Migratory Reed Warblers Need Intact Trigeminal Nerves to Correct for a 1,000 km Eastward Displacement

Several studies have shown that experienced night-migratory songbirds can determine their position, but it has remained a mystery which cues and sensory mechanisms they use, in particular, those used to determine longitude (east–west position). One potential solution would be to use a magnetic map or signpost mechanism like the one documented in sea turtles. Night-migratory songbirds have a magnetic compass in their eyes and a second magnetic sense with unknown biological function involving the ophthalmic branch of the trigeminal nerve (V1). Could V1 be involved in determining east–west position? We displaced 57 Eurasian reed warblers (Acrocephalus scirpaceus) with or without sectioned V1. Sham operated birds corrected their orientation towards the breeding area after displacement like the untreated controls did. In contrast, V1-sectioned birds did not correct for the displacement. They oriented in the same direction after the displacement as they had done at the capture site. Thus, an intact ophthalmic branch of the trigeminal nerve is necessary for detecting the 1,000 km eastward displacement in this night-migratory songbird. Our results suggest that V1 carries map-related information used in a large-scale map or signpost sense that the reed warblers needed to determine their approximate geographical position and/or an east–west coordinate.     

Where in Europe should we look for sources of the cutaneous trematode Collyriclum faba infections in migrating birds?

Cutaneous cysts with trematodes of Collyriclum faba have been found in birds during their spring and post-breeding migrations in the Czech Republic. During spring migrations, C. faba was found in one dunnock Prunella modularis, two European robins Erithacus rubecula, three common nightingales Luscinia megarhynchos, one song thrush Turdus philomelos and one great reed warbler Acrocephalus arundinaceus. During post-breeding migration, the same parasite was found in one garden warbler Sylvia borin, one whitehroat S. communis, three goldcrests Regulus regulus and one Eurasian treecreeper Certhia familiaris. The newly identified hosts of C. faba are dunnock, common nightingale, song thrush, great reed warbler and Eurasian treecreeper. Geographical areas of the birds' infection were identified from an analysis of reports on ringed birds of the same species, the time necessary for the development of cutaneous cysts with C. faba and the time of their survival, and hitherto known geographical areas of endemic occurrence of C. faba. It is presumed that birds trapped during spring migrations were infected in some montane and submontane regions in south-western Europe (the Alps, the Apennines). Birds infected during autumn migration or post-breeding vagrancy could have been infected in the Central European Carpathians, the region of C. faba endemic occurrence. For migrating birds, the impact of C. faba infections has not been hitherto assessed.     

Dramatic orientation shift of white-crowned sparrows displaced across longitudes in the high Arctic

Advanced spatial-learning adaptations have been shown for migratory songbirds, but it is not well known how the simple genetic program encoding migratory distance and direction in young birds translates to a navigation mechanism used by adults. A number of convenient cues are available to define latitude on the basis of geomagnetic and celestial information, but very few are useful to defining longitude. To investigate the effects of displacements across longitudes on orientation, we recorded orientation of adult and juvenile migratory white-crowned sparrows, Zonotrichia leucophrys gambelii, after passive longitudinal displacements, by ship, of 266-2862 km across high-arctic North America. After eastward displacement to the magnetic North Pole and then across the 0 degrees declination line, adults and juveniles abruptly shifted their orientation from the migratory direction to a direction that would lead back to the breeding area or to the normal migratory route, suggesting that the birds began compensating for the displacement by using geomagnetic cues alone or together with solar cues. In contrast to predictions by a simple genetic migration program, our experiments suggest that both adults and juveniles possess a navigation system based on a combination of celestial and geomagnetic information, possibly declination, to correct for eastward longitudinal displacements.     

Longitude perception and bicoordinate magnetic maps in sea turtles

Long-distance animal migrants often navigate in ways that imply an awareness of both latitude and longitude. Although several species are known to use magnetic cues as a surrogate for latitude, it is not known how any animal perceives longitude. Magnetic parameters appear to be unpromising as longitudinal markers because they typically vary more in a north-south rather than an east-west direction. Here we report, however, that hatchling loggerhead sea turtles (Caretta caretta) from Florida, USA, when exposed to magnetic fields that exist at two locations with the same latitude but on opposite sides of the Atlantic Ocean, responded by swimming in different directions that would, in each case, help them advance along their circular migratory route. The results demonstrate for the first time that longitude can be encoded into the magnetic positioning system of a migratory animal. Because turtles also assess north-south position magnetically, the findings imply that loggerheads have a navigational system that exploits the Earth's magnetic field as a kind of bicoordinate magnetic map from which both longitudinal and latitudinal information can be extracted.     

Earlier Arctic springs cause phenological mismatch in long-distance migrants

An uneven change in climate across the Northern Hemisphere might severely affect the phenology of migrating animals, and especially long-distance migrating birds relying on local climatic cues to regulate the timing of migration. We examine the forward displacement of spring in both staging areas and breeding grounds of one such population, the East Atlantic light-bellied brent goose Branta bernicla hrota, and evaluate to what extent their migration has made a proportional response. On the breeding grounds in Svalbard the onset of spring advanced 2 weeks during the 24-year period, whereas no significant trend was found in the temperate staging areas. The timing of migration was constant throughout the study period, mirroring the static climatic conditions in the spring staging areas. These findings indicate a global warming-induced phenological mismatch in light-bellied brent geese, as these might arrive on their breeding grounds well beyond optimal breeding conditions. Our data indicated that productivity was negatively influenced by phenological delay and positively influenced by prolonged snow cover. We argue that both these effects might be representative of a negative influence of the growing phenological mismatch, because years with later thaw might partly offset the effects of increasingly earlier Svalbard springs. During the study period reproduction fell below annual mortality, and the population declined in recent years. The wider implications of these findings may extend to many migrating species, and highlight the urgent need to clarify how global change may influence cues and the associated timing of important life history activities.     

Nocturnal life of young songbirds well before migration

In songbirds, nocturnal activity is believed to be a characteristic feature of migration. However, unlike experimental conditions where the onset of nocturnal restlessness is defined as a shift of activity leading up to the dark period, this behaviour has, until now, not been observed in natural conditions. Here we studied the nocturnal behaviour of radio-tagged juvenile Eurasian reed warblers (Acrocephalus scirpaceus) during the pre-migratory period. The birds started nocturnal flights at the age of 38 days, whereas migration did not commence until they were at least 50 days old. The birds left their natal site by nocturnal flights and repeatedly returned to it. Such shuttle movements suggest the existence of a previously unknown period of nocturnal activity. Motivation to perform such night flights gradually increases with age. We relate the function of these nocturnal pre-migratory flights to the development of a stellar compass, necessary for detecting the compass direction towards winter quarters and for the formation of a navigational target, which will be used during return (spring) migration.     

Inability to regain normal body mass despite extensive refuelling in great reed warblers following the trans‐Sahara crossing during spring migration

Migratory birds wintering in Africa face the challenge of passing the Sahara desert with few opportunities to forage. During spring migration birds thus arrive in the Mediterranean area with very low energy reserves after crossing the desert. Since early arrival to the breeding grounds often is of importance to maximize reproductive success, finding stopover sites with good refuelling possibilities after the Saharan passage is of utmost importance. Here we report on extensive fuelling in the great reed warbler Acrocephalus arundinaceus on the south coast of Crete in spring, the first land that they encounter after crossing the Sahara desert and the Mediterranean Sea in this area. Birds were studied at a river mouth and due to an exceptional high recapture rate (45 and 51% in two successive years), we were able to get information about stopover behaviour in 56 individual great reed warblers during two spring seasons. The large proportion of trapped great reed warbler compared to other species and the large number of recaptures suggest that great reed warblers actively choose this area for stopover. They stayed on average 3–4 d, increased on average about 3.5 g in body mass and the average rate of body mass increase was 4.8% of lean body mass d^–1. Wing length affected the rate of increase and indicated that females have a slower increase than males. The results found show that great reed warblers at this site regularly deposit larger fuel loads than needed for one continued flight stage. The low body mass found in great reed warblers (also in birds with high fat scores) is a strong indication that birds staging at Anapodaris still had not been able to rebuild their structural tissue after the strenuous Sahara crossing, suggesting that rebuilding structural tissue may take longer time than previously thought.     

Regional wind patterns likely shape a seasonal migration detour

Migrating animals should optimise time and energy use when migrating, travelling directly to their destination. Detours from the most direct route may arise however because of barriers and weather conditions. Identifying how such situations arise from variable weather conditions is crucial to understand population response in the light of increased anthropogenic climate change. Here we used light-level geolocators to follow Cyprus wheatears for their full annual cycle in two separate years migrating between Cyprus, over the Mediterranean and the Sahara to winter in north–east sub-Saharan Africa. We predicted that any route detours would be related to wind conditions experienced during migration. We found that spring migration for all birds included an eastern detour, whilst autumn migrations were direct across the Sahara. The direct autumn migration was likely a consequence of consistent tail-winds, whilst the eastern detour in spring is likely to be more efficient given the wind conditions which are against a direct route. Such variable migration routes shaped by coincidence with prevailing winds are probably common suggesting that some birds may be able to adapt to future changes in wind conditions.     

Juvenile songbirds compensate for displacement to oceanic islands during autumn migration

To what degree juvenile migrant birds are able to correct for orientation errors or wind drift is still largely unknown. We studied the orientation of passerines on the Faroe Islands far off the normal migration routes of European migrants. The ability to compensate for displacement was tested in naturally occurring vagrants presumably displaced by wind and in birds experimentally displaced 1100 km from Denmark to the Faroes. The orientation was studied in orientation cages as well as in the free-flying birds after release by tracking departures using small radio transmitters. Both the naturally displaced and the experimentally displaced birds oriented in more easterly directions on the Faroes than was observed in Denmark prior to displacement. This pattern was even more pronounced in departure directions, perhaps because of wind influence. The clear directional compensation found even in experimentally displaced birds indicates that first-year birds can also possess the ability to correct for displacement in some circumstances, possibly involving either some primitive form of true navigation, or 'sign posts', but the cues used for this are highly speculative. We also found some indications of differences between species in the reaction to displacement. Such differences might be involved in the diversity of results reported in displacement studies so far.     

Supplemental food alters nest defence and incubation behaviour of an open‐nesting wetland songbird

Climate‐driven increases in spring temperatures are expected to result in higher prey availability earlier in the breeding season for insectivorous birds breeding in wetland habitats. Predation during the incubation phase is a major cause of nesting failure in open‐nesting altricial birds such as the Eurasian reed warbler. The nest predation rate in this species has recently been shown to be substantially reduced under conditions of experimentally elevated invertebrate prey availability. Food availability near the nest may be an important determinant of adult incubation and nest defence behaviours during the incubation period. We used two experimental studies to compare incubation behaviour and nest defence in food‐supplemented and unsupplemented adult Eurasian reed warblers during the incubation phase. In the first study we measured nest defence behavioural responses to a taxidermic mount of a native predator (stoat Mustela erminea). In the second study we used temperature loggers installed in nests to measure breaks in incubation as a measure of nest vulnerability. Food‐supplemented birds responded aggressively to the presence of a predator more quickly than those in the unsupplemented group, suggesting they are closer to their nest and can more quickly detect a predator in the vicinity. Food‐supplemented birds also had shorter breaks in incubation (both in terms of maximum and mean off‐bout durations), presumably because they were foraging for shorter periods or over shorter distances from the nest. This study therefore identifies the behavioural mechanisms by which changes in food availability may lead to changes in nest survival and thus breeding productivity, in open‐nesting insectivorous birds.     

Towards a new understanding of migration timing: slower spring than autumn migration in geese reflects different decision rules for stopover use and departure

According to migration theory and several empirical studies, long‐distance migrants are more time‐limited during spring migration and should therefore migrate faster in spring than in autumn. Competition for the best breeding sites is supposed to be the main driver, but timing of migration is often also influenced by environmental factors such as food availability and wind conditions. Using GPS tags, we tracked 65 greater white‐fronted geese Anser albifrons migrating between western Europe and the Russian Arctic during spring and autumn migration over six different years. Contrary to theory, our birds took considerably longer for spring migration (83 days) than autumn migration (42 days). This difference in duration was mainly determined by time spent at stopovers. Timing and space use during migration suggest that the birds were using different strategies in the two seasons: In spring they spread out in a wide front to acquire extra energy stores in many successive stopover sites (to fuel capital breeding), which is in accordance with previous results that white‐fronted geese follow the green wave of spring growth. In autumn they filled up their stores close to the breeding grounds and waited for supportive wind conditions to quickly move to their wintering grounds. Selection for supportive winds was stronger in autumn, when general wind conditions were less favourable than in spring, leading to similar flight speeds in the two seasons. In combination with less stopover time in autumn this led to faster autumn than spring migration. White‐fronted geese thus differ from theory that spring migration is faster than autumn migration. We expect our findings of different decision rules between the two migratory seasons to apply more generally, in particular in large birds in which capital breeding is common, and in birds that meet other environmental conditions along their migration route in autumn than in spring.     

Understanding the migratory orientation program of birds: extending laboratory studies to study free-flying migrants in a natural setting

For many years, orientation in migratory birds has primarily been studied in the laboratory. Although a laboratory-based setting enables greater control over environmental cues, the laboratory-based findings must be confirmed in the wild in free-flying birds to be able to fully understand how birds orient during migration. Despite the difficulties associated with following free-flying birds over long distances, a number of possibilities currently exist for tracking the long distance, sometimes even globe-spanning, journeys undertaken by migrating birds. Birds fitted with radio transmitters can either be located from the ground or from aircraft (conventional tracking), or from space. Alternatively, positional information obtained by onboard equipment (e.g., GPS units) can be transmitted to receivers in space. Use of these tracking methods has provided a wealth of information on migratory behaviors that are otherwise very difficult to study. Here, we focus on the progress in understanding certain components of the migration-orientation system. Comparably exciting results can be expected in the future from tracking free-flying migrants in the wild. Use of orientation cues has been studied in migrating raptors (satellite telemetry) and thrushes (conventional telemetry), highlighting that findings in the natural setting may not always be as expected on the basis of cage-experiments. Furthermore, field tracking methods combined with experimental approaches have finally allowed for an extension of the paradigmatic displacement experiments performed by Perdeck in 1958 on the short-distance, social migrant, the starling, to long-distance migrating storks and long-distance, non-socially migrating passerines. Results from these studies provide fundamental insights into the nature of the migratory orientation system that enables experienced birds to navigate and guide inexperienced, young birds to their species-specific winter grounds.     

Breeding latitude and timing of spring migration in songbirds crossing the Gulf of Mexico

Each spring, millions of songbirds migrate across the Gulf of Mexico on their way to breeding sites in North America. Data from radar and migration monitoring stations have revealed broad patterns in the spatial and temporal course of trans-Gulf migration. Unfortunately, we have limited information on where these birds have previously spent the winter and where they are migrating to breed. Here we measure stable-hydrogen isotopes in feathers (δD_f) to infer the breeding latitude of five species of songbirds – hooded warblers Wilsonia citrina , American redstarts Setophaga ruticilla , black-and-white warblers Mniotilta varia , ovenbirds Seiurus aurocapilla , and northern waterthrushes S. noveboracensis – that were captured at a stopover site along the coast of southwestern Louisiana in spring 2004. Values of δD_f across all species ranged from −163 to −35‰ (n=212), and within most species the range was consistent with the latitudinal extent of known breeding sites in central and eastern North America. Individuals that arrived first along the northern Gulf coast had δD_f values indicative of southerly breeding sites in hooded warblers, American redstarts, black-and-white warblers, and ovenbirds, but no relationship was found between passage timing and δD_f for northern waterthrushes. Our findings suggest that spring passage is often timed to coincide with the emergence of suitable conditions on breeding areas, with southern breeding birds migrating first.     

Flexibility of Continental Navigation and Migration in European Mallards

The ontogeny of continent-wide navigation mechanisms of the individual organism, despite being crucial for the understanding of animal movement and migration, is still poorly understood. Several previous studies, mainly conducted on passerines, indicate that inexperienced, juvenile birds may not generally correct for displacement during fall migration. Waterbirds such as the mallard (Anas platyrhynchos, Linnaeus 1758) are more flexible in their migration behavior than most migratory songbirds, but previous experiments with waterbirds have not yet allowed clear conclusions about their navigation abilities. Here we tested whether immature mallard ducks correct for latitudinal displacement during fall migration within Europe. During two consecutive fall migration periods, we caught immature females on a stopover site in southeast Sweden, and translocated a group of them ca. 1,000 km to southern Germany. We followed the movements of the ducks via satellite GPS-tracking and observed their migration decisions during the fall and consecutive spring migration. The control animals released in Ottenby behaved as expected from banding recoveries: they continued migration during the winter and in spring returned to the population’s breeding grounds in the Baltics and Northwest Russia. Contrary to the control animals, the translocated mallards did not continue migration and stayed at Lake Constance. In spring, three types of movement tactics could be observed: 61.5% of the ducks (16 of 26) stayed around Lake Constance, 27% (7 of 26) migrated in a northerly direction towards Sweden and 11.5% of the individuals (3 of 26) headed east for ca. 1,000 km and then north. We suggest that young female mallards flexibly adjust their migration tactics and develop a navigational map that allows them to return to their natal breeding area.     

Geolokation

Tracking bird migration with light‐level geolocators Bird ringing started to revolutionize our understanding of bird migration about 100 years ago. Since about 25 years satellite tracking of bird movements has increased our knowledge about migration strategies and migratory routes of large birds considerably. Nowadays miniature light‐level geolocators enable tracking of even small birds, though geolocators require recapture to obtain the data. Light‐level geolocators save basically the experienced sunrise and sunset events of the bird. By determining midday, midnight and length of day and night one can estimate longitude and latitude of birds' whereabouts and hence, map their migration.     

Clock gene polymorphism,migratory behaviour and geographic distribution: a comparative study of trans‐Saharan migratory birds

Migratory behaviour is controlled by endogenous circannual rhythms that are synchronized by external cues, such as photoperiod. Investigations on the genetic basis of circannual rhythmicity in vertebrates have highlighted that variation at candidate ‘circadian clock’ genes may play a major role in regulating photoperiodic responses and timing of life cycle events, such as reproduction and migration. In this comparative study of 23 trans‐Saharan migratory bird species, we investigated the relationships between species‐level genetic variation at two candidate genes, Clock and Adcyap1, and species’ traits related to migration and geographic distribution, including timing of spring migration across the Mediterranean Sea, migration distance and breeding latitude. Consistently with previous evidence showing latitudinal clines in ‘circadian clock’ genotype frequencies, Clock allele size increased with breeding latitude across species. However, early‐ and late‐migrating species had similar Clock allele size. Species migrating over longer distances, showing delayed spring migration and smaller phenotypic variance in spring migration timing, had significantly reduced Clock (but not Adcyap1) gene diversity. Phylogenetic confirmatory path analysis suggested that migration date and distance were the most important variables directly affecting Clock gene diversity. Hence, our study supports the hypothesis that Clock allele size increases poleward as a consequence of adaptation to the photoperiodic regime of the breeding areas. Moreover, we show that long‐distance migration is associated with lower Clock diversity, coherently with strong stabilizing selection acting on timing of life cycle events in long‐distance migratory species, likely resulting from the time constraints imposed by late spring migration.     

The effect of wind, season and latitude on the migration speed of white storks Ciconia ciconia, along the eastern migration route

The relation between wind, latitude and daily migration speed along the entire migration route of white storks was analysed. Mean daily migration speed was calculated using satellite telemetry data for autumn and spring migration of white storks from their breeding grounds in Germany and Poland to wintering grounds in Africa and back. The National Center for Environmental Prediction (NCEP) reanalysis data were used to systematically fit 850 mb wind vectors to daily migration speed along the migration route. White storks migrated significantly faster and had a shorter migration season in autumn (10 km/h) compared to spring (6.4 km/h). In autumn mean daily migration speed was significantly slower in Europe (8.0 km/h) than in the Middle East (11.1 km/h) and Africa (11.0 km/h). In spring mean daily migration speed was significantly faster in Africa (10.5 km/h) as birds left their wintering grounds than in the Middle East (4.3 km/h). Migration speed then increased in Europe (6.5 km/h) as birds approached their breeding grounds. In both spring and autumn tailwind (at 850mb) and latitude were found to be significant variables related to daily migration speed.     

Avian navigation and geographic positioning

Site fidelity to breeding and wintering grounds, and even stopover sites, suggests that passerines are capable of accurate navigation during their annual migrations. Geolocator‐based studies are beginning to demonstrate precise population‐specific migratory routes and even some interannual consistency in individual routes. Displacement studies of birds have shown that at least adult birds are capable of goal‐oriented movements, likely involving some type of map or geographic position system. In contrast, juveniles on their first migration use a clock‐and‐compass orientation strategy, with limited knowledge about locations along their migratory routes. Positioning information could come from a variety of cues including visual, olfactory, acoustic, and geomagnetic sources. How information from these systems is integrated and used for avian navigation has yet to be fully articulated. In this review, we (1) define geographic positioning and distinguish the types of navigational strategies that birds could use for orientation, (2) describe sensory cues available to birds for geographic positioning, (3) review the evidence for geographic positioning in birds and methods used to collect that evidence, and (4) discuss ways ornithologists, particularly field ornithologists, can contribute to and advance our knowledge of the navigational abilities of birds. Few studies of avian orientation and navigation mechanisms have been conducted in the Western Hemisphere. To fully understand migratory systems in the Western Hemisphere and develop better conservation policies, information about the orientation and navigation mechanisms used by specific species needs to be integrated with other aspects of their migration ecology and biology.     

A place to land: spatiotemporal drivers of stopover habitat use by migrating birds

Migrating birds require en route habitats to rest and refuel. Yet, habitat use has never been integrated with passage to understand the factors that determine where and when birds stopover during spring and autumn migration. Here, we introduce the stopover‐to‐passage ratio (SPR), the percentage of passage migrants that stop in an area, and use 8 years of data from 12 weather surveillance radars to estimate over 50% SPR during spring and autumn through the Gulf of Mexico and Atlantic coasts of the south‐eastern US, the most prominent corridor for North America’s migratory birds. During stopovers, birds concentrated close to the coast during spring and inland in forested landscapes during autumn, suggesting seasonal differences in habitat function and highlighting the vital role of stopover habitats in sustaining migratory communities. Beyond advancing understanding of migration ecology, SPR will facilitate conservation through identification of sites that are disproportionally selected for stopover by migrating birds.     

A test of the influence of continental axes of orientation on patterns of human gene flow

The geographic distribution of genetic variation reflects trends in past population migrations and can be used to make inferences about these migrations. It has been proposed that the east-west orientation of the Eurasian landmass facilitated the rapid spread of ancient technological innovations across Eurasia, while the north-south orientation of the Americas led to a slower diffusion of technology there. If the diffusion of technology was accompanied by gene flow, then this hypothesis predicts that genetic differentiation in the Americas along lines of longitude will be greater than that in Eurasia along lines of latitude. We use 678 microsatellite loci from 68 indigenous populations in Eurasia and the Americas to investigate the spatial axes that underlie population-genetic variation. We find that genetic differentiation increases more rapidly along lines of longitude in the Americas than along lines of latitude in Eurasia. Distance along lines of latitude explains a sizeable portion of genetic distance in Eurasia, whereas distance along lines of longitude does not explain a large proportion of Eurasian genetic variation. Genetic differentiation in the Americas occurs along both latitudinal and longitudinal axes and has a greater magnitude than corresponding differentiation in Eurasia, even when adjusting for the lower level of genetic variation in the American populations. These results support the view that continental orientation has influenced migration patterns and has played an important role in determining both the structure of human genetic variation and the distribution and spread of cultural traits.