Stingless Bee Antennae: A Magnetic Sensory Organ?

Abstract

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, J
s and remanent, J
r, magnetizations and coercive field H
c are determined from the hysteresis curves. From H
c and J
r/J
s the magnetic particle sizes are estimated. The J
s 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.

Full text

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PROOF
2 Stingless bee antennae: A magnetic sensory organ?
3
4
M. J. Lucano, G. Cernicchiaro, E. Wajnberg & D. M. S. Esquivel*
5 Centro Brasileiro de Pesquisas Fı
´
sicas, R Xavier Sigaud 150, Rio de Janeiro, RJ 22290-180, Brazil; *Author
6 for correspondence (E-mail: darci@cbpf.br)
7
Received 14 April 2005; accepted 05 July 2005
8 Key words: stingless bee, pair of antennae, SQUID, FMR
9 Abstract
10 Magnetic material in the body parts of the stingless bee Schwarziana quadripunctata, heads, pairs of
11 antennae, thorax and abdomens, were investigated by SQUID magnetometry and Ferromagnetic Reso-
12 nance (FMR). The saturation, J
s
and remanent, J
r
, magnetizations and coercive field H
c
are determined
13 from the hysteresis curves. From H
c
and J
r
/J
s
the magnetic particle sizes are estimated. The J
s
and the FMR
14 spectral absorption areas yield 23±3%, 45±5%, 15±2% and 19±4% magnetic material contributions of
15 head, pair of antennae, thorax and abdomen, respectively, similar to those observed in the migratory ant
16 Pachycondyla marginata. This result is discussed in light of the hypothesis of antennae as a magnetosensor
17 structure.
18
19
20 Introduction
21 For the last 30 years, since the evidence of mag-
22 netotactic bacteria magnetosomes containing
23 magnetite biomineralized nanoparticles (Blake-
24 more 1975), several works on different fields have
25 been developed in order to understand geomag-
26 netic orientation in organisms. Behavioural exper-
27 iments were performed involving several species of
28 animals (Wiltschko & Wiltschko 1995; Va
´
cha &
29 Soukopova
´
2004; Wiltschko et al. 2004) and pur-
30 suing the comprehension of the mechanism
31 underneath this phenomenon. In particular,
32 extensive studies on insects have been focused on
33 the honeybee Apis mellifera. The correlation
34 between honeybee behaviour and the geomagnetic
35 field was firstly proved in 1968 (Lindauer & Mar-
36 tin 1968). Later on, magnetic material was
37 detected in their body using superconducting
38 magnetometers and pointing to a putative mech-
39 anism made of minute particles acting as a mag-
40 netic sensor (Gould et al. 1978). Iron-containing
41 trophocytes were found within the fat body of this
42 adult honeybee (Kuterbach & Walcott 1986),
43 identified as superparamagnet ic (SPM) magnetite
44particles (Hsu & Li 1994), although this result was
45not reproduced. Electron-dense material found in
46the hairs of honeybee abdomens or near the cutex
47was proposed as single domain or SPM magnetite
48(Schiff 1991) and a hypothesis was developed for
49associative learning of visual and magnetic stimuli
50(Schiff & Canal 1993). The presence of iron par-
51ticles were also observed by optical and electron
52microscopy in the trophocytes of adult Scapto-
53trigona postica, a stingless honeybee (Cunha et al.
541987). More recently, iron- rich granules found in
55the fat body of queen honeybees A. mellifera and
56S. postica, were proposed to be formed by holof-
57erritin molecules with inorganic phosphate and
58calcium (and magnesium in S. postica ) with
59diameters smaller than those previously described
60in the literature (Keim et al. 2002).
61A motivation for searching such a sensor would
62be the confirmation that the species behaviour is
63sensitive to the geomagnetic field. The first steps
64are to detect and localize magnetic nanoparticles
65as candidates for magnetic receptors, determining
66their magnetic properties. The following step,
67more complex, is to understand the physiological
68process that is involved in the magnetoreception
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AUTHOR’S PROOF!
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69 mechanism. This seems to be the case of the
70 Schwarziana quadripunctata bee for which the
71 magnetic field effect was observed in the frequency
72 of nest exiting (Nascimento et al. 2001).
73 In this report we present room temperature (RT)
74 SQUID magnetic measurements and ferromagnetic
75 resonance technique (FMR) results for magnetic
76 material in the body parts of the S. quadripunctata
77 bee, aiming to existence of a magnetoreceptor.
78 Methods and materials
79 The meliponini stingless bee S. quadripunctata,
80 native of the Atlantic Mata Forest, was found in
81 an underground nest located at Tereso
´
polis, Rio
82 de Janeiro-Brazil, at 1000 m above the sea level
83 and geomagnetic field intensity 0.238 Oe, inclina-
84 tion )32 and declination )2030¢. Adult foragers
85 were collected in the summer between 8–13 h, a
86 period of maximum foraging activity within the
87 optimal flying temperature range of 21–26 C
88 (Imperatriz-Fons eca & Darakjian 1994). Bees were
89 collected still alive, put in a refrigerator and after a
90 week transferred to cacodylate buffer 0.1 M
91 pH 7.4. Ten individuals were used without tho-
92 raxical members. Two groups of four bees each
93 were separated in four parts: head, pair of anten-
94 nae, thorax and abdomen, for SQUID and FMR
95 experiments. To minimize contamination, stain-
96 less-steel instruments were used. Two whole bees
97 were kept for control. The SQUID sample holder
98 does not fit more than two individu als.
99 Just before measurements, samples were dried
100 at 50 C for 1 h. Four units of each body part were
101 oriented one unit close to each other fixed on a
102kapton tape and on a Teflon sample holder for
103SQUID and FMR measurements, respectively. X-
104band FMR spectra (Bruker ESP 300E) at 4 mW
105microwave power, with 210
4
receiver gain and
1062.018 Oe field modulation amplitude and hystere-
107sis curves (MPMS-XL Quantum Design SQUID
108magnetometer) were obtained at room tempera-
109ture with the magnetic fie ld applied parallel to the
110long body axis of the insect, as shown in Figure 1.
111The FMR absorption spectra areas (second inte-
112gral of the derivative spectra) were calculated with
113a software developed using the graphic language
114LabVIEW

, starting at the high field values where
115the baseline is better defined.
116Results
117Hysteresis curves present a straight line with po-
118sitive or negative slope at very strong fields due to
119paramagnetic or diamagnetic contributions, respec-
120tively. Bee, head, thorax and abdomen present a
121diamagnetic contribution (figure not shown), while
Figure 1. Insect orientation relative to the magnetic field.
Table 1. Magnetic parameters of one S. quadripunctata bee
a
and body parts
b
.
Whole bee Head Antennae Thorax Abdomen
J
s
(10
)6
emu) 3.3±0.4 1.1±0.3 2.1±0.3 0.7±0.3 0.9±0.5
H
c
(Oe) 43±15 32±8 130±5 44±18 90±20
J
r
(10
)7
emu) 2.0±0.8 1.4±0.4 5±0.5 0.8±0.1 0.8±0.4
v (10
)9
emu/Oe) )4.2±0.5 )2±0.2 +0.4±0.1 )3.6±0.2 )1.6±0.2
J
r
/J
s
0.06±0.03 0.12±0.06 0.24±0.03 0.12±0.03 0.09±0.03
Magnetic (%) 23±3 44±4 15±2 19±4
c
S (10
8
a. u.) 2.1±0.1 5±0.2 1.8±0.1 1.7±0.1
FMR (%) 20±1 47±3 16±1 \16±1
a
Two bees average values.
b
Four bees parts average values.
c
Taking the control bee J
s
value it increases to 30%.
2
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137137the antennae a paramagnetic one . The dia/para-
138 magnetic susceptibilities (Table 1) are obtained by
139 a linear fit of the curve at magnetic fields higher
140 than that where ferromagnetic saturation is
141 achieved and their contributions subtracted. Fig-
142 ure 2 presents the RT hysteresis curves normalized
143 to one pa rt and one individual, with the highest
144 magnetic contribution coming from the antennae
145 part. For clearness, thorax and head loops are not
146 shown and only one branch of the abdomen and
147 antennae loop were measured. The magnetic
148 parameters: saturation magnetization, J
s
, rema-
149 nent magnetization, J
r
and coercive field H
c
, ob-
150 tained for each body part and for one bee are given
151 in Table 1 , including the J
r
/J
s
ratio. The J
s
sum of
152 each body part average, 4.8±1.410
)6
emu, is
153 taken to calculate the percentual contributions to
154 J
s
as 44±4%, 23±3%, 15±2%, 19±4% for an-
155 tenna, head, thorax and abdomen, respectively.
156 Considering the magnetic material differences
157 content among individuals an d the error bars, the
158 total J
s
is in good agreement with the average J
s
of
159 the two bees used as control.
160 The low field region of the head and antennae
161 hysteresis curves in Figure 2, normalized to their
162 J
s
values, are given in the insert. The antennae
163present the highest H
c
value (130 Oe) and J
r
/J
s
164ratio (0.24), comparatively to the H
c
(32–90 Oe)
165and J
r
/J
s
(0.09– 0.12) values of other parts. Con-
166sidering magnetite as the magnetic particles
167material, the antennae particle sizes fall between
1680.037 and 0.10 lm while the other body part par-
169ticles are about 0.22 l m (Ozdemir et al. 2002).
170Figure 3 shows the FMR spectra of the bee
171body parts with the magnetic field oriented parallel
172to the long body axis. Diamagnetism does not
173contribute to the FMR spectra while paramagne-
174tism does and was not subtracted, as in the hys-
175teresis curves. The four parts spectra present a
176broad (linewidth 550–900 Oe) component at high
177field, HF, centred at about 3000 Oe, with the
178antennae HF line intensity higher than the other
179ones. Only the antennae spectrum clearly presents
180another component at low field, LF, at about
1811300 Oe. The values of the absorption areas S,
182(the second integral of the FMR derivative spec-
183tra) of the parts of the S. quadripunctata bee are
184given in Table 1. S calculated with the WINEPR
185(Bruker) software is not accurate when a compo-
186nent spreads out to zero field, as in the antennae
187case. The specially developed software used in this
188paper, corrects the assumption of zero intensity at
189the first spectrum field value by integrating from
190high to low field values. Even so, the antenna S
191value is a low limit value because the LF line is
192incomplete and the respective contribution cannot
Figure 2. RT Hysteresis curves of S. quadripunctata whole bee,
pair of antennae and abdomen, oriented parallel to the mag-
netic field, normalized to one individual and part. Insert low
field region of head (dashed line) and antennae (solid line)
normalized hysteresis curves.
0 2000 4000 6000
LF
HF
abdomen
pair of antennae
head
thorax
H (Oe)
Figure 3. RT X-band ferromagnetic resonance spectra of
S. quadripunctata body parts. Lines are guide to the eyes.
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193 be fully calculated. S values of the HF at RT are
194 related to the magnetic material amou nt, as shown
195 by its linear relation to the saturation magnetiza-
196 tion in termites (Oliveira et al. 2005). Correlation
197 between integrated FMR intensity and the mag-
198 netization was also observed in Si doping of fer-
199 rihydrite nanoparticles (Seehra et al. 2001).
200 Taking S as proportional to the number of reso-
201 nant spins in the sample, the magnetic mate rial
202 percentages in each body part are: 47±3%,20±1%,
203 16±1% and 16±1% in the antennae, head, thorax
204 and abdomen, respectively. These values are in
205 very good agreement with those above, obtained
206 by SQUID magnetometry.
207 Discussion
208 Magnetoreception is a mechanism of magnetic
209 field perception and transduction used for an
210 organism’s orientation. Two hypotheses have
211 arisen to explain its basis: one considering bio-
212 chemical reactions modulated by magnetic field,
213 and another the presence of biogenic magnetic
214 particles as magnetosensors. For now, much of
215 what is known about this mechanism has been
216 accumulated from behavioural experiments, theo-
217 retical proposals and a few electrophysiological
218 and anatomical studies (Lohmann & Johnsen
219 2000). Recent results suggested the involvement of
220 at least two types of receptors in obtaining mag-
221 netic compass information, with the specific
222 interaction of these receptors being rather complex
223 (Wiltschko et al. 2004). Biogenic magnetic parti-
224 cles have gained relevance as they have been
225 reported in several species (Wiltschko & Wiltschko
226 1995; Safarik & Safarikova 2002), but their con-
227 nections to nervous structures still need to be
228 proved. Despite the difficulty of locating tiny
229 magnetoreceptors, that might be dispersed any-
230 where within the animal body, FMR or SQUID
231magnetometry can be used to characterize their
232properties present in some social insects (Wajnberg
233et al. 2000; El-Jaick et al. 2001; Esquivel et al.
2342002; Alves et al. 2004; Esquivel et al. 2004
1;
235Wajnberg et al. 2004; Oliveira et al. 2005a). In this
236paper, both techniques were used to study the
237body parts of S. quadripunctata bees. The HF and
238LF FMR components presen t in this bee body
239parts have already been observed in the abdomen
240of A. mellifera and P. marginata and associated to
241isolated and aggregated magnetite nanoparticles,
242respectively (Wajnberg et al. 2000; El-Jaick et al.
2432001). Moreover, the relative amounts of magnetic
244material obtained from J
s
and S strongly agree,
245confirming the usefulness of the latter in compar-
246ing amounts of magnetic materials at RT. The
247joint analysis of the magnetic material with both
248techniques in all body parts results as 23±3%,
24945±5%, 15±2% and 19±4% magnetic material
250contributions of head, antennae, thorax and
251abdomen, respectively. It agrees on the stingless
252bee antennae containing the highest amount. As
253far as we know, this is the first study on magnetic
254material in all body parts of a honeybee other than
255Apis mellifera, the most studied one, besides opti-
256cal and Electron Microscopy observations on S.
257postica abdomens (Cunha et al. 1987; Keim et al.
2582002). A few previous FMR results (Takagi 1995;
259El-Jaick et al. 2001) confirmed the presence of
260ferromagnetic and paramagnetic material in A.
261mellifera abdomens, without measuring the other
262body parts. On the other hand, magnetic mea-
263surements of whole A. mellifera (Oliveira et al.
2642005a), body parts (Takagi 1995) and particularly
265abdomens (Esquivel et al. 2002) have shown the
266presence of superparamagnetic and larger mag-
267netic particles or aggregates in this body part.
268Hysteresis parameters of whole honeybees and
269respective abdomens are compared in Table 2.
270Honeybees A. mellifera and S. quadripunctata
271present very different magnetic material properties,
Table 2. A. mellifera and S. quadripunctata magnetic parameters.
S. quadripunctata A. mellifera S. quadripunctata abdomen A. mellifera abdomen
J
s
(10
)6
emu) 3.3±0.4 39±4 0.9±0.5 2.5
H
c
(Oe) 43±15 93±10 90±20 44
J
r
(10
)7
emu) 2.0±0.8 46±5 0.8±0.4 2.4
v (10
)9
emu/Oe) )4.2±0.5 – )1.6±0.2 –
J
r
/J
s
0.06±0.03 0.11±0.03 0.09±0.03 0.09
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272 except for the J
r
/J
s
ratio. The amount of magnetic
273 material in S. quadripunctata is approxim ately 10
274 times lower than in A. mellifera, and almost three
275 times lower in the abdomens as observed from the J
s
276 values. For comparison, A. mellifera workers are
277 about 12 mm long while S. quadripunctata about
278 6 mm, and the abdomens present the same length
279 ratio.
280 The magnetic fraction present in the S. quad-
281 ripunctata abdomen (19% Table 2) is higher than
282 in A. mellifera (6%). Even considering the differ-
283 ences in magnetic material among individuals of
284 the same species, this J
s
fraction calculated based
285 on the control bee J
s
value (30%) evidences even
286 more the honeybee differences. The estimated size
287 of the particles in S. quadripunctata abdomens
288 (220 nm) is much larger than 13 nm of the A.
289 mellifera estimated from FMR experiments. This
290 difference can be related to: genus specificity,
291 technique sensitivity (SQUID and FMR), sample
292 preparations and environment conditions. The
293 large size is in good agreement with 40–160 nm
294 size range of the iron granules found in another
295 stingless bee S. postica (Cunha et al. 1987), al-
296 though ferritin-like granules were observed as
297 electron-dense particles measuring 2.1±0.5 nm in
298 their abdomen (Keim et al. 2002). Stress should be
299 given to the ingested magnetic material contribu-
300 tion in the thorax and abdomen, which is not
301 biomineralized, and could be the cause of the dif-
302 ferent nanoparticle size and concentrations in
303 abdomens. On the other hand, the head and
304 antennae material can only be the result of a bio-
305 mineralization process, which from an evolution-
306 ary point of view can produce a specific and
307 efficient size and geometry. It is interesting to note
308 that the Pachycondyla marginata ant, which
309 migratory behaviour was related to the geomag-
310 netic field (Acosta-Avalos et al. 2001), shows a
311 similar result, with 42±3% of the magnetic
312 material in the antennae (Wajnberg et al. 2004).
313 As far as we know, no experiments have been
314 carried out concerning the antennae as a magne-
315 toreceptor for orientation; however, the sensitivity
316 of beetle and bug antennae to non-uniform
317 microwave electromagnetic fields was studied,
318 indicating that they can detect and respond to the
319 radiation (Ondracek et al. 1976). Although no
320 obvious organ or structure devoted to magneto-
321 reception necessarily exists, bees possess complex
322 sensory organs, as antennae and eyes, which
323should be considered. The antennae are composed
324of thousands of sensilla, which are con nected to
325the central nervous system (Dade 1994). More
326than one decade ago, magnetite particles found in
327A. mellifera bee abdomens were suggested for
328magnetic orientation (Kirschvink & Walker 1985);
329nevertheless, the high fraction and size of this
330biomineralized magnetic material in the S. quad-
331ripunctata antennae led us to speculate that this
332part may be a magnetosensor organ. These pre-
333liminary findings should be corroborated with
334further behavioural studies and complementary
335physical characterization techniques to compare to
336other insect species, whose orientation behaviour
337is known to be influenced by the geomagnetic field.
338Acknowledgements
339We are grateful to R. Eizemberg for samples
340supply, Dr M. Castro for taxonomic information
341and to Dr O.C. Alves, Dr H.G.P. Lins de Barros
342for helpful discussion and Dr D. Guenzburger for
343carefully reading. MJL thanks CLAF-CNPq and
344EW thanks CNPq for financial support.
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