Magnetic compass orientation in birds and its physiological basis

A current model suggests that magnetoreception of compass information starts with light-dependent primary processes. Light-dependency of magnetoreception is supported by behavioral experiments with homing pigeons and caged migratory birds. Three passerine species showed normal orientation under dim monochromatic light from the blue-green range of the spectrum, while they were disoriented under yellow and red light. A sevenfold increase in intensity and pre-exposure to specific wavelengths caused changes in behavior. The behavioral data indicate a complex relationship between the wavelength of light and magnetoreception, suggesting the involvement of more than one type of receptors. Extracellular recordings from the nucleus of the basal optic root and the tectum opticum identified units that responded to changes in magnetic North. Each unit showed a peak in a distinct spatial direction, so that the input of these units, processed collectively and integrated, would indicate compass directions.     

Magnetic compass orientation of European robins under 565 nm green light

European robins tested under monochromatic green light with a peak wavelength of 565 nm at an intensity of 2.1 mW m^-2 in the local geomagnetic field preferred their migratory direction, heading southward in autumn and northward in spring. Inverting of the vertical component of the magnetic field caused the robins to reverse their headings, indicating that the birds used a magnetic inclination compass to locate their migratory direction. The behavior recorded under green light at an intensity of 2.1 mW m^-2 is thus not different from that previously recorded under "white" light; it represents normal migratory orientation.     

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 μT, a field of twice this intensity, 92 μT, and a field of three times this intensity, 138 μT. 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.     

Light-dependent magnetic compass in Iberian green frog tadpoles

Here, we provide evidence for a wavelength-dependent effect of light on magnetic compass orientation in Pelophylax perezi (order Anura), similar to that observed in Rana catesbeiana (order Anura) and Notophthalmus viridescens (order Urodela), and confirm for the first time in an anuran amphibian that a 90° shift in the direction of magnetic compass orientation under long-wavelength light (≥500 nm) is due to a direct effect of light on the underlying magnetoreception mechanism. Although magnetic compass orientation in other animals (e.g., birds and some insects) has been shown to be influenced by the wavelength and/or intensity of light, these two amphibian orders are the only taxa for which there is direct evidence that the magnetic compass is light-dependent. The remarkable similarities in the light-dependent magnetic compasses of anurans and urodeles, which have evolved as separate clades for at least 250 million years, suggest that the light-dependent magnetoreception mechanism is likely to have evolved in the common ancestor of the Lissamphibia (Early Permian, ~294 million years) and, possibly, much earlier. Also, we discuss a number of similarities between the functional properties of the light-dependent magnetic compass in amphibians and blue light-dependent responses to magnetic stimuli in Drosophila melanogaster, which suggest that the wavelength-dependent 90° shift in amphibians may be due to light activation of different redox forms of a cryptochrome photopigment. Finally, we relate these findings to earlier studies showing that the pineal organ of newts is the site of the light-dependent magnetic compass and recent neurophysiological evidence showing magnetic field sensitivity in the frog frontal organ (an outgrowth of the pineal).     

Retinal cryptochrome in a migratory passerine bird: a possible transducer for the avian magnetic compass

The currently discussed model of magnetoreception in birds proposes that the direction of the magnetic field is perceived by radical-pair processes in specialized photoreceptors, with cryptochromes suggested as potential candidate molecules mediating magnetic compass information. Behavioral studies have shown that magnetic compass orientation takes place in the eye and requires light from the blue-green part of the spectrum. Cryptochromes are known to absorb in the same spectral range. Because of this we searched for cryptochrome (CRY) in the retina of European robins, Erithacus rubecula, passerine birds that migrate at night. Here, we report three individually expressed cryptochromes, eCRY1a, eCRY1b, and eCRY2. While eCRY1a and eCRY2 are similar to the cryptochromes found in the retina of the domestic chicken, eCRY1b has a unique carboxy (C)-terminal. In light of the radical-pair model, our findings support a potential role of cryptochromes as transducers for the perception of magnetic compass information in birds.     

Spontaneous expression of magnetic compass orientation in an epigeic rodent: the bank vole,Clethrionomys glareolus

Magnetoreception has been convincingly demonstrated in only a few mammalian species. Among rodents, magnetic compass orientation has been documented in four species of subterranean mole rats and two epigeic (i.e. active above ground) species—the Siberian hamster and the C57BL/6J mouse. The mole rats use the magnetic field azimuth to determine compass heading; their directional preference is spontaneous and unimodal, and their magnetic compass is magnetite-mediated. By contrast, the primary component of orientation response is learned in the hamster and the mouse, but both species also exhibit a weak spontaneous bimodal preference in the natural magnetic field. To determine whether the magnetic compass of wild epigeic rodents features the same functional properties as that of laboratory rodents, we investigated magnetic compass orientation in the bank vole Clethrionomys glareolus (Cricetidae, Rodentia). The voles exhibited a robust spontaneous bimodal directional preference, i.e. built nests and slept preferentially along the north-south axis, and deflected their directional preference according to a shift in the direction of magnetic north, clearly indicating that they were deriving directional information from the magnetic field. Thus, bimodal, axially symmetrical directional choice seems to be a common feature shared by epigeic rodents. However, spontaneous directional preference in the bank vole appeared to be more pronounced than that reported in the hamster and the mouse. These findings suggest that bank voles are well suited for future studies investigating the adaptive significance and mechanisms of magnetic orientation in epigeic rodents.     

Wind and sky as compass cues in desert ant navigation

While integrating their foraging and homing paths, desert ants, Cataglyphis fortis, depend on external compass cues. Whereas recent research in bees and ants has focused nearly exclusively on the polarization compass, two other compass systems—the sun compass and the wind (anemo) compass—as well as the mutual interactions of all these compass systems have received little attention. In this study, we show that of the two visual compass systems, it is only the polarization compass that invariably outcompetes the wind compass, while the sun compass does so only under certain conditions. If the ants are experimentally deprived of their polarization compass system, but have access simultaneously to both their sun compass and their wind compass, they steer intermediate courses. The intermediate courses shift the more towards the wind compass course, the higher the elevation of the sun is in the sky.     

Avian magnetic compass: fast adjustment to intensities outside the normal functional window

To determine how fast birds can adapt to magnetic intensities outside the normal functional window of their magnetic compass, we tested migratory birds in a magnetic field of 92,000 nT, twice the intensity of the local geomagnetic field at the test site in Frankfurt a.M., Germany. In the local field, robins showed a significant preference of their southerly migratory direction, whereas in the 92,000-nT field, they were initially disoriented. However, when the birds were preexposed to 92,000 nT for 1 h before being tested, they were able to orient under this intensity, and their behavior did not differ from that in the geomagnetic field. These data show that birds require only a short time to adjust to magnetic intensities, which they cannot spontaneously use for orientation. Interpreting these findings in view of the radical pair model (Ritz et al. 2000), this means that they can learn rather quickly to interpret novel activation patterns on their retina.     

Magnetic compass orientation of migratory birds in the presence of a 1.315 MHz oscillating field

The radical pair model of magnetoreception predicts that magnetic compass orientation can be disrupted by high frequency magnetic fields in the Megahertz range. European robins, Erithacus rubecula, were tested under monochromatic 565 nm green light in 1.315 MHz fields of 0.48 T during spring and autumn migration, with 1.315 MHz being the frequency that matches the energetic splitting induced by the local geomagnetic field. The birds responses depended on the alignment of the oscillating field with respect to the static geomagnetic field: when the 1.315 MHz field was aligned parallel with the field lines, birds significantly preferred northerly directions in spring and southerly directions in autumn. These preferences reflect normal migratory orientation, with the variance slightly increased compared to control tests in the geomagnetic field alone or to tests in a 7.0 MHz field. However, in the 1.315 MHz field aligned at a 24° angle to the field lines, the birds were disoriented in both seasons, indicating that the high frequency field interfered with magnetoreception. These finding are in agreement with theoretical predictions and support the assumption of a radical-pair mechanism underlying the processes mediating magnetic compass information in birds.     

<Emphasis Type="Italic">Tenebrio</Emphasis> beetles use magnetic inclination compass

Animals that guide directions of their locomotion or their migration routes by the lines of the geomagnetic field use either polarity or inclination compasses to determine the field polarity (the north or south direction). Distinguishing the two compass types is a guideline for estimation of the molecular principle of reception and has been achieved for a number of animal groups, with the exception of insects. A standard diagnostic method to distinguish a compass type is based on reversing the vertical component of the geomagnetic field, which leads to the opposite reactions of animals with two different compass types. In the present study, adults of the mealworm beetle Tenebrio molitor were tested by means of a two-step laboratory test of magnetoreception. Beetles that were initially trained to memorize the magnetic position of the light source preferred, during the subsequent test, this same direction, pursuant geomagnetic cues only. In the following step, the vertical component was reversed between the training and the test. The beetles significantly turned their preferred direction by 180 degrees. Our results brought until then unknown original findings that insects, represented here by the T. molitor species, use-in contrast to another previously researched Arthropod, spiny lobster-the inclination compass.     

The sea-finding behavior of hatchling olive ridley sea turtles, Lepidochelys olivacea, at the beach of San Miguel (Costa Rica)

Newly hatched olive ridley sea turtles (Lepidochelys olivacea) were tested for their directional preferences in a sand-filled circular arena in total darkness. Hatchlings that had crawled about 5 m on the beach, toward the sea preferred the southwesterly direction that would have brought them to the water line, whereas hatchlings that had been denied this experience headed eastward, a direction of unclear origin. These data suggest that a short crawl across the natural beach can set the direction in which the young turtles subsequently move. The crawling experience was sufficient to acquire the compass course that they later follow, probably with the help of a magnetic compass, not only in the water, but already while still on land.     

Navigation mit Duftkarte und Sonnenkompaß: Das Heimfindevermögen der Brieftauben

Pigeon homing, investigated as a paradigmatic example of bird navigation, appears to be based on two mechanisms of orientation whose functions correspond to those of map and compass. Tasks of the latter are usually accomplished by a sun compass, taking into account the sun's movement and time of day. Under overcast skies, the magnetic field of the earth may be used for compass orientation. The "map" part of the system, responsible for site localization, makes use of olfactory perception of atmospheric trace compounds, which must be concluded to contain positional information in unfamiliar areas up to several hundreds of kilometers from home.     

Light-Dependent Magnetoreception in Birds: Does Directional Information Change with Light Intensity?

 Magnetic compass orientation in birds is based on light-dependent processes, with magnetoreception being possible only under light containing blue and green wavelengths. To look for possible intensity-dependent effects we tested Australian silvereyes during autumn migration under monochromatic green light (565 nm) produced by light-emitting diodes at various light levels. At intensities of 0.0021 and 0.0075 W/m², the birds showed normal activity and were oriented in their seasonally appropriate migratory direction. Under low light of 0.0002 W/m² the birds were less active; scatter increased, but they still oriented in their migratory direction. Under a high light level of 0.0150 W/m², however, the test birds showed a counterclockwise shift in direction, preferring west-northwest instead of north. This change in behavior may reflect a change in the output of the magnetoreception system, resulting from a disruption of the natural balance between the wavelengths of light. Received: 18 June 1999 / Accepted in revised form: 20 September 1999     

Loft features reveal the functioning of the young pigeon’s navigational system

It is thought that young homing pigeons are able to use information acquired en route for their initial homeward orientation. However, the cues involved and mechanisms utilised are under discussion. Blocking light-dependent route-specific information during the first leg of an outward journey detour, together with analysis of pigeons that were raised under different loft conditions, allowed us to correctly evaluate the functioning of this mechanism and, more generally, the navigational map of birds. Pigeons from the same stock were raised and kept in two different lofts. The birds in the experimental groups were transported to the release sites via detours, and light-dependent information was denied during the first half of the outward journey (no compass information was available). Control birds were transported by the most direct route and had access to all available information. In general, the results showed that the low-loft birds preferred to use magnetic compass cues, whereas the high-loft birds preferred to use navigational map cues to collect information of the first part of the outward journey. The impairments observed in the homing performances of the experimental groups highlight the reliability of information collected inside the map area. Relevant to an understanding of the route-reversal mechanism was the evidence that this mechanism is able to function in the absence of compass information (birds raised in a wind-exposed loft show a detour effect). In systems where directional information could be provided by multiple sources, processing and extracting accurate course trajectories through a common mechanism may prove more efficient and reliable.     

Light-dependent magnetoreception in birds: the effect of intensity of 565-nm green light

 In a previous study, Australian silvereyes tested in autumn under monochromatic 565-nm green light at intensities of 2.1 and 7.5 mW m^–2 preferred their normal northerly migratory direction, whereas they showed a significantly different tendency towards northwest at 15.0 mW m^–2. Repeating these experiments in spring with silvereyes migrating southward, we again observed well-oriented tendencies in the migratory direction at 2.1 and 7.5 mW m^–2. At 15.0 mW m^–2, however, the birds once more preferred northwesterly directions, i.e. their response under this condition proved to be independent of the migratory direction. This contradicts the interpretation that monochromatic green light of this high intensity leads to a rotation of compass information; instead, it appears to produce sensory input that causes birds to give up their migratory direction in favor of a fixed direction of as yet unknown origin. Received: 3 April 2000 / Accepted in revised form: 19 June 2000     

In search of the sky compass in the insect brain

Like many vertebrate species, insects rely on a sun compass for spatial orientation and long- range navigation. In addition to the sun, however, insects can also use the polarization pattern of the sky as a reference for estimating navigational directions. Recent analysis of polarization vision pathways in the brain of orthopteroid insects sheds some light onto brain areas that might act as internal navigation centers. Here I review the significance, peripheral mechanisms, and central processing stages for polarization vision in insects with special reference to the locust Schistocerca gregaria. As in other insect species, polarization vision in locusts relies on specialized photoreceptor cells in a small dorsal rim area of the compound eye. Stages in the brain involved in polarized light signaling include specific areas in the lamina, medulla and lobula of the optic lobe and, in the midbrain, the anterior optic tubercle, the lateral accessory lobe, and the central complex. Integration of polarized-light signals with information on solar position appears to start in the optic lobe. In the central complex, polarization-opponent interneurons form a network of interconnected neurons. The organization of the central complex, its connections to thoracic motor centers, and its involvement in the spatial control of locomotion strongly suggest that it serves as a spatial organizer within the insect brain, including the functions of compass orientation and path integration. Time compensation in compass orientation is possibly achieved through a neural pathway from the internal circadian clock in the accessory medulla to the protocerebral bridge of the central complex.     

Pigeon orientation: effects of the application of magnets under overcast skies

 To verify the existence of a magnetic compass in birds, researchers have often released homing pigeons under overcast skies that are equipped with bar magnets on various parts of their body. In particular, Keeton was successful in finding disorientation in overcast conditions in a first series of tests, but not in a second series. The experiments reported here attempt to explain this contradiction on the basis of findings obtained by releasing pigeons equipped in a way similar to that reported in Keeton's tests and pigeons equipped in a way similar to that reported by other authors. Received: 15 November 1999 / Accepted in revised form: 28 February 2000     

Tracking pigeons in a magnetic anomaly and in magnetically “quiet” terrain

Pigeons were released at two sites of equal distance from the loft, one within a magnetic anomaly, the other in magnetically quiet terrain, and their tracks were recorded with the help of GPS receivers. A comparison of the beginning of the tracks revealed striking differences: within the anomaly, the initial phase lasted longer, and the distance flown was longer, with the pigeons' headings considerably farther from the home direction. During the following departure phase, the birds were well homeward oriented at the magnetically quiet site, whereas they continued to be disoriented within the anomaly. Comparing the tracks in the anomaly with the underlying magnetic contours shows considerable differences between individuals, without a common pattern emerging. The differences in magnetic intensity along the pigeons' path do not differ from a random distribution of intensity differences around the release site, indicating that the magnetic contours do not directly affect the pigeons' routes. Within the anomaly, pigeons take longer until their flights are oriented, but 5 km from the release point, the birds, still within the anomaly, are also significantly oriented in the home direction. These findings support the assumption that magnetically anomalous conditions initially interfere with the pigeons' navigational processes, with birds showing rather individual responses in their attempts to overcome these problems.     

水稻成熟衰老期叶际及根际氮氧化物排放的光控机制

为研究水稻成熟衰老期叶际及根际NOGs(nitrogen oxides gases, 氮氧化物)排放的光控机制,在同步测定条件下,采用密闭箱法,研究了不同光质(黄、绿、白、红、蓝光)、光强〔0.00、(50.00±2.35)(75.00±2.32)(100.00±3.89) μmol/(m2·s)〕对水稻成熟衰老期叶际及根际NOGs排放的影响. 结果表明:在相同氮源〔NH₄NO₃-N,ρ(N)为90 mg/L〕下,日间光强为(75.00±2.32) μmol/(m2·s)时,水稻成熟衰老期叶际N₂O和NO的平均排放速率分别为18.09、0.39 μg/(pot·h),二者排放量分别占各自总排放量的28.88%、30.78%;在(100.00±3.89)μmol/(m2·s)光强条件下,叶际N₂O和NO的平均排放速率则分别为23.27、0.50 μg/(pot·h),二者排放量分别占各自总排放量的36.74%、27.92%. 在0.00～(100.00±3.89)μmol/(m2·s)日间光强下,水稻叶际及根际N₂O和NO排放随随光强增加而增强,但不同光照条件下水稻叶际及根际均无明显的NO₂净排放作用. 在光强一致〔(20.00±0.48)μmol/(m2·s)〕条件下,同期黄、绿、白、红、蓝光处理的水稻叶际N₂O平均排放速率分别为24.90、15.46、13.85、16.40和19.77 μg/(pot·h),红、蓝光在抑制水稻叶际N₂O及根际NO排放的同时,也促进了水稻根际N₂O的排放. 研究显示,水稻成熟衰老期叶际及根际NOGs排放均以N₂O为主,叶际N₂O的排放可以反映根际N₂O的排放情况. 光照越强,NOGs排放就越明显. 适度控制日间光强并增加红、蓝光比例,可抑制N₂O和NO排放.      

Polarization-Sensitive Interneurons in the Optic Lobe of the Desert Ant Cataglyphis bicolor

 Desert ants, Cataglyphis bicolor (Hymenoptera), navigate by using compass information provided by skylight polarization. In this study, electrophysiological recordings were made from polarization-sensitive interneurons (POL-neurons) in the optic lobe of Cataglyphis. The POL-neurons exhibit a characteristic polarization opponency. They receive monochromatic input from the UV receptors of the specialized dorsal rim area of the compound eye. Both polarization opponency and monochromacy are features also found in the POL-neurons of crickets (Orthoptera). Received: 29 September 1999 / Accepted in revised form: 13 December 1999