Characterizing the Role of Magnetic Cues Underlying Spatial Behavior

In the 50+ years since the discovery of magnetic compass orientation by migratory songbirds, evidence for the use of magnetic cues has been obtained for a range of taxonomic groups, including several classes of vertebrate and invertebrate taxa. Surprisingly, however, the biophysical mechanisms and biological substrate that underlie magnetic sensing are still not fully understood. Moreover, while use of magnetic cues for compass orientation is intuitive, the functional significance of other forms of behavioral responses mediated by magnetic cues, such as spontaneous magnetic alignment, is less clear. The following research was carried out to investigate the mechanisms underlying magnetic orientation in vertebrates and invertebrates. This involved the modification of existing experimental systems to characterize responses to magnetic cues in laboratory animals (flies, mice) and the development of novel techniques for studying the role of magnetic cues in the spatial behavior of free-living animals (red foxes). Chapter II examines magnetic orientation in wild-type Drosophila melanogaster larvae. We show that three strains of larvae reared under non-directional ultraviolet (UV) light exhibit quadramodal spontaneous orientation along the anti-cardinal compass directions (i.e. northeast, southeast, southwest, northwest) when tested in a radially symmetrical environment under UV light. Double-blind experiments cancelling the horizontal component of the magnetic field confirmed that the response is dependent on magnetic cues rather non-magnetic features of the test environment. Furthermore, we argue that the larval quadramodal pattern of response is consistent with properties of magnetic compass orientation observed in previous studies of adult Drosophila and laboratory mice, both of which have been proposed to be mediated by a light-dependent magnetic compass mechanism. Chapter III explores the use of novel biologging techniques to collect behavioral and spatial data from free-roaming mammals. Specifically, a previous observational study of freeroaming red foxes found a 4-fold increase in the success of predatory ‘mousing’ attacks when foxes were facing ~north-northeast, consistent with magnetic alignment responses reported for a range of terrestrial animals. The authors propose that the magnetic field may be used to increase accuracy of mousing attacks. Using tri-axial accelerometer and magnetometer bio-loggers fitted to semi-domesticated red foxes, we created ‘magnetic ethograms’ from behavioral and magnetic machine learning algorithms ‘trained’ to identify three discrete behaviors (i.e. foraging, trotting, and mousing-like jumps) from raw accelerometer signatures and to classify the magnetic headings of mousing-like jumps into 45° sectors from raw magnetometer data. The classifier’s ability to accurately identify behaviors from a separate fox not used to train the algorithm suggests that these techniques can be used in future experiments to obtain reliable magnetic ethograms for free-roaming foxes. We also developed the first radiofrequency emitting collar that broadcasts in the low MHz frequency range shown to disrupt magnetic compass responses in a host of animals. The radio-frequency collars coupled with biologgers will provide a powerful tool to characterize magnetic alignment responses in predatory red foxes and can be adapted for use in studies of magnetic alignment and magnetic compass orientation in other free-roaming mammals. Chapter 3 discusses findings from a magnetic nest building assay involving male labratory mice. Mice trained to position nests in one of four directions relative to the magnetic field exhibited both learned magnetic compass responses and fixed magnetic nest positioning orientation consistent with northeast-southwest spontaneous magnetic alignment behavior previously reported for wild mice and bank voles. This is the first mammalian assay in which both learned magnetic compass orientation and spontaneous magnetic alignment were exhibited in the same species, and suggests that the use of magnetic cues in rodents may be more flexible that previously realized. Characterizing the Role of Magnetic Cues Underlying Spatial Behavior Michael Scott Painter GENERAL AUDIENCE ABSTRACT A variety of animals have been shown to use the Earth’s magnetic field to help guide diverse spatial behaviors, however, the underlying sensory mechanisms mediating this sense remain elusive. Evidence for two distinct sensory mechanisms has come from behavioral studies involving a wide range of organisms, including migratory birds, newts, mole rats, mice, and several classes of invertebrates. The following research was carried out to determine the underlying sensory mechanisms mediating magnetic sensing in larval fruit flies. Properties consistent with a light-dependent, photoreceptor-based mechanism were found to underlie innate magnetic alignment behavior in larval flies, similar to the proposed compass mechanism thought to mediate compass responses in migratory birds and newts. A reanalysis of two previous studies of learned magnetic compass responses in adult fruit flies and laboratory mice show similar behaviors when compared to that of larval flies, suggesting a common underlying light-dependent magnetic mechanism across these groups. Furthermore, we provide evidence for learned magnetic compass responses in laboratory mice, where the orientation of individuals appears to be dependent on properties of the local environment (e.g. electromagnetic, temperature, humidity) in training and testing. These data suggest that the use of magnetic cues in mammals is context-dependent and more flexible than previously recognized. We have also developed new technologies for studies of magnetic orientation in free-roaming animals. Specifically, bio-logging devices containing triaxial accelerometer and magnetometer sensors where used to create ‘magnetic ethograms’, where the behavior and magnetic alignment of an animal can be reliably and accurately extracted from raw sensor data. We also discuss possible field experiments that can be performed to provide a specific test of the underlying sensory mechanism mediating magnetic behavior in free-roaming animals. This work will likely be of interest to a broad range of disciplines including sensory ecology, ethology, quantum chemistry, biophysics, wildlife management, and conservation.