomitant physiological trade‐offs, nothing is known about the metabolic adjustments experienced by immunochallenged birds under resource limitation, or about the basal metabolism cost of mounting cell‐mediated immune (CMI) responses in bird species other than non‐migratory passerines. Here we measured the basal metabolic rate (BMR), inflammatory response, and body mass in ad libitum fed and food‐restricted little ringed plovers Charadrius dubius challenged with phytohemagglutinin (PHA) in order to assess the energy cost, the strength, and the time course of the CMI response in a long‐distance migratory bird in different nutritional states. We found that ad libitum birds injected with PHA significantly increased both mass‐independent BMR and inflammatory response, whereas birds with an induced food restriction‐immune response overlap experienced a mass‐independent BMR downregulation and decreased inflammatory response relative to ad libitum birds. We suggest that both the BMR downregulation and the diminished inflammatory response observed in birds facing such an overlap could be energy‐saving mechanisms to maintain the body mass above a critical level and maximize fitness.     

Climatic connectivity between Africa and Europe may serve as a basis for phenotypic adjustment of migration schedules of trans-Saharan migratory birds

Most European migratory birds wintering in sub‐Saharan Africa have anticipated arrival to the breeding areas over the past decades. This phenological change may be ultimately caused by warming of the Northern Hemisphere via evolutionary changes or phenotypic plasticity in migration behavior. First arrival dates are negatively predicted by temperatures upon arrival to the breeding grounds. This seems puzzling, because migrants should be unable to predict weather conditions at long range. Migrants can enjoy diverse fitness benefits from early arriving. However, if weather conditions at destination cannot be predicted, early arrival can also entail severe costs. If meteorological conditions in Europe during breeding covary with those in sub‐Saharan Africa during late winter, long‐distance migrants may have a clue to predict meteorological conditions in their breeding areas while they are still in Africa and adjust their migration schedule consequently, an idea that has never been tested. We analyzed the correlation between March–April temperature anomalies (T_an) in Europe and February T_an in the Sahel and sub‐Sahel, where long‐distance migrants winter or stop‐over. T_an in Africa negatively predicted T_an in Europe, the association being particularly strong (unsigned effect size, z_r>0.35) for eastern Sahel and northern and eastern Europe, where the risks of early arrival may be larger. However, the strength of the correlations between T_an in the two continents has declined during the last 25 years; thus, possibly, partly compromising adaptive mechanisms of adjustment of migration. The existence of such climatic connectivity leads to several predictions, including that positive T_an in Africa should delay arrival. Consistent with this prediction, we found that first arrival dates of seven long‐distance migratory species positively covaried with February T_an in Africa. Thus, while wintering, migrants might be able to predict meteorological conditions at the beginning of the breeding season, and phenotypically adjust migration schedules to optimally tune arrival date.     

Prey abundance and the strength of interference in a foraging shorebird

Interference is an important component of food competition but is often difficult to detect and measure in natural animal populations. Although interference has been shown to occur between oystercatchers Haematopus ostralegus L. feeding on mussels Mytilus edulis L., four previous studies have not detected interference between oystercatchers feeding on cockles Cerastoderma edule L. In contrast, this study detected interference between cockle-feeding oystercatchers in the Baie de Somme, France. Prey stealing (kleptoparasitism), one of the main causes of interference between mussel-feeders, also occurred between oystercatchers in the Baie de Somme. The kleptoparasitism rate was related to the natural variation in the food supply, tending to be higher when cockles were rare. Feeding rate was negatively related to competitor density, so providing evidence for interference, but, as in mussel-feeders, only above a threshold density of about 50–100 birds ha⁻¹. The strength of interference at a fixed competitor density was related to the cockle food supply, usually being greater when cockles were rare. Previous studies probably failed to detect interference between cockle-feeders because competitor densities were too low, or cockles were too abundant, or because they were not conducted during late winter when interference is most intense. The study shows that natural variation in the food supply can influence the strength of interference within an animal population and provides support for those behaviour-based interference models which predict that the strength of interference will be greatest when competitor densities are high and prey scarce.     

Reconstructing an annual cycle of interaction: natural infection and antibody dynamics to avian influenza along a migratory flyway

Migratory animals may play an important role in connecting disparate ecosystems, including the introduction of various pathogens. The incidence of these pathogens may vary over time and space, such that events along the entire migratory flyway are likely to be important in the interaction between pathogens and their migratory hosts. On this premise, the annual cycle of a naturally occurring host–pathogen system was reconstructed by examining infection with and antibodies to avian influenza virus along the flyway of a long‐distance Arctic migrant, the Svalbard‐breeding pink‐footed goose Anser brachyrhynchus. A highly‐localized transmission period was identified in winter, in contrast to the north–south decline expected from dabbling ducks, indicating the dynamics of infection may differ among host species. In spring, 63% (95% CI: 57.1, 68.9) of adults had detectable antibodies to the nucleoprotein of avian influenza virus, compared to just 15% (95% CI: 8.7, 23.4) of juveniles, suggesting inter‐annual antibody maintenance. Nevertheless, adult seroprevalence declined by approximately 30% from spring to late summer, indicating significant seroreversion in the population. Integrating these findings in an epidemiological model, detectable antibodies to nucleoprotein were estimated to persist for just 343 days (95% CI: 221, 607); considerably shorter than for other wildlife diseases in long‐lived bird species. The investigation of wildlife diseases in migratory populations is an inherently complex task, yet, by integrating disease incidence and seroprevalence along a migratory flyway, our findings suggest that the ecological interactions and life history of the host, as well as the life‐history of the pathogen, can influence the dynamics of infection and host immune response.