Differentiating between stopover and staging sites: functions of the southern and northern Yellow Sea for long‐distance migratory shorebirds

Evidence‐based protection of migratory birds at flyway levels requires a solid understanding of their use of ‘stopping sites’ during migration. To characterize the site use of northward‐migration great knots Calidris tenuirostris in China, we compared length of stay and fuel deposition during northward migration at areas in the south and the north of the Yellow Sea, a region critical for migrating shorebirds. Radio‐tracking showed that at the southern site great knots stayed for only short periods (2.3 ± 1.9 d, n = 40), and bird captures showed that they did not increase their mean body mass while there. In the north birds stayed for 1 month (31.0 ± 13.6 d, n = 22) and almost doubled their mean body mass. Fuel consumption models suggest that great knots departing from the northern Yellow Sea should be able to fly nonstop to the breeding grounds, whereas those from the south would require a refueling stop further north. These results indicate that the study sites in the northern and southern Yellow Sea serve different roles: the southern site acts as a temporary stopover area that enables birds with low fuel stores to make it to main staging areas further north, while the northern site serves as the critical staging site where birds refuel for the next leg of their migration. The rapid turnover rate in the southern Yellow Sea indicates that many more birds use that area than are indicated by peak counts. Differential use of the southern and northern sites indicates that both play crucial roles in the ability of great knots to migrate successfully.     

Timing of nocturnal autumn migratory departures in juvenile European robins (Erithacus rubecula) and endogenous and external factors

Many passerine medium distance nocturnal migrants take off from stopover sites not only at the beginning of the night, but also in the middle and at the end of the night. In this paper, we tested two explanations for this phenomenon: (1) that departure time is governed by fuel stores, and (2) that departure time is influenced by the weather. The relationship of temporal distribution of migratory nocturnal departures with body condition and weather factors was studied in juvenile European robins (Erithacus rubecula) during autumn migration. The study was done on the Courish Spit on the Baltic Sea in 1997–2003 by retrapping 74 ringed birds in high mist nets during nocturnal migratory departure. Departure time was not related to fuel stores at arrival and departure, stopover duration, fuel deposition rate or progress of the season. Nor did the local weather at departure influence departure time. A possible reason was a large variation in the behaviour of the birds. European robins which made 1-day stopovers arrived and departed during better weather conditions than birds that stopped over for longer periods. In the former cohort, a significant model with four predictors explained 55% of variation in departure time. It is assumed that weather at the night of departure and during the previous night influenced the time of take-offs in these birds. In robins which made long stopovers, departure time is probably governed by their individual endogenous circadian rhythms of activity, which are related to the environment in a complex way.     

Temporal and spatial variation in dispersal in the greater flamingo (Phoenicopterus ruber roseus)

We studied movements of individually marked greater flamingos (Phoenicopterus ruber roseus) born in the Camargue, southern France, between their two most important breeding colonies in the western Mediterranean (Camargue and Fuente de Piedra, Spain) from 1986 to 1992. The two sites differ in the frequency with which they offer suitable conditions for breeding. Flamingos have bred each year in the Camargue since 1974, but in only 12 of the past 22 years at Fuente de Piedra. Higher colony fidelity is thus expected in the less variable environment (Camargue), but if dispersal occurs competition might be an important factor causing this dispersal. Following years during which breeding birds in the Camrgue were disturbed (1988 and 1990) a higher proportion of adults changed colonies between breeding attempts (= breeding dispersal, 12.4%), while only 0.4% of flamingos breeding in the Camargue dispersed in the other years. As expected, flamingos breeding at Fuente de Piedra showed a higher rate of breeding dispersal (8.14%). No differences were observed between males and females. The importance of breeding failure as a factor causing breeding dispersal in flamingos was also confirmed by the movements of individual birds. The proportion of young flamingos that moved from their natal colony to start breeding at Fuente de Piedra (= natal dispersal) was independent of sex and age, but increased when breeding access to the Camargue colony was more difficult. However, natal dispersal was also higher in 1988 and 1990 (40.5%) than in the remaining years (1.2%), as was breeding dispersal. We discuss possible ways in which the increased natal dispersal among inexperienced birds could be linked with the increased breeding dispersal of adults in the same year.     

Wide ranging stopover movements and substantial fuelling in first year garden warblers at a northern stopover site

Migratory birds use stopovers to replenish their fuel reserves and they generally spend more time at stopover sites than they do in actual flight. When arriving at a new stopover site birds may need to search extensively to find a suitable feeding area and this search and settling period may affect the duration of stopover. Stopover behaviour can thus have profound effects on the migratory programme and studies on stopover behaviour are important to understand migratory strategies. We followed 51 first‐year garden warblers Sylvia borin with radio‐transmitters at an autumn stopover site on the island of Gotland in southern Sweden. Our aim was to determine the distance birds relocated from the coastal capture site when searching for an area to settle in, and also to establish the duration of stopover and put it in relation to refuelling rate by recapturing a subset of the radio‐tracked individuals. Sixteen birds made an extended stopover (> 2 d), relocated inland from the capture site and settled on average 5.6 km from the capture site, with the longest recorded relocation being fourteen kilometres. Birds that relocated nocturnally settled in areas further away than birds that relocated diurnally. Thirteen birds that continued migration after a short stop carried larger fuel stores than birds that stopped over longer and they remained close to the capture site until departure. Three birds were re‐trapped and showed high fuelling rates, between 0.3 and 1.1 g d^–1. They left the stopover site with fuel loads between 40–56 percent of lean body mass, which possibly would have allowed them to reach the Mediterranean area without additional refuelling stops.     

Field evidence of dispersal of branchiopods, ostracods and bryozoans by teal (Anas?crecca) in the Camargue (southern France)

Invertebrate propagules may survive internal and external transports by waterbirds, thus facilitating their dispersal between aquatic habitats. However, field data on such transport remain limited, especially for exozoochory. We quantified and compared the rates of internal and external invertebrate transports simultaneously in a wintering population of teal (Anas crecca) in the Camargue (southern France). We inspected lower gut (rectum) contents of birds that had been shot (N = 366) and washed birds that had been live-trapped (N = 68) during the winters 2006–2007 and 2007–2008. At least one propagule was recorded in 2.5% and 10.3% of internal and external samples, respectively. Cladoceran, ostracod, plumatellid bryozoan and anostracan propagules were all recorded in both internal and external samples. Hatching confirmed their viability, except for anostracan eggs. At least three cladoceran species and two ostracod species were recorded, none of which had previously been shown to be dispersed by birds. Amongst external samples, we recorded a significant seasonal trend in 1 year with most propagules recorded before December, keeping with a seasonal decline in the availability of propagules on the water surface. This study provides evidence that teal may be important vectors of invertebrate dispersal both within the Camargue and along migratory flyways.     

Prevalence of West Nile virus neutralizing antibodies in wild birds from the Camargue area, southern France

The Camargue area of southern France experienced the re-emergence of West Nile Virus (WNV) in the late summer of 2000 and 2004. Immediately preceding the 2004 outbreak, samples were collected from 432 birds of 32 different species captured in mist nets and from 201 Cattle Egret (Bubulcus ibis) nestlings sampled in their nests between 1 April and 12 June 2004. West Nile virus neutralizing titers of >/=40 were detected in 4.8% (95% confidence limit, 2.9-7.5%) of the adult birds and in 1.6% (0.3-4.6%) of the egret nestlings. Migratory passerines had a higher prevalence of WNV neutralizing antibodies (7.0%) than did resident and short-distance migratory passerines (0.8%), suggesting exposure to WNV or a related flavivirus during overwintering in Africa.     

Determining the boundaries of migratory bird flyways: a Bayesian model for Eurasian teal Anas crecca in western Europe

Accurate flyway delineation is a prerequisite for effective conservation and management of migratory bird populations, yet such limits have so far mostly been set subjectively. We present a statistical method to infer population boundaries from the analysis of ring recoveries, using a Bayesian framework. The approach was applied to Eurasian teal Anas crecca ringed in Camargue, southern France, and Abberton Reservoir, Essex, eastern England. The results presented show the boundaries of the two teal flyways in western Europe, with a zone of overlap, broadly matching those previously defined. The percentage of teal switching flyways (abmigration rate) was 2.4–2.6%, greater in birds ringed as juveniles than as adults. Abmigrants ended up at sites within the other flyway where the density of local birds was lower than expected by chance, suggesting abmigration resulted from exploratory or aberrant behaviour. The methodology presented here can be used to infer flyway boundaries of any bird with an adequate ring‐re‐encounter dataset, which has crucial consequences for the evaluation of their trends in abundance and hence conservation status, and the management of sustainable harvests.     

A new exploratory approach to the study of the spatio-temporal distribution of ring recoveries: the example of Teal (Anas crecca) ringed in Camargue, Southern France

We use a new method called “product kernel estimator” to explore the spatial and temporal distribution of 9,114 recoveries of Teal (Anas crecca) ringed in Camargue, southern France, and recovered over the whole of Europe. This method allows exploration of the changes in time of the probability density to recover a ringed bird over a grid covering the study area. We thus identified two migration corridors for this species to the north and south of the Alps, whereas earlier analyses mostly suggested a southern route from Camargue, especially in spring. The northern route seems to be used to a greater extent in autumn than in spring, indicating a frequent abmigration (animals switching from one corridor to the other). Moreover, migration of the population seems faster in spring than in autumn. The simultaneous presence of Teal recoveries in many distinct geographical areas in spring is consistent with the idea that these ducks are not limited by their migratory speed in spring, nor do they wait until favorable environmental conditions before colonizing their breeding areas.     

Effects of migration distance and sex on stopover timing and refueling by Wilson's Warblers

Migration distance and sex are integral to avian migration strategies, yet these intrinsic factors are understudied with respect to their effects on stopover ecology and behavior. We investigated how individual variation in migration distance and sex affected body condition, refueling performance, and stopover durations of Wilson's Warblers (Cardellina pusilla) during spring and fall 2006 at a stopover site in southern Arizona. Migration distance of individuals was inferred using the hydrogen stable isotope ratio of feathers (δ²H_f) as an index of breeding latitude, refueling rate was assessed using plasma triglyceride and β‐OH‐butyrate, and minimum length of stay was estimated by re‐sighting color‐banded birds. In the spring, migration distance and sex were strong determinants of the timing of migration by Wilson's Warblers, with males and shorter‐distance migrants passing through the site earlier than females and longer‐distance migrants. Later‐arriving migrants also had higher fat scores and refueling rates. However, neither migration distance nor sex independently affected body condition (fat score or size‐corrected mass), refueling rate, or minimum length of stay. In a smaller sample of fall migrants, we found that longer‐distance migrants and males had higher refueling rates than shorter‐distance migrants and females. Our results show that differences in migration distance can, under some circumstances, affect how birds use stopover sites. Stable isotope analysis and other methods can provide information on migration distance, and should be integrated with measurements of timing, fuel stores, refueling performance, and departure behavior to gain a deeper understanding of bird migration.     

Optimal fat loads and long-distance flights by migrating Knots Calidris canutus, Sanderlings C. alba and Turnstones Arenaria interpres

Arctic waders often build up large fat loads and complete their migratory journeys by a few long-distance flights between traditional staging sites. Optimal fat loads and choices of staging sites differ depending on whether the birds are adapted to minimize energy or time spent on migration. In the latter case, we predict that the birds will depart for the next staging site when the instantaneous speed of migration expected after arrival at the next site, exceeds the corresponding speed at the departure site. The instantaneous migration speed is a function of the rate of fat deposition and the current fat load. As a consequence of this, overloading (birds deposit larger fat loads than needed merely for covering the flight distance to the next destination) and by-passing of possible, but low-quality staging sites, are expected under specific conditions in time-selected migration.
Estimates of fat deposition rates and departure fat loads were obtained by captures of Knots Calidris canutus , Sanderlings C. alba and Turnstones Arenaria interpres in W. Iceland during spring migration. Further fat deposition data referring to spring migration of these species were compiled from the literature. Fat deposition rates at different sites, as measured by the daily gain in mass relative to lean body-mass, range between 1.0 and 3.6%/day, and departure fuel loads (in % of lean body-mass) between 27 and 73%.
Comparison with flight range estimates suggests that overloading may be a regular phenomenon during spring migration of Knots, Sanderlings and Turnstones. Furthermore, fat deposition rates at different staging sites, and the general difference in migration patterns between spring and autumn, indicate that by-passing of possible staging sites may well occur. Hence, it cannot be excluded that the waders' migratory habits primarily serve to maximize the overall speed of migration.     

Longer is fatter: body mass changes of migrant Reed Warblers (Acrocephalus scirpaceus) staging at Eilat,Israel

Ecological barriers are the riskiest phases of the annual migrations for migratory birds. Comparatively little field data exists pertaining to the ability of migratory birds to prepare for the challenges of crossing ecological barriers, or their ability to recuperate afterward. Migrating Reed Warblers (Acrocephalus scirpaceus) were captured in Eilat, Israel, during their spring and autumn migrations. Data on spring and autumn body masses, their inter-annual variation, and the pattern of body mass increase were analysed. The birds show a significant inter-annual variation in their body mass and body condition index in both seasons, which is consistent with the data from other sites and for other passerine species. During stopovers, mass gain occurred in both seasons. Birds in poor initial condition, and those that stop over for a longer period of time, gained more body mass faster. In spring, but not in autumn, the progress of the season was also an important factor; late-arriving birds gained more fuel faster. The average rate of fuel gain was 0,157g·day^?1 ± 0.018 SE.     

The effect of water availability on fuel deposition of two staging Sylvia warblers

In order to succeed in crossing extensive ecological barriers, migratory birds usually deposit fuel en route. High rates of fuel deposition may enable birds to shorten their total migration time and are therefore advantageous for time‐minimizing migrants. Several studies have suggested that water provision may increase food utilization in non‐migratory birds. The goal of this study was to test the influence of water availability on the fuel deposition of en route migratory passerines. We studied fuel deposition of blackcaps Sylvia atricapilla and lesser whitethroats S. curruca staging in a plantation of Mount Atlas gum‐tree Pistacia atlantica in the northern Negev desert, Israel, during the autumns of 2000 and 2002. We manipulated water availability at the site and measured the effect of water supplementation on fuel deposition of birds of both species. We found that when water was available, blackcaps had higher fuel loads and higher fuel deposition rates than during control trials. However, water availability had no effect on fuel deposition of lesser whitethroats. Species‐specific differences in adaptations to arid conditions, reflected in the species’ winter habitat preferences, may be responsible for the between‐species dissimilarity in responding to water provision. We suggest that water availability may have strong ecological and evolutionary consequences for birds migrating through arid environments, by its possible effect on bird behavior and physiology.     

Individual differences in migratory behavior shape population genetic structure and microhabitat choice in sympatric blackcaps (Sylvia atricapilla)

In migratory birds, traits such as orientation and distance are known to have a strong genetic background, and they often exhibit considerable within‐population variation. How this variation relates to evolutionary responses to ongoing selection is unknown because the underlying mechanisms that translate environmental changes into population genetic changes are unclear. We show that within‐population genetic structure in southern German blackcaps (Sylvia atricapilla) is related to individual differences in migratory behavior. Our 3‐year study revealed a positive correlation between individual migratory origins, denoted via isotope (δ²H) values, and genetic distances. Genetic diversity and admixture differed not only across a recently established migratory polymorphism with NW‐ and SW‐migrating birds but also across δ²H clusters within the same migratory route. Our results suggest assortment based on individual migratory origins which would facilitate evolutionary responses. We scrutinized arrival times and microhabitat choice as potential mechanisms mediating between individual variation in migratory behavior and assortment. We found significant support that microhabitat choice, rather than timing of arrival, is associated with individual variation in migratory origins. Moreover, examining genetic diversity across the migratory divide, we found migrants following the NW route to be genetically more distinct from each other compared with migrants following the traditional SW route. Our study suggests that migratory behavior shapes population genetic structure in blackcaps not only across the migratory divide but also on an individual level independent of the divide. Thus, within‐population variation in migratory behavior might play an important role in translating environmental change into genetic change.     

Spring nocturnal migration of Reed Warblers Acrocephalus scirpaceus: departure, landing and body condition

Nocturnal migration of Reed Warblers Acrocephalus scirpaceus was studied by trapping with 'high nets' on the Courish Spit (Eastern Baltic) during spring 1998–2000. In spring, Reed Warblers left the stopover site between 45 and 240 min after sunset (median 84 min), although 85% of birds took off between 45 and 120 min after sunset. Birds did not arrive until the fifth hour after sunset; 67% of birds ended their nocturnal flights in the penultimate hour before sunrise, i.e. at dawn. At the moment of migratory departure, the average Reed Warbler body mass was 12.79 ± 0.66 g ( n  = 60). Average body mass of birds ending migratory flight was 11.69 ± 0.67 g ( n  = 18). The difference was highly significant. However, more than half of the birds completed migratory flights with a considerable fuel load, and some even had energy stores sufficient for a migratory flight on the next night. The spring migratory strategy of Reed Warblers over Central and Northern Europe probably includes a succession of short migratory flights (4–6 h) during several subsequent nights with 1-day stopovers.     

Magnetic cues and time of season affect fuel deposition in migratory thrush nightingales (Luscinia luscinia)

Bird migration requires high energy expenditure, and long-distance migrants accumulate fat for use as fuel during stopovers throughout their journey. Recent studies have shown that long-distance migratory birds, besides accumulating fat for use as fuel, also show adaptive phenotypic flexibility in several organs during migration. The migratory routes of many songbirds include stretches of sea and desert where fuelling is not possible. Large fuel loads increase flight costs and predation risk, therefore extensive fuelling should occur only immediately prior to crossing inhospitable zones. However, despite their crucial importance for the survival of migratory birds, both strategic refuelling decisions and variation in phenotypic flexibility during migration are not well understood. First-year thrush nightingales (Luscinia luscinia) caught in the early phase of the onset of autumn migration in southeast Sweden and exposed to a magnetic treatment simulating a migratory flight to northern Egypt increased more in fuel load than control birds. By contrast, birds trapped during the late phase of the onset of autumn migration accumulated a high fuel load irrespective of magnetic treatment. Furthermore, early birds increased less in flight-muscle size than birds trapped later in autumn. We suggest that the relative importance of endogenous and environmental factors in individual birds is affected by the time of season and by geographical area. When approaching a barrier, environmental cues may act irrespective of the endogenous time programme.     

What determines probability of surviving predator attacks in bird migration?: the relative importance of vigilance and fuel load

Migrating birds must accumulate fuel during their journeys and this fuel load should incur an increased risk of predation. Migratory fuelling should increase individual mass-dependent predation risk for two reasons. First, acquisition costs are connected to the increased time a bird must spend foraging to accumulate the fuel loads and the reduced predator detection that accompanies foraging. Second, birds with large fuel loads have been shown to suffer from impaired predator evasion which makes them more vulnerable when actually attacked. Here, I investigate the relative importance of these two aspects of mass-dependent predation risk and I have used published data and a hypothetical situation for a foraging bird to investigate how much migratory fuelling in terms of escape performance and natural variation in predator detection contribute to individual risk during foraging. Results suggest that for birds foraging close to protective cover the negative impact of fuel load on flight performance is very small, whereas variation in time to predator detection is of great importance for a bird's survival. However, the importance of flight performance for predation risk increases as the distance to cover increases. Hence, variation in predator detection (and vigilance) probably influences individual survival much more than migratory fuel load and consequently, to understand risk management during migration studies that focus on vigilance and predator detection during fuelling are much needed.     

Wind conditions affect stopover decisions and fuel stores of shorebirds migrating through the south Yellow Sea

We assessed the effects of wind conditions on stopover decisions and fuel stores of migratory shorebirds at Chongming Dongtan in the south Yellow Sea along the East Asian–Australasian Flyway. In spring and autumn, wind directions differed among altitudes and wind speed generally increased with altitude. Numbers of shorebirds were related to wind effects at low altitudes (on the ground and at 300 and 800 m above the ground), wind effects at 300 m being the best predictor of shorebird numbers. In spring, total number of shorebirds and numbers of the four most abundant shorebird species were negatively related to wind assistance at low altitudes, more birds departing when tailwinds prevailed and more arriving when headwinds prevailed. In autumn, however, total number of shorebirds and numbers of the four most abundant species were positively related to wind assistance at low altitudes, more birds departing and more arriving with tailwinds than with headwinds. When tailwinds prevailed, the number of arriving birds was higher than the number of departing birds. The fuel stores of captured shorebirds, represented by their body mass, was related to wind effects and change in wind conditions between two consecutive days in both spring and autumn, captured birds being heavier when headwinds prevailed than in tailwind conditions, and when the wind conditions became less favourable for flight between two consecutive days. Our results suggest that wind conditions affect stopover decisions and fuel stores, and thus the optimal migration and fuel deposition strategies of migratory shorebirds.     

Arrival fat and reproductive performance in a long-distance passerine migrant

Long-distance passerine migrants deposit substantial fat stores to fuel their migratory journey. Many of those migratory birds arrive at their northerly breeding grounds with larger fat stores than were necessary to reach their breeding area. Both male and female American Redstarts ( Setophaga ruticilla) arrived to breed in Michigan's Upper Peninsula with fat, and females arrived with more fat than males in 2 out of 3 years. We test the hypothesis that migrants arriving at the breeding grounds with more body fat have higher reproductive success than birds arriving with little or no fat. Females, and to a lesser extent males, that arrive with fat experience gains in reproductive performance as evidenced by increased clutch size, egg volume, and nestling mass. The results have implications for understanding how events occurring during one phase of the annual cycle influence survival and/or reproductive performance in subsequent phases.     

Stopover ecology of Red-flanked Bush Robin (Tarsiger cyanurus) at Maoershan, Northeast China

The conservation of migratory songbirds in China faces challenges similar to those in other parts of the world such as Europe and North America. Migratory songbirds have a complex life history and are associated with large spatial scale. Events that occur during migration play a vital role in determining population status. Little is known about the stopover behavior of migratory songbirds in China during their passage, including stopover duration, energetic condition (e.g., the amount of fat stores), and the habitat of these birds. We investigated migration timing, stopover duration, change of energetic condition and sex-related variations among Red-flanked Bush Robins (Tarsiger cyanurus) at a stopover site in Northeast China. A total of 1 751 Red-flanked Bush Robins were captured in the fall of 2002, with further 684 captured in the spring of 2003. The body mass of the fall birds was higher than that of the spring ones. The condition index (i.e., body mass adjusted for body size) was lowest among spring females. Birds were more likely to stay longer in fall than in spring. We detected a positive relationship between the time of initial capture and condition index regardless of season or sex, suggesting that the birds were able to replenish energy stores. The net daily mass gain was the highest among males in the fall (3% of body mass). The net daily mass gain would sustain a flight of 0.6 hours for females and 3.1 hours for males in the fall. The stopover biology of Red-flanked Bush Robins is similar to that of some migratory songbirds in Europe and North America. For example, the spring passage time and fat store variation between the sexes concurs with the hypothesis that males are selected to arrive at their breeding grounds as early as food resources or climatic conditions are adequate in the spring. Further research on stopover ecology is urgently required in China to achieve a better understanding of migratory behavior and ensure the conservation of these migratory songbirds.     

Differential migration of the sexes cannot be explained by the body size hypothesis in Teal

The “body size hypothesis” predicts that if individuals of a population migrate different distances from the breeding to the wintering grounds, the distance should be related to the differential ability to cope with adverse conditions, with larger individuals wintering further north. Data collected over a 40-year period in Essex, UK and the Camargue, southern France, revealed that the average body mass of Teal ringed in Essex during these years was actually not greater than that of Teal ringed in the Camargue. A higher proportion of males were included in the UK ringing catch than in the French catch, but we found no support for the body size hypothesis to explain such differential migration of the sexes.