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First published online February 15, 2008
Journal of Experimental Biology 211, 678-685 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.013920
Thoracic vibrations in stingless bees (Melipona seminigra): resonances of the thorax influence vibrations associated with flight but not those associated with sound production
1 Department of Biology, University of São Paulo, FFCLRP, Av.
Bandeirantes 3900, 14040–901 Ribeirão Preto, SP, Brazil
2 Department of Neurobiology and Cognition Research, University of Vienna,
Althanstrasse 14, A-1090 Vienna, Austria
3 Department of Biology, York University, 4700 Keele Street, Toronto, Ontario,
M3J 1P3, Canada
* Author for correspondence (e-mail: michael.hrncir{at}gmx.at)
Accepted 14 November 2007
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: stingless bees, thoracic vibration, forager vibration, annoyance buzzing, flight vibration, resonance, natural frequency, laser vibrometry
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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; Nachtigall,
2003). During flight, the stretch activation occurs at the natural
frequency of the oscillating system. The natural frequency of the thorax is
determined by a variety of parameters such as the elasticity of the thoracic
capsule, the muscle tension and the moment of inertia due to the wing loading
(Roeder, 1951;
Soltavalta, 1952;
Nachtigall, 2003;
Darveau et al., 2005). As in
other resonant mechanical systems, the frequency of the thorax oscillations,
and thus that of the wingbeats, changes when the natural frequency of the
system is modified. Experimentally, such modifications can be achieved through
partly clipping or complete removal of the wings. The reduction in wing area
reduces the mass and inertial load on the oscillating system and, therefore,
increases the oscillation frequency
(Chadwick and Williams, 1949;
Roeder, 1951;
Soltavalta, 1952).
In addition to the most prominent purpose, which is to move the wings for
flight, thoracic vibrations are produced by eusocial bees (bumble bees,
stingless bees and honey bees) in the contexts of recruitment communication
(Esch, 1961;
Wenner, 1962;
Michelsen et al., 1986;
Hrncir et al., 2006a), pollen
collection (Michener, 1962;
Wille, 1963;
Buchmann, 1983;
King, 1993) and defence
(Schneider, 1972;
Sen Sarma et al., 2002).
During these vibrations, the wings are usually folded over the abdomen, which
results in them decoupling from the indirect flight mechanism
(Snodgrass, 1956). Generally,
such non-flight vibrations are characterized by a main frequency component
higher than that of the flight vibrations
(King, 1993;
King et al., 1996;
Nachtigall, 2003), which was
explained by an increase in resonant frequency of the oscillating system as a
consequence of wing folding. The folding and decoupling of the wings reduces
the inertial load on the oscillating system
(Esch and Wilson, 1967;
Nachtigall, 2003) and the
thoracic capsule might be stiffened through an increased muscle tension
associated with wing adduction (Seeley and
Tautz, 2001).
In sonograms of the sounds and vibrations produced by bees, however, both
an increase in the main frequency component during the build-up of `sound'
pulses and a decrease during their decay phase can be detected
(Esch and Wilson, 1967;
Seeley and Tautz, 2001;
Sen Sarma et al., 2002;
Hrncir et al., 2006a;
Hrncir et al., 2006b). This
evident, but never described, change in frequency points to driven
oscillations: an oscillating system driven by a periodic force with a
frequency higher than its natural frequency will vibrate at this excitation
frequency as long as the force is applied. As soon as the force stops,
however, the vibration will decay and drop to the resonant frequency of the
system (Nocke, 1971).
In the present study, we analysed details of the thoracic oscillations associated with wing movements during stationary flight and those associated with `sound' production during two different types of non-flight vibrations (annoyance buzzing, recruitment sounds). We asked the following two questions. (1) To which extent are resonances involved in both flight and non-flight vibrations? (2) How similar to or different from flight vibrations are vibrations generated in different behavioural contexts?
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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), and were
connected to the outside via plastic tubes through the laboratory
wall. A glass-covered acrylic observation box (10x5x4
cm3) was inserted between the nest and the entrance/exit tubes for
recording the thorax vibrations of returning foragers.
Sling-tethering for stationary flight and annoyance buzzing
Stingless bees reliably produce annoyance buzzing when tethered around the
neck (Fig. 1). A lasso-sling
was formed using a nylon thread (diameter: 0.35 mm) through an injection
needle (1 mm i.d.), and loosely tightened around the neck of a bee. The thread
was fixed by attaching the injection needle to the syringe. As soon as the
sling-tethered bees touched any kind of substrate with their tarsi, they
usually started to generate thorax vibrations. Pulsed annoyance buzzing was
emitted for about 10 min before the bees stopped – probably due to
exhaustion. Stationary flight was initiated by removing the substrate from
underneath the tarsi.
|
). The
individuals used for stationary flight and annoyance buzzing were taken from
the observation box and instantly tethered. These bees were foragers,
potential recruits or food storing bees. Their vibrations were measured on the
scutum, with the laser beam oriented perpendicular to the surface of the
thorax. In some of the experiments, the vibrations of the wings and legs were
recorded simultaneously with those of the thorax, using an identical, second
laser vibrometer. The output of the vibrometers was fed into a notebook
(Pentium IV, 2.4 GHz) using a 24-bit stereo soundcard (PSC 805, Philips,
Amsterdam, The Netherlands) and the software Soundforge 7.0 (Sony Pictures
Digital Inc., Madison, WI, USA), at a sampling rate of 44.1 kHz. For analysis
of the recorded vibrations we used the software SpectraPro 3.32 (Sound
Technology Inc., Campbell, CA, USA), SigmaPlot 2001 (SPSS Inc., Chicago, IL,
USA) and SigmaStat 3.10 (Systat Software Inc., San Jose, CA, USA).
Thoracic vibrations
To evaluate similarities or differences between the different types of
thoracic vibrations (stationary flight, FL; annoyance buzzing, AB; forager
vibrations, FO), the following parameters of the oscillations were analysed
(Fig. 1): the main frequency
component (MF, defined as the frequency with highest energy content
in the power spectrum), the velocity amplitude (VA), and the
displacement amplitude (DA). The displacement of the oscillation was
derived through an integration of the recorded vibration velocity using the
software Microsoft® Office Excel 2003 (Microsoft Corporation, Bellevue,
WA, USA). The resulting waveforms showing the displacement oscillations
(Fig. 1D) were printed out on
paper, and the displacement amplitudes (peak to peak, p-p) were measured to
the nearest µm.
In all three experimental groups (flight, annoyance buzzing and forager vibrations), changes in amplitude as well as main frequency during the build-up and the decay phase of the vibratory pulses were studied as indicators of resonance. In the non-flight groups (annoyance buzzing and forager vibrations) we measured the velocity values peak to peak (p-p) of the first 15 cycles (build-up) and of the last 15 cycles (decay phase) of a vibrational pulse (Fig. 2), considering only pulses with at least 30 cycles. In case of the thorax vibrations during stationary flight, we measured the first 30 cycles and the last 30 cycles of the thoracic oscillations. Cycle frequency was calculated in a simple way from the time between two subsequent peaks (Fig. 2A). Because of inter-individual differences, we normalized the measurements taking the maximum velocity amplitude and the main frequency component as 100%. Both the magnitude and cycle frequency of the vibrations fluctuated slightly after having reached the maximum values (Fig. 2). We therefore defined the build-up as the phase of continuous increase in magnitude and frequency from the onset of the pulse up to 95% of its maximum value. Correspondingly, the decay was defined as the continuous decrease from 95% to the cessation of the vibration (Fig. 2).
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Wing removal and mass loading experiments
In sling-tethered individuals, the natural frequency of the oscillating
system was modified either by first cutting one and then the second pair of
wings close to the thorax (decreasing the inertial load on the system), or by
attaching additional mass to the thorax. To increase the thoracic mass, a tiny
piece of lead (average mass: 31.4 mg) was glued onto the thorax of a bee.
Taking the thoracic mass of M. seminigra into account (33.6 mg, mean
of 15 thoraces, all additional body parts removed), the oscillating thorax was
almost doubled in mass by this experimental treatment. We measured MF,
VA and DA (see above) of the sling-tethered individuals during
stationary flight and during annoyance buzzing, both before the respective
experimental treatment and after wing removal (N=12 bees) or after
additional loading (N=10 bees). For each of the tested individuals,
we recorded the thoracic vibrations during both stationary flight and
annoyance buzzing.
Leg- and wing vibrations
Using two identical laser vibrometers, we simultaneously recorded the
vibrations of the thorax and the distal part of the mesothoracic femur, or of
the thorax and the wingtip. The femoral measurement point was chosen because
it is easily accessible for the laser beam during trophallaxis
(Hrncir et al., 2006b). We
analysed the gain in vibration velocity between thorax and femur/wingtips, and
the transmission of the temporal signal pattern (PD, pulse duration;
PS, pulse sequence; MF, main frequency component;
Fig. 1B) from the thorax to the
femur/wingtips. The transmission was quantified as:
 | (1) |
Statistics
For each tested individual the mean value of the respective vibration
parameter was calculated from 15–30 vibratory pulses. The statistical
tests were performed using these representative mean values. When the data
showed normal distribution (Kolmogorov–Smirnov test, P>0.05)
and equal variance (Levene median test, P>0.05), we applied
parametric tests (Student t-test; paired t-test; one-way
repeated-measures ANOVA followed by a Tukey test for pairwise comparison). If
one of these requirements was not met, we applied non-parametric tests
(Mann–Whitney U-test; Wilcoxon Signed Ranks test; Friedman
repeated measures ANOVA on Ranks; Kruskal–Wallis test followed by a
Dunn's test for pairwise comparison). The degree of correlation between signal
parameters (PD, PS, MF) registered simultaneously on the thorax or
the wings and legs, was tested using the Spearman rank correlation. The
correlation coefficient (rS) indicates the degree of
correlation between the simultaneously measured vibrations
(rS=1, highly correlated; rS=0, not
correlated). Throughout the text, values are presented as median [1st
quartile/3rd quartile]. N refers to the number of different
individuals tested, and n to the number of pulses included in the
calculations of the mean values. The level of significance of differences was
taken as P
0.05.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The role of resonances in thoracic vibrations
To find out about the potential role of resonances involved in the
generation of the thoracic vibrations, we analysed (1) the changes in both
velocity amplitude and main frequency during the build-up and the decay of the
vibrations, and (2) the changes in main frequency, velocity amplitude and
displacement amplitude due to a decrease in inertial loading by wing removal
or due to an increase in the mass of the oscillating system.
Build-up and decay of vibratory pulses
Flight
The velocity of the thoracic vibrations associated with wing movements had
an average build-up of about 14 cycles and a decay phase of about 16 cycles
(Fig. 4;
Table 1). The main frequency,
on the other hand, showed almost no changes at the beginning and at the end of
the vibration. After the first cycle the average cycle frequency increased
from 177 Hz [164/191] to its maximum value of 181 Hz [175/186]. During the
last two cycles, the cycle frequency dropped from 181 Hz [163/185] to 160 Hz
[153/175].
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Comparison flight with non-flight vibrations
The build-up and the decay in velocity were significantly longer in the
vibrations during stationary flight than during the non-flight vibrations
(Table 1). However, there was
no significant difference in cycle number among the three different types of
vibrations during the build-up and decay in main frequency
(Table 1). The final cycle
frequencies of annoyance buzzing (AB) and forager vibrations (FO) were
significantly higher than that of the flight vibrations (FL)
(Kruskal–Wallis test: H=23.4; P<0.001; d.f.=2;
NAB, NFO, NFL=15;
Dunn's test: AB vs FL: Q=3.4; P<0.05; FO
vs FL: Q=4.7; P<0.05).
Wing removal and loading experiments
After wing removal, the main frequency component (MF), the
velocity amplitude (VA) and the displacement amplitude (DA)
of the thoracic vibrations during stationary flight changed significantly
(MF, one-way repeated-measures ANOVA:
F2,11=135.1; P<0.001;
Fig. 5A; VA, one-way
repeated-measures ANOVA: F2,11=3.75; P=0.04;
Fig. 5B; DA, Friedman
repeated-measures ANOVA on ranks: 
2=8.17; P=0.017;
Fig. 5C). In the case of
annoyance buzzing, however, neither of the investigated vibration parameters
changed due to the removal of the wings (MF, one-way
repeated-measures ANOVA: F2,11=1.75; P=0.20;
Fig. 5D; VA, one-way
repeated-measures ANOVA: F2,11=2.18; P=0.14;
Fig. 5E; DA, Friedman
repeated-measures ANOVA on ranks: 2=2.00; P=0.368;
Fig. 5F).
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Doubling the thoracic mass resulted in a significant decrease in the main frequency component and of the velocity amplitude of the vibrations during stationary flight. The displacement amplitude of the oscillations in this type of thoracic vibrations, however, did not change after the experimental treatment (MF, paired t-test: t9=4.02; P=0.003; Fig. 6A; VA, paired t-test: t9=2.87; P=0.019; Fig. 6B; DA, paired t-test: t9=0.51; P=0.62; Fig. 6C). In the case of annoyance buzzing, we observed a significant decrease in velocity amplitude and displacement amplitude after attaching a piece of lead to the thorax. The main frequency component of the vibrations, however, remained unaffected by this experimental treatment (MF, Wilcoxon signed ranks test: W=–15; P=0.49; d.f.=9; Fig. 6D; VA, Wilcoxon signed ranks test: W=–55; P=0.002; d.f.=9; Fig. 6E; DA, paired t-test: t9=3.45; P=0.007; Fig. 6F).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Nachtigall et al., 1998;
Nachtigall, 2003). Conclusions
about non-flight thoracic vibrations, which eusocial bees generate in a
variety of behavioural contexts, are primarily based on findings regarding the
thoracic oscillations associated with the wing movements
(Esch and Wilson, 1967;
Seeley and Tautz, 2001;
Nachtigall, 2003). Now a
detailed comparison of the thoracic oscillations during flight with those
during `sound' production (non-flight vibrations) in the stingless bee
Melipona seminigra provides evidence of mechanical differences
between these two types of thoracic oscillations.
Different role of resonances in flight and non-flight vibrations
Different from the thoracic oscillations associated with wing movements
during flight, non-flight vibrations in M. seminigra were not
generated at the natural frequency of the oscillating system. Thus, resonances
do not play an important role in the latter type of vibrations. Whereas all
assumptions in favour of resonant vibrations tested in the present study were
met in the thoracic oscillations associated with flight, none of the criteria
applied to the non-flight vibrations.
When a simple oscillating system is excited by a periodic force at its
natural frequency, the cycle frequency does not change during the build-up and
the decay phase of the pulses. Driven by a periodic force at a frequency
higher than its natural frequency, the system will vibrate at the excitation
frequency as long as the force is applied. As soon as the force stops, the
vibration will decay and drop to the resonant frequency of the system
(Nocke, 1971;
Bennet-Clark, 1999). Already
the first oscillation cycle of the flight movements in M. seminigra
was executed at the average flight frequency
(Fig. 4D;
Table 1). Admittedly, the
`lift-off' in our experiments, which occurred through the sudden deprivation
of the contact between the bees' tarsi and the substrate, is not the natural
situation. During a natural take-off, as shown by detailed studies in flies
(reviewed in Nachtigall,
2003), the stiffness and consequently the resonant properties of
the thorax change within the last 50 ms prior to the onset of the indirect
wing mechanism due to the increasing tension of the thoracic pleurosternal and
tergotrochanter muscles. Yet, the indirect wing mechanism only starts to
operate after a `jump-start' of the animal, or in other words, only after the
tarsi have lost the contact with the substrate. This jump to initiate flight
is typical not only for flies but also for various other insects
(Nachtigall, 2003), and
probably also for bees. Therefore, the `forced take-off' applied in our
experiments can be considered a proper replicate of the natural situation.
Although in M. seminigra the oscillation frequency remained
approximately constant during the entire stationary flight, it decreased from
181 Hz to 160 Hz (by about 12%) during the last two cycles of the vibrations
(Fig. 3B). Similar to our
findings, the cycle frequency of the thoracic vibrations during flight of
Calliphora and Eristalis decreased by about 13% during the
last 2–4 cycles [measured from fig.
3 in Roeder (Roeder,
1951)]. Therefore, either flight vibrations are driven at a
frequency slightly above the natural frequency of the oscillating system, or
changes in the stiffness of the system occur during these last few cycles due
to changes in muscle tension (Nachtigall
and Wilson, 1967).
Both cutting the wings and increasing the mass of the oscillating system
resulted in changes of the main frequency component of flight vibrations (Figs
5,
6). From this we conclude that
resonances are indeed important for the generation of this type of thoracic
oscillation. In contrast to the flight vibrations, however, thorax
oscillations underlying annoyance buzzing remained largely uninfluenced by our
experimental treatments. Doubling the mass of the thorax experimentally did
not reduce the main frequency component of annoyance buzzing
(Fig. 6D), only its
displacement amplitude (Fig.
6F). An explanation for this could be that the driving force
remained more or less constant during annoyance buzzing, and did not
compensate for the additional mass on the oscillating system (simplified as:
F=ma
constant, where F=force, m=mass
and a=acceleration, which is proportional to displacement
amplitudexmain frequency).
As with bumble bee queens (Schneider,
1975), ablation of the wings did not influence the main frequency
component of annoyance buzzing in M. seminigra. Although the wings
are folded above the abdomen during this type of thoracic vibration and thus
decoupled from the indirect wing mechanism
[(Snodgrass, 1956); for a
comparative study of the thoracic muscles and their function in bees see Wille
(Wille, 1956)], they still are
attached to the thoracic capsule. This inevitably leads to oscillations of the
wings along with the thorax (Fig.
7) which, consequently, influences the natural frequency of the
oscillating system through the damping caused by the mass of air moved by the
wings. Hence, a reduction of the wing area not only decreases the inertial
load on the thorax during flight but also, to a minor extent, during annoyance
buzzing. Even so, wing removal had no influence on the main frequency
component of the annoyance buzzing (Fig.
5D).
Our results suggest that in M. seminigra the natural frequency of
the oscillating system during non-flight vibrations is higher than that during
flight vibrations, and that non-flight vibrations are driven at a frequency
higher than the natural frequency of the oscillating system. The final cycle
frequency was very similar in annoyance buzzing (215 Hz) and in the forager
vibrations (225 Hz). This indicates that the natural frequency of the
oscillating thorax is similar during these two types of non-flight vibrations
despite differences observed between their main frequency components
(Table 1). The elevated natural
frequency of the thorax during non-flight vibrations, in comparison to that
during flight vibrations, supposedly is a result of an increased tension of
the thoracic muscles (Nachtigall and
Wilson, 1967; Seeley and
Tautz, 2001).
In insects with an indirect flight mechanism, the wingbeat frequency
increases with the frequency of motor action potentials
(Roeder, 1951;
Esch and Bastian, 1968;
Bastian and Esch, 1970). The
damping of the vibrating system can be deduced from the decay in amplitude at
the end of the thoracic vibrations. In flight vibrations of M.
seminigra, this decay took an average of 16 cycles
(Fig. 3A;
Table 1) or about 0.09 s, which
corresponds to a motor input every 10–20 wingbeats (action potential
frequency: 8–16 Hz), as found in honey bees and flies
(Roeder, 1951;
Esch, 1964). In the non-flight
vibrations, the decay took an average of six cycles (
0.02 s) in the case
of annoyance buzzing and eight cycles (0.02 s) in that of forager
vibrations. To offset this damping in the non-flight vibrations, the neural
excitation would have to occur at a rate of about 50 Hz. This complies with
electromyogram recordings during non-flight buzzing (`sonication') in bees of
the genera Bombus and Xylocopa
(King et al., 1996). Here, the
authors measured a maximum excitation frequency of the indirect flight muscles
of approximately 60 Hz. Therefore, the higher main frequency component found
in non-flight vibrations compared to the flight vibrations can be explained by
the higher action potential rate rather than by changes in the natural
frequency of the oscillating thorax.
Analysis of signal generation and signal transmission under controlled conditions
In stingless bees of the genus Melipona, thoracic vibrations
related to recruitment behaviour are supposedly transmitted to hive bees
through substrate vibrations (Lindauer and
Kerr, 1958), airborne signals
(Esch, 1967), or direct contact
during trophallaxis (Hrncir et al.,
2006b). With the exception of the third pathway, neither the
transformation of the thoracic vibrations into relevant signals
(substrate-borne or airborne) nor their actual transmission to potential
recruits has been studied in detail within their natural context. This is
largely due to the fact that the trophallactic food transfer involves
movements by the foragers themselves, and also by the hive bees in their
proximity. Therefore, the accurate positioning of measuring devices close to
the vibrating forager is an almost impossible task. The limitations for exact
measurements around foragers within the nest call for alternative methods that
allow a detailed study of the signal generation and signal transmission in a
controlled laboratory situation
(Michelsen, 2003).
Annoyance buzzing and forager vibrations are very similar in terms of the
mechanism of their generation, and they result in similar vibrations of the
legs and wingtips (Fig. 7),
which transform thoracic vibrations into substrate vibrations and airborne
sounds (Michelsen et al.,
1987; Tautz et al.,
2001; Michelsen,
2003; Hrncir et al.,
2008). Our data suggest that thoracic vibrations are transformed
into mechanical signals in both annoyance buzzing and forager vibrations with
similar efficiency. Annoyance buzzing of sling-tethered bees, therefore,
permits study mechanisms of signal generation and transmission under
controlled conditions in stingless bees, as recently demonstrated for the
transformation of thoracic vibrations into air particle movements
(Hrncir et al., 2008).
LIST OF ABBREVIATIONS
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Acknowledgments |
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|
References |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Bastian, J. and Esch, H. (1970). The nervous control of the indirect flight muscles of the honey bee. Z. Vergl. Physiol. 67,307 -324.[CrossRef]
Bennet-Clark, H. C. (1999). Resonators in insect sound production: how insects produce loud pure-tone songs. J. Exp. Biol. 202,3347 -3357.[Abstract]
Buchmann, S. L. (1983). Buzz pollination in angiosperms. In Handbook of Experimental Pollination Biology (ed. C. E. Jones and R. J. Little), pp.73 -113. New York, Cincinnati, Toronto, London, Melburne: Van Nostrand Reinhold.
Chadwick, L. E. and Williams, C. M. (1949). The
effects of atmospheric pressure and composition on the flight of
Drosophila. Biol. Bull.
97,115
-137.
Darveau, C.-A., Peter, W., Hochachka, P. W., Welch, Jr, K. C.,
Roubik, D. W. and Suarez, R. K. (2005). Allometric scaling of
flight energetics in Panamanian orchid bees: a comparative phylogenetic
approach. J. Exp. Biol.
208,3581
-3891.
Esch, H. (1961). Über die Schallerzeugung beim Werbetanz der Honigbiene. Z. Vergl. Physiol. 45, 1-11.[CrossRef]
Esch, H. (1964). Über den Zusammenhang zwischen Temperatur, Aktionspotentialen und Thoraxbewegungen bei der Honigbiene (Apis mellifica L.). Z. Vergl. Physiol. 48,547 -551.
Esch, H. (1967). Die Bedeutung der Lauterzeugung für die Verständigung der stachellosen Bienen. Z. Vergl. Physiol. 56,199 -220.
Esch, H. and Bastian, J. (1968). Mechanical and electrical activity in the indirect flight muscles of the honey bee. Z. Vergl. Physiol. 58,429 -440.[CrossRef]
Esch, H. and Wilson, D. (1967). The sounds produced by flies and bees. Z. Vergl. Physiol. 54,256 -267.[CrossRef]
Hrncir, M., Jarau, S., Zucchi, R. and Barth, F. G. (2004). Thorax vibrations in stingless bees (Melipona seminigra). II. Dependence on sugar concentration. J. Comp. Physiol. A 190,549 -560.[Medline]
Hrncir, M., Barth, F. G. and Tautz, J. (2006a). Vibratory and airborne sound-signals in bee communication. In Insect Sounds and Communication: Physiology, Behaviour, Ecology, and Evolution (ed. S. Drosopoulos and M. Claridge), pp.421 -436. Boca Raton, London, New York: CRC Press, Taylor & Francis Group.
Hrncir, M., Schmidt, V. M., Schorkopf, D. L. P., Jarau, S., Zucchi, R. and Barth, F. G. (2006b). Vibrating the food receivers: a direct way of signal transmission in stingless bees (Melipona seminigra). J. Comp. Physiol. A 192,879 -887.[CrossRef][Medline]
Hrncir, M., Schorkopf, D. L. P., Schmidt, V. M., Zucchi, R. and
Barth, F. G. (2008). The sound field generated by tethered
stingless bees (Melipona scutellaris): inferences on its potential as
a recruitment mechanism inside the hive. J. Exp. Biol.
211,686
-698.
King, M. J. (1993). Buzz foraging mechanism of bumble bees. J. Apic. Res. 32, 41-49.
King, M. J., Buchmann, S. L. and Spangler, H. (1996). Activity of asynchronous flight muscle from two bee families during sonication (buzzing). J. Exp. Biol. 199,2317 -2321.[Abstract]
Lindauer, M. and Kerr, W. E. (1958). Die gegenseitige Verständigung bei den stachellosen Bienen. Z. Vergl. Physiol. 41,405 -434.[CrossRef]
Michelsen, A. (2003). Signals and flexibility in the dance communication of honeybees. J. Comp. Physiol. A 189,165 -174.[Medline]
Michelsen, A., Kirchner, W. H. and Lindauer, M. (1986). Sound and vibrational signals in the dance language of the honeybee, Apis mellifera. Behav. Ecol. Sociobiol. 18,207 -212.[CrossRef]
Michelsen, A., Towne, W. F., Kirchner, W. H. and Kryger, P. (1987). The acoustic near field of a dancing honeybee. J. Comp. Physiol. A 161,633 -643.[CrossRef]
Michener, C. D. (1962). An interesting method of pollen collecting by bees from flowers with tubular anthers. Rev. Biol. Trop. 10,167 -175.
Nachtigall, W. (2003). Insektenflug. Berlin, Heidelberg, New York: Springer Verlag.
Nachtigall, W. and Wilson, D. M. (1967).
Neuro-muscular control of dipteran flight. J. Exp.
Biol. 47,77
-97.
Nachtigall, W., Wisser, A. and Eisinger, D. (1998). Flight of the honey bee. VIII. Functional elements and mechanics of the `flight motor' and the wing joint-one of the most complicated gear-mechanisms in the animal kingdom. J. Comp. Physiol. B 168,323 -344.[CrossRef]
Nocke, H. (1971). Biophysik der Schallerzeugung durch die Vorderflügel der Grillen. Z. Vergl. Physiol. 74,272 -314.[CrossRef]
Roeder, K. D. (1951). Movements of the thorax
and potential changes in the thoracic muscles of insects during flight.
Biol. Bull. 100,95
-106.
Schneider, P. (1972). Akustische Signale bei Hummeln. Naturwissenschaften 59,168 -169.[Medline]
Schneider, P. (1975). Versuche zur Erzeugung des Verteidigungstones bei Hummeln. Zool. Jb. Physiol. 79,111 -127.
Seeley, T. D. and Tautz, J. (2001). Worker piping in honey bee swarms and its role in preparing for liftoff. J. Comp. Physiol. A 187,667 -676.[CrossRef][Medline]
Sen Sarma, M., Fuchs, S., Werber, C. and Tautz, J. (2002). Worker piping triggers hissing for coordinated colony defence in the dwarf honeybee Apis florea. Zoology 105,215 -223.[CrossRef][Medline]
Snodgrass, R. E. (1956). Anatomy of the Honey Bee. Ithaca, NY: Comstock Publishing Associates.
Soltavalta, O. (1952). The esential factor regulating the wing-stroke frequency of insects in wing mutilation and loading experiments and in experiments at subatmospheric pressure. Ann. Zool. Soc. Vanamo 15,1 -67.
Tautz, J., Casas, J. and Sandeman, D. C.
(2001). Phase reversal of vibratory signals in honeycomb may
assist dancing honeybees to attract their audience. J. Exp.
Biol. 204,3737
-3746.
Wenner, A. M. (1962). Sound production during the waggle dance of the honeybee. Anim. Behav. 10, 79-95.[CrossRef]
Wille, A. (1956). Comparative studies of the thoracic musculature of bees. Univ. Kansas Sci. Bull. 38,439 -499.
Wille, A. (1963). Behavioral adaptations of bees for pollen collecting from Cassia flowers. Rev. Biol. Trop. 11,205 -210.
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