The effect of yellow and blue light on magnetic compass orientation in European robins, Erithacus rubecula

To analyze the wavelength dependency of magnetic compass orientation, European robins were tested during spring migration under light of various wavelengths. Under 565-nm green light (control) the birds showed excellent orientation in their migratory direction; a 120° deflection of magnetic North resulted in a corresponding shift in the birds' directional tendencies, indicating the use of the magnetic compass. Under 443-nm blue light, the robins were likewise well oriented. Under 590-nm yellow, however, oriented behavior was no longer observed, although the activity was at the same level as under blue and green light. The spectral range where magnetic orientation is possible thus differs from the range of vision, the former showing parallels to that of rhodopsin absorption. The interpretation of the abrupt change in behavior observed between 565 green to 590 yellow is unclear. There is no simple relationship between magnetoreception and the known color receptors of birds. Accepted: 17 December 1998     

The puzzle of magnetic resonance effect on the magnetic compass of migratory birds

Experiments on the effect of radio‐frequency (RF) magnetic fields on the magnetic compass orientation of migratory birds are analyzed using the theory of magnetic resonance. The results of these experiments were earlier interpreted within the radical‐pair model of magnetoreception. However, the consistent analysis shows that the amplitudes of the RF fields used are far too small to noticeably influence electron spins in organic radicals. Other possible agents that could mediate the birds' response to the RF fields are discussed, but apparently no known physical system can be responsible for this effect. Bioelectromagnetics 30:402–410, 2009. © 2009 Wiley‐Liss, Inc.     

Development of lateralization of the magnetic compass in a migratory bird

The magnetic compass of a migratory bird, the European robin (Erithacus rubecula), was shown to be lateralized in favour of the right eye/left brain hemisphere. However, this seems to be a property of the avian magnetic compass that is not present from the beginning, but develops only as the birds grow older. During first migration in autumn, juvenile robins can orient by their magnetic compass with their right as well as with their left eye. In the following spring, however, the magnetic compass is already lateralized, but this lateralization is still flexible: it could be removed by covering the right eye for 6 h. During the following autumn migration, the lateralization becomes more strongly fixed, with a 6 h occlusion of the right eye no longer having an effect. This change from a bilateral to a lateralized magnetic compass appears to be a maturation process, the first such case known so far in birds. Because both eyes mediate identical information about the geomagnetic field, brain asymmetry for the magnetic compass could increase efficiency by setting the other hemisphere free for other processes.     

Migratory orientation of European Robins is affected by the wavelength of light as well as by a magnetic pulse

The object of this study was to test the alternative hypotheses of magnetoreception by photopigments and magnetoreception based on magnetite. Migratory European Robins, Erithacus rubecula, were tested under light of different wavelengths; after these tests, they were subjected to a brief, strong magnetic pulse designed to alter the magnetization of single domain magnetite. In control tests under white light, the birds preferred the normal, seasonally appropriate migratory direction. Under 571 nm green light, they continued to be well oriented in the migratory direction, whereas under 633 nm red light, their behaviour was not different from random. The magnetic pulse had a significant effect on migratory orientation, but the response varied between individuals: some showed a persistent directional shift, while others exhibited a change in scatter; one bird was seemingly unaffected.These findings indicate a light-dependent process and, at the same time, suggest an involvement of magnetizable material in migratory orientation. They are in agreement with the model of a light-dependent compass and a magnetite-based map, even if some questions concerning the effect of the pulse remain open.     

Avian magnetic compass can be tuned to anomalously low magnetic intensities

The avian magnetic compass works in a fairly narrow functional window around the intensity of the local geomagnetic field, but adjusts to intensities outside this range when birds experience these new intensities for a certain time. In the past, the geomagnetic field has often been much weaker than at present. To find out whether birds can obtain directional information from a weak magnetic field, we studied spontaneous orientation preferences of migratory robins in a 4 µT field (i.e. a field of less than 10 per cent of the local intensity of 47 µT). Birds can adjust to this low intensity: they turned out to be disoriented under 4 µT after a pre-exposure time of 8 h to 4 µT, but were able to orient in this field after a total exposure time of 17 h. This demonstrates a considerable plasticity of the avian magnetic compass. Orientation in the 4 µT field was not affected by local anaesthesia of the upper beak, but was disrupted by a radiofrequency magnetic field of 1.315 MHz, 480 nT, suggesting that a radical-pair mechanism still provides the directional information in the low magnetic field. This is in agreement with the idea that the avian magnetic compass may have developed already in the Mesozoic in the common ancestor of modern birds.     

Contradictory results on the role of polarized light in compass calibration in migratory songbirds

Experiments with migrating birds on the interaction between magnetic and celestial cues have produced heterogeneous results. A recent study claimed that the magnetic compass in passerine migrants is calibrated by the pattern of polarized light at sunset and sunrise and that the area just above the horizon is crucial for this calibration. To test the latter hypothesis, we performed a similar experiment with Australian Silvereyes. It produced contrary results, however, the birds, in spite of observing the natural polarization pattern at sunrise and sunset down to the horizon in an altered magnetic field, continued in their normal southerly magnetic direction when subsequently tested in the local geomagnetic field—the conflict between magnetic and polarized light cues had not caused them to recalibrate their magnetic compass. This contradicts the assumption that skylight polarization patterns generally serve as a primary calibration reference for migratory songbirds.

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

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

Behavioural and physiological mechanisms of polarized light sensitivity in birds

Polarized light (PL) sensitivity is relatively well studied in a large number of invertebrates and some fish species, but in most other vertebrate classes, including birds, the behavioural and physiological mechanism of PL sensitivity remains one of the big mysteries in sensory biology. Many organisms use the skylight polarization pattern as part of a sun compass for orientation, navigation and in spatial orientation tasks. In birds, the available evidence for an involvement of the skylight polarization pattern in sun-compass orientation is very weak. Instead, cue-conflict and cue-calibration experiments have shown that the skylight polarization pattern near the horizon at sunrise and sunset provides birds with a seasonally and latitudinally independent compass calibration reference. Despite convincing evidence that birds use PL cues for orientation, direct experimental evidence for PL sensitivity is still lacking. Avian double cones have been proposed as putative PL receptors, but detailed anatomical and physiological evidence will be needed to conclusively describe the avian PL receptor. Intriguing parallels between the functional and physiological properties of PL reception and light-dependent magnetoreception could point to a common receptor system.     

A geomagnetic declination compass for horizontal orientation in fruit flies

The Earth's geomagnetic field (GMF) is known to act as a sensory cue for magnetoreceptive animals such as birds, sea turtles, and butterflies in long‐distance migration, as well as in flies, cockroaches, and cattle in short‐distance movement or body alignment. Despite a wealth of information, the way that GMF components are used and the functional modality of the magnetic sense are not clear. A GMF component, declination, has never been proven to be a sensory cue in a defined biological context. Here, we show that declination acts as a compass for horizontal food foraging in fruit flies. In an open‐field test, adopting the food conditioning paradigm, food‐trained flies significantly orientated toward the food direction under ambient GMF and under eastward‐turned magnetic field in the absence of other sensory cues. Moreover, a declination change within the natural range, by alteration only of either the east–west or north–south component of the GMF, produced significant orientation of the trained flies, indicating that they can detect and use the difference in these horizontal GMF components. This study proves that declination difference can be used for horizontal foraging, and suggests that flies have been evolutionarily adapted to incorporate a declination compass into their multi‐modal sensorimotor system.     

Use of a magnetic compass for Y-axis orientation in premetamorphic newts (Triturus boscai)

Experiments were carried out to investigate whether premetamorphic larvae of Boscas newt (Triturus boscai) are capable of using the geomagnetic field for Y-axis orientation (i.e., orientation toward and away from shore). Larvae were trained outdoor in two different training configurations, using one training tank aligned along the magnetic north–south axis, with shore facing north, and another training tank positioned with its length along the east–west axis, with shore located west. After training, premetamorphic newts were tested in an outdoor circular arena surrounded by a pair of orthogonally aligned cube-surface coils used to alter the alignment of the Earths magnetic field. Each newt was tested only once, in one of four magnetic field alignments: ambient magnetic field (i.e., magnetic north at North), and three altered fields (magnetic north rotated to East, West, South). Distributions of magnetic bearings from tested larvae indicated that they oriented bimodally along the magnetic direction of the trained Y-axis. These findings demonstrate that T. boscai larvae are sensitive to the geomagnetic field and can use it for orienting along a learned Y-axis. This study is the first to provide evidence of Y-axis orientation, accomplished by a magnetic compass, in larval urodeles.     

Honeybee navigation: critically examining the role of the polarization compass

Although it is widely accepted that honeybees use the polarized-light pattern of the sky as a compass for navigation, there is little direct evidence that this information is actually sensed during flight. Here, we ask whether flying bees can obtain compass cues derived purely from polarized light, and communicate this information to their nest-mates through the ‘waggle dance’. Bees, from an observation hive with vertically oriented honeycombs, were trained to fly to a food source at the end of a tunnel, which provided overhead illumination that was polarized either parallel to the axis of the tunnel, or perpendicular to it. When the illumination was transversely polarized, bees danced in a predominantly vertical direction with waggles occurring equally frequently in the upward or the downward direction. They were thus using the polarized-light information to signal the two possible directions in which they could have flown in natural outdoor flight: either directly towards the sun, or directly away from it. When the illumination was axially polarized, the bees danced in a predominantly horizontal direction with waggles directed either to the left or the right, indicating that they could have flown in an azimuthal direction that was 90° to the right or to the left of the sun, respectively. When the first half of the tunnel provided axial illumination and the second half transverse illumination, bees danced along all of the four principal diagonal directions, which represent four equally likely locations of the food source based on the polarized-light information that they had acquired during their journey. We conclude that flying bees are capable of obtaining and signalling compass information that is derived purely from polarized light. Furthermore, they deal with the directional ambiguity that is inherent in polarized light by signalling all of the possible locations of the food source in their dances, thus maximizing the chances of recruitment to it.     

Field evidence of compass orientation in migrating juvenile grunts (Haemulidae)

Juvenile French and white grunts, Haemulon flavolineatum (Desmarest) and H. plumieri (Lacé-pède), were captured during their daily migrations between diurnal resting sites on coral patch reefs and nocturnal feeding grounds in seagrass beds. Grunts captured during morning and evening migrations were released on the route and after displacement up to 100 m or 5 km away. Grunts generally moved in the direction which would have taken them back towards their home reef or to their accustomed feeding sites, indicating that familiar landmarks are not essential for orientation. The spatial precision of migration may serve to partition the feeding area most efficiently. The timing of migrations is also very precise, and appears to be adapted to reduce the vulnerability of grunts to predation near their home reef.     

The role of the sun in the celestial compass of dung beetles

Recent research has focused on the different types of compass cues available to ball-rolling beetles for orientation, but little is known about the relative precision of each of these cues and how they interact. In this study, we find that the absolute orientation error of the celestial compass of the day-active dung beetle Scarabaeus lamarcki doubles from 16° at solar elevations below 60° to an error of 29° at solar elevations above 75°. As ball-rolling dung beetles rely solely on celestial compass cues for their orientation, these insects experience a large decrease in orientation precision towards the middle of the day. We also find that in the compass system of dung beetles, the solar cues and the skylight cues are used together and share the control of orientation behaviour. Finally, we demonstrate that the relative influence of the azimuthal position of the sun for straight-line orientation decreases as the sun draws closer to the horizon. In conclusion, ball-rolling dung beetles possess a dynamic celestial compass system in which the orientation precision and the relative influence of the solar compass cues change over the course of the day.     

An extremely low frequency magnetic field increases unconditioned larval movement of the common cutworm,Spodoptera litura: A novel model for a magnetoreceptive neurobehavioral study

One of the most interesting features of magnetic field (MF) responsiveness in animals is the signal transduction mechanism from sensing MF to behavior. To develop a model system for understanding the process, we performed a preliminary behavioral assay using an insect, the common cutworm, Spodoptera litura (Fabricius). In contrast to sham exposure, a continuous 60 Hz oscillating MF (0.2 mT) induced a significant increase in movement in third instar larvae: the MF‐induced movement was longer in total duration and had an earlier onset than movement from sham exposure. Not surprisingly, the movement duration of the group test was notably higher than that of the individual test, suggesting that the individual test is more favorable for assessing the MF effect on movement. Considering the simplicity of the experimental operation and obvious non‐conditioned responsiveness to the MF, this model might be suitable for studying magnetoreception and following the signal transduction mechanism between neurons and behavior.     

Seasonal differences in the hormonal control of territorial aggression in free-living European stonechats

In birds, territorial aggression during the breeding season is regulated by testosterone (T). However, many bird species also express aggressive behavior during the nonbreeding season, when plasma levels of T are low. It has been suggested that during this period estrogens might play a major role in regulating territorial aggression. In the present study we compared the effects of simultaneous blockage of androgenic and estrogenic actions on territorial aggression during the breeding and nonbreeding seasons in free-living male European stonechats (Saxicola torquata rubicola). European stonechats are of particular interest since they establish territories and form pairs during both the breeding and the nonbreeding seasons. Thus territorial aggression and its endocrine control can be compared between reproductive and non-reproductive contexts. Inhibition of androgenic and estrogenic actions by simultaneous application of Flutamide and ATD reduced territorial aggression during the breeding season, but not during the nonbreeding season. Our results show that androgens and/or estrogens are involved in the endocrine control of territorial aggression in stonechats only in a reproductive context, but not in a non-reproductive one.     

Flight-induced compass representation in the monarch butterfly heading network

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Magnetic material in the ocellar spot and lateral line of tomtates Haemulon aurolineatum

The presence of magnetic material in tissues of lateral line and ocellar spot of tomtates Haemulon aurolineatum is shown using the ferromagnetic resonance technique. For the first time magnetic material is reported in the ocellar spot. The magnetic material detected in these structures of H. aurolineatum suggests that this species could use magnetic orientation during its nocturnal foraging, and the relevance and role of this material with respect to schooling movements is discussed.     

Natal imprinting to the Earth’s magnetic field in a pelagic seabird

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