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Magnetic anisotropy and organization of nanoparticles in heads and antennae of neotropical

leaf-cutter ants, Atta colombica

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2014 J. Phys. D: Appl. Phys. 47 435401

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1. Introduction

Sensory acquisition, transduction and use of magnetic signals are among the most intriguing processes of information use by a wide spectrum of organisms [1]. In bacteria, the presence of organelles (magnetosomes) containing magnetic material

represents one of the best understood examples of a highly specialized magnetic compass. In such a system, orientation of the bacterium to the magnetic field direction is due to the passive alignment of the magnetosome. Other environmental cues, time of reorientation, as well as bacterial size may affect the bacterium’s orientation [2, 3].

Journal of Physics D: Applied Physics

Magnetic anisotropy and organization of nanoparticles in heads and antennae of neotropical leaf-cutter ants, Atta colombica

Odivaldo C Alves1, Robert B Srygley3,4, Andre J Riveros5, Marcia A Barbosa2, Darci M S Esquivel2 and Eliane Wajnberg2

1 Departamento de Físico-Química, Instituto de Química, Universidade Federal Fluminense, Outeiro de São João Batista s/n, Niterói 24020–150, RJ, Brazil2 Coordenação de Física Aplicada, Centro Brasileiro de Pesquisas Físicas, R. Xavier Sigaud 150, Rio de Janeiro 22290-180, RJ, Brazil3 USDA-Agricultural Research Service, Northern Plains Agricultural Research Lab, 1500N. Central Ave, Sidney, MT 59270, USA4 Smithsonian Tropical Research Institute, Apdo. 2072, Balboa, Republic of Panama5 Departamento de Ciencias Fisiológicas, Facultad de Medicina, Pontificia Universidad Javeriana, Bogotá, Colombia

E-mail: elianew@cbpf.br

Received 20 May 2014, revised 6 August 2014Accepted for publication 10 September 2014Published 3 October 2014

AbstractOriented magnetic nanoparticles have been suggested as a good candidate for a magnetic sensor in ants. Behavioural evidence for a magnetic compass in neotropical leaf-cutter ants, Atta colombica (Formicidae: Attini), motivated a study of the arrangement of magnetic particles in the ants’ four major body parts by measuring the angular dependence of the ferromagnetic resonance spectra at room temperature. Spectra of the thoraces and those of the abdomens showed no significant angular dependence, while those of the antennae and those of the heads exhibited a periodic dependence relative to the magnetic field. Fitting of the angular dependence of the resonant field resulted in an unexpected magnetic anisotropy with uniaxial symmetry. High values of the first order anisotropy constant were observed for the magnetic material in antennae (−2.9  ×  105 erg cm−3) and heads (−1  ×  106 erg cm−3) as compared to body parts of other social insects. In addition, the magnitude of the anisotropy in the heads was comparable to that observed in magnetite nanoparticles of 4–5 nm diameter. For the antennae, the mean angle of the particles’ easy magnetization axis (EA) was estimated to be 41° relative to the straightened antenna’s long axis. For the heads, EA was approximately 60° relative to the head’s axis running from midway between the spines to the clypeus. These physical characteristics indicate organized magnetic nanoparticles with a potential for directional sensitivity, which is an important feature of magnetic compasses.

Keywords: magnetic characterization, magnetic sensor, spatial orientation, homing

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Across animals, behavioural evidence is ample and solid, and reflects widespread use of magnetic information [1, 4–6]. Diverse species use the geomagnetic field as a cue for spatial orientation and navigation, ranging from movements of a few centimeters to long range migrations by air, sea or land [7, 8]. In insects, for example, long distance migratory movements as well as short foraging excursions can be supported by the use of magnetic cues [4]. During foraging, species such as the honeybee Apis mellifera [9] and the neotropical leaf-cutter ant Atta colombica navigate over relatively (to their body size) long distances supported by diverse sources of information, including pheromones and celestial cues, as well as magnetic compasses. A. colombica workers, for instance, can forage for distances of up to several hundred meters, following phero-mone cues in architecturally modified foraging trails [10]. Orientation under deterioration or destruction of such trails, or during trail formation indicates the use of celestial cues, such as the Sun’s azimuth and polarized skylight, as well as landmarks. However, workers are also active in deep shaded forest, during overcast conditions or at night, all conditions when and where skylight and Sun are not reliable cues. Under such conditions A. colombica workers use the geomagnetic field as a reference for a magnetic compass used to update a home vector when all other cues are absent, a behavioural pro-cess known as path integration [11, 12]. Thus, if the polarity of the local magnetic field is modified, the path-integrated home vector switches accordingly, a behaviour observed, so far, only in A. colombica [11, 12].

Unfortunately, internal mechanisms of transduction and overall use of magnetic information by animals are not as well understood as in magnetotactic bacteria. Such understanding is limited by a lack of information on the location and com-position of magnetic compasses and associated neural mech-anisms that incorporate more elaborate steps of sensing, transduction, storage and retrieval of magnetic information embedded across the process of decision-making. However much of the research focuses on magnetite as the most likely biological magnet because it comprises the compass in mag-netotactic bacteria and has been found associated with neu-rons in vertebrate species (fish and birds) [13].

Recent behavioural evidence supports the idea that contact with soil during development is required for A. colombica workers in order to acquire a functional magnetic com-pass, pointing to the incorporation of soil magnetic particles that could be used as a magnetic sensor [14]. This finding is consistent with evidence from other eusocial insects. Theoretically, magnetoreception that is based on a magnetic particle sensor in a specialized organ and coupled to struc-tures so as to transmit signals from the geomagnetic field is well accepted across social insects. Specifically, two models for magnetic field sensitivity of arranged superparamagnetic particles have been proposed: for those in the dorsal hair of honeybee abdomens [15] and in the antenna of Pachycondyla marginata ants [16]. Both hypothesized systems assume that such particles can provide information on field direction as well as intensity; however, the existence of other receptors and modes of action in A. colombica cannot be discarded. Moreover, although workers of A. colombica developed in

soil-free colonies exhibited an impaired magnetic compass, they had magnetic particles [14], which might play a role in other mechanisms of navigation. Hence, understanding the features of the magnetic particles in A. colombica will provide us with information on a magnetic compass uniquely used during navigation (i.e. during path integration), and on the potential use of magnetic particles by other systems.

Thus, in this paper we aim to analyze in detail the char-acteristics of the magnetic particles present in the body of A. colombica, which can be potentially used as part of the behav-iourally demonstrated magnetic compass [12, 14]. We relied on the ferromagnetic resonance (FMR) technique, which allows verifying the presence of ferromagnetic particles without the need for purification [17]. In previous accounts, the physical properties of the magnetic particles, such as shape, size and anisotropy constants have been estimated mainly from tem-perature dependence, but angular dependence of the FMR spectra can add information on the particle arrangement Thus, we also measured the angular dependence of the spectra of Atta body parts to obtain the mean angle of the easy mag-netization axis (EA) relative to the axes of symmetry for the three major body sections and the antennae of the ant and the magnetic anisotropy constants. The angular dependence of the effective resonant field was simulated based on the model that was used for termites [18].

2. Materials and methods

Leaf-cutter ants of the same colony tested for magnetic ori-entation [12] were collected in Gamboa, Republic of Panama (elevation 30 m; 9° 07′N, 79° 42′W) and killed by submer-sion in 80% ethanol. The ants were rinsed with dilute HCl to remove surface contaminants, and immersed in 2.5% glu-taraldehyde in 0.1 M cacodylate buffer solution (pH 7.4) for 12–24 h. The ants were washed three times in 0.1 M caco-dylate buffer solution and stored in this solution at 4 °C. They were separated into four parts; pair of antennae, head, thorax and abdomen just before FMR measurements. Four samples of each part (i.e. from four different insects) were placed close to each other and oriented on a Teflon holder with vacuum grease and transferred to FMR quartz tubes.

Room temperature measurements were performed with a commercial X-band electron paramagnetic resonance (EPR) spectrometer (Bruker ESP300E) operating at a microwave power of 4 mW and 2 Oe modulation field amplitude.

The heads were oriented on the Teflon holder in two ini-tial positions: (1) the frontal plane parallel to the laboratory vertical plane yz with the axis of symmetry, which runs from the medial point between the head spines to the clypeus, par-allel to the magnetic field, H and to the laboratory horizontal direction, y (named PAR for parallel, figures 1(a) and 2(a), φ = 0) or (2) with the axis of symmetry in the laboratory ver-tical direction, z (named PER for perpendicular, figures 1(b) and 2(b), θ = 0). The antennae were only oriented parallel to the z axis (PER orientation), arranged so that they were as straight as possible and parallel to one another (figure 1(c)). The thoraces and abdomens were also tested separately with

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their long body axes, assuming these sections  are approxi-mately cylindrical, in only the PER orientation. The spectral angular dependences were performed by rotating the sample holder around the laboratory vertical axis, z (figures 1(a)–(c)). Note in figure 1(d) that the axis of orientation of the heads cannot be related to that of the antenna.

The effective resonance field, HR was measured as the peak position of the spectral first integral using the Winepr software (Bruker). The HR angular dependence curves were fitted using Origin® software (Microcal).

3. Basis of FMR angular dependence

The resonant condition is given by ω = γHeff, where ω and γ are the Larmor frequency and gyromagnetic ratio, respectively and Heff, is the effective magnetic field composed by the external applied field H, and the anisotropy field Ha. Contributions from the demagnetization field can be disregarded because there was no evidence of particle elongation or chain formation in the heads and antennae of the tested ants, which would appear as a low field component in the spectra [17]. As magnetite is the most frequent magnetic material in animals, a cubic mag-netocrystalline symmetry was expected for Ha, however, the experimental angular dependence of the resonant field, HR = ωR/γ − Ha, could neither be fitted with a cubic expression of

1st nor with a 2nd order one. A combination of cubic and uni-axial expressions also failed to fit the data. A uniaxial mag-netic anisotropy with second order terms provided the best fit (minimizing the root mean square error). In typical magnetic resonance conditions the Zeeman interaction is stronger than the other interactions, with the M direction close to that of H. The resonance conditions is then given by [19]

ϖγ

= − −

+ −

HK

MeH

K

MeH eH eH

  [3cos ( ) 1]

[8 cos ( ) sin ( ) 2 sin ( ) ]

R1 2

2 2 2 4(1)

where K1 and K2 are the first and second order magnetic anisotropy constants, respectively, M is saturation magnetiza-tion of material, and eH is the angle of easy magnetization axis, EA (figure 2, dashed arrow), relative to the magnetic field direction, y. Angles α and β position EA relative to the body part’s axis of symmetry and to the laboratory vertical axis z, respectively (figure 2). Both angles are necessary to solve for eH (equations (2a) and (2b)).

In the PAR orientation, φ and φ0 are the experimental and initial rotation angles, respectively. At the initial position, the body axis is parallel to H (y axis) so that cos (eH) = cos α = sin β cos φ0 (figure 2(a)). At a general orientation, cos (eH) = sin β cos (φ + φ0), and as the angle β does not change with the rota-tion of the sample,

Figure 1. (a) PAR and (b) PER initial orientation (φ and θ = 0, see figure 2 for angles definition) of ant heads on the Teflon holder relative to the xyz laboratory axis (four heads mounted in a square formation). z is the vertical direction and y the magnetic field direction (H), (c) initial orientation of straightened pairs of antennae arranged in the PER orientation (four pairs mounted side by side) and (d) dorsal view of A. colombica showing the relative orientation of its body parts.

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αϕ

ϕ ϕ= +( )eHcos ( )cos

coscos

00 (2a)

In the PER orientation the experimental and initial rotation angles are named θ and θ0, respectively (figure 2(b)), with

α θ θ= +eHcos ( ) sin  cos ( )0 (2b)

4. Results

The FMR spectra of the ant body parts are shown in figure 3 at room temperature and initial orientations (φ0 = 0 and θ0  =  0). A broad line with linewidth about 700 Oe in the g =  3 region is observed in the spectra of the heads and thoraces. Narrow lines (170 Oe) in the g = 2 region occur in spectra of the antennae and abdomens and at g = 5 in the spectrum of the thoraces (350 Oe). A free radical line is present in all spectra.

The narrow line of the antennal spectrum and broad line of the head spectrum show angular dependence at room tem-perature (figure 4) while spectra of the thoraces and abdomens presented no significant angular dependence (not shown). The angular dependence of the head spectra in the PAR orientation was similar to that in PER one (figure 5).

The HR angular dependence and fitting curves using equa-tions (1) and (2) are shown in figure 5. The HR angular depend-ence of antennal spectra presents two local maxima or minima with a period of about 180°. This feature is not expected for a first order uniaxial symmetry system, but a second order axial provided a good fit.

Although angular dependence in HR of the head spectra presents one peak, typical of a first order axial symmetry, the equation  for this condition failed in fitting the experimental curves. The second order approximation was necessary and resulted in a good fit.

The independent fitting parameters K1/M, K2/M, were used in the fitting procedure. The anisotropy constants, K1 and K2, were then estimated assuming the magnetite value M = 470 Oe and are given in table 1.

5. Discussion

The physical evidence, here presented, corroborates behav-ioural evidence that leaf-cutter ants use a magnetic compass to orient spatially. FMR results indicate that their compass or compasses can be found in tissues located in the head and antennae. A narrow line in the g = 2.3 region, similar to that observed in the spectrum for the antennae, was previously observed in the spectra of the nomadic ant Labidus predator [20] and of the antennae of the honey bee A. mellifera [21] at room temperature, but their angular dependence was not

Figure 2. EA in the (a) PAR and (b) PER orientations. Angle α of EA is relative to the body part’s axis of symmetry and angle β of EA is relative to the laboratory vertical axis z. φ and θ are the rotation angles in (a) and (b), respectively. Expressions along axis directions are the unitary projections of EA at initial positions (φ0 = 0 and θ0 = 0).

Figure 3. FMR spectra of A. colombica body parts at room temperature and initial orientations (φ and θ = 0, see text). Thoracic and abdominal spectra multiplied by 20.

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explored. Broad lines in the g = 2 region of the spectra of other social insects were interpreted as isolated magnetic nanopar-ticles [17]. Ferritin and haemosiderin are proteins with super-paramagnetic cores of ferric hydroxide that in mammals present FMR spectra with high and low field features [22]. As far as we know, there are no FMR studies on these proteins extracted from insects. However the 3D structure of these proteins is well conserved throughout the animal and plant kingdoms, and so the high and low field features should be present in the FMR spectra of insect protein. Because the low field shoulder was not observed, these proteins were not con-tributing to the spectra.

In comparison, angular dependence of FMR spectra provides much more information on the properties of indi-vidual magnetic nanoparticles and their arrangement. For leaf-cutter ants A. colombica, the effective resonant field, HR, of the spectra for their antennae and heads was periodic when the sample was rotated relative to the magnetic field, whereas those of the thoraces and abdomens were isotropic. Anisotropy in HR was also recently shown to be character-istic of whole A. colombica ants collected from a colony in Panama that showed a shift in orientation with an experi-mental shift in polarity of the horizontal component of the local magnetic field [14].

The spectral anisotropy of the ant heads suggests that the magnetic material in this body part is oriented relative to the head’s symmetry axis by the EA angle α. The angle α from PER and PAR orientations of the heads was expected to be the same. Difficulty in aligning the heads identically in the two orientations would introduce some error, and so we conclude that the values of α = 69° and 51° (table 1) are reasonably close and support this prediction. The mean orientation of EA in the head (as a resultant of a set of particles and considering

Table 1. Fitting parameters of curves in figure 5 using equations (1) and (2). K1,2 are the first and second order magnetic anisotropy constants, α the angle of EA relative to the body part’s axis of symmetry (see material and methods), Θ0 and φ0 the initial rotation.

Antenna PER Head PER Head PAR

K1 (erg cm−3) −2.9  ×  105 −10  ×  105 −9  ×  105

K2 (erg cm−3) 2.0  ×  105 2.0  ×  105 1.6  ×  105

α 0.71 rad = 41° 0.90 rad = 51° 1.2 rad = 69°Θ0 0.64 rad = 37° 1.1 rad = 63° —φ0 — — 1.0 rad = 57°

Figure 4. Examples of FMR spectra of A. colombica (a) antennae and (b) heads in the PER orientation as a function of the rotation angle θ.

Figure 5. Angular dependence of the resonant field (HR) of antennae and heads of A. colombica (full symbol PER orientation and open symbol PAR orientation, see text). Lines are the fitting curves with parameters given in table 1.

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individual differences) lies in the plane 27° from the sagittal plane (xz in figure  1(b)) (positive sense from front to back of the head) and 60° from the symmetry axis. An uncertainty of ±15° was estimated from successive measurements of the same samples and attributed to differences in placement of the samples oriented because they were oriented with the unaided eye. Similarly, spectral anisotropy of the antennae suggests that the magnetic material in this body part is oriented 41° rel-ative to the long axis of each rectified antenna. The antennae were artificially positioned in the Teflon holder such that they had a single axis, but in nature, the antennae are positioned on either side of the head and are jointed such that the ant flexes them independently (figure 1(d)). As a result, the antennae can be positioned in parallel but their orientations may also diverge greatly. The antennae might be waved to sense varia-tion in the direction and intensity of the magnetic field [23].

Because the spectra of the heads and antennae were so dif-ferent, they probably represent two very different magnetic systems. If both systems are involved in magnetoreception, then they might be used to sense different aspects of the mag-netic field (polarity, inclination, or intensity) or they might be integrated to reinforce the same sensory information from the magnetic field [24]. The head has less freedom of movement than the antennae, and so scanning by the head to sense vari-ation in the magnetic field might require some rotation of the entire body [25].

The fitting of angular dependence of HR allowed estima-tion of the 1st and 2nd order magnetic anisotropy constants of the magnetic particles. K1 and K2 values for the heads were expected to be independent of the sample orientations. The obtained values (table 1) differed by 10%, which like the angle of easy magnetization, can be attributed to the difficulty in aligning the heads. However this difference can also be associated with other anisotropic contributions, such as shape anisotropy, that are not considered explicitly in equation (1).

Interestingly, the angular dependence of the antennal spectra presented two local maxima (minima) with a 180° period. A similar periodicity in the angular dependence was observed in human and animal brain tissues [26] and in the head and antennae of Solenopsis interrupta ants [27], whole Tetragonisca angustula bees [28] and Neocapritermes opacus termites [18]. This feature in social insects was interpreted as due to the magnetic anisotropy of magnetite. Magnetite is characterized by a cubic structure at room temperature [29]. At the Verwey temperature, the crystal symmetry is lowered to monoclinic. For N. opacus termites, angular dependence of HR of the particles was indeed successfully fitted with a cubic symmetry expression for the anisotropy energy [18]. For S. interrupta ants, angular dependence of HR of the spectra of the head and antennae also presented two local maxima (minima) with 180° period [29]. With support from similar results for N. opacus, this periodicity was suggested to be due to cubic sym-metry of particles in both the head and antennae. Nevertheless the S. interrupta data were not fitted to confirm it, as done in this paper. The methods applied to FMR spectra from ter-mites to determine the anisotropy properties of nanocrystals [18] were also applied here. More recently, similar methods were also used for magneto tactic bacteria for which particle

chain alignment is well known. In the bacteria, the ellipsoid approximation with its long axis parallel to the [1 1 1] crystal-lographic direction was found to simplify the angles defined from a sample of bacteria oriented in a parallel configuration [30, 31]. For heads and antennae of termites and leaf-cutter ants, the chain structure was not observed and the spectral fea-tures of bacteria were not present.

Surprisingly, the HR angular dependence of the magnetic material in A. colombica resulted in a magnetic anisotropy with uniaxial symmetry. Because the fitting procedure takes into account the particles’ mean orientation of the EA and mean magneto-crystalline energy, this unexpected symmetry is probably associated with the arrangement of the particles. In support of this conclusion, the angular dependences of HR for magnetite and maghemite nanoparticles were anisotropic with uniaxial symmetry when suspended in liquid and cooled [32]. In addition, a uniaxial magnetic anisotropy was observed for partially aligned iron oxide nanoparticles encapsulated within protein capsids and suspended in water [33]. Similar results were obtained for magnetotactic bacteria: FMR of cultured samples during particle-chain growth revealed a threshold average diameter of 23 nm for the generation of a dipole field with uniaxial symmetry, that increases with particle size. In 1D assemblies, generation of a dipole field with uniaxial sym-metry dominates the crystalline fields and gives thermal sta-bility to the system [34]. Although aggregations of magnetic particles, in general, are recognized by a low field component [17], that was not observed in spectra of heads and antennae of A. colombica (figure 2), there is considerable support from these experiments for our interpretation that the spectra from A. colombica heads and antennae are indicative of oriented iron oxide nanoparticles.

Finally, the absolute value of the anisotropy constants (e.g. −10  ×  105 erg cm−3) obtained from the heads of A. colom-bica were surprisingly high as compared to body parts of other insects, which range from 0.2  ×  105 to 0.7  ×  105 erg cm−3 [17] or to that of bulk magnetite (−1.34  ×  105 erg cm−3) and bulk maghemite (−0.47   ×  105 erg cm−3). An anisotropy constant (3.56  ×  106 erg cm−3) comparable to those from the heads of A. colombica was observed in magnetite nanoparticles with a diameter of 5 nm in polyvinyl alcohol (PVA), and it was inter-preted to be a signal of dipolar interactions [35]. Similar to the absolute value of 1  ×  106 erg cm−3 for the Atta heads, a K value of 1.2  ×  106 erg cm−3 obtained from iron oxide cores of magnetite or maghemite with a diameter ca. 4 nm capped with ferritin was attributed to the contribution of a large surface anisotropy [36].

The amplitude of variation in HR, difference between the maximum and minimum measured in the fitted curves, was 590 Oe for the antennae and that for the heads was 2500 Oe and 1700 Oe for PAR and PER orientation, respectively. The amplitudes of variation in HR of magnetite (1410 Oe) and maghemite (350 Oe) nanoparticle suspensions were similar to those for A. colombica. The larger amplitude of magnetite relative to maghemite was attributed to the greater effective anisotropy of magnetite due to its larger size, more irregular shape, and broader distributions of size and shape relative to those of maghemite in the samples [32]. The differences in

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the results from the antennae and heads can be attributed to any of these factors as well as to different compositions of the magnetic particles.

The presented results confirm the strong potential of FMR for identifying oriented magnetic particles and estimating the magnetic anisotropy constants. Most interesting, it can also esti-mate the mean orientation of the EA relative to the body parts of social insects, based on the angular dependence of the HR at room temperature. The revealed axial symmetry of magne-tocrystalline instead of a cubic as expected for magnetite parti-cles, suggest the presence of oriented nanosized particles. Based on the torque transducer model [37], an organized ensemble of magnetic particles that together show remanence or anisotropic magnetic susceptibility is one characteristic expected of a bio-logical magnetic sensor of the type that appears to be involved in path integration by A. colombica [11, 12, 14].

Acknowledgments

We thank the Autoridad Nacional del Ambiente (ANAM) of the Republic of Panama for permission to export ants to Brazil for physical analysis. This project was supported in part by Centro Brasileiro de Pesquisas Fisicas (CBPF) of the Minis-tério da Ciência, Tecnologia e Inovação (MCTI), the National Geographic Society Committee for Research and Exploration, the US Department of Agriculture and the Smithsonian Tropi-cal Research Institute. AJR received support from National Science Foundation.

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