Behavioural studies underpin the weight of experimental evidence for the existence of a magnetic sense in animals. In contrast, studies aimed at understanding the mechanistic basis of magnetoreception by determining the anatomical location, structure and function of sensory cells have been inconclusive. In this review, studies attempting to demonstrate the existence of a magnetoreceptor based on the principles of the magnetite hypothesis are examined. Specific attention is given to the range of techniques, and main animal model systems that have been used in the search for magnetite particulates. Anatomical location/cell rarity and composition are identified as two key obstacles that must be addressed in order to make progress in locating and characterizing a magnetite-based magnetoreceptor cell. Avenues for further study are suggested, including the need for novel experimental, correlative, multimodal and multidisciplinary approaches. The aim of this review is to inspire new efforts towards understanding the cellular basis of magnetoreception in animals, which will in turn inform a new era of behavioural research based on first principles.

The honeybee Apis mellifera is one of many animal species for which empirical evidence of a magnetic sense has been provided. The underlying mechanisms postulated for magnetoreception in bees are varied, but most point towards the abdomen as the most likely anatomical region for its location, partly owing to the large accumulation of iron in trophocyte cells that comprise the honeybee fat body. Using a multi-modal imaging and analysis approach, we have investigated iron in the honeybee, with a particular focus on the abdomen and the utility of such techniques as applied to magnetoreception. Abdominal iron is shown to accumulate rapidly, reaching near maximum levels only 5 days after emerging from the comb and is associated with the accumulation of iron within the fat body. While fat body iron could be visualized, no regions of interest, other than perhaps the fat body itself, were identified as potential sites for magnetoreceptive cells. If an iron-based magnetoreceptor exists within the honeybee abdomen the large accumulation of iron in the fat body is likely to impede its discovery.

Extended abstract of a paper presented at Microscopy and Microanalysis 2013 in Indianapolis, Indiana, USA, August 4 – August 8, 2013.

Magnetic field perception (magnetoreception) has been described across a broad spectrum of animals, including insects, birds, reptiles and mammals. Despite extensive behavioural evidence demonstrating that these animals are able to sense magnetic fields, the cellular mechanisms involved in transducing a magnetic stimulus to a neuronal response remain a long standing mystery in biology.The magnetite hypothesis is one possible explanation for how a putative magnetoreceptor might function, and is based on neuronal activation by intracellular nanoparticles of magnetite (Fe 3 O 4 ) [1]. This is expected to occur when torque is applied to the membrane anchored particles of magnetite in response to changes in Earth-strength magnetic fields. Magnetotactic bacteria provide good evidence for the magnetite hypothesis in animals as they are able to produce chains of magnetite nanoparticles (magnetosomes) in their cytosol (Fig. 1A) and use them for orientation in the Earth's magnetic field.Finding the cells responsible for magnetoreception has proven to be extremely challenging. The search has been hampered by the fact that only few cells are expected to harbour the sense and they could be located anywhere in the body. Additionally, iron is a widespread biological and environmental element, which can result in contamination of samples and misinterpretation of results [2 and 3]. For these reasons, finding an iron-based magnetoreceptor in situ within an organism or tissue using optical or electron microscopic methods is comparable to the classic needle-in-ahaystack problem. New methodological developments addressing these limitations are timely.The presence of magnetic particles is a key attribute of magnetoreceptive cells, which can be exploited experimentally in the search for the anatomical location of these cells. Bulk extraction methods that can separate inorganic particles from organic tissue are promising approaches for confirming the presence or absence of magnetite particles.We used such an approach and developed a novel procedure to extract and concentrate magnetosome particles from bacteria and prepare them for examination using a range of imaging and analytical platforms, including optical, X-ray and electron based microscopy. As a proof of concept, we demonstrate that these particles can be recovered from honey bee abdomen tissue that has been spiked with magnetotactic bacteria (Fig. 1B). Our data show that the magnetosome particles retain their mineral/crystallographic properties after the extraction process, as demonstrated by selected area electron diffraction patterns obtained from undigested and spiked particles ( Fig. 1C and Table 1). Our technique was also able to extract iron oxide granules from the honey bee fat body (Fig. 1B). Although these granules are not believed to play a role in magnetoreception, our method can efficiently capture a range of iron materials, which can then be screened for the presence of candidate magnetoreceptor particles. The ultimate aim is to then locate and characterise these p...

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