Migratory stopover conditions affect the developmental state of male gonads in garden warblers (Sylvia borin)

Long-distance migrants face the challenge of a short window for reproduction that requires optimal timing and full functional gonads. Male garden warblers (Sylvia borin) meet these demands by initiating testicular recrudescence during spring migration, enabling them to reproduce immediately after arrival at the breeding grounds. In a combined field and laboratory study, we investigated testicular size, plasma levels of luteinizing hormone (LH), androstenedione (AE), 5α-dihydrotestosterone (DHT), testosterone and nocturnal migratory restlessness (Zugunruhe) under different stopover conditions. We manipulated food availability, the duration of stopover and simulated migration by food deprivation. Garden warblers showed significantly retarded testicular development after nine days of stopover under limited food conditions compared to birds that had ad libitum access to food. However, there was no significant difference in Zugunruhe between the two groups. Thus, the degree of Zugunruhe was unaffected by the quality of the stopover site and migration continued independent of the developmental state of the testis. We suggest that male garden warblers face the necessity to either compensate for slowed testicular recrudescence during the subsequent leg of migration and delay arrival at the breeding grounds, or arrive with less developed testes. Either of these may reduce annual reproductive success.     

Energetics of fattening and starvation in the long-distance migratory garden warbler,Sylvia borin,during the migratory phase

Garden warblers (Sylvia borin) were subjected to starvation trials during their autumnal migratory phase in order to simulate a period of non-stop migration. Before, during and after this treatment the energy expenditure, activity, food intake and body mass of the subjects were monitored. Assimilation efficiency was constant throughout the experiments. The catabolized (during starvation) and deposited body tissue (during recovery) consisted of 73% fat. Basal metabolic rate was decreased during the starvation period and tended to a gradual increase during the recovery period. The reduced basal metabolic rate can possibly be attributed to a reduced size/function of the digestive system, which is consistent with the sub-maximal food intake immediately after resuming the supply of food to the experimental birds. The observed reductions in basal metabolic rate during starvation and activity during recovery can be viewed as adaptations contributing to a higher economization of energy supplies. The experimental birds were unable to eat large quantities of food directly after a period of starvation leading to a comparatively low, or no increase in body mass. Such a slow mass increase is in agreement with observations of migratory birds on arrival at stop-over sites.Abbreviations BM body mass - BMR basal metabolic rate - LBM lean body mass - RQ respiratory quotient     

Melatonin reduces migratory restlessness in <Emphasis Type="Italic">Sylvia</Emphasis> warblers during autumnal migration

Introduction

A remarkable aspect of bird migration is its nocturnality, particularly common in Passeriformes. The switch in activity from purely diurnal to also nocturnal is evident even in caged birds that during migratory periods develop an intense nocturnal restlessness, termed Zugunruhe. The mechanisms that control this major change in activity are mostly unknown. Previous work with Sylvia warblers suggested an involvement of melatonin, a hormone associated with day-night cycles in most vertebrates. In a recent study we found no effects of melatonin administration on Zugunruhe during spring migration. However, previous studies indicated that the response to melatonin manipulation could differ between spring and autumn migration, which are in fact separate life history stages. Here we tested whether a non-invasive treatment with melatonin can alter Zugunruhe in wild garden warblers S. borin and blackcaps S. atricapilla subject to temporary captivity at an autumnal stopover site. Food availability in the cage (yes/no) was added as a second factor because previous work showed that it enhanced Zugunruhe.

Results

The melatonin treatment significantly decreased the amount of Zugunruhe, while the availability of food only tended to increase the amount of Zugunruhe. Fuel deposits also had a strong effect on the amount of nocturnal activity: lean birds with a fat score of 1 showed significantly less Zugunruhe than fatter birds. The change in body mass during the time spent in the recording cage depended on food availability, but not on any of the other factors.

Conclusions

This study shows that the migratory programme of two Sylvia warblers can be manipulated by administration of exogenous melatonin and confirms that this hormone is involved in the control of migratory behaviour. To our knowledge, this is one of the first demonstrations that the autumn migratory programme can be altered by hormonal manipulation in migrating birds. The comparison with a similar study carried out with the same modalities during spring migration suggests that there are seasonal differences in the sensitivity of the migratory programme to hormonal factors. In birds breeding in the northern hemisphere, the importance of a timely arrival to the breeding sites could explain why the control of the migratory programme is more rigid in spring.

     

Body fat influences departure from stopover sites in migratory birds: evidence from whole-island telemetry

Migration remains one of the great mysteries of animal life. Small migratory birds rely on refuelling stopovers after crossing ecological barriers such as deserts or seas. Previous studies have suggested that fuel reserves may determine stopover duration but this hypothesis could not be tested because of methodological limitations. Here, we provide evidence that subcutaneous fat stores determine stopover duration by measuring the permanence of migratory garden warblers (Sylvia borin) on a small Mediterranean island during spring migration with telemetry methods. Garden warblers with large amounts of fat stores departed the island significantly sooner than lean birds. All except one fat bird left the island on the same evening after capture, with a mean total stopover estimate of 8.8 hours. In contrast, the mean estimated total stopover duration of lean birds was 41.3 hours. To our knowledge, this is the first study that measures the true minimum stopover duration of a songbird during migration.     

Food availability but not melatonin affects nocturnal restlessness in a wild migrating passerine

A large number of passerine species migrate at night, although most of them are diurnal outside the migratory seasons. This diurnal-to-nocturnal transition is a major life-history event, yet little is known about its physiological control. Previous work showed that during the migratory periods captive birds showing nocturnal migratory restlessness (Zugunruhe) have reduced concentrations of circulating melatonin at night compared to non-migratory periods. This suggested that the hormone melatonin, a main component of the avian circadian system, is involved in the expression of Zugunruhe. Other studies demonstrated that the relationship between low melatonin levels and Zugunruhe is not a seasonal correlation. When Zugunruhe was interrupted by exposing birds to a fasting-and-refeeding protocol, melatonin levels increased. Here we studied whether melatonin and food availability influence the intensity of Zugunruhe in wild migrating garden warblers (Sylvia borin) at a stopover site. Birds were held in recording cages overnight, with or without food available, and either bled to determine melatonin concentrations or treated transdermally with melatonin. We found that melatonin levels at night were correlated with the intensity of diurnal locomotor activity and with condition, but were not correlated with Zugunruhe. Similarly, the melatonin treatment did not have effects on Zugunruhe, whereas food availability increased it. Our study shows that the nocturnal melatonin levels in migrating warblers depend on food availability and are correlated with condition. In addition, it suggests that melatonin does not control Zugunruhe and might rather be involved in energy conservation and/or clock synchronization during migration.     

The seasonal development of photoperiodic responsiveness in an equatorial migrant, the garden warblerSylvia borin

Summary Garden warblers (Sylvia borin) are migrating European passerines that spend the winter in tropical Africa. To investigate how photoperiod controls the annual cycles of reproduction, molt and migration, garden warblers were exposed to photoperiodic changes simulating those experienced by conspecifics with an equatorial wintering area. At three different times groups of birds were moved from a constant equatorial photoperiod of 12.8 h to a 15-h photoperiod: group 1 on November 19, group 2 on February 24, and group 3 on April 12. In all birds the changes in body weight, nocturnal migratory restlessness, testicular width or diameter of the largest oocyte, and plasma LH concentrations were determined. In addition, the birds were examined for molt. In all birds of groups 2 and 3 the transfer to long photoperiods induced a gonadal cycle associated with spring migratory restlessness and, in the group 3 birds, an increase in LH. In group 1 only few birds showed marginal gonadal responses and the gonadal cycles of the group 2 birds were less pronounced than those of group 3. The results suggest that the hypothalamo-pituitary-gonadal axis was refractory to stimulation by long photoperiods in autumn but, later in the season, became responsive to the same long photoperiods. Unlike the situation in other temperate zone birds, the transition from the photorefractory to the photosensitive state seems to be a gradual process which develops spontaneously and with the appropriate temporal characteristics in the absence of photoperiodic change.Abbreviation LH luteinizing hormone     

Testicular development during long-distance spring migration

In birds, gonadal size varies between fully functional and maximally sized during reproduction and a regressed state with limited function during the non-reproductive periods. Recent findings show that testicular mass of the long-distance migratory garden warbler begins to increase during spring migration. Therefore, we sampled garden warblers during spring migration from Tanzania to Ethiopia, and finally to Egypt to determine if this mass increase is functional in terms of sperm and hormone production. In addition, we compared these birds, with garden warblers sampled after a 9-day recovery period following the crossing of the Sahara Desert (simulation of stopover) in Egypt and a group sampled in breeding condition in the laboratory. During migration there was a significant increase in testicular mass that was correlated with seminiferous tubule area and the stage of spermatogenesis. Plasma testosterone levels were low during migration, but were significantly correlated with testicular mass. LH concentration was not related to testicular mass, and, surprisingly, remained constant during migration. We suggest that previous experiments that found a tight relationship between testicular growth and LH level in the laboratory may not reflect the situation during long-distance migration where the great physical and energetic demands of migration likely affect the reproductive axis and, consequently, the relationship between testicular growth and LH titer. However, testes do develop to a considerable extent during spring migration and the present data suggest that initiation of testicular maturation during spring migration is necessary to ensure full spermatogenetic development soon after arrival at the breeding area.     

Circannual variation in blood parasitism in a sub‐Saharan migrant passerine bird,the garden warbler

Knowing the natural dynamics of pathogens in migratory birds is important, for example, to understand the factors that influence the transport of pathogens to and their transmission in new geographical areas, whereas the transmission of other pathogens might be restricted to a specific area. We studied haemosporidian blood parasites of the genera Plasmodium, Haemoproteus and Leucocytozoon in a migratory bird, the garden warbler Sylvia borin. Birds were sampled in spring, summer and early autumn at breeding grounds in Sweden, on migration at Capri, Italy and on arrival and departure from wintering staging areas in West Africa: mapping recoveries of garden warblers ringed in Fennoscandia and Capri showed that these sites are most probably on the migratory flyway of garden warblers breeding at Kvismaren. Overall, haemosporidian prevalence was 39%, involving 24 different parasite lineages. Prevalence varied significantly over the migratory cycle, with relatively high prevalence of blood parasites in the population on breeding grounds and at the onset of autumn migration, followed by marked declines in prevalence during migration both on spring and autumn passage. Importantly, we found that when examining circannual variation in the different lineages, significantly different prevalence profiles emerged both between and within genera. Our results suggest that differences in prevalence profiles are the result of either different parasite transmission strategies or coevolution between the host and the various parasite lineages. When separating parasites into common vs. rare lineages, we found that two peaks in the prevalence of rare parasites occur; on arrival at Swedish breeding grounds, and after the wintering period in Africa. Our results stress the importance of appropriate taxonomic resolution when examining host‐parasite interactions, as variation in prevalence both between and within parasite genera can show markedly different patterns.     

Digestive tract function in the long-distance migratory garden warbler,Sylvia borin

Digestive tract morphology and function of captive garden warblers (Sylvia borin) were measured during four stages of their endogenous circannual rhythm: before, during and after their autumn fattening prior to migration to wintering grounds in Africa, and after a partially simulated migratory flight. Food intake increased by 33% during fattening, utilization efficiency of dry matter tended to increase, and that of energy increased significantly (P0.01). This was because digestive tract capacity (measured as dry tissue mass) increased, so that mean retention time of food remained constant before, during and after fattening (80–84 min). After a 48-h period of starvation of fattened birds to partially simulate a migratory flight, food intake was lower on the first day of refeeding than on the next 4 days, and utilization efficiency was higher on that day, at least partly because of a longer mean retention time (111 min versus 78 min on the third day). Digestive tract dry tissue mass fell by 50% during starvation, and that of the small intestine by 63%. It is concluded that the garden warbler adapts to long-distance migration without feeding by rapidly reducing the size of its digestive tract, an expensive tissue to maintain, during migration in order to save weight and energy, and possibly also to supply part of the fuel and protein required for the flight. The cost of this strategy appears to be the time taken to rebuild the gut at stopover sites with food, but the low probability of finding such a site in the Sahara Desert means that this strategy is probably optimal for garden warblers.     

Fat stores in a migratory bird: a reservoir of carotenoid pigments for times of need?

Carotenoids are well known for their immune-stimulant function in birds and other vertebrates. Moreover, they have potential antioxidant capacity, scavenging free radicals and protecting cell compartments from oxidation. Most essential carotenoids are fat soluble and could be stored for times of need especially in adipose tissues, built up by migratory birds as the main source of energy on long-distance flights. In an exclusive diet experiment, garden warblers (Sylvia borin) were fed ad libitum with an experimental diet, enriched with two different dose rates of carotenoids, or with control food, during the period of their first autumn migration. Plasma carotenoid content was measured via HPLC and chroma of plasma and fat examined with a spectrophotometer. Birds were infected with Isospora spp. and intensity of infection determined by oocyst counts 3 days post infection. Plasma lutein levels and chroma of subcutaneous fat stores were positively correlated and chroma values of these fat stores increased in the birds that got the higher dose rate, whereas they decreased significantly in the control group after infection with Isospora spp. Chroma of subcutaneous fat deposits in vivo and intensity of Isospora infection were negatively correlated. By measuring the chroma of fat deposits in vivo, we show that fat can be a reservoir for carotenoids. These colorful antioxidants are stored in the fat and taken from there in times of a higher demand, e.g. when mounting an immune response to parasites.     

The autumnal fattening of the long-distance migratory garden warbler (Sylvia borin) is stimulated by intermittent fasting

To investigate the proximate influence of a changing food availability on the seasonal fattening of migratory birds, garden warblers (Sylvia borin) following postnuptial moult were food restricted once a week. Body mass, food intake, plasma hormone and metabolite levels were measured and compared to birds which always had ad libitum food access. The food-restricted birds increased their body mass significantly earlier than the controls. The accelerated fattening was initially not accompanied by hyperphagia and may be due to either an increased food utilisation efficiency or a reduced metabolic rate. An increase of basal glucagon and corticosterone and a decrease of insulin levels prior to fattening were not significant, however, they resulted in a significant decrease of the insulin:glucagon ratio. This ratio was also lower in food-restricted birds than in control birds and may account for the difference in the fattening progress. We conclude that seasonal fattening may be stimulated by a catabolic impulse which could be imposed in free-living birds by a decrease of food availability and/or by an increase of energy expenditure. A negative energy balance is hypothesised to be a common proximate factor affecting migratory as well as winter fattening. Accepted: 24 August 2000     

WEIGHTS OF SOME PALAEARCTIC MIGRANTS IN SOUTHERN UGANDA

Between March 1966 and May 1968 Palaearctic passerines were mist-netted in thick bush and lightly wooded savannah habitats near Kampala, on the northern shore of Lake Victoria. This paper reports weights of the seven principal species involved. Most migrants appeared to be in a lean condition during the winter months, when weights were relatively low and varied little in each species. Birds were not particularly light on arrival. In fact, autumn Garden Warblers Sylvia borin and Willow Warblers Phylloscopus trochilus were sometimes markedly heavy, and for the former species there was some evidence that the individuals concerned were passage migrants. Autumn weights of Swallows Hirundo rustica, Reed Warblers Acrocephalus scirpaceus and Yellow Wagtails Motacilla flava were similar to those recorded in winter. The mean weight of all species rose during late March or early April. Although most Garden Warblers and Willow Warblers trapped at the time of spring migration were within the normal winter weight range, many Acrocephalus warblers and the majority of Sand Martins Riparia riparia and Yellow Wagtails were rather heavy. Spring weights 40% or more above mean winter weight were not uncommon in the Sedge Warbler Acrocephalus schoenobaenus, but were recorded only occasionally in other species. Although most passerine migrants evidently left Kampala with substantial fat reserves, it was concluded that a considerable number of warblers departed at rather low weight. High spring weights were mainly confined to a period of two or three weeks in each of the warbler species. Locally wintering Acrocephalus warblers must have attained full premigratory weights within three weeks, and a number of spring retraps showed substantial gains at minimum mean rates of between 0–1 and 0–35 g per day. Most heavy Garden Warblers were probably on passage. Significant correlations between weight and wing-length were obtained for all species investigated, regressions of weight on wing-length being in the range 011-0-25 g/mm. Spring weights are briefly compared with data from Nigeria, and the northward migration of passerines from Lake Victoria is discussed.     

Corticosterone and growth hormone levels in shorebirds during spring and fall migration stopover.

Large numbers of shorebirds stop over at Delaware Bay during spring migration and undergo major mass increases within a two- to three-week period. We studied plasma levels of corticosterone and growth hormone in three species of migrants that use this site, sanderlings, Calidris alba, semipalmated plovers, Charadrius semipalmatus, and semipalmated sandpipers, Calidris pusilla. Semipalmated sandpipers were also studied at a fall migration stopover in Manomet, Massachusetts. These two hormones were chosen because they modulate the physiological processes of lipogenesis/lipolysis and promote increased feeding in birds. The stress response was not suppressed in the shorebirds studied, and plasma levels of corticosterone were elevated compared to other studies. We believe that the high levels of corticosterone relate to the rapid fat deposition that takes place at this stop-over site. There was a significant negative correlation between plasma growth hormone and body mass, indicating the lipolytic effects of the growth hormone. Because the lighter birds are recent arrivals to Delaware Bay they may have elevated plasma growth because of fat breakdown during flight to this stop-over site. High levels of growth hormone may also result in protein synthesis, replenishing tissues broken down during the previous migratory bout. J. Exp. Zool. 284:645-651, 1999.     

Simulation of migratory flight and stopover affects night levels of melatonin in a nocturnal migrant

Several species of diurnal birds are nocturnal migrants. The activation of nocturnal activity requires major physiological changes, which are essentially unknown. Previous work has shown that during migratory periods nocturnal migrants have reduced night-time levels of melatonin. Since this hormone is involved in the modulation of day-night rhythms, it is a good candidate regulator of nocturnal migratory activity. We studied whether melatonin levels change when nocturnally active blackcaps (Sylvia atricapilla) are experimentally transferred from a migratory to a non-migratory state. We simulated a long migratory flight by depriving birds of food for 2 days, and a refuelling stopover by subsequently re-administering food. Such a regimen is known to induce a reduction in migratory restlessness ('Zugunruhe') in the night following food reintroduction. The experiments were performed in both autumn and spring using blackcaps taken from their breeding grounds (Sweden) and their wintering areas (Kenya). In autumn, the food regimen induced a suppression of Zugunruhe and an increase in melatonin in the night following food reintroduction. In spring, the effects of the treatment were qualitatively similar but their extent depended on the amount of body-fat reserves. This work shows that the reduction of night-time melatonin during migratory periods is functionally related to nocturnal migration, and that fat reserves influence the response of the migratory programme to food deprivation.     

Annual cycles of migratory fattening, reproduction and moult in European quail (Coturnix coturnix)

Experimental studies of the physiological mechanisms underlying avian migration have concentrated on small passerines. The present study is concerned with the regulation of migratory fat deposition in a galliform. the European quail (Coturnix coturnix). The increased mass associated with migration was due exclusively to the deposition of fat whereas the increased body mass of laying females was due to increases in lean tissue and water as well as fat. Annual cycles of body mass, moult, gonadal size and plasma luteinizing hormone were measured every other week in captive males and females held outdoors under natural daylengths and temperatures in Bristol, UK (51° 27' N). Males and females showed two peaks of fat deposition each year which occurred at the migratory passage times reported in wild birds. Luteinizing hormone levels and gonadal size increased in parallel with vernal fat deposition, and remained high until late summer. The pattern of primary feather moult in the intact birds was similar to that of wild quail, with moult following gonadal regression and being suspended during autumnal fattening. Castration of European quail did not inhibit the expression of migratory fattening, as it does In certain passerines. In fact, castrates displayed fattening cycles that were more clearly defined and of greater amplitude than those in the intact males. The annual cycle of European quail differs from that of other well-studied passerine migrants such as Zonotrichia sparrows, and this is most likely associated with differences in breeding ecology. In addition, the ability of quail to express vernal fattening independently of the presence of the gonads suggests that taxonomic differences between migratory species are also apparent in the physiological mechanisms of migratory fattening.     

Involvement of thyroid gland in the development of migratory disposition in the redheaded bunting, Emberiza bruniceps

In the redheaded bunting Emberiza bruniceps, thyroidectomy inhibited premigratory fattening and nocturnal restlessness—two characteristics of avian migration—observed in caged birds during the premigratory period (March/April). Thyroxine (T₄) and triiodothyronine (T₃) administration in thyroidectomized birds stimulated locomotor activity and restored the loss in body weight. Annual variations in circulating thyroid hormone concentrations revealed a significant rise in $\text{T}{}_3\text{T}{}_4$ ratio prior to spring migration in both years studied. This increase in circulating $\text{T}{}_3\text{T}{}_4$ ratio may be associated with the development of migratory disposition in this bird. There was no increase in circulating $\text{T}{}_3\text{T}{}_4$ ratio prior to autumnal migration, however, plasma T₄ increased significantly. Different thyroidal mechanisms are most likely involved in spring and fall migratory periods. While T₃ remained low throughout, apart from the characteristic spring rise, high T₄ levels in E. bruniceps were associated with periods of reproduction and molting, the latter coinciding partly with autumnal migration.     

Linking the wintering and breeding grounds of warblers along the Pacific Flyway

Long‐distance migration is a behavior that is exhibited by many animal groups. The evolution of novel migration routes can play an important role in range expansions, ecological interactions, and speciation. New migration routes may evolve in response to selection in favor of reducing distance between breeding and wintering areas, or avoiding navigational barriers. Many migratory changes are likely to evolve gradually and are therefore difficult to study. Here, we attempt to connect breeding and wintering populations of myrtle warblers (Setophaga coronata coronata) to better understand the possible evolution of distinct migration routes within this species. Myrtle warblers, unlike most other warblers with breeding ranges primarily in eastern North America, have two disjunct overwintering concentrations—one in the southeastern USA and one along the Pacific Coast—and presumably distinct routes to‐and‐from these locations. We studied both myrtle and Audubon's warblers (S. c. auduboni) captured during their spring migration along the Pacific Coast, south of the narrow region where these two taxa hybridize. Using stable hydrogen isotopes and biometric data, we show that those myrtle warblers wintering along the southern Pacific Coast of North America are likely to breed at high latitudes in Alaska and the Yukon rather than in Alberta or further east. Our interpretation is that the evolution of this wintering range and migration route along the Pacific Coast may have facilitated the breeding expansion of myrtle warblers into northwestern North America. Moreover, these data suggest that there may be a migratory divide within genetically similar populations of myrtle warblers.     

Seasonally Changing Cryptochrome 1b Expression in the Retinal Ganglion Cells of a Migrating Passerine Bird

Cryptochromes, blue-light absorbing proteins involved in the circadian clock, have been proposed to be the receptor molecules of the avian magnetic compass. In birds, several cryptochromes occur: Cryptochrome 2, Cryptochrome 4 and two splice products of Cryptochrome 1, Cry1a and Cry1b. With an antibody not distinguishing between the two splice products, Cryptochrome 1 had been detected in the retinal ganglion cells of garden warblers during migration. A recent study located Cry1a in the outer segments of UV/V-cones in the retina of domestic chickens and European robins, another migratory species. Here we report the presence of cryptochrome 1b (eCry1b) in retinal ganglion cells and displaced ganglion cells of European Robins, Erithacus rubecula. Immuno-histochemistry at the light microscopic and electron microscopic level showed eCry1b in the cell plasma, free in the cytosol as well as bound to membranes. This is supported by immuno-blotting. However, this applies only to robins in the migratory state. After the end of the migratory phase, the amount of eCry1b was markedly reduced and hardly detectable. In robins, the amount of eCry1b in the retinal ganglion cells varies with season: it appears to be strongly expressed only during the migratory period when the birds show nocturnal migratory restlessness. Since the avian magnetic compass does not seem to be restricted to the migratory phase, this seasonal variation makes a role of eCry1b in magnetoreception rather unlikely. Rather, it could be involved in physiological processes controlling migratory restlessness and thus enabling birds to perform their nocturnal flights.     

盐城沿海海堤林带柳莺属(Phylloscopus)鸟类秋季迁徙规律

江苏盐城沿海具有广阔的平原与湿地滩涂,但缺少自然林地。经过多年的防风林建设,沿海海堤逐渐形成了特有的、南北走向的条带林生境,为迁徙鸟类提供了通道和停歇地,是研究鸟类迁徙规律的理想地点。柳莺属鸟类个体小,野外种类识别难,其迁徙规律缺乏深入研究。分别于2018年和2019年两个秋季,采用雾网法对盐城沿海海堤林带柳莺属鸟类的迁徙规律进行研究。结果表明：两个秋季共捕获柳莺属鸟类8种608只,其中极北柳莺（Phylloscopus borealis）、冕柳莺（P. coronatus）、淡脚柳莺（P. tenellipes）和黄眉柳莺（P. inornatus）的捕获数量分别为245只、131只、107只和94只,占捕获总数量的95%,是秋季迁徙期的优势种。对优势种柳莺日捕获率进行比较：2019年极北柳莺的日捕获率显著高于淡脚柳莺和黄眉柳莺（U test,P<0.05）。对捕获数量随时间变化进行分析,4种柳莺都以集中在短时间内快速通过的迁徙策略穿越盐城沿海海堤林带,符合秋季小型雀形目鸟类迁徙采取时间最小化假说。不同种类的柳莺在通过盐城沿海海堤林带的时间顺序上存在显著差异（K-W test,P<0.05）,2018年和2019年均以黄眉柳莺通过最晚。随着时间的推移,四种柳莺的脂肪度都逐渐下降。繁殖地纬度的差异可能是导致4种柳莺通过盐城沿海海堤林带时间差异的原因。盐城沿海海堤林带为柳莺属等雀形目小型鸟类的迁徙提供了非常理想的迁徙通道,应当加强海堤林带在鸟类迁徙和保护中的作用研究。