Magnetoreception

The vector of the geomagnetic field provides animals with directional information, while intensity and/or inclination provide them with positional information. For magnetoreception, two hypotheses are currently discussed: one proposing magnetite-based mechanisms, the other suggesting radical pair processes involving photopigments. Behavioral studies indicate that birds use both mechanisms: they responded to a short, strong magnetic pulse designed to change the magnetization of magnetite particles, while, at the same time, their orientation was found to be light-dependent and could be disrupted by high-frequency magnetic fields in the MHz range, which is diagnostic for radical pair processes. Details of these findings, together with electrophysiological and histological studies, suggest that, in birds, a radical pair mechanism located in the right eye provides directional information for a compass, while a magnetite-based mechanism located in the upper beak records magnetic intensity, thus providing positional information. The mechanisms of magnetoreception in other animals have not yet been analyzed in detail.     

Migratory orientation of European Robins is affected by the wavelength of light as well as by a magnetic pulse

The object of this study was to test the alternative hypotheses of magnetoreception by photopigments and magnetoreception based on magnetite. Migratory European Robins, Erithacus rubecula, were tested under light of different wavelengths; after these tests, they were subjected to a brief, strong magnetic pulse designed to alter the magnetization of single domain magnetite. In control tests under white light, the birds preferred the normal, seasonally appropriate migratory direction. Under 571 nm green light, they continued to be well oriented in the migratory direction, whereas under 633 nm red light, their behaviour was not different from random. The magnetic pulse had a significant effect on migratory orientation, but the response varied between individuals: some showed a persistent directional shift, while others exhibited a change in scatter; one bird was seemingly unaffected.These findings indicate a light-dependent process and, at the same time, suggest an involvement of magnetizable material in migratory orientation. They are in agreement with the model of a light-dependent compass and a magnetite-based map, even if some questions concerning the effect of the pulse remain open.     

Sea turtles, lobsters, and oceanic magnetic maps

Numerous marine animals can sense the Earth's magnetic field and use it as a cue in orientation and navigation. Two distinct types of information can potentially be extracted from the Earth's field. Directional or compass information enables animals to maintain a consistent heading in a particular direction such as north or south. In contrast, positional or map information can be used by animals to assess geographic location and, in some cases, to navigate to specific target areas. Marine animals exploit magnetic positional information in at least two different ways. For hatchling loggerhead sea turtles, regional magnetic fields function as open-sea navigational markers, eliciting changes in swimming direction at crucial points in the migratory route. Older sea turtles, as well as spiny lobsters, use magnetic information in a more complex way, exploiting it as a component of a classical navigational map, which permits an assessment of position relative to specific geographic destinations. These “magnetic maps” have not yet been fully characterized. They may be organized in several fundamentally different ways, some of which bear little resemblance to human maps, and they may also be used in conjunction with unconventional navigational strategies. Unraveling the nature of magnetic maps and exploring how they are used represents one of the most exciting frontiers of behavioral and sensory biology.     

Magnetosome magnetite biomineralization in a flagellated protist: evidence for an early evolutionary origin for magnetoreception in eukaryotes

The most well-recognized magnetoreception behaviour is that of the magnetotactic bacteria (MTB), which synthesize membrane-bounded magnetic nanocrystals called magnetosomes via a biologically controlled process. The magnetic minerals identified in prokaryotic magnetosomes are magnetite (Fe₃O₄) and greigite (Fe₃S₄). Magnetosome crystals, regardless of composition, have consistent, species-specific morphologies and single-domain size range. Because of these features, magnetosome magnetite crystals possess specific properties in comparison to abiotic, chemically synthesized magnetite. Despite numerous discoveries regarding MTB phylogeny over the last decades, this diversity is still considered underestimated. Characterization of magnetotactic microorganisms is important as it might provide insights into the origin and establishment of magnetoreception in general, including eukaryotes. Here, we describe the magnetotactic behaviour and characterize the magnetosomes from a flagellated protist using culture-independent methods. Results strongly suggest that, unlike previously described magnetotactic protists, this flagellate is capable of biomineralizing its own anisotropic magnetite magnetosomes, which are aligned in complex aggregations of multiple chains within the cell. This organism has a similar response to magnetic field inversions as MTB. Therefore, this eukaryotic species might represent an early origin of magnetoreception based on magnetite biomineralization. It should add to the definition of parameters and criteria to classify biogenic magnetite in the fossil record.     

Chains of single-domain magnetite particles in chinook salmon,Oncorhynchus tshawytscha

Summary Although the presence of magnetite in their tissues is correlated with the ability of different species to detect magnetic fields, proof that the magnetite is involved in magnetoreception has not yet been provided. Using the approach employed to localize and isolate magnetic particles in the yellowfin tuna, we found that single-domain magnetite occurs in chains of particles in tissue contained within the dermethmoid cartilage of adult chinook salmon,Oncorhynchus tshawytscha. The particles are present in sufficient numbers to provide the adult fish with a very sensitive magnetoreceptor system. Magnetite in the chinook can be correlated with responses to magnetic fields in a congeneric species, the sockeye salmon. Based on the presence of the chains of particles, we propose behavioral experiments that exploit the responses of sockeye salmon fry to magnetic fields to test explicit predictions of the ferromagnetic magnetoreception hypothesis.     

The physics and neurobiology of magnetoreception

Diverse animals can detect magnetic fields but little is known about how they do so. Three main hypotheses of magnetic field perception have been proposed. Electrosensitive marine fish might detect the Earth's field through electromagnetic induction, but direct evidence that induction underlies magnetoreception in such fish has not been obtained. Studies in other animals have provided evidence that is consistent with two other mechanisms: biogenic magnetite and chemical reactions that are modulated by weak magnetic fields. Despite recent advances, however, magnetoreceptors have not been identified with certainty in any animal, and the mode of transduction for the magnetic sense remains unknown.     

Magnetic orientation and magnetoreception in birds and other animals

Animals use the geomagnetic field in many ways: the magnetic vector provides a compass; magnetic intensity and/or inclination play a role as a component of the navigational map, and magnetic conditions of certain regions act as sign posts or triggers, eliciting specific responses. A magnetic compass is widespread among animals, magnetic navigation is indicated e.g. in birds, marine turtles and spiny lobsters and the use of magnetic sign posts has been described for birds and marine turtles. For magnetoreception, two hypotheses are currently discussed, one proposing a chemical compass based on a radical pair mechanism, the other postulating processes involving magnetite particles. The available evidence suggests that birds use both mechanisms, with the radical pair mechanism in the right eye providing directional information and a magnetite-based mechanism in the upper beak providing information on position as component of the map. Behavioral data from other animals indicate a light-dependent compass probably based on a radical pair mechanism in amphibians and a possibly magnetite-based mechanism in mammals. Histological and electrophysiological data suggest a magnetite-based mechanism in the nasal cavities of salmonid fish. Little is known about the parts of the brain where the respective information is processed.     

Compatibility of magnetic imprinting and secular variation

Diverse ocean migrants, including some sea turtles, elephant seals, and salmon, begin life in particular reproductive areas along coastlines, disperse across vast expanses of sea, and then return as adults to their natal areas to reproduce [1], [2] and [3]. Little is known about how such marine animals guide themselves to the correct coastal region from hundreds or thousands of kilometers away and after absences ranging in duration from a few months to a decade or more. One hypothesis is that animals imprint on the magnetic field of their home area and use this information to return [1]. The Earth's field varies predictably across the globe, so different geographic areas are marked by distinctive magnetic fields that might, in principle, provide unique magnetic signatures for natal areas [4]. A potentially serious complication for this hypothesis is that the Earth's field changes gradually over time [1] and [4], causing the magnetic signatures that define natal areas to slowly drift. This secular variation could make natal homing via magnetic imprinting impossible if the magnetic signatures moved too far from the natal area [1], [5] and [6]. To investigate whether magnetic imprinting is compatible with secular variation, we sought a species with a life history that poses challenges for the hypothesis, reasoning that if magnetic imprinting is consistent with natal homing under unfavorable circumstances, then it would also be plausible in most other cases. We chose the Kemp's ridley sea turtle (Lepidochelys kempii), an endangered species that ranges widely over the Gulf of Mexico, northern Caribbean, and the eastern U.S. coast, but returns to nest along a single, limited region of coastline in northern Mexico [7]. This species requires approximately 10–15 years to reach sexual maturity [7] and is thus absent from its natal area for much longer than animals such as salmon and elephant seals [2] and [3]. Given this long absence, the Kemp's ridley appears to be particularly susceptible to effects of secular variation if it relies on magnetic imprinting. The modeling results we report here show that the magnetic imprinting hypothesis can account for how the Kemp's ridley turtle returns to its natal region even after absences of a decade or more.     

Comparison of functional aspects of the coagulation cascade in human and sea turtle plasmas

Functional hemostatic pathways are critical for the survival of all vertebrates and have been evolving for more than 400 million years. The overwhelming majority of studies of hemostasis in vertebrates have focused on mammals with very sparse attention paid to reptiles. There have been virtually no studies of the coagulation pathway in sea turtles whose ancestors date back to the Jurassic period. Sea turtles are often exposed to rapidly altered environmental conditions during diving periods. This may reduce their blood pH during prolonged hypoxic dives. This report demonstrates that five species of turtles possess only one branch of the mammalian coagulation pathway, the extrinsic pathway. Mixing studies of turtle plasmas with human factor-deficient plasmas indicate that the intrinsic pathway factors VIII and IX are present in turtle plasma. These two factors may play a significant role in supporting the extrinsic pathway by feedback loops. The intrinsic factors, XI and XII are not detected which would account for the inability of reagents to induce coagulation via the intrinsic pathway in vitro. The analysis of two turtle factors, factor II (prothrombin) and factor X, demonstrates that they are antigenically/functionally similar to the corresponding human factors. The turtle coagulation pathway responds differentially to both pH and temperature relative to each turtle species and relative to human samples. The coagulation time (prothrombin time) increases as the temperature decreases between 37 and 15 °C. The increased time follows a linear relationship, with similar slopes for loggerhead, Kemps ridley and hawksbill turtles as well as for human samples. Leatherback turtle samples show a dramatic nonlinear increased time below 23 °C, and green turtle sample responses were similar but less dramatic. All samples also showed increased prothrombin times as the pH decreased from 7.8 to 6.4, except for three turtle species. The prothrombin times decreased, to varying extents, in a linear fashion relative to reduced pH with the rate of change greatest in leatherbacks>greenloggerhead turtles. All studies were conducted with reagents developed for human samples which would impact on the quantitative results with the turtle samples, but are not likely to alter the qualitative results. These comparative studies of the coagulation pathway in sea turtles and humans could enhance our knowledge of structure/function relationships and evolution of coagulation factors.     

The horizontal magnetic dance of the honeybee is compatible with a single-domain ferromagnetic magnetoreceptor

Although honeybees are able to sense the geomagnetic field, very little is known about the method in which they are able to detect it. The recent discovery of biochemically precipitated magnetite (Fe₃O₄) in bees, however, suggests the possibility that they might use a simple compass organelle for magnetoreception. If so, their orientation accuracy ought to be related to the accuracy of the compass, e.g. it should be poor in weak background fields and enhanced in strong fields. When dancing to the magnetic directions on a horizontal honeycomb, bees clearly show this type of alignment behavior. A least-squares fit between the expected alignment of a compass and this horizontal dance data is consistent with this hypothesis, and implies that the receptors have magnetic moments of 5 × 10^?13 emu, or magnetite volumes near 10^?15 cm³. Additional considerations suggests that these crystals are slightly sub-spherical and single-domain in size, held symmetrically in their receptors, and have a magnetic orientation energy of approximately to 6 kT in the geomagneticfield. A model of a magnetite-based magnetoreceptor consistent with these constraints is discussed.     

Influence of weak magnetic fields on fish retina photoreceptors

It has been shown for the first time that retina photoreceptors of the salmon Oncorhynchus masou (masu salmon) fry exposed to a constant magnetic field (80 Gs) in conditions of twilight illumination demonstrated not a twilight reaction, as in the control, but a darkness (scotopic) reaction. The pigment epithelium in this case reacted as to bright light. Under the influence of long wavelength red light, the retinomotor reaction corresponded to partial light adaptation. After the indemnification of the horizontal component (0.1 Gs) of the geomagnetic field, fish retina adapted to complete darkness demonstrated changes that could not be attributed to one of standard conditions of light exposure. Thus, the rods and cones demonstrated a reaction similar to that to twilight, double cones reacted as to complete darkness ("correct" reaction), and PE borrowed a position as at twilight. Apparently, the basic stimuli of the retina reactions were not light but changes of the magnetic field. Based on these results and the results available in literature, the authors offer a new variant of the hypothesis of light-dependent magnetoreception, which is based on the assumption that the liquid crystals of retina pigments are very sensitive receptors of magnetic field and do not require the presence of magnetite crystals. We assume that the layer of retina pigment epithelium participates in the complex process of transformation of a light signal, which takes into account the influence of magnetic field but not simply absorbs light superfluous for photoreceptors. The changes in magnetic field cause a distortion of the liquid crystal line structure of the pigment, which results in the transformation of the light signal acting on the photoreceptors. Monochromatic red light in the same way deforms the response to the native magnetic signal.     

Magnetic orientation and navigation in marine turtles, lobsters, and molluscs: concepts and conundrums

The Earth's magnetic field provides a pervasive source of directionalinformation used by phylogenetically diverse marine animals.Behavioral experiments with sea turtles, spiny lobsters, andsea slugs have revealed that all have a magnetic compass sense,despite vast differences in the environment each inhabits andthe spatial scale over which each moves. For two of these animals,the Earth's field also serves as a source of positional information.Hatchling loggerhead sea turtles from Florida responded to themagnetic fields found in three widely separated regions of theAtlantic Ocean by swimming in directions that would, in eachcase, facilitate movement along the migratory route. Thus, foryoung loggerheads, regional magnetic fields function as navigationalmarkers and elicit changes in swimming direction at crucialgeographic boundaries. Older turtles, as well as spiny lobsters,apparently acquire a "magnetic map" that enables them to usemagnetic topography to determine their position relative tospecific goals. Relatively little is known about the neuralmechanisms that underlie magnetic orientation and navigation.A promising model system is the marine mollusc Tritonia diomedea,which possesses both a magnetic compass and a relatively simplenervous system. Six neurons in the brain of T. diomedea havebeen identified that respond to changes in magnetic fields.At least some of these appear to be ciliary motor neurons thatgenerate or modulate the final behavioral output of the orientationcircuitry. These findings represent an encouraging step towarda holistic understanding of the cells and circuitry that underliemagnetic orientation behavior in one model organism.     

The role of geomagnetic cues in green turtle open sea navigation

Background

Laboratory and field experiments have provided evidence that sea turtles use geomagnetic cues to navigate in the open sea. For instance, green turtles (Chelonia mydas) displaced 100 km away from their nesting site were impaired in returning home when carrying a strong magnet glued on the head. However, the actual role of geomagnetic cues remains unclear, since magnetically treated green turtles can perform large scale (>2000 km) post-nesting migrations no differently from controls.

Methodology/Principal Findings

In the present homing experiment, 24 green turtles were displaced 200 km away from their nesting site on an oceanic island, and tracked, for the first time in this type of experiment, with Global Positioning System (GPS), which is able to provide much more frequent and accurate locations than previously used tracking methods. Eight turtles were magnetically treated for 24–48 h on the nesting beach prior to displacement, and another eight turtles had a magnet glued on the head at the release site. The last eight turtles were used as controls. Detailed analyses of water masses-related (i.e., current-corrected) homing paths showed that magnetically treated turtles were able to navigate toward their nesting site as efficiently as controls, but those carrying magnets were significantly impaired once they arrived within 50 km of home.

Conclusions/Significance

While green turtles do not seem to need geomagnetic cues to navigate far from the goal, these cues become necessary when turtles get closer to home. As the very last part of the homing trip (within a few kilometers of home) likely depends on non-magnetic cues, our results suggest that magnetic cues play a key role in sea turtle navigation at an intermediate scale by bridging the gap between large and small scale navigational processes, which both appear to depend on non-magnetic cues.     

鸟类磁感受的生物物理机制研究进展

行为学实验表明,许多鸟类能够感受到地磁信息,并利用地磁信息完成迁徙或归巢。地磁场信息能提供可靠导航信息,磁力线可提供罗盘信息,而磁场强度和倾角可提供位置信息。文章介绍了鸟类磁感受机制的两种重要假说——基于磁铁矿的磁感受假说和化学磁感受假说,阐明了两种假说的理论原理及实验证据,对地磁信息传导神经通路与处理脑区做了评述,并展望了其发展方向。     

Measuring energy expenditure in sub-adult and hatchling sea turtles via accelerometry

Measuring the metabolic of sea turtles is fundamental to understanding their ecology yet the presently available methods are limited. Accelerometry is a relatively new technique for estimating metabolic rate that has shown promise with a number of species but its utility with air-breathing divers is not yet established. The present study undertakes laboratory experiments to investigate whether rate of oxygen uptake ( o ₂) at the surface in active sub-adult green turtles Chelonia mydas and hatchling loggerhead turtles Caretta caretta correlates with overall dynamic body acceleration (ODBA), a derivative of acceleration used as a proxy for metabolic rate. Six green turtles (25–44 kg) and two loggerhead turtles (20 g) were instrumented with tri-axial acceleration logging devices and placed singly into a respirometry chamber. The green turtles were able to submerge freely within a 1.5 m deep tank and the loggerhead turtles were tethered in water 16 cm deep so that they swam at the surface. A significant prediction equation for mean o ₂ over an hour in a green turtle from measures of ODBA and mean flipper length (R² = 0.56) returned a mean estimate error across turtles of 8.0%. The range of temperatures used in the green turtle experiments (22–30°C) had only a small effect on o ₂. A o ₂-ODBA equation for the loggerhead hatchling data was also significant (R² = 0.67). Together these data indicate the potential of the accelerometry technique for estimating energy expenditure in sea turtles, which may have important applications in sea turtle diving ecology, and also in conservation such as assessing turtle survival times when trapped underwater in fishing nets.     

A Comparison of the Seasonal Movements of Tiger Sharks and Green Turtles Provides Insight into Their Predator-Prey Relationship

During the reproductive season, sea turtles use a restricted area in the vicinity of their nesting beaches, making them vulnerable to predation. At Raine Island (Australia), the highest density green turtle Chelonia mydas rookery in the world, tiger sharks Galeocerdo cuvier have been observed to feed on green turtles, and it has been suggested that they may specialise on such air-breathing prey. However there is little information with which to examine this hypothesis. We compared the spatial and temporal components of movement behaviour of these two potentially interacting species in order to provide insight into the predator-prey relationship. Specifically, we tested the hypothesis that tiger shark movements are more concentrated at Raine Island during the green turtle nesting season than outside the turtle nesting season when turtles are not concentrated at Raine Island. Turtles showed area-restricted search behaviour around Raine Island for ∼3–4 months during the nesting period (November–February). This was followed by direct movement (transit) to putative foraging grounds mostly in the Torres Straight where they switched to area-restricted search mode again, and remained resident for the remainder of the deployment (53–304 days). In contrast, tiger sharks displayed high spatial and temporal variation in movement behaviour which was not closely linked to the movement behaviour of green turtles or recognised turtle foraging grounds. On average, tiger sharks were concentrated around Raine Island throughout the year. While information on diet is required to determine whether tiger sharks are turtle specialists our results support the hypothesis that they target this predictable and plentiful prey during turtle nesting season, but they might not focus on this less predictable food source outside the nesting season.     

Bats use magnetite to detect the earth's magnetic field

While the role of magnetic cues for compass orientation has been confirmed in numerous animals, the mechanism of detection is still debated. Two hypotheses have been proposed, one based on a light dependent mechanism, apparently used by birds and another based on a "compass organelle" containing the iron oxide particles magnetite (Fe(3)O(4)). Bats have recently been shown to use magnetic cues for compass orientation but the method by which they detect the Earth's magnetic field remains unknown. Here we use the classic "Kalmijn-Blakemore" pulse re-magnetization experiment, whereby the polarity of cellular magnetite is reversed. The results demonstrate that the big brown bat Eptesicus fuscus uses single domain magnetite to detect the Earths magnetic field and the response indicates a polarity based receptor. Polarity detection is a prerequisite for the use of magnetite as a compass and suggests that big brown bats use magnetite to detect the magnetic field as a compass. Our results indicate the possibility that sensory cells in bats contain freely rotating magnetite particles, which appears not to be the case in birds. It is crucial that the ultrastructure of the magnetite containing magnetoreceptors is described for our understanding of magnetoreception in animals.     

A first estimate of sea turtle bycatch in the industrial trawling fishery of Gabon

Gabon hosts nesting grounds for several sea turtle species, including the world’s largest rookery for the leatherback turtle (Dermochelys coriacea), Africa’s largest rookery for the olive ridley turtle (Lepidochelys olivacea) and smaller aggregations of the hawksbill turtle (Eretmochelys imbricata) and green turtle (Chelonia mydas). To assess the level of incidental captures of turtles by the Gabonese trawl fishery, an onboard observer program was conducted in the period 2012–2013. A total of 143 turtles were captured by 15 trawlers during 271 fishing days. The olive ridley turtle was the main species captured (80% of bycaught turtles), with mostly adult-sized individuals. The remaining 20% included green turtles, hawksbill turtles, leatherback turtles and undetermined species. Bycatch per unit of effort (BPUE) of olive ridley turtles varied greatly depending on the period of the year (range of means: 0.261–2.270). Dead and comatose turtles were 6.2 and 24.6% respectively (n = 65). By applying the available fishing effort to two BPUE scenarios (excluding or considering a seasonal peak), the total annual number of captures was estimated as ranging between 1026 (CI 95% 746–1343) and 2581 (CI 95% 1641–3788) olive ridley turtles, with a mortality ranging from 63 (CI 95% 13–135) to 794 (CI 95% 415–1282) turtles per year depending on the scenario and on the fate of comatose turtles. Such a potential mortality may be reason for concern for the local breeding population of olive ridley turtles and recommendations in terms of possible conservation measures and further research are given.     

Primary physical mechanism of the biological effects of weak magnetic fields

The primary physical mechanism of the magnetoreception of weak magnetic fields is considered. It imposes limits on the magnetic biological effect at the stage prior to the involvement of specific biophysical and biochemical mechanisms, i.e., regardless of the nature of the target of the magnetic field. It has been shown that the biological effects of weak magnetic fields have, in general, non-linear and spectral properties. Observation of these characteristics gives information not only on the gyromagnetic ratio, but also on the parameters of the interaction between the target and its immediate surroundings. This makes it possible for one to develop schemes for the identification of the biophysical mechanisms of magnetoreception.     

Titanium and iron titanium oxide nanoparticles in antennae of the migratory ant <Emphasis Type="Italic">Pachycondyla marginata</Emphasis>: an alternative magnetic sensor for magnetoreception?

The most accepted hypothesis of magnetoreception for social insects is the ferromagnetic hypothesis which assumes the presence of magnetic material as a sensor coupled to sensitive structures that transmit the geomagnetic field information to the nervous system. As magnetite is the most common magnetic material observed in living beings, it has been suggested as basic constituent of the magnetoreception system. Antennae and head have been pointed as possible magnetosensor organs in social insects as ants, bees and termites. Samples of three antenna joints: head-scape, scape-pedicel and pedicel-third segment joints were embedded in epoxi resin, ultrathin sectioned and analyzed by transmission electron microscopy. Selected area electron diffraction patterns and X-ray energy dispersive spectroscopy were obtained to identify the nanoparticle compound. Besides iron oxides, for the first time, nanoparticles containing titanium have been identified surrounded by tissue in the antennae of ants. Given their dimension and related magnetic characteristics, these nanoparticles are discussed as being part of the magnetosensor system.