IEEE TRANSACTIONS ON MAGNETICS, VOL. 45, NO. 12, DECEMBER 2009 5259 Advances in Magnetics The Physics of Geomagnetic-Field Transduction in Animals Michael Winklhofer Department of Earth and Environmental Science, Ludwig-Maximilians-University Munich, 80333 Munich, Germany Birds, fish, sea turtles, and various other animals have been reported to sense the geomagnetic field and to use it for orientation, navigation, and homing. In recent years, exciting progress has been made towards elucidating the physical and structural basis of this remarkable phenomenon. This paper focuses on the two hypotheses that drive current research into magnetoreception. One proposal relies on the presence of molecules that undergo magnetically anisotropic chemical reactions due to transient formation of a radical pair. The proposed mechanism—essentially a chemical compass—is theoretically well-established and specifically designed behavioral experiments may indeed be interpreted that way, which has sparked a hunt for the molecules and structures in question. The ferrimag- netic transduction hypothesis, on the other hand, draws its plausibility from both theoretical considerations and the fact that magnetite has been detected in sensory neurons, with stable single-domain particles in fish and micrometer-scale clusters of superparamagnetic nanocrystals in birds. We discuss the limitations of our current knowledge and suggest future studies. Index Terms—Biomineralization, biophysics, ferrimagnetic materials, geomagnetism, radical-pair chemistry. I. INTRODUCTION T HE question “How do migrating organisms find their way?” has always puzzled humans and a great deal of re- search has been conducted to identify possible orientation cues. In 2005, Science magazine still considered that question as one of the big problems to be solved. There is sound evidence from behavioral experiments with artificially altered magnetic fields that various animals use the geomagnetic field as an important orientation cue [1]. Owing to its predominantly dipolar char- acter, the geomagnetic field can be used as a reliable frame of reference (see http://geomag.usgs.gov/charts/ for charts). The initial question thus shifts to the problem of how to pick up the magnetic field in the first place (magnetoreception) and how to transduce it into a nerve stimulus. This review focuses on the current trends in magnetoreception research. It is instructive to start out with the temporal variations of the geomagnetic field, which impose important constraints on the adaptability and sensitivity of magnetoreception. These considerations will be exemplified by key observations from biological experiments. II. GEOMAGNETIC CONSTRAINTS ON THE MAGNETIC SENSE Paleomagnetic studies on ancient rocks indicate that Earth has had a global magnetic field long before the first documented appearance of multicellular animals about 600 million years ago. That implies that evolution has taken place in the presence of a magnetic field and it would be rather surprising if organ- isms had not found a way of taking advantage of the spatial and directional information provided by a global magnetic field. Manuscript received October 16, 2008; revised March 09, 2009. Current version published November 18, 2009. Corresponding author: M. Winklhofer (e-mail: michael@geophysik.uni-muenchen.de). This paper comes with supplementary downloadable material available at http://ieeexplore.ieee.org. Digital Object Identifier 10.1109/TMAG.2009.2017940 The geomagnetic reference frame varies slowly with time, a phenomenon referred to as secular variation. The declina- tion, i.e., the angle between true (geographic) north and the locally determined magnetic north direction, drifts with rates of 0.1 –0.3 per year. It is not known if the magnetic com- pass sense is accurate enough to resolve such a minute drift, which from year to year would result in a magnetic misori- entation of only a few kilometers per 1000 km migration dis- tance. These small directional changes accumulate over gener- ations, and it is not known how migratory animals adapt to the changing frame of reference. It was suggested in a different con- text that night migratory birds calibrate the directional informa- tion from the magnetic compass with the solar azimuth during the sunset period [2]. Such a habitual calibration of the magnetic compass also appears to be an evolutionarily robust strategy for migrants to continuously adapt to secular variation and even to geomagnetic polarity reversals. During a reversal, the magnetic field morphology can change drastically. For instance, 775,000 years ago, at the climax of the last geomagnetic reversal, several poles emerged at mid latitudes [3] (see also Supplement), which may have rendered magnetic orientation ambiguous. Also, since magnetic orientation does not work near the magnetic pole [4], we can expect mid-latitude poles to have represented major bar- riers, which might even have deflected migration routes. Impor- tantly, a reversal takes several thousand years to complete and provided that migratory species can adapt to a slowly shifting magnetic reference frame, they can be expected to adapt to a slowly reversing field, too. Therefore, there is no need for them to evolve a magnetic compass that is indifferent to the polarity of the field, but solely detects the axial orientation of the field. Surprisingly, however, the internal magnetic compass of migra- tory birds has exactly that characteristics, as demonstrated by behavioral experiments under well-controlled field conditions [1]. For, a polarity reversed magnetic field caused the same ori- entation as under normal field conditions, while a reversal of either the horizontal or the vertical component did lead to a 180 change in orientation [5]. As stated above, this axial com- pass, also referred to as inclination compass [5], has no evolu- 0018-9464/$26.00 © 2009 IEEE