Eliane Wajnberg

Magnetoreception in eusocial insects: an update

Behavioural experiments for magnetoreception in eusocial insects in the last decade are reviewed. Ants and bees use the geomagnetic field to orient and navigate in areas around their nests and along migratory paths. Bees show sensitivity to small changes in magnetic fields in conditioning experiments and when exiting the hive. For the first time, the magnetic properties of the nanoparticles found in eusocial insects, obtained by magnetic techniques and electron microscopy, are reviewed. Different magnetic oxide nanoparticles, ranging from superparamagnetic to multi-domain particles, were observed in all body parts, but greater relative concentrations in the abdomens and antennae of honeybees and ants have focused attention on these segments. Theoretical models for how these specific magnetosensory apparatuses function have been proposed. Neuron-rich ant antennae may be the most amenable to discovering a magnetosensor that will greatly assist research into higher order processing of magnetic information. The ferromagnetic hypothesis is believed to apply to eusocial insects, but interest in a light-sensitive mechanism is growing. The diversity of compass mechanisms in animals suggests that multiple compasses may function in insect orientation and navigation. The search for magnetic compasses will continue even after a magnetosensor is discovered in eusocial insects.

Electron paramagnetic resonance study of the migratory ant Pachycondyla marginata abdomens.

Electron paramagnetic resonance was used to investigate the magnetic material present in abdomens of Pachycondyla marginata ants. A g congruent with 4.3 resonance of high-spin ferric ions and a very narrow g congruent with 2 line are observed. Two principal resonance broad lines, one with g > 4.5 (LF) and the other in the region of g congruent with 2 (HF), were associated with the biomineralization process. The resonance field shift between these two lines, HF and LF, associated with magnetic nanoparticles indicates the presence of cluster structures containing on average three single units of magnetite-based nanoparticles. Analysis of the temperature dependence of the HF resonance linewidths supports the model picture of isolated magnetite nanostructures of approximately 13 nm in diameter with a magnetic energy of 544 K. These particles are shown to present a superparamagnetic behavior at room temperature. The use of these superparamagnetic particle properties for the magnetoreception process of the ants is suggested.

Antennae: the strongest magnetic part of the migratory ant.

Pachycondyla marginata (P.m.), a migratory and termitophageous ant, hunting only the termite species Neocapritermes opacus,migrates significantly oriented 13° with respect to the magnetic North-South axis. Results of hysteresis curves at room temperature of four Pachycondyla marginata heads, thorax, pairs of antennae and abdomens, oriented parallel to the magnetic field, indicate that the antennae give the strongest saturation magnetization, suggesting this sensory organ as being also a magnetic sensory organ. The total saturation magnetization in a whole P.m. is composed by 42±3%, 24±3%, 19±3% and 15±3% of antennae, head, thorax and abdomen contributions, respectively. The abdomen hysteresis curve presents a wasp-waisted loop with Hcr/Hc of 4.75, characteristic of mixed magnetic systems.

Seasonal patterns in the orientation system of the migratory ant Pachycondyla marginata

Abstract. Route directions of migrations by the neotropical termite-hunting ant Pachycondyla marginata at a forest reserve in Southeast Brazil were analysed by circular statistic. Colony movement patterns were compared between the rainy/hot and dry/cold seasons. Migrations during the dry/cold season are significantly oriented 13° with the magnetic North–South axis, while rainy/hot migrations do not exhibit a preferred direction. This result is discussed considering the hypothesis that P. marginata ants may use the geomagnetic field as an orientation cue for migrations in the dry/cold season. The presence of magnetic iron oxides in the head and abdomen of P. marginata is consistent with this suggestion.

Stingless Bee Antennae: A Magnetic Sensory Organ?

Magnetic material in the body parts of the stingless bee Schwarziana quadripunctata, heads, pairs of antennae, thorax and abdomens, were investigated by SQUID magnetometry and Ferromagnetic Resonance (FMR). The saturation, Js and remanent, Jr, magnetizations and coercive field Hc are determined from the hysteresis curves. From Hc and Jr/Js the magnetic particle sizes are estimated. The Js and the FMR spectral absorption areas yield 23±3%, 45±5%, 15±2% and 19±4% magnetic material contributions of head, pair of antennae, thorax and abdomen, respectively, similar to those observed in the migratory ant Pachycondyla marginata. This result is discussed in light of the hypothesis of antennae as a magnetosensor structure.

Heat denaturation of metHb and HbNO: e.p.r. evidence for the existence of a new hemichrome

Electron paramagnetic resonance was used to follow the time dependence of heat denaturation of met- and nitrosyl-haemoglobin (metHb and HbNO) at 60 degrees C, 70 degrees C and 80 degrees C. The spectral changes of both complexes indicate that conformational changes in the protein manifest themselves in changes of the equilibrium of hemichromes in metHb and of six- and five-coordinated iron in HbNO. The formation of a hemichrome which has not been described before, with g = 2.45, 2.27 and 1.85, is observed. A His-Fe-Cys complex is proposed for its structure.

Nitrosyl hemoglobin: EPR components at low temperatures

The EPR spectrum of nitrosyl hemoglobin has been studied from 7.5 K to 104 K. It is composed of at least three components (A, B and C) which have a different dependence on temperature and power level. The A component decreases with increasing temperature. The B component disappears at around 30 K and is replaced by C. Relaxation of A follows the Orbach mechanism with an energy of 28 cm−1. This behavior can be attributed to phonon induced changes in the orientation of NO with respect to the heme plane.

Temperature dependence of Q-band electron paramagnetic resonance spectra of nitrosyl heme proteins

The Q-band (35 GHz) electron paramagnetic resonance (EPR) spectra of nitrosyl hemoglobin (HbNO) and nitrosyl myoglobin (MbNO) were studied as a function of temperature between 19 K and 200 K. The spectra of both heme proteins show two classes of variations as a function of temperature. The first one has previously been associated with the existence of two paramagnetic species, one with rhombic and the other with axial symmetry. The second one manifests itself in changes in the g-factors and linewidths of each species. These changes are correlated with the conformational substates model and associate the variations of g-values with changes in the angle of the N(his)-Fe-N(NO) bond in the rhombic species and with changes in the distance between Fe and N of the proximal (F8) histidine in the axial species.

Magnetic properties of the microorganism Candidatus Magnetoglobus multicellularis

Magnetotactic microorganisms use the interaction of internal biomineralized nanoparticles with the geomagnetic field to orientate. The movement of the magnetotactic multicellular prokaryote Candidatus Magnetoglobus multicellularis under an applied magnetic field was observed. A method using digital image processing techniques was used to track the organism trajectory to simultaneously obtain its body radius, velocity, U-turn diameter, and the reorientation time. The magnetic moment was calculated using a self-consistent method. The distribution of magnetic moments and radii present two well-characterized peaks at (9 ± 2) × 10−15 and (20 ± 3) × 10−15 A m2 and (3.6 ± 0.1) and (4.3 ± 0.1) μm, respectively. For the first time, simultaneous determination of the distribution of the organism radii and magnetic moment was obtained from the U-turn method by a new digital imaging processing. The bimodal distributions support an organism reproduction process model based on electron microscopy observations. These results corroborate the prokaryote multicellular hypothesis for Candidatus M. multicellularis.

E.p.r. studies of photolysis of nitrosyl haemoglobin at low temperatures

Photolysis of HbNO has been studied from 6.2 K to 15.5 K by electron spin resonance during and after continuous illumination. Non-exponential kinetics of both dissociation and reassociation of NO was observed. The prolonged illumination separates the fast and slow ligands. This picture is consistent with NO tunnelling from two sites at different distances from the bound position. This result is obtained using a model of a sum of two exponentials or of conformational substates.