Rachel Muheim

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.

Magnetic compass orientation in C57BL/6J mice.

We report evidence for a robust magnetic compass response in C57BL/6J mice. Mice were trained to build their nests in one of four magnetic directions by creating a light gradient along the long axis of a rectangular cage and positioning a nest box at the opposite (dark) end. The mice were then tested overnight in a circular, visually symmetrical arena in one of four magnetic field alignments. The positions of the nests built in the test arena showed strong unimodal orientation in the magnetic direction coinciding with the dark end of the training cage.

Light-dependent magnetic compass orientation in amphibians and insects: candidate receptors and candidate molecular mechanisms

Magnetic compass orientation by amphibians, and some insects, is mediated by a light-dependent magnetoreception mechanism. Cryptochrome photopigments, best known for their role in circadian rhythms, are proposed to mediate such responses. In this paper, we explore light-dependent properties of magnetic sensing at three levels: (i) behavioural (wavelength-dependent effects of light on magnetic compass orientation), (ii) physiological (photoreceptors/photopigment systems with properties suggesting a role in magnetoreception), and (iii) molecular (cryptochrome-based and non-cryptochrome-based signalling pathways that are compatible with behavioural responses). Our goal is to identify photoreceptors and signalling pathways that are likely to play a specialized role in magnetoreception in order to definitively answer the question of whether the effects of light on magnetic compass orientation are mediated by a light-dependent magnetoreception mechanism, or instead are due to input from a non-light-dependent (e.g. magnetite-based) magnetoreception mechanism that secondarily interacts with other light-dependent processes.

A behavioral perspective on the biophysics of the light-dependent magnetic compass: a link between directional and spatial perception?

Summary In terrestrial organisms, sensitivity to the Earths magnetic field is mediated by at least two different magnetoreception mechanisms, one involving biogenic ferromagnetic crystals (magnetite/maghemite) and the second involving a photo-induced biochemical reaction that forms long-lasting, spin-coordinated, radical pair intermediates. In some vertebrate groups (amphibians and birds), both mechanisms are present; a light-dependent mechanism provides a directional sense or ‘compass’, and a non-light-dependent mechanism underlies a geographical-position sense or ‘map’. Evidence that both magnetite- and radical pair-based mechanisms are present in the same organisms raises a number of interesting questions. Why has natural selection produced magnetic sensors utilizing two distinct biophysical mechanisms? And, in particular, why has natural selection produced a compass mechanism based on a light-dependent radical pair mechanism (RPM) when a magnetite-based receptor is well suited to perform this function? Answers to these questions depend, to a large degree, on how the properties of the RPM, viewed from a neuroethological rather than a biophysical perspective, differ from those of a magnetite-based magnetic compass. The RPM is expected to produce a light-dependent, 3-D pattern of response that is axially symmetrical and, in some groups of animals, may be perceived as a pattern of light intensity and/or color superimposed on the visual surroundings. We suggest that the light-dependent magnetic compass may serve not only as a source of directional information but also provide a spherical coordinate system that helps to interface metrics of distance, direction and spatial position.

Dramatic orientation shift of white-crowned sparrows displaced across longitudes in the high arctic

Advanced spatial-learning adaptations have been shown for migratory songbirds, but it is not well known how the simple genetic program encoding migratory distance and direction in young birds translates to a navigation mechanism used by adults. A number of convenient cues are available to define latitude on the basis of geomagnetic and celestial information, but very few are useful to defining longitude. To investigate the effects of displacements across longitudes on orientation, we recorded orientation of adult and juvenile migratory white-crowned sparrows, Zonotrichia leucophrys gambelii, after passive longitudinal displacements, by ship, of 266-2862 km across high-arctic North America. After eastward displacement to the magnetic North Pole and then across the 0 degrees declination line, adults and juveniles abruptly shifted their orientation from the migratory direction to a direction that would lead back to the breeding area or to the normal migratory route, suggesting that the birds began compensating for the displacement by using geomagnetic cues alone or together with solar cues. In contrast to predictions by a simple genetic migration program, our experiments suggest that both adults and juveniles possess a navigation system based on a combination of celestial and geomagnetic information, possibly declination, to correct for eastward longitudinal displacements.

Migratory Navigation in Birds: New Opportunities in an Era of Fast-Developing Tracking Technology

Summary Birds have remained the dominant model for studying the mechanisms of animal navigation for decades, with much of what has been discovered coming from laboratory studies or model systems. The miniaturisation of tracking technology in recent years now promises opportunities for studying navigation during migration itself (migratory navigation) on an unprecedented scale. Even if migration tracking studies are principally being designed for other purposes, we argue that attention to salient environmental variables during the design or analysis of a study may enable a host of navigational questions to be addressed, greatly enriching the field. We explore candidate variables in the form of a series of contrasts (e.g. land vs ocean or night vs day migration), which may vary naturally between migratory species, populations or even within the life span of a migrating individual. We discuss how these contrasts might help address questions of sensory mechanisms, spatiotemporal representational strategies and adaptive variation in navigational ability. We suggest that this comparative approach may help enrich our knowledge about the natural history of migratory navigation in birds.

Weather and fuel reserves determine departure and flight decisions in passerines migrating across the Baltic Sea

Departure decisions of how and when to leave a stopover site may be of critical importance for the migration performance of birds. We used an automated radiotelemetry system at Falsterbo peninsula, Sweden, to study stopover behaviour and route choice in free-flying passerines departing on flights across the Baltic Sea during autumn migration. In addition, we had an offshore receiver station (FINO 2) located about 50 km southeast from Falsterbo. Of 91 birds equipped with radiotransmitters, 19 passed FINO 2. The probability that a departing migrant passed near FINO 2 was primarily affected by winds and timing of departure. Probably, the migrants were subjected to drift by westerly winds, leading to southeasterly flight paths and an enhanced probability of passing FINO 2. Most birds passing the offshore station departed early in the night, which indicates that southward departures across the Baltic Sea usually take place during this time window. Wind condition was the dominant factor explaining the variation in flight duration between Falsterbo and FINO 2. After considering wind influence, we found additional effects of fat score and cloud cover. Birds with a higher fat score performed the flight faster than leaner individuals, as did birds that departed under clear skies compared to birds departing during overcast skies. These effects may reflect a difference in migratory motivation and airspeed between lean and fat birds together with difficulties in controlling orientation in overcast situations on oversea flights when celestial cues are unavailable. Thus, winds, clouds and fuel reserves were the primary factors determining departure and flight decisions in passerine migrants at Falsterbo in autumn

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.

Spike dives of juvenile southern bluefin tuna (Thunnus maccoyii): a navigational role?

Tunas make sharp descents and ascents around dawn and dusk called spike dives. We examine spike dives of 21 southern bluefin tuna (Thunnus maccoyii) implanted with archival tags in the Great Australian Bight. Using a new way to categorize this behavior, we show that spike dives are similar among all the fish in the study. The dive profiles are mirror images at dawn and dusk and are precisely timed with respect to sunrise and sunset. We analyze the possible reasons for spike dives, considering the timing of spike dives, the characteristic dive profile, and the tunas magnetic habitat. In addition, we present anatomical evidence for elaboration of the pineal organ, which is light mediated and has been implicated in navigation in other vertebrates. The new evidence presented here leads us to suspect that spike dives represent a survey related to navigation.

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.