Michael S. Painter

Spontaneous magnetic orientation in larval Drosophila shares properties with learned magnetic compass responses in adult flies and mice

SUMMARY We provide evidence for spontaneous quadramodal magnetic orientation in a larval insect. Second instar Berlin, Canton-S and Oregon-R × Canton-S strains of Drosophila melanogaster exhibited quadramodal orientation with clusters of bearings along the four anti-cardinal compass directions (i.e. 45, 135, 225 and 315 deg). In double-blind experiments, Canton-S Drosophila larvae also exhibited quadramodal orientation in the presence of an earth-strength magnetic field, while this response was abolished when the horizontal component of the magnetic field was cancelled, indicating that the quadramodal behavior is dependent on magnetic cues, and that the spontaneous alignment response may reflect properties of the underlying magnetoreception mechanism. In addition, a re-analysis of data from studies of learned magnetic compass orientation by adult Drosophila melanogaster and C57BL/6 mice revealed patterns of response similar to those exhibited by larval flies, suggesting that a common magnetoreception mechanism may underlie these behaviors. Therefore, characterizing the mechanism(s) of magnetoreception in flies may hold the key to understanding the magnetic sense in a wide array of terrestrial organisms.

Rapid Learning of Magnetic Compass Direction by C57BL/6 Mice in a 4-Armed 'Plus' Water Maze

Magnetoreception has been demonstrated in all five vertebrate classes. In rodents, nest building experiments have shown the use of magnetic cues by two families of molerats, Siberian hamsters and C57BL/6 mice. However, assays widely used to study rodent spatial cognition (e.g. water maze, radial arm maze) have failed to provide evidence for the use of magnetic cues. Here we show that C57BL/6 mice can learn the magnetic direction of a submerged platform in a 4-armed (plus) water maze. Naïve mice were given two brief training trials. In each trial, a mouse was confined to one arm of the maze with the submerged platform at the outer end in a predetermined alignment relative to magnetic north. Between trials, the training arm and magnetic field were rotated by 180° so that the mouse had to swim in the same magnetic direction to reach the submerged platform. The directional preference of each mouse was tested once in one of four magnetic field alignments by releasing it at the center of the maze with access to all four arms. Equal numbers of responses were obtained from mice tested in the four symmetrical magnetic field alignments. Findings show that two training trials are sufficient for mice to learn the magnetic direction of the submerged platform in a plus water maze. The success of these experiments may be explained by: (1) absence of alternative directional cues (2), rotation of magnetic field alignment, and (3) electromagnetic shielding to minimize radio frequency interference that has been shown to interfere with magnetic compass orientation of birds. These findings confirm that mice have a well-developed magnetic compass, and give further impetus to the question of whether epigeic rodents (e.g., mice and rats) have a photoreceptor-based magnetic compass similar to that found in amphibians and migratory birds.

Magnetic compass orientation by larval Drosophila melanogaster.

We report evidence for magnetic compass orientation by larval Drosophila melanogaster. Groups of larvae were exposed from the time of hatching to directional ultraviolet (365nm) light emanating from one of four magnetic directions. Larvae were then tested individually on a circular agar plate under diffuse light in one of four magnetic field alignments. The larvae exhibited magnetic compass orientation in a direction opposite that of the light source in training. Evidence for a well-developed magnetic compass in a larval insect that moves over distances of at most a few tens of centimeters has important implications for understanding the adaptive significance of orientation mechanisms like the magnetic compass. Moreover, the development of an assay for studying magnetic compass orientation in larval D. melanogaster will make it possible to use a wide range of molecular genetic techniques to investigate the neurophysiological, biophysical, and molecular mechanisms underlying the magnetic compass.

Spontaneous Magnetic Alignment by Yearling Snapping Turtles: Rapid Association of Radio Frequency Dependent Pattern of Magnetic Input with Novel Surroundings

We investigated spontaneous magnetic alignment (SMA) by juvenile snapping turtles using exposure to low-level radio frequency (RF) fields at the Larmor frequency to help characterize the underlying sensory mechanism. Turtles, first introduced to the testing environment without the presence of RF aligned consistently towards magnetic north when subsequent magnetic testing conditions were also free of RF (‘RF off → RF off’), but were disoriented when subsequently exposed to RF (‘RF off → RF on’). In contrast, animals initially introduced to the testing environment with RF present were disoriented when tested without RF (‘RF on → RF off’), but aligned towards magnetic south when tested with RF (‘RF on → RF on’). Sensitivity of the SMA response of yearling turtles to RF is consistent with the involvement of a radical pair mechanism. Furthermore, the effect of RF appears to result from a change in the pattern of magnetic input, rather than elimination of magnetic input altogether, as proposed to explain similar effects in other systems/organisms. The findings show that turtles first exposed to a novel environment form a lasting association between the pattern of magnetic input and their surroundings. However, under natural conditions turtles would never experience a change in the pattern of magnetic input. Therefore, if turtles form a similar association of magnetic cues with the surroundings each time they encounter unfamiliar habitat, as seems likely, the same pattern of magnetic input would be associated with multiple sites/localities. This would be expected from a sensory input that functions as a global reference frame, helping to place multiple locales (i.e., multiple local landmark arrays) into register to form a global map of familiar space.

Compass-controlled escape behavior in roe deer

We tested the hypothesis that magnetic alignment, a tendency to align the body axis with a certain angle to the field lines of the geomagnetic field, provides direction indicator (the so-called nonsense orientation) also in mammals. We measured alignment of free-ranging (grazing or standing) roe deer and the compass direction of their escape trajectories as well as the direction from the threat and to the next shelter. Roe deer were significantly nonrandomly aligned along the north-south axis when grazing. In 188 provocations performed in open flat habitats, deer also tended to escape along this axis and avoided to escape westwards or eastwards. Thus, in many provocations (those from east or west), animals fled at wide angles, either northwards or southwards and not straight away from the threat, a strategy that would maximize the distance between the animal and the danger. Since all the factors which might influence direction of escape (sun position, wind direction, direction to the shelter, straight direction from danger) were randomly distributed in time and space, they constitute just statistical noise which does not add. The only common denominator of all data sets was the magnetic field. We conclude that the north-south alignment expresses the readiness to escape along this axis and might help to synchronize the movement and cohesion of the group and also supports mental mapping of space.Significance statementThis is the first study of escape behavior in animals which considers also the role of absolute compass direction. Our findings confirm existence of magnetic alignment and thus magnetosensitivity in the roe deer and provide first evidence for its role as the so-called direction indicator in control of escape behavior in roe deer in particular and in mammals in general. Our results make the speculations more plausible that the magnetic alignment helps to organize and read the mental (cognitive) map of space. (In analogy, humans are more efficient in reading and commenting the map, if it is held in an accustomed direction: with north pointing upwards and if the person aligns with the map and with the visible landmarks.)

Shifted magnetic alignment in vertebrates: Evidence for neural lateralization?

A wealth of evidence provides support for magnetic alignment (MA) behavior in a variety of disparate species within the animal kingdom, in which an animal, or a group of animals, show a tendency to align the body axis in a consistent orientation relative to the geomagnetic field lines. Interestingly, among vertebrates, MA typically coincides with the north-south magnetic axis, however, the mean directional preferences of an individual or group of organisms is often rotated clockwise from the north-south axis. We hypothesize that this shift is not a coincidence, and future studies of this subtle, yet consistent phenomenon may help to reveal some properties of the underlying sensory or processing mechanisms, that, to date, are not well understood. Furthermore, characterizing the fine structure exhibited in MA behaviors may provide key insights to the biophysical substrates mediating magnetoreception in vertebrates. Therefore, in order to determine if a consistent shift is exhibited in taxonomically diverse vertebrates, we performed a meta-analysis on published MA datasets from 23 vertebrate species that exhibited an axial north-south preference. This analysis revealed a significant clockwise shift from the north-south magnetic axis. We summarize and discuss possible competing hypotheses regarding the proximate mechanisms underlying the clockwise shifted MA and conclude that the most likely cause of such a shift would be a lateralization in central processing of magnetic information.

High levels of maternally transferred mercury disrupt magnetic responses of snapping turtle hatchlings (Chelydra serpentina)

The Earths magnetic field is involved in spatial behaviours ranging from long-distance migration to non-goal directed behaviours, such as spontaneous magnetic alignment (SMA). Mercury is a harmful pollutant most often generated from anthropogenic sources that can bio-accumulate in animal tissue over a lifetime. We compared SMA of hatchling snapping turtles from mothers captured at reference (i.e., low mercury) and mercury contaminated sites. Reference turtles showed radio frequency-dependent SMA along the north-south axis, consistent with previous studies of SMA, while turtles with high levels of maternally inherited mercury failed to show consistent magnetic alignment. In contrast, there was no difference between reference and mercury exposed turtles on standard performance measures. The magnetic field plays an important role in animal orientation behaviour and may also help to integrate spatial information from a variety of sensory modalities. As a consequence, mercury may compromise the performance of turtles in a wide variety of spatial tasks. Future research is needed to determine the threshold for mercury effects on snapping turtles, whether mercury exposure compromises spatial behaviour of adult turtles, and whether mercury has a direct effect on the magnetoreception mechanism(s) that mediate SMA or a more general effect on the nervous system.

Use of bio-loggers to characterize red fox behavior with implications for studies of magnetic alignment responses in free-roaming animals

Background Spontaneous magnetic alignment (SMA), in which animals position their body axis in fixed alignments relative to magnetic field lines, has been shown in several classes of vertebrates and invertebrates. Although these responses appear to be widespread, the functional significance and sensory mechanism(s) underlying SMA remain unclear. An intriguing example comes from observations of wild red foxes (Vulpes vulpes) that show a ~fourfold increase in hunting success when predatory ‘mousing’ attacks are directed toward magnetic north-northeast. This form of SMA is proposed to receive input from a photoreceptor-based magnetoreception mechanism perceived as a ‘visual pattern’ and used as a targeting system to increase the accuracy of mousing attempts targeting hidden prey. However, similar to previous observational studies of magnetic orientation in vertebrates, direct evidence for the use of magnetic cues, and field-based experiments designed to characterize the biophysical mechanisms of SMA are lacking. Here, we develop a new approach for studies of SMA using triaxial accelerometer and magnetometer bio-loggers attached to semidomesticated red foxes.ResultsAccelerometer data were recorded from 415 ground-truth events of three behaviors exhibited by an adult red fox. A 5-nearest neighbor classifier was developed for behavioral analysis and performed with an accuracy of 95.7% across all three behaviors. To evaluate the generalizability of the classifier, data from a second fox were tested yielding an accuracy of 66.7%, suggesting the classifier can extract behaviors across multiple foxes. A similar classification approach was used to identify the fox’s magnetic alignment using two 8-way classifiers with differing underlying assumptions to distinguish magnetic headings in eight equally spaced 45° sectors. The magnetic heading classifiers performed with 90.0 and 74.2% accuracy, suggesting a realistic performance range for a classifier based on an independent set of training events equal in size to our sample.ConclusionsWe report the development of ‘magnetic ethograms’ in which the behavior and magnetic alignment of foxes can be accurately extracted from raw sensor data. These techniques provide the basis for future studies of SMA where direct observation is not necessary and may allow for more sophisticated experimental designs aimed to characterize the sensory mechanisms mediating SMA behavior.

First findings of brown hare (Lepus europaeus) reintroduction in relation to seasonal impact

In Europe, brown hare (Lepus europaeus) populations have been declining steadily since the 1970s. Gamekeepers can help to support brown hare wild populations by releasing cage-reared hares into the wild. Survival rates of cage-reared hares has been investigated in previous studies, however, survival times in relation to seasonality, which likely plays a crucial role for the efficacy of this management strategy, has not been evaluated. Here we examine the survival duration and daytime home ranges of 22 hares released and radio-tracked during different periods of the year in East Bohemia, Czech Republic. The majority of hares (82%) died within the first six months after release, and 41% individuals died within the first 10 days. Significant differences were found in the duration of survival with respect to the release date. Hares released in the summer months (July and August) survived the longest (on average 103.2 days, SD ± 23.8) and hares released throughout all other months of the year survived for significantly shorter periods of time (on average 20.4 days, SD ± 11.5). The most likely cause of death was red fox predation (38.9%) followed by disease (coccidiosis and other health problems) (27.8%). Three hares (16.6%) were killed by automobile traffic. After six months of radiotracking, we found the average survival time of all hares released was 58 (SD ± 70.9) days. Hares in this study preferred to remain in the vicinity of the release area and the average distance from release point to the center of the home range was 471 m.

Spatial orientation of foraging corvids consistent with spontaneous magnetic alignment responses observed in a variety of free-roaming vertebrates

Abstract. Spontaneous magnetic alignment, in which an animal or group of animals, aligns its body axis in a fixed orientation relative to the geomagnetic field has been observed across a variety of vertebrates. Although a seemingly ubiquitous spatial behaviour, the adaptive significance and sensory mechanisms underlying spontaneous magnetic alignment remain unclear. Here we report another example of spontaneous alignment during feeding behaviour from five corvid species, a well-known and geographically widespread avian taxon. Consistent with previous observational studies of magnetic alignment in free-roaming vertebrates, first- and second-order analyses show that corvids exhibit robust axial alignment corresponding with the north-south magnetic axis. In contrast, when the data is pooled relative to the suns azimuth, the first-order analysis is indistinguishable from random and the second-order statistics, although statistically significant, are a much weaker predictor of axial orientation compared to the distribution pooled relative to the magnetic field. The magnetic alignment behaviour exhibited by foraging crows reported here is compatible with previous hypotheses proposing that spontaneous magnetic alignment may help to coordinate and structure spatial behaviours in free-living organisms. Clearly, an experimental approach in future studies is needed to help shed light on the functional significance and biophysical mechanisms mediating spontaneous magnetic alignment. These data provide support for spontaneous magnetic alignment in free-roaming corvids, a widespread taxon with exceptional cognitive abilities that may offer unique advantages for future laboratory and field-based studies of magnetoreception.