Magnetic Navigation

Recent evidence suggests that some amphibians, reptiles and birds may be capable of homing using information about geographic position (“map” information) derived from subtle geographic gradients in the earth's magnetic field. The “magnetic map” hypothesis faces numerous theoretical difficulties, however, due to the extremely high level of sensitivity that would be necessary to detect natural magnetic gradients, and to the presence of spatial irregularities and temporal variation in the geomagnetic field that might make map coordinates derived from magnetic gradients unreliable. To date, the majority of studies carried out to test the magnetic map hypothesis have involved field observations of the effects on homing orientation of naturally occurring spatial or temporal variation in the geomagnetic field. While providing an important first step, these studies are subject to the criticism that the observed changes in homing orientation could result from effects on a magnetic compass, or some other unidentified component of the navigational system, rather than from effects on a magnetic map. The recent development of experimental systems in which navigational ability can be studied under controlled or semi-controlled laboratory conditions has opened up the possibility of using new experimental approaches to more rigorously test the magnetic map hypothesis. After briefly reviewing the available evidence of the geomagnetic field's involvement in the map component of homing, a simple graphical model is presented which describes how the home direction derived from a bicoordinate map varies as a function of the value of one of the map coordinates when the value of the second map coordinate is held constant. In studies of homing orientation in which the value of a specific magnetic field parameter (e.g., total intensity, inclination, etc.) can be varied independently of other putative map parameters, the graphical model can be used to generate qualitative predictions about the changes in the direction of homing orientation that should be observed if the magnetic field parameter being manipulated serves as one coordinate of a bicoordinate map. The relationship between the direction of homing orientation and the value of a putative magnetic map parameter can also be used to generate quantitative predictions about characteristics of the local gradient of that magnetic field parameter in the vicinity of the home site (i.e., the alignment and “home value” of the local gradient) which can then be compared with actual measured values. Together, the qualitative and quantitative predictions of the graphical model permit rigorous tests of whether one or both coordinates of a bicoordinate navigational map are derived from the geomagnetic field.     

Orientation and navigation in Amphibia

Aquatic and terrestrial amphibians integrate acoustic, magnetic, mechanical, olfactory and visual directional information into a redundant-multisensory orientation system. The sensory information is processed to accomplish homing following active or passive displacement by either path integration, beaconing, pilotage, compass orientation or true navigation. There is evidence for two independent compass systems, a time-compensated compass based on celestial cues and a light-dependent magnetic inclination compass. Beaconing along acoustic or olfactory gradients emanating from the home site, as well as pilotage along fixed visual landmarks also form an important part in the behaviour of many species. True navigation has been shown in only one species, the aquatic salamander Notophthalmus viridescens. Evidence on the nature of the navigational map obtained so far is compatible with the magnetic map hypothesis.     

Use of a Magnetic Compass for Nocturnal Homing Orientation in the Palmate Newt, Lissotriton helveticus

Previous studies have shown that migrating palmate newts (Lissotriton helveticus) can rely on acoustic cues for orientation to breeding ponds. Nonetheless, although acoustic cues are reliable over relatively short distances, they are unlikely to account for the long‐distance homing demonstrated in several other species of newts. Most individuals of L. helveticus migrate only a few hundred meters (Diego‐Rasilla, F. J. & Luengo, R. M. 2007: Acoustic orientation in the palmate newt, Lissotriton helveticus. Behav. Ecol. Sociobiol. 61, 1329—1335), raising the possibility that this species may only utilize short‐distance cues (Joly, P. & Miaud, C. 1993: How does a newt find its pond? The role of chemical cues in migrating newts (Triturus alpestris). Ethol. Ecol. Evol. 5, 447—455; Russell, A. P., Bauer, A. M. & Johnson, M. K. 2005: Migration of amphibians and reptiles: an overview of patterns and orientation mechanisms in relation to life history strategies. In: Migration of Organisms (Elewa, M. T., ed). Springer‐Verlag, Berlin Heidelberg, pp. 151—203; Sinsch, U. 2006: Orientation and navigation in Amphibia. Mar. Freshw. Behav. Phy. 39, 65—71). Therefore, experiments were carried out to investigate the use of the geomagnetic field in the nocturnal homing orientation of L. helveticus. Tests were carried out at night in an outdoor circular arena, under total overcast sky that prevented access to celestial compass cues. Individual newts were tested in one of four symmetrical alignments of an earth‐strength magnetic field. We studied the orientation behaviour of newts from two breeding ponds located 9.05 km west‐southwest and 19 km east‐northeast of the testing site. The distribution of magnetic bearings from both groups of newts exhibited significant orientation in the homeward direction. These findings indicate that palmate newts are capable of long‐distance homing and are able to orient in the homeward direction at night using the magnetic compass as the sole source of directional (i.e., compass) information.     

Magnetic maps in animals: a theory comes of age?

The magnetic map hypothesis proposes that animals can use spatial gradients in the Earth's magnetic field to help determine geographic location. This ability would permit true navigation--reaching a goal from an entirely unfamiliar site with no goal-emanating cues to assist. It is a highly contentious hypothesis since the geomagnetic field fluctuates in time and spatial gradients may be disturbed by geological anomalies. Nevertheless, a substantial body of evidence offers support for the hypothesis. Much of the evidence has been indirect in nature, such as the identification of avian magnetoreceptor mechanisms with functional properties that are consistent with those of a putative map detector or the patterns of orientation of animals exposed to temporal and/or spatial geomagnetic anomalies. However; the most important advances have been made in conducting direct tests of the magnetic map hypothesis by exposing experienced migrants to specific geomagnetic values representing simulated displacements. Appropriate shifts in the direction of orientation, which compensate for the simulated displacements, have been observed in newts, birds, sea turtles, and lobsters, and provide the strongest evidence to date for magnetic map navigation. Careful experimental design and interpretation of orientation data will be essential in the future to determine which components of the magnetic field are used to derive geographic position.     

Innate preference for magnetic compass direction in the Alpine newt, <Emphasis Type="Italic">Triturus alpestris</Emphasis> (Salamandridae,Urodela)?

Magnetic compass orientation was first discovered for migrating/homing birds in which all individuals of a population or species prefer a predictable magnetic direction during a particular migratory situation. If all other sensory cues are absent, the Earth’s magnetic field may serve as a reference for other orientation mechanisms. It will be demonstrated that alpine newts (Triturus alpestris, Salamandridae) spontaneously align according to the natural or the deviated magnetic field lines of the Earth. They are able to do this in the dark and by apparently seeking to maintain a specific angle with respect to the magnetic field vector. When the horizontal component of the magnetic vector was eliminated, animals became disoriented, and orientation became random. We infer that the animals observed had learned to prefer a particular magnetic direction following environmental/geographical cues. Alternatively, the magnetic directional alignments are innate as, e.g. in migrating birds, but these may be modified/altered according to season, age, hormonal status, and environmental factors such as “landmarks”, light-, sound-, or olfactory cues. Numerous observations of the aligning showed that the preference for a certain magnetic compass direction/axis was not only individual but also specific for the population-subgroups tested. Specimens roughly preferred magnetic directions close to east or west. However, the larvae were able to learn to align to obviously attractive hiding spots (tubes) that were provided in a direction that deviated with respect to the first magnetic preference. The new conditioned alignments were, again, referred to magnetically by the animals and remained stable, even if the hiding tubes were absent. Animals preferred that direction until, eventually, a new directional cue became attractive.     

鸟类磁感受的生物物理机制研究进展

行为学实验表明,许多鸟类能够感受到地磁信息,并利用地磁信息完成迁徙或归巢。地磁场信息能提供可靠导航信息,磁力线可提供罗盘信息,而磁场强度和倾角可提供位置信息。文章介绍了鸟类磁感受机制的两种重要假说——基于磁铁矿的磁感受假说和化学磁感受假说,阐明了两种假说的理论原理及实验证据,对地磁信息传导神经通路与处理脑区做了评述,并展望了其发展方向。     

生物磁学在鸟类定向研究中的进展

地球上广泛存在的地磁场能够为导航提供可靠的信息,因此很多鸟类在迁徙和归巢过程中都使用地磁信息来保证航行方向的正确,在迁徙的鸟类中已经发现有18种是利用地磁罗盘进行定向和导航的。本文从鸟类使用的磁罗盘、航行地图以及磁感应机制等几方面阐述了目前在鸟类生物磁学方面的研究进展。     

The osmotic magnetometer: a new model for magnetite-based magnetoreceptors in animals

Homing pigeons and migratory birds are well known examples for animals that use the geomagnetic field for their orientation. Yet, neither the underlying receptor mechanism nor the magnetoreceptor itself is known. Recently, an innervated structure containing clusters of magnetite nanocrystals was identified in the upper beak skin of the homing pigeon. Here we show theoretically that such a cluster has a magnetic-field-dependent shape, even in fields as weak as the Earth's magnetic field; by converting magnetic stimuli into mechanical strain, the clusters can be assumed as primary units of magnetoperception in homing pigeons. Since the orientation of the strain ellipsoid indicates the direction of the external magnetic field, a cluster of magnetite nanocrystals also has the potential to serve as the basis of the so-called inclination compass of migratory birds. It is quantitatively demonstrated that the magnetic-field-induced shape change of a cluster can be amplified as well as counterbalanced by means of osmotic pressure regulation, which offers an elegant possibility to determine the magnetic field strength just by measuring changes in concentration. Received: 18 May 1998 / Revised version: 11 February 1999 / Accepted: 11 February 1999     

Light-Dependent Shift in Bullfrog Tadpole Magnetic Compass Orientation: Evidence for a Common Magnetoreception Mechanism in Anuran and Urodele Amphibians

Previous studies have demonstrated the presence of a light‐dependent magnetic compass in a urodele amphibian, the eastern red‐spotted newt Notophthalmus viridescens, mediated by extraocular photoreceptors located in or near the pineal organ. Newts tested under long‐wavelength (≥500 nm) light exhibited a 90° shift in the direction of orientation relative to newts tested under full spectrum (white) or short‐wavelength light. Here we report that bullfrog tadpoles Rana catesbeiana (an anuran amphibian) exhibit a 90° shift in the direction of magnetic compass orientation under long‐wavelength (≥500 nm) light similar to that observed in newts, suggesting that a common light‐dependent mechanism mediates these responses. These findings suggest that a light‐dependent magnetic compass may have been the ancestral state in this group of vertebrates.     

Magnetic compass orientation in the Eastern red-spotted newt (Notophthalmus viridescens)

Summary Laboratory tests were carried out to examine the orientation behavior of adult Eastern red-spotted newts (Notophthalmus viridescens) to earth-strength magnetic fields. Groups of 30 to 40 newts were housed in water-filled, all-glass aquaria with an artificial shoreline at one end. The aquaria were located in a greenhouse or outdoors adjacent to the laboratory building, and aligned on either the magnetic north-south or east-west axis. Tests were carried out in an enclosed indoor arena. Newts were tested in four horizontal alignments of the magnetic field: the ambient magnetic field (magnetic north at North) and three altered fields (magnetic north rotated to East, South or West). Data were analyzed after pooling the magnetic bearings from all four conditions in such a way as to retain the component of the newts' orientation that was a consistent response to the magnetic field. Elevation of training tank water temperature was used to increase the newts' motivation to orient in the direction of shore. Newts exposed to a training tank water temperature of 33–34 °C just prior to testing exhibited consistent unimodal magnetic compass orientation. The direction of orientation was altered predictably by changing training tank alignment and location relative to the laboratory building. The results provide the first evidence of a strong, replicable magnetic compass response in a terrestrial vertebrate under controlled laboratory conditions. Further, the present study demonstrates that the Eastern newt is able to learn a directional response relative to the earth's magnetic field.     

Spontaneous preferences for magnetic compass direction in the American red-spotted newt, <Emphasis Type="Italic">Notophthalmus viridescens</Emphasis> (Salamandridae,Urodela)

In addition to other sensory modalities, migratory vertebrates are able to use the earths’ magnetic field for orientation and navigation. The magnetic cue may also serve as a reference for other orientation mechanisms. In this study, significant evidence is shown that, even in darkness, newts (Notophthalmus viridescens, Salamandridae) spontaneously align according to the natural or to the deviated earth’s magnetic field lines, thereby demonstrating a magnetic compass sensitivity. All newts preferred compass directions close to east or west or chose the E/W axially and hence sought to maintain a specific angle or axis relative to the magnetic field vector. Such an active alignment is considered an essential precondition for magnetic orientation. When the horizontal magnetic vector was experimentally compensated, animals became disoriented. We infer that the animals have either learned the preferred magnetic direction/axis individually or that these choices are innate and could even be seasonally different as in migrating birds. It is still an unanswered question as to how and where the physical and physiological mechanisms of magnetic transduction and reception take place. The visual system and other light-dependent (radical pairs) mechanisms alone are often claimed to be in function, but this must now be reconsidered given the results from animals when deprived of light. The results may therefore point to putative receptor mechanisms involving magnetite elements in specialized magneto-receptors.     

Evidence that pigeons orient to geomagnetic intensity during homing

The influence of the Earth's magnetic field on locomotory orientation has been studied in many taxa but is best understood for homing pigeons (Columba livia). Effects of experimentally induced and naturally occurring perturbations in the geomagnetic field suggest that pigeons are sensitive to changes in geomagnetic parameters. However, whether pigeons use the Earth's magnetic field for position determination remains unknown. Here we report an apparent orientation to the intensity gradient of the geomagnetic field observed in pigeons homing from sites in and around a magnetic anomaly. From flight trajectories recorded by GPS-based tracking devices, we noted that many pigeons released at unfamiliar sites initially flew, in some cases up to several kilometres, in directions parallel and/or perpendicular to the bearing of the local intensity field. This behaviour occurred irrespective of the homeward direction and significantly more often than what was expected by random chance. Our study describes a novel behaviour which provides strong evidence that pigeons when homing detect and respond to spatial variation in the Earth's magnetic field--information of potential use for navigation.     

Pineal Body and Magnetic Sensitivity: Homing in Pinealectomized Pigeons under Overcast Skies

Since birds use the earth's magnetic field for compass orientation when astronomical cues are lacking and it has recently been suggested that the pineal body is part of their magnetic compass, test releases have been performed in overcast conditions with pigeons deprived of the pineal body. On the whole, both experimental and control birds were capable of homeward orientation, though the bearings of experimental were rather more scattered. No differences in homing speed or success were recorded. Thus, the pineal body does not appear to play an important role in the homing of pigeons.     

Homing pigeons as a model for avian navigation?

The findings on the navigational mechanisms of homing pigeons and the available data on those of wild birds, in particular migrants, are compared. There are important parallels in the use of the magnetic field and the sun for directional orientation. Also the findings on the navigational ‘map’, its preferred use by experienced birds and the strategy of using route information to acquire the necessary knowledge to establish the ‘map’, obtained in pigeons studies, can probably be generalized to wild birds and migrants in their home region. It seems that birds share a common navigational system. Special development of migratory birds, however, is the innate migration program that enables young first‐time migrants to reach their still unknown wintering area.     

Avian magnetic compass: Its functional properties and physical basis

The avian magnetic compass was analyzed in bird species of three different orders - Passeriforms, Columbiforms and Galliforms - and in three different behavioral contexts, namely migratory orientation, homing and directional conditioning. The respective findings indicate similar functional properties: it is an inclination compass that works only within a functional window around the ambient magnetic field intensity, it tends to be lateralized in favor of the right eye, and it is wavelength-dependent, requiring light from the short-wavelength range of the spectrum. The underlying physical mechanisms have been identified as radical pair processes, spin-chemical reactions in specialized photopigments. The iron-based receptors in the upper beak do not seem to be involved. The existence of the same type of magnetic compass in only very distantly related bird species suggests that it may have been present already in the common ancestors of all modern birds, where it evolved as an all-purpose compass mechanism for orientation within the home range.     

The magnetite-based receptors in the beak of birds and their role in avian navigation

Iron-rich structures have been described in the beak of homing pigeons, chickens and several species of migratory birds and interpreted as magnetoreceptors. Here, we will briefly review findings associated with these receptors that throw light on their nature, their function and their role in avian navigation. Electrophysiological recordings from the ophthalmic nerve, behavioral studies and a ZENK-study indicate that the trigeminal system, the nerves innervating the beak, mediate information on magnetic changes, with the electrophysiological study suggesting that these are changes in intensity. Behavioral studies support the involvement of magnetite and the trigeminal system in magnetoreception, but clearly show that the inclination compass normally used by birds represents a separate system. However, if this compass is disrupted by certain light conditions, migrating birds show ‘fixed direction’ responses to the magnetic field, which originate in the receptors in the beak. Together, these findings point out that there are magnetite-based magnetoreceptors located in the upper beak close to the skin. Their natural function appears to be recording magnetic intensity and thus providing one component of the multi-factorial ‘navigational map’ of birds.     

Effects of Ultraviolet Radiation on Locomotion and Orientation in Roughskin Newts (Taricha granulosa)

Environmental changes, including those associated with the atmosphere may significantly affect individual animals and ultimately populations. Ultraviolet (UV) radiation, perhaps increasing due to stratospheric ozone depletion, has been linked to mortality in a number of organisms, including amphibians. The eggs and larvae of certain amphibian species hatch at significantly lower rates when exposed to ambient ultraviolet light. Yet little is known about the sublethal effects of UV radiation. For example, UV radiation may affect specific behaviors of an animal that could alter its ability to survive. To examine if UV radiation affects amphibian behavior, we used roughskin newts ( Taricha granulosa ) as a model. Newts were exposed to low-level doses of UV in the laboratory and then tested in the field to examine if UV-exposed and control (no UV) newts differed in orientation towards water or in locomotor activity levels. UV-exposed and control newts both exhibited a significant orientation towards water in field tests but there was no significant difference in orientation between treatments. However, UV-exposed newts were significantly more active than control newts. Our results suggest that exposure to short-term low levels of UV radiation alters certain behaviors. Environmentally induced changes in behavior may have significant ecological and evolutionary consequences.     

Two different types of light-dependent responses to magnetic fields in birds

A model of magnetoreception proposes that the avian magnetic compass is based on a radical pair mechanism, with photon absorption leading to the formation of radical pairs. Analyzing the predicted light dependency by testing migratory birds under monochromatic lights, we found that the responses of birds change with increasing intensity. The analysis of the orientation of European robins under 502 nm turquoise light revealed two types of responses depending on light intensity: under a quantal flux of 8.10(15) quanta m(-2) s(-1), the birds showed normal migratory orientation in spring as well as in autumn, relying on their inclination compass. Under brighter light of 54.10(15) quanta m(-2) s(-1), however, they showed a "fixed" tendency toward north that did not undergo the seasonal change and proved to be based on magnetic polarity, not involving the inclination compass. When birds were exposed to a weak oscillating field, which specifically interferes with radical pair processes, the inclination compass response was disrupted, whereas the response to magnetic polarity remained unaffected. These findings indicate that the normal inclination compass used for migratory orientation is based on a radical-pair mechanism, whereas the fixed direction represents a novel type of light-dependent orientation based on a mechanism of a different nature.     

Protein synthesis in the brain of newts undergoing limb regeneration.

The nervous system plays an important role during the process of amphibian limb regeneration. However, the molecules that are involved in such a control of regeneration are largely unknown. We have attempted to map protein synthesis in the brains of intact newts and from newts undergoing limb or tail regeneration. Our results show unique protein synthesis in the brain of newts undergoing limb regeneration. Such an analysis can lead to the identification and characterization of these proteins.     

Orientation by pigeons deprived of olfaction by nasal tubes

Summary In an effort to avoid the trauma and other nonolfactory effects produced by surgical sectioning of pigeons' olfactory nerves, and to avoid the interference with breathing produced by nostril plugs, a way of making pigeons anosmic by inserting plastic tubes in their nostrils was developed. A total of 16 experimental releases were conducted from unfamiliar sites to compare the homing behavior of birds wearing a tube in each nostril with controls wearing a tube in only one nostril. In five short-distance releases (less than 25 km), no convincing differences in initial orientation, vanishing intervals, or homing success were observed. In eleven releases from longer distances (more than 76 km), the experimental birds were random in three cases and the controls were random in two. In no case were the differences in the distributions of the bearings of experimental and control birds statistically significant, nor were there ever significant differences in vanishing intervals. However, experimental birds had much poorer homing success from these long-distance releases. It is concluded, in view of the anosmic pigeons' good orientation at distant unfamiliar sites, that olfaction is not necessary for homeward orientation and hence that it cannot be the basis of the birds' navigational map. Poor homing success from long distances is probably a consequence of the physical irritation and interference with breathing unfortunately produced by the nasal tubes.We thank our colleagues, Irene Brown, Timothy Larkin, and André Gobert for their help in conducting the releases. This research was supported by Grant BMS 75 18905 AO2 from the National Science Foundation.