Night-migratory Songbirds Research Articles

Viability of superoxide-containing radical pairs as magnetoreceptors.

The ability of night-migratory songbirds to sense the direction of the Earth's magnetic field is increasingly attributed to a photochemical mechanism in which the magnetic field acts on transient radical pairs in cryptochrome flavoproteins located in the birds' eyes. The magnetically sensitive species is commonly assumed to be [FAD•- TrpH•+], formed by sequential light-induced intraprotein electron transfers from a chain of tryptophan residues to the flavin adenine dinucleotide chromophore. However, some evidence points to superoxide, O2 •-, as an alternative partner for the flavin radical. The absence of hyperfine interactions in O2 •- could lead to a more sensitive magnetic compass, but only if the electron spin relaxation of the O2 •- radical is much slower than normally expected for a small mobile radical with an orbitally degenerate electronic ground state. In this study we use spin dynamics simulations to model the sensitivity of a flavin-superoxide radical pair to the direction of a 50 μT magnetic field. By varying parameters that characterize the local environment and molecular dynamics of the radicals, we identify the highly restrictive conditions under which a O2 •--containing radical pair could form the basis of a geomagnetic compass sensor. We conclude that the involvement of superoxide in compass magnetoreception must remain highly speculative until further experimental evidence is forthcoming.

Migratory Eurasian Reed Warblers Can Use Magnetic Declination to Solve the Longitude Problem

The longitude problem (determining east-west position) is a classical problem in human sea navigation. Prior to the use of GPS satellites, extraordinarily accurate clocks measuring the difference between local time and a fixed reference (e.g., GMT) [1] were needed to determine longitude. Birds do notappear to possess a time-difference clock sense[2]. Nevertheless, experienced night-migratory songbirds can correct for east-west displacements to unknown locations [3-9]. Consequently, migratory birds must solve the longitude problem in a different way, but how they do so has remained a scientific mystery [10]. We suggest that experienced adult Eurasian reed warblers (Acrocephalus scirpaceus) can use magnetic declination to solve the longitude problem at least under some circumstances under clear skies. Experienced migrants tested during autumn migration in Rybachy, Russia, were exposed to an 8.5° change in declination while all other cues remained unchanged. This corresponds to a virtual magnetic displacement to Scotland if and only if magnetic declination is a part of their map. The adult migrants responded by changing their heading by 151° from WSW to ESE, consistent with compensation for the virtual magnetic displacement. Juvenile migrants that had not yet established a navigational map also oriented WSW at the capture site but became randomly oriented when the magnetic declination was shifted 8.5°. Incombination with latitudinal cues, which birds are known to detect and use [10-12], magnetic declination could provide the mostly east-west component for a true bi-coordinate navigation system under clear skies for experienced migratory birds in some areas of the globe.

Geomagnetic information modulates nocturnal migratory restlessness but not fueling in a long distance migratory songbird

Geomagnetic cues have been shown to influence migratory orientation and migratory fuelling in night‐migratory songbird species. Here, we used captive‐bred northern wheatears Oenanthe oenanthe from the southern Norwegian population to show that other aspects of the birds’ migratory program can be influenced by magnetic cues as well. We observed that the amount of migratory restlessness increased strongly with progression of the migratory season when the birds were kept constantly in the magnetic field of northern Germany, but the amount of migratory restlessness decreased when the magnetic field changed along the birds’ natural flyway are simulated. Thus, the Earth's magnetic field can also act as a ‘signpost’ cue for fine‐tuning the spatio‐temporal course of migration.

Migratory blackcaps can use their magnetic compass at 5 degrees inclination, but are completely random at 0 degrees inclination.

It is known that night-migratory songbirds use a magnetic compass measuring the magnetic inclination angle, i.e. the angle between the Earth’s surface and the magnetic field lines, but how do such birds orient at the magnetic equator? A previous study reported that birds are completely randomly oriented in a horizontal north-south magnetic field with 0° inclination angle. This seems counter-intuitive, because birds using an inclination compass should be able to separate the north-south axis from the east-west axis, so that bimodal orientation might be expected in a horizontal field. Furthermore, little is known about how shallow inclination angles migratory birds can still use for orientation. In this study, we tested the magnetic compass orientation of night-migratory Eurasian blackcaps (Sylvia atricapilla) in magnetic fields with 5° and 0° inclination. At 5° inclination, the birds oriented as well as they did in the normal 67° inclined field in Oldenburg. In contrast, they were completely randomly oriented in the horizontal field, showing no sign of bimodality. Our results indicate that the inclination limit for the magnetic compass of the blackcap is below 5° and that these birds indeed seem completely unable to use their magnetic compass for orientation in a horizontal magnetic field.

Weak Broadband Electromagnetic Fields are More Disruptive to Magnetic Compass Orientation in a Night-Migratory Songbird (Erithacus rubecula) than Strong Narrow-Band Fields.

Magnetic compass orientation in night-migratory songbirds is embedded in the visual system and seems to be based on a light-dependent radical pair mechanism. Recent findings suggest that both broadband electromagnetic fields ranging from ~2 kHz to ~9 MHz and narrow-band fields at the so-called Larmor frequency for a free electron in the Earth’s magnetic field can disrupt this mechanism. However, due to local magnetic fields generated by nuclear spins, effects specific to the Larmor frequency are difficult to understand considering that the primary sensory molecule should be organic and probably a protein. We therefore constructed a purpose-built laboratory and tested the orientation capabilities of European robins in an electromagnetically silent environment, under the specific influence of four different oscillating narrow-band electromagnetic fields, at the Larmor frequency, double the Larmor frequency, 1.315 MHz or 50 Hz, and in the presence of broadband electromagnetic noise covering the range from ~2 kHz to ~9 MHz. Our results indicated that the magnetic compass orientation of European robins could not be disrupted by any of the relatively strong narrow-band electromagnetic fields employed here, but that the weak broadband field very efficiently disrupted their orientation.

Daily Expression of Six Clock Genes in Central and Peripheral Tissues of a Night-Migratory SongBird: Evidence for Tissue-Specific Circadian Timing

In birds, independent circadian clocks reside in the retina, pineal, and hypothalamus, which interact with each other and produce circadian time at the functional level. However, less is known of the molecular clockwork, and of the integration between central and peripheral clocks in birds. The present study investigated this, by monitoring the timed expression of five core clock genes (Per2. Cry1. Cry2. Bmal1, and Clock) and one clock-controlled gene (E4bp4) in a night-migratory songbird, the redheaded bunting (rb; Emberiza bruniceps). The authors first partially cloned these six genes, and then measured their 24-h profiles in central (retina, hypothalamus) and peripheral (liver, heart, stomach, gut, testes) tissues, collected at six times (zeitgeber time 2 [ZT2], ZT6, ZT11, ZT13, ZT18, and ZT23; ZT0 = lights on) from birds (n = 5 per ZT) on 12 h:12 h light-dark cycle. rbPer2. rbCry1. rbBmal1, and rbClock were expressed with a significant rhythm in all the tissues, except in the retina (only rbClock) and testes. rbCry2, however, had tissue-specific expression pattern: a significant rhythm in the hypothalamus, heart, and gut, but not in the retina, liver, stomach, and testes. rbE4bp4 had a significant mRNA rhythm in all the tissues, except retina. Further, rbPer2 mRNA peak was phase aligned with lights on, whereas rbCry1. rbBmal1, and rbE4bp4 mRNA peaks were phase aligned with lights off. rbCry2 and rbClock had tissue-specific scattered peaks. For example, both rbCry2 and rbClock peaks were close to rbCry1 and rbBmal1 peaks, respectively, in the hypothalamus, but not in other tissues. The results are consistent with the autoregulatory circadian feedback loop, and indicate a conserved tissue-level circadian time generation in buntings. Variable phase relationships between gene pairs forming positive and negative limbs of the feedback loop may suggest the tissue-specific contribution of individual core circadian genes in the circadian time generation.

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.

Temperature alters the photoperiodically controlled phenologies linked with migration and reproduction in a night-migratory songbird

We investigated the effects of temperature on photoperiodic induction of the phenologies linked with migration (body fattening and premigratory night-time restlessness, Zugunruhe) and reproduction (testicular maturation) in the migratory blackheaded bunting. Birds were exposed for four weeks to near-threshold photoperiods required to induce testicular growth (11.5 L:12.5 D and 12 L:12 D) or for 18 weeks to a long photoperiod (13 L:11 D) at 22°C or 27°C (low) and 35°C or 40°C (high) temperatures. A significant body fattening and half-maximal testicular growth occurred in birds under the 12 L, but not under the 11.5 L photoperiod. Further, one of six birds in both temperature groups on 11.5 L, and four and two of six birds, respectively, in low- and high-temperature groups on 12 L showed the Zugunruhe. Buntings on 13 L in both temperature groups showed complete growth-regression cycles in body fattening, Zugunruhe and testis maturation. In birds on 13 L, high temperature attenuated activity levels, delayed onset of Zugunruhe by about 12 days, reduced body fattening and slowed testicular maturation. The effect of temperature seems to be on the rate of photoperiodic induction rather than on the critical day length. It is suggested that a change in temperature could alter the timing of the development of phenologies linked with seasonal migration and reproduction in migratory songbirds.

Night‐time neuronal activation of Cluster N in a day‐ and night‐migrating songbird

Magnetic compass orientation in a night-migratory songbird requires that Cluster N, a cluster of forebrain regions, is functional. Cluster N, which receives input from the eyes via the thalamofugal pathway, shows high neuronal activity in night-migrants performing magnetic compass-guided behaviour at night, whereas no activation is observed during the day, and covering up the birds’ eyes strongly reduces neuronal activation. These findings suggest that Cluster N processes light-dependent magnetic compass information in night-migrating songbirds. The aim of this study was to test if Cluster N is active during daytime migration. We used behavioural molecular mapping based on ZENK activation to investigate if Cluster N is active in the meadow pipit (Anthus pratensis), a day- and night-migratory species. We found that Cluster N of meadow pipits shows high neuronal activity under dim-light at night, but not under full room-light conditions during the day. These data suggest that, in day- and night-migratory meadow pipits, the light-dependent magnetic compass, which requires an active Cluster N, may only be used during night-time, whereas another magnetosensory mechanism and/or other reference system(s), like the sun or polarized light, may be used as primary orientation cues during the day.

Weather significantly influences the migratory behaviour of night-migratory songbirds tested indoors in orientation cages

Each year, millions of birds migrate from their breeding grounds to their overwintering sites and back. The success, duration and effort of such a long journey depend strongly on the meteorological parameters the birds encounter en route. The behaviour of free-flying migratory birds and those studied outdoors in orientation cages has been shown to be influenced by local weather factors. However, only a few, mostly descriptive, studies have analysed whether meteorological parameters should be considered when testing captive migratory birds indoors in orientation cages. Here, we used a statistical approach to analyse how meteorological parameters affect orientation performance in a night-migrating songbird, the garden warbler (Sylvia borin), when tested indoors in Emlen funnels. Our results show that the activity and directionality of the tested birds is influenced significantly by local atmospheric pressure. Together with previous studies, these results suggest that weather conditions have an impact on orientation behaviour even during indoor experiments. The findings emphasize the importance of mixing up and/or randomizing different conditions on any given night. Ideally, during any given test night, the same number of birds should be tested in each condition involved in a given study. Thereby, the documented weather effects will influence the results of all experimental groups equally.

Thermal paper can replace typewriter correction paper in Emlen funnels

Emlen funnels are small funnel-shaped orientation cagesused to record the spontaneously directed migratory rest-lessness (Zugunruhe) of night-migratory songbirds (Emlenand Emlen 1966). Today, almost every group studying thecompass orientation capabilities of migratory songbirdsuses the Emlen funnel method (e.g., Sandberg et al. 2002;Wiltschko and Wiltschko 2003; Ritz et al. 2004; Muheimet al. 2006; Chernetsov et al. 2008). This method providesthe most reliable and cost effective tool to analyze thespontaneous directional preference of many migratorysongbirds during the migratory season. Results from Emlenfunnel experiments also play a key role in the current rushtowards understanding how the magnetic compass sense inmigratory songbirds works (e.g., Ritz et al. 2004; Mouritsenand Ritz 2005).When Emlen first invented the method (Emlen andEmlen 1966), he used an inkpad at the bottom of the cageand lined the walls of the funnel with blotting paper toscore the ink marks as a measure of the bird’s directionalchoice. Later, Rabol (1979) got the idea to use typewritercorrection paper on the walls instead of ink and blottingpaper to record the birds’ directional preferences. This wasa significant improvement for the birds, since ‘‘Rotkehl-chen’’ (Robin Erithacus rubecula) would no longer become‘‘Blaukehlchen’’ (Bluethroat Luscinia svecica) after severalnights hopping on the inkpad. The refined typewriter cor-rection paper version of the Emlen funnel was adopted byvirtually every study using Emlen funnels after 1980 (e.g.,Mouritsen and Larsen 1998; Sandberg et al. 2002;Wiltschko and Wiltschko 2003; Ritz et al. 2004; Muheimet al. 2006). However, over the last 10 years, researchersusing the Emlen funnel method have been challengedby the disappearance of typewriters, which has made itexceedingly difficult to find a reliable supplier of appro-priately sized rolls of typewriter correction paper needed todo Emlen funnel experiments.The Wiltschko-lab in Frankfurt (e.g., Wiltschko andWiltschko 2003; Ritz et al. 2004) were instrumental inconvincing one of the producers of typewriter correctionpaper to make a final production run, which helped manycolleagues stock up on paper for several years. Unfortu-nately, the chalk-like coating on typewriter correctionpaper tends to harden with time, which means that itbecomes more and more difficult to accurately scorescratches on the paper. In addition to this problem, ourstock ran out several years ago, which made us initiate asearch for an alternative solution, as going back to the inkmethod would not be acceptable for animal welfarereasons.First, we visited the local crime unit to see if fingerprintdetection dust could help us. It did not work because itsfunction is based on the fat on the fingers which the duststicks to. But the claws of birds are normally fat free andthus claw marks cannot be visualized with fingerprintdetection dust. Second, we got the idea that maybe thepaper used in trucks to record their speed (tachopgraphcharts, ‘‘Fahrtenschreiberpapier’’ in German) could also beused to record the scratches left in Emlen funnels bymigratory birds. As a result, we tested various such papersfrom several different producers with variable success untilwe received a sample of ‘‘Thermal paper’’ product number‘‘SC55’’ from the company ‘‘Blumberg Systempapiere’’,Kalkumerstrasse 46, 40885 Ratingen-Lintorf, Germany;

A Long-Distance Avian Migrant Compensates for Longitudinal Displacement during Spring Migration

In order to perform true bicoordinate navigation, migratory birds need to be able to determine geographic latitude and longitude. The determination of latitude is relatively easy from either stellar or magnetic cues [1-3], but the determination of longitude seems challenging [4, 5]. It has therefore been suggested that migrating birds are unable to perform bicoordinate navigation and that they probably only determine latitude during their return migration [5]. However, proper testing of this hypothesis requires displacement experiments with night-migratory songbirds in spring that have not been performed. We therefore displaced migrating Eurasian reed warblers (Acrocephalus scirpaceus) during spring migration about 1000 km toward the east and found that they were correcting for displacements by shifting their orientation from the northeast at the capture site to the northwest after the displacement. This new direction would lead them to their expected breeding areas. Our results suggest that Eurasian reed warblers are able to determine longitude and perform bicoordinate navigation. This finding is surprising and presents a new intellectual challenge to bird migration researchers, namely, which cues enable birds to determine their east-west position.

A Visual Pathway Links Brain Structures Active during Magnetic Compass Orientation in Migratory Birds

The magnetic compass of migratory birds has been suggested to be light-dependent. Retinal cryptochrome-expressing neurons and a forebrain region, “Cluster N”, show high neuronal activity when night-migratory songbirds perform magnetic compass orientation. By combining neuronal tracing with behavioral experiments leading to sensory-driven gene expression of the neuronal activity marker ZENK during magnetic compass orientation, we demonstrate a functional neuronal connection between the retinal neurons and Cluster N via the visual thalamus. Thus, the two areas of the central nervous system being most active during magnetic compass orientation are part of an ascending visual processing stream, the thalamofugal pathway. Furthermore, Cluster N seems to be a specialized part of the visual wulst. These findings strongly support the hypothesis that migratory birds use their visual system to perceive the reference compass direction of the geomagnetic field and that migratory birds “see” the reference compass direction provided by the geomagnetic field.

Lateralized activation of Cluster N in the brains of migratory songbirds

Cluster N is a cluster of forebrain regions found in night-migratory songbirds that shows high activation of activity-dependent gene expression during night-time vision. We have suggested that Cluster N may function as a specialized night-vision area in night-migratory birds and that it may be involved in processing light-mediated magnetic compass information. Here, we investigated these ideas. We found a significant lateralized dominance of Cluster N activation in the right hemisphere of European robins (Erithacus rubecula). Activation predominantly originated from the contralateral (left) eye. Garden warblers (Sylvia borin) tested under different magnetic field conditions and under monochromatic red light did not show significant differences in Cluster N activation. In the fairly sedentary Sardinian warbler (Sylvia melanocephala), which belongs to the same phyolgenetic clade, Cluster N showed prominent activation levels, similar to that observed in garden warblers and European robins. Thus, it seems that Cluster N activation occurs at night in all species within predominantly migratory groups of birds, probably because such birds have the capability of switching between migratory and sedentary life styles. The activation studies suggest that although Cluster N is lateralized, as is the dependence on magnetic compass orientation, either Cluster N is not involved in magnetic processing or the magnetic modulations of the primary visual signal, forming the basis for the currently supported light-dependent magnetic compass mechanism, are relatively small such that activity-dependent gene expression changes are not sensitive enough to pick them up.

Night-vision brain area in migratory songbirds

Twice each year, millions of night-migratory songbirds migrate thousands of kilometers. To find their way, they must process and integrate spatiotemporal information from a variety of cues including the Earth's magnetic field and the night-time starry sky. By using sensory-driven gene expression, we discovered that night-migratory songbirds possess a tight cluster of brain regions highly active only during night vision. This cluster, here named "cluster N," is located at the dorsal surface of the brain and is adjacent to a known visual pathway. In contrast, neuronal activation of cluster N was not increased in nonmigratory birds during the night, and it disappeared in migrants when both eyes were covered. We suggest that in night-migratory songbirds cluster N is involved in enhanced night vision, and that it could be integrating vision-mediated magnetic and/or star compass information for night-time navigation. Our findings thus represent an anatomical and functional demonstration of a specific night-vision brain area.

Migratory Birds Use Head Scans to Detect the Direction of the Earth's Magnetic Field

Night-migratory songbirds are known to use a magnetic compass , but how do they detect the reference direction provided by the geomagnetic field, and where is the sensory organ located? The most prominent characteristic of geomagnetic sensory input, whether based on visual patterns or magnetite-mediated forces , is the predicted symmetry around the north-south or east-west magnetic axis. Here, we show that caged migratory garden warblers perform head-scanning behavior well suited to detect this magnetic symmetry plane. In the natural geomagnetic field, birds move toward their migratory direction after head scanning. In a zero-magnetic field , where no symmetry plane exists, the birds almost triple their head-scanning frequency, and the movement direction after a head scan becomes random. Thus, the magnetic sensory organ is located in the bird's head, and head scans are used to locate the reference direction provided by the geomagnetic field.

Migrating songbirds recalibrate their magnetic compass daily from twilight cues.

Night migratory songbirds can use stars, sun, geomagnetic field, and polarized light for orientation when tested in captivity. We studied the interaction of magnetic, stellar, and twilight orientation cues in free-flying songbirds. We exposed Catharus thrushes to eastward-turned magnetic fields during the twilight period before takeoff and then followed them for up to 1100 kilometers. Instead of heading north, experimental birds flew westward. On subsequent nights, the same individuals migrated northward again. We suggest that birds orient with a magnetic compass calibrated daily from twilight cues. This could explain how birds cross the magnetic equator and deal with declination.