Abstract
The first demonstrations of magnetic effects on the behaviour of migratory birds and homing pigeons in laboratory and field experiments, respectively, provided evidence for the longstanding hypothesis that animals such as birds that migrate and home over long distances would benefit from possession of a magnetic sense. Subsequent identification of at least two plausible biophysical mechanisms for magnetoreception in animals, one based on biogenic magnetite and another on radical-pair biochemical reactions, led to major efforts over recent decades to test predictions of the two models, as well as efforts to understand the ultrastructure and function of the possible magnetoreceptor cells. Unfortunately, progress in understanding the magnetic sense has been challenged by: (i) the availability of a relatively small number of techniques for analysing behavioural responses to magnetic fields by animals; (ii) difficulty in achieving reproducible results using the techniques; and (iii) difficulty in development and implementation of new techniques that might bring greater experimental power. As a consequence, laboratory and field techniques used to study the magnetic sense today remain substantially unchanged, despite the huge developments in technology and instrumentation since the techniques were developed in the 1950s. New methods developed for behavioural study of the magnetic sense over the last 30 years include the use of laboratory conditioning techniques and tracking devices based on transmission of radio signals to and from satellites. Here we consider methodological developments in the study of the magnetic sense and present suggestions for increasing the reproducibility and ease of interpretation of experimental studies. We recommend that future experiments invest more effort in automating control of experiments and data capture, control of stimulation and full blinding of experiments in the rare cases where automation is impossible. We also propose new experiments to confirm whether or not animals can detect magnetic fields using the radical-pair effect together with an alternate hypothesis that may explain the dependence on light of responses by animals to magnetic field stimuli.
Highlights
During the past 50 years, suggestions that migratory and homing animals might use geomagnetic cues for navigation have moved from being a scientific fringeOne contribution of 13 to a Theme Supplement ‘Magnetoreception’.field to being a recognized discipline in animal behaviour and neuroscience
We suggest design of laboratory behavioural experiments should: (i) begin with the stimuli delivered to the subject animal in the experimental situation, (ii) ensure that the magnetic field stimuli provided are the only source of information that could be used by the animal to direct its responding in behavioural experiments, and (iii) make certain that the response produced by the animal is an unambiguous, measurable bit of behaviour that can be collected automatically wherever possible
RF sensor inclinationonly magnetic compass response in migratory birds (b) axial magnetite receptor cells or network blue signal inclinationonly magnetic compass response in migratory birds gravity sensor biophysical mechanisms for magnetic field transduction in animals as has been implied (magnetite and a radical-pair compass (Phillips 1986; Wiltschko, R. et al 2007)) or whether the data are compatible with a set of magnetite-based receptor cells, the responses of which are combined with other sensory inputs to yield the observed behaviour
Summary
During the past 50 years, suggestions that migratory and homing animals might use geomagnetic cues for navigation have moved from being a scientific fringe. Conditioning experiments were a tough nut to crack, but subsequent work demonstrated that most animals are more conditioned when they are presented with fields that are spatially distinctive (usually as a consequence of variations in magnetic intensity) and produce responses that require movement, which will expose the animals to the spatial variations within experimental spaces This is the common feature for tuna swimming in big outdoor tanks (Walker 1984), free-flying honeybees (Walker & Bitterman 1985, 1989; Walker et al 1989; Kirschvink & KobayashiKirschvink 1991; Kirschvink et al 1997), pigeons in flight cages (Mora et al 2004), trout (Walker et al 1997), zebra fish and tilapia (Shcherbakov et al 2005) as well as sharks and rays (Kirschvink et al 2001; Meyer et al 2005). The data obtained in well-designed experiments are typically much easier to analyse and provide a stronger basis for interpretation of experimental results whether those results are positive, negative or inconclusive
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