Migratory Direction Research Articles

Four-and-a-Half LIM Domain Protein 2 Is a Novel Regulator of Sphingosine 1-Phosphate Receptor 1 in CCL19-Induced Dendritic Cell Migration

We identified the four-and-a-half LIM domain protein 2 (FHL2) as a novel regulator of CCL19-induced dendritic cell (DC) migration. Initiation of migration is a hallmark of DC function and plays a central role in the induction and regulation of immune responses. In vivo, DCs continuously acquire Ag in the periphery and migrate to draining lymph nodes, under the influence of local environmental chemotactic factors like CCL19/21 or sphingosine 1-phosphate (S1P). We investigated the role of S1P- and RhoA-regulated FHL2 in this process. We found reduced nuclear localization of FHL2 in mature bone marrow-derived DCs (BMDCs), compared with immature BMDCs, following stimulation with CCL19. Furthermore, in vitro-generated murine FHL2(-/-) BMDCs displayed a significantly increased migratory speed, directionality, and migratory persistence toward the chemokine CCL19 compared with wild-type BMDCs. Moreover, in vivo, FHL2(-/-) BMDCs showed increased migration toward lymphoid organs. FHL2(-/-) BMDCs increased the expression of S1PR1, which was associated with greater Rac activation. An S1PR1 antagonist and knock-down of S1PR1 abrogated the increased migratory speed of FHL2(-/-) BMDCs. Our results identify FHL2 as an important novel regulator of DC migration via regulation of their sensitivity toward environmental migratory cues like S1P and CCL19.

Autumn orientation behaviour of paddyfield warblers, Acrocephalus agricola, from a recently expanded breeding range on the western Black Sea coast

The paddyfield warbler, Acrocephalus agricola, has extended its breeding range from Central Asia to the western Black Sea coast. The Balkan population offers a unique chance to test the effect of breeding range expansion on the genetically programmed migratory direction. We studied 21 paddyfield warblers at Durankulak Lake, NE Bulgaria, by recording their autumn migratory orientation in circular orientation cages. Our data show that the preferred migratory orientation is directed along a NE-SW axis. Paddyfield warblers seem to avoid direct crossing of the Black Sea by following the western coast. The mean bearing was parallel to the nearest coastline and corresponds to the direction of the historical breeding range expansion of the species. In our experiment many individuals showed south-western orientation in autumn, a course which would potentially lead the birds to exploratory movements outside the current breeding range. An axial orientation response has been often shown in circular cage tests, and can be due to factors such as coastal orientation or reverse orientation triggered by the physiological condition of some individuals. However, it might also be one of the driving mechanisms for range expansion. Hence, we can expect the future expansion of Balkan paddyfield warblers to continue towards south-west.

Two‐year oscillation cycle in abundance of soybean aphid in Indiana

The present study evaluated the population dynamics of the heteroecious soybean aphid Aphis glycines Matsumura (Hemiptera: Aphididae) during an 8‐year period in Indiana, shortly after its detection in North America. Sampling conducted at multiple locations revealed that A. glycines exhibited a 2‐year oscillation cycle that repeated itself four times between 2001 and 2008: years of low aphid abundance were consistently followed by years of high aphid abundance. Similar patterns of abundance of A. glycines and coccinellids (Coleoptera: Coccinellidae) in soybean fields, both within and between‐years, suggest that late season predation by coccinellids plays a role in the oscillatory cycle of aphids. Insidious flower bugs Orius insidiosus (Say) (Hemiptera: Anthocoridae) were numerically more abundant than coccinellids, although the lack of synchrony between aphids and predatory bugs suggests that O. insidiosus has a limited influence on between‐year variations in aphid density. The inverse relationship between aphid densities before and after the start of the autumn migratory period changes direction in alternate years. High aphid density on soybean in the summer is associated with a reduced number of alate migrants produced in the autumn. Conversely, years with low density aphids on soybean in the summer are characterized by high numbers of alates that migrate to the primary host in the autumn. From a pest management perspective, the 2‐year oscillation cycle of A. glycines is a desirable attribute with respect to population dynamics because it implies that aphids cause significant economic damage only in alternate years (as opposed to every year). Cultural practices enhancing the conservation biological control of Coccinellidae may help to preserve the periodicity of aphid infestation and restrict the pest status of A. glycines.

Magnetoreception of Directional Information in Birds Requires Nondegraded Vision

The magnetic compass orientation of birds is light dependent. The respective directional information, originating in radical pair processes, is mediated by the right eye. These findings suggest possible interactions between magnetoreception and vision, in particular with the perception of contours, because the right eye has been found to be dominant in discrimination tasks requiring object vision. Here we report tests in the local geomagnetic field with European robins wearing goggles equipped with a clear and a frosted foil of equal translucence of 70%. Robins with a clear foil on the right eye and a frosted foil on the left eye oriented in the migratory direction as well as birds using both eyes. Birds with a frosted foil that blurred vision on the right eye and a clear foil on the left eye, in contrast, were disoriented. These findings are the first to show that avian magnetoreception requires, in addition to light, a nondegraded image formation along the projectional streams of the right retina. This suggests crucial interactions between the processing of visual pattern information and the conversion of magnetic input into directional information.

Orientation and autumn migration routes of juvenile sharp-tailed sandpipers at a staging site in Alaska

Arctic waders are well known for their impressive long-distance migrations between their high northerly breeding grounds and wintering areas in the Southern hemisphere. Performing such long migrations requires precise orientation mechanisms. We conducted orientation cage experiments with juvenile sharp-tailed sandpipers (Calidris acuminata) to investigate what cues they rely on when departing from Alaska on their long autumn migration flights across the Pacific Ocean to Australasia, and which possible migration routes they could use. Experiments were performed under natural clear skies, total overcast conditions and in manipulated magnetic fields at a staging site in Alaska. Under clear skies the juvenile sharp-tailed sandpipers oriented towards SSE, which coincides well with reported sun compass directions from their breeding grounds in Siberia towards Alaska and could reflect their true migratory direction towards Australasia assuming that they change direction towards SW somewhere along the route. Under overcast skies the sandpipers showed a mean direction towards SW which would lead them to Australasia, if they followed a sun compass route. However, because of unfavourable weather conditions (headwinds) associated with overcast conditions, these south-westerly directions could also reflect local movements. The juvenile sharp-tailed sandpipers responded clearly to the manipulated magnetic field under overcast skies, suggesting the use of a magnetic compass for selecting their courses.

The interaction of stars and magnetic field in the orientation system of night migrating birds. I. Autumn experiments with European Warblers (gen. Sylvia).

In the autumn migration periods of 1971, 1972, and 1973 the orientation behavior in registration cages of Sylvia communis, S. borin and S. cantillans was analyzed to find out what relative importance the birds assign to information from the stars and from the magnetic field for direction finding. We obtained the following results: 1. Under clear sky in the local earth's magnetic field (Control) the warblers showed directional preferences that corresponded to their expected migratory direction based on ringing recoveries. 2. When magnetic north was turned by 120 degrees to ESE (Test), all three species preferred on clear nights their migratory direction according to the magnetic field, in spite of contradicting information from the stars. 3. In a partly compensated magnetic field, which could not be used for orientation any more, no significant directional preference could be observed, although the stars were visible. Dividing these data into two groups according to whether the birds had been tested in Control or Test previously, we found a tendency for the directions selected here to depend upon the north direction of the magnetic field during the bird's previous tests. From this and from the observation that the concentration of orientation behavior decreases in the absence of stars, we derive the following orientational model: The magnetic field provides the primary directional information for migrating birds. The stars do not contain directional information in themselves, but they can become secondary sources of orientation when information from the magnetic field has been transferred to them previously. The importance of this mechanism lies in making it easier for the birds to maintain their migratory direction. The ecological advantages of such a system are discussed and critically compared to the other models of star orientation.

The effect of celestial cues on the ontogeny of non-visual orientation in the garden warbler (Sylvia borin).

It was the aim of this study to find out whether additional information from the sun and the stars during early development leads to an improvement in the young birds' non-visual orientation performance during their first autumn migration period. The results indicate that the birds' ability to determine their migratory direction can mature independently of celestial information. Celestial cues, however, appear to be involved in the normal maturation process of migratory orientation, since the availability of celestial information during ontogeny tends to impair the birds' non-visual orientation.

The Magnetic Field as a Reference System for Genetically Encoded Migratory Direction in Pied Flycatchers (Ficedula hypoleuca Pallas)

To see whether the migratory orientation of pied flycatchers (Ficedula hypoleuca Pallas) is genetically encoded with respect to the earth magnetic field a group of young birds was hand-raised. They were thus prevented from ever experiencing the sky. The birds were tested in autumn 1980 and 1981 in the local geomagnetic field (Fig. 1) and in three artificial fields (Fig. 2a-c). The results show that their magnetic compass matures independent of any experience with the sky and contains sufficient information for the birds to orient toward their migratory direction.

Geomagnetic field affects spring migratory direction in a long distance migrant

Night-migrating song birds travel to and from their wintering and breeding areas often separated thousands of kilometers apart and are clearly capable of finding intended goal areas from a distant location. Displacement experiments provide a useful way to highlight orientation and navigational skills in migrants. To investigate which cues birds actually use to compensate for displacement and the exact mechanism of each cue, experiments with manipulation of single cues are required. We conducted a simulated displacement of lesser whitethroats Sylvia curruca on spring migration. Birds were displaced not geographically but in geomagnetic space only, north and south of their breeding area to test whether they incorporate information from the geomagnetic field to find their breeding area. Lesser whitethroats held in southeast Sweden but experiencing a simulated displacement north of their breeding area (Norway) failed to show a consistent direction of orientation, whereas birds displaced south of their breeding area (Czech Republic) exhibited consistent northerly orientation, close to the expected seasonally appropriate direction, after displacement toward the trapping location. The absence of a clear compensatory direction in birds displaced north might be due to unfamiliar magnetic information or lack of sufficient information such as a magnetic gradient when moving around. By isolating one orientation cue, the geomagnetic field, we have been able to show that lesser whitethroats might incorporate geomagnetic field information to determine latitude during spring migration.

Interaction of magnetite-based receptors in the beak with the visual system underlying 'fixed direction' responses in birds

BackgroundEuropean robins, Erithacus rubecula, show two types of directional responses to the magnetic field: (1) compass orientation that is based on radical pair processes and lateralized in favor of the right eye and (2) so-called 'fixed direction' responses that originate in the magnetite-based receptors in the upper beak. Both responses are light-dependent. Lateralization of the 'fixed direction' responses would suggest an interaction between the two magnetoreception systems.ResultsRobins were tested with either the right or the left eye covered or with both eyes uncovered for their orientation under different light conditions. With 502 nm turquoise light, the birds showed normal compass orientation, whereas they displayed an easterly 'fixed direction' response under a combination of 502 nm turquoise with 590 nm yellow light. Monocularly right-eyed birds with their left eye covered were oriented just as they were binocularly as controls: under turquoise in their northerly migratory direction, under turquoise-and-yellow towards east. The response of monocularly left-eyed birds differed: under turquoise light, they were disoriented, reflecting a lateralization of the magnetic compass system in favor of the right eye, whereas they continued to head eastward under turquoise-and-yellow light.Conclusion'Fixed direction' responses are not lateralized. Hence the interactions between the magnetite-receptors in the beak and the visual system do not seem to involve the magnetoreception system based on radical pair processes, but rather other, non-lateralized components of the visual system.

Speciation: New Migratory Direction Provides Route toward Divergence

<h2>Summary</h2> Biogeographic patterns suggest that divergent migratory behaviors can drive the evolution of new species. New research on warblers reveals that a novel migratory direction has resulted in genetic and phenotypic divergence.

Magnetoreception in birds: no intensity window in “fixed direction” responses

Under 502 nm turquoise light combined with 590 nm yellow light and in total darkness, European robins, Erithacus rubecula, no longer prefer their migratory direction, but exhibit so-called fixed direction responses that do not show the seasonal change between spring and autumn. We tested robins under these light conditions in the local geomagnetic field of 46 microT, a field of twice this intensity, 92 microT, and a field of three times this intensity, 138 microT. Under all three magnetic conditions, the birds preferred the same easterly direction under turquoise-and-yellow light and the same northwesterly direction under dark, while they were oriented in their seasonally appropriate direction under control conditions. "Fixed direction" responses are thus not limited to a narrow intensity window as has been found for normal compass orientation. This can be attributed to their origin in the magnetite-based receptor in the upper beak, which operates according to fundamentally different principles than the radical pair mechanism in the retina mediating compass orientation. "Fixed direction" responses are possibly a relict of a receptor mechanism that changed its function, now mainly providing information on magnetic intensity.

Magnetic and sunset orientation in migratory redwings, Turdus iliacus

The migratory orientation behaviour of redwings (Turdus iliacus) was studied by orientation cage and release experimentation, performed in eastern Finland after sunset periods during the three autumn migration seasons of 1999–2001. The experiments were conducted outdoors under clear and overcast skies in control and two magnetic conditions: (1) in a deflected horizontal magnetic field (mN shifted 90° CCW towards geographic west); and (2) in a reversed vertical magnetic field (to test for inclination compass). Redwings showed a mean orientation towards the SW in control clear sky tests, which is an appropriate autumn migratory direction for the season. Under overcast skies, control birds' orientation was scattered. In the horizontal (1) magnetic tests, redwings showed orientation towards the direction of the setting sun under clear skies, but were likely to choose random directions under overcast skies. In the vertical (2) magnetic tests, redwings were oriented again towards the west under clear skies, but chose northern directions under overcast skies. This suggests different integration of directional information between clear and overcast conditions. With these results, one can demonstrate that redwings use a magnetic compass during the autumn migratory period, and that their magnetic compass may function as an inclination compass. In the release tests, redwings showed consistency with cage tests in both magnetic test conditions, which indicate that they had recalibrated their celestial compasses on the basis of the manipulated magnetic field they had just experienced in orientation cages. The results indicate a compromise orientation between the position of the setting sun and the expected magnetic direction, rather than a pure phototactic response.

Phylogenetic biogeography of Euphrasia section Malesianae (Orobanchaceae) in Taiwan and Malesia

Species of Euphrasia are distributed in both hemispheres with a series of connecting localities on the mountain peaks of Taiwan and the Malesian region including Luzon, Borneo, Sulawesi, Seram and New Guinea. Two hypotheses are proposed to explain this distribution pattern. The Northern Hemisphere might have been the centre of origin or the Southern Hemisphere. This study aims to reconstruct the core phylogeny of Euphrasia in the connecting areas and tries to identify the migratory direction of Euphrasia in Taiwan and Malesia. The phylogeny of Euphrasia, including sections Euphrasia, Malesianae and Pauciflorae, is reconstructed with the chloroplast molecular markers rps2 gene, trnL intron and trnL-trnF intergenic spacer. The results suggest that the migratory direction between Taiwan and the Philippines is possibly from the north to the south. However, the migratory direction within section Malesianae and the centre of origin of Euphrasia remain unanswered from our data. More data is needed to clarify this issue.

COUP-TFII Is Preferentially Expressed in the Caudal Ganglionic Eminence and Is Involved in the Caudal Migratory Stream

While the cortical interneurons derived from the medial ganglionic eminence (MGE) migrate rather diffusely into the cortex, interneurons that migrate out from the caudal ganglionic eminence (CGE) mainly move caudally into the caudal cerebral cortex and the hippocampus in the form of the caudal migratory stream (CMS) (Yozu et al., 2005). Although transplantation experiments at embryonic day 13.5 had revealed that the migrating cells in these two populations are already intrinsically different in regard to their ability to respond to the CGE environment (Yozu et al., 2005), it is not known how the CGE cells are specified and how their migratory behavior is determined. In this study we showed that, although CGE and lateral ganglionic eminence (LGE) express almost the same marker molecules, LGE cells do not migrate caudally when transplanted into the CGE, suggesting that LGE cells are intrinsically different from CGE cells. We therefore compared the transcriptomes of the CGE, MGE, and LGE, and the results showed that COUP-TFII was expressed preferentially in the CGE as well as in the migrating interneurons in the CMS. Transplantation experiments revealed that COUP-TFII is sufficient to change the direction of MGE cell migration to caudal when transplanted into the CGE environment, and knockdown of COUP-TFII inhibited the caudal migration of the CGE cells. These results suggest that COUP-TFII is both required and sufficient for the CGE-cell-specific migratory behavior in the caudal direction. Thus, a locally expressed transcription factor determines the migratory direction of the cortical interneurons in a region-specific manner.

Effects of Structure of Rho GTPase-activating Protein DLC-1 on Cell Morphology and Migration

DLC-1 encodes a Rho GTPase-activating protein (RhoGAP) and negative regulator of specific Rho family proteins (RhoA-C and Cdc42). DLC-1 is a multi-domain protein, with the RhoGAP catalytic domain flanked by an amino-terminal sterile α motif (SAM) and a carboxyl-terminal START domain. The roles of these domains in the regulation of DLC-1 function remain to be determined. We undertook a structure-function analysis involving truncation and missense mutants of DLC-1. We determined that the amino-terminal SAM domain functions as an autoinhibitory domain of intrinsic RhoGAP activity. Additionally, we determined that the SAM and START domains are dispensable for DLC-1 association with focal adhesions. We then characterized several mutants for their ability to regulate cell migration and identified constitutively activated and dominant negative mutants of DLC-1. We report that DLC-1 activation profoundly alters cell morphology, enhances protrusive activity, and can increase the velocity but reduce directionality of cell migration. Conversely, the expression of the amino-terminal domain of DLC-1 acts as a dominant negative and profoundly inhibits cell migration by displacing endogenous DLC-1 from focal adhesions.

GREAT-CIRCLE MIGRATION OF ARCTIC PASSERINES

Abstract Birds can save distance and time on their migratory journeys by following great circles rather than rhumblines, but great-circle routes require more complex orientation with changing courses. Flight directions at different places along the route and in relation to the destination can be used to test whether birds migrate along great circles or rhumblines. Such data have indicated great-circle migration among shorebirds at high latitudes, but no critical tests have been made for passerines. Using tracking radar on board the icebreaker Oden in August 2005, we recorded westerly flight directions of passerine migrants over the Chukchi Sea. The main sector of migratory directions was 237–311° centered on a mean heading direction of 274°. The most likely species to participate in this westward trans-Beringia migration, mainly departing from Alaska, were Eastern Yellow Wagtail (Motacilla tschutschensis), Arctic Warbler (Phylloscopus borealis kennicotti), Northern Wheatear (Oenanthe oenanthe), and Blueth...

Radiotelemetric Analysis of the Effects of Prevailing Wind Direction on Mormon Cricket Migratory Band Movement

During outbreaks, flightless Mormon crickets [Anabrus simplex Haldeman (Orthoptera: Tettigoniidae)] form large mobile groups known as migratory bands. These bands can contain millions of individuals that march en masse across the landscape. The role of environmental cues in influencing the movement direction of migratory bands is poorly understood and has been the subject of little empirical study. We examined the effect of wind direction on Mormon cricket migratory band movement direction by monitoring the local weather conditions and daily movement patterns of individual insects traveling in bands over the same time course at three close, but spatially distinct sites. Although weather conditions were relatively homogeneous across sites, wind directions tended to be more variable across sites during the morning hours, the period during which directional movement begins. Migratory bands at different sites traveled in distinctly different directions. However, we failed to find any evidence to suggest that the observed variation in migratory band movement direction was correlated with local wind direction at any time during the day. These results support the notion that the cues mediating migratory band directionality are likely to be group specific and that a role for landscape-scale environmental cues such as wind direction is unlikely.

Response to the comments by R. Muheim, S. Åkesson, and J.B. Phillips to our paper “Contradictory results on the role of polarized light in compass calibration in migratory songbirds”

We will not respond in detail to the lengthy and speculative arguments by which Muheim et al. try to maintain the general validity of their hypothesis, although we are surprised by their negative attitude toward adaptations of birds to specific situations of their migration, in particular concerning rapid changes in declination. Instead, we will focus on some crucial points: (1) There is agreement that birds can recalibrate celestial cues—stars and the polarisation pattern—by use of the magnetic field, if they can see the central part of the sky. Muheim et al. (2006a, b) claim, however, that birds recalibrate the magnetic course by the pattern of polarisation at sunrise and sunset, if they can see the area just above the horizon. Assigning particular importance to the area just above horizon makes little sense, when considering the degree of polarisation of the natural sky—it has its maximum, about 70%, at the zenith, but is substantially less near the horizon (Wehner 1982), with the amount depending strongly on the haze in the atmosphere. Also, as we have already pointed out, assuming a reversal of the calibration processes depending on whether or not the birds can see the sky just above horizon is counter-intuitive and makes no sense. (2) In their argument in support of the crucial importance of the area just above horizon for the calibration of the magnetic compass, Muheim et al. (2006a, b) rely heavily on two papers, those by Able and Able (1995a) and Cochran et al. (2004). The latter, as we detailed in a footnote in our paper (Wiltschko et al. 2008), might involve an entirely different phenomenon. Using the paper by Able and Able (1995a) to support their argument is problematic, as it is not clear at all whether these birds could see the sky down to the horizon—it does not say so in the paper. Muheim et al. seem to base their hypothesis on a mere assumption. Another paper (Able and Able 1995b) describes how handraised savannah sparrows recalibrated their magnetic compass to polarized light when exposed in Emlen funnels. Hence the studies by Able and Able (1995a, b) do not support the assumption that the area just above horizon is crucially important for compass calibration. (3) Selecting birds that happen by chance to head in the migratory semicircle from a randomly oriented sample does not mean that these birds are in migratory mood. Muheim et al. quote a high fat score and restlessness as evidence for the migratory state of their birds, but this is not convincing as long as the crucial criterion, namely orientation in a migratory direction, is lacking. (4) Faced with the differing results of their study (Muheim et al. 2006b) and ours (Wiltschko et al. 2008) Muheim et al. now present another highly speculative explanation based on mere assumptions, namely that our birds may have completed compass calibration prior to the experimental exposure, e.g., when they were held in the outdoor aviary. Yet our birds could not see the horizon or the experimental site from the aviary, as it was partly Communicated by H. Mouritsen.

Wind Selection and Drift Compensation Optimize Migratory Pathways in a High-Flying Moth

Numerous insect species undertake regular seasonal migrations in order to exploit temporary breeding habitats [1]. These migrations are often achieved by high-altitude windborne movement at night [2-6], facilitating rapid long-distance transport, but seemingly at the cost of frequent displacement in highly disadvantageous directions (the so-called "pied piper" phenomenon [7]). This has lead to uncertainty about the mechanisms migrant insects use to control their migratory directions [8, 9]. Here we show that, far from being at the mercy of the wind, nocturnal moths have unexpectedly complex behavioral mechanisms that guide their migratory flight paths in seasonally-favorable directions. Using entomological radar, we demonstrate that free-flying individuals of the migratory noctuid moth Autographa gamma actively select fast, high-altitude airstreams moving in a direction that is highly beneficial for their autumn migration. They also exhibit common orientation close to the downwind direction, thus maximizing the rectilinear distance traveled. Most unexpectedly, we find that when winds are not closely aligned with the moth's preferred heading (toward the SSW), they compensate for cross-wind drift, thus increasing the probability of reaching their overwintering range. We conclude that nocturnally migrating moths use a compass and an inherited preferred direction to optimize their migratory track.