Tuning of host plants with vibratory songs of Nezara viridula L (Heteroptera: Pentatomidae)
okl*
uni
Department of Entomology, National Institute of Biology, Vena
pot 111, SI-1000 Ljubljana, Slovenia
* Author for correspondence (e-mail: andrej.cokl{at}nib.si)
Accepted 23 February 2005
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Summary |
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Key words: vibratory communication, vibratory song, resonance, host plant, Nezara viridula, southern green stink bug
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Introduction |
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All species of the subfamily Pentatominae are entirely plant feeders
(Panizzi et al., 2000). On
branched dycotyledonous plants with different impedance characteristics one
can expect high distortion of low frequency and narrow-band signals, due to
reflections and frequency-dependent standing wave patterns
(Michelsen et al., 1982
;
Barth, 1998
). In such
conditions, songs of N. viridula should be less suitable for
communication through plants. Furthermore, vibratory sensory organs of N.
viridula are not precisely tuned with the spectral properties of
loudspeaker recorded songs (
okl,
1983
). Nevertheless, behavioural experiments prove that male and
female N. viridula communicate efficiently with vibratory songs on
the same plant. Female calling-song signals, for example, mediate vibrational
directionality of males on stem/stalk crossings
(
okl et al., 1999
) and
mates differentiate the conspecific song from those of other stink bug species
at long distances (Hrabar et al.,
2004
).
The impact of substrate type on vibratory communication was first shown in
N. viridula: males differentiate temporally different female
calling-song pulse trains on a non-resonant loudspeaker membrane but not on a
plant (Miklas et al., 2001).
The leaf and its structural components play an important role in the
propagation of the short transient signals produced by insects
(Magal et al., 2000
).
Significantly higher attenuation of the harklequin bug vibratory signals was
demonstrated in leaf lamina than in leaf vein
(
okl et al., 2004
). In
several examples of lacewing species confined to conifers vs those on
herbacous vegetation, song phenotype showed a correlation with substrate
independent of phylogeny; nevertheless the pattern suggestive of environmental
adaptation of songs to their substrates was not experimentally supported
(Henry and Martinez Wells,
2004
). The effect of substrate on the efficacy of seismic
courtship signal transmission in the jumping spider was recently investigated
(Elias et al., 2004
). It has
been demonstrated that despite different filtering properties, the male
courtship behaviour was not modified on different substrates, but the
proportion of males mating successfully on leaf litter was significantly
higher than on rocks or desert sand.
The aim of our study was to elucidate the apparent inconsistency between spectral properties of loudspeaker-recorded songs and tuning of vibrational receptors on the one hand and efficient substrate-borne communication through plants on the other. We propose the hypothesis that singing stink bugs induce resonant vibration of a plant with frequency characteristics reflected in the spectra of the transmitted signals. To confirm this hypothesis we measured resonant frequency characteristics of stink bug host plants and compared them with the spectra of naturally or artificially induced vibrations, measured simultaneously from the body of a singing bug and different parts on a plant. To avoid potential impact on the mechanical properties of plants, we used noncontact stimulation and recording techniques.
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Materials and methods |
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Vibratory signals were recorded from different points on the surface of fresh green bean, grown in the laboratory and harvested fresh that day. Each bean plant had a 1524 cm long stem and two 47 cm long stalks, each with a 59 cm long and 4-8 cm wide leaf at its distal end. Resonant properties were determined in detail for ten green bean plants (leaf length 6.1±0.9 cm, leaf width 5.9±0.9 cm, stalk length 4.3±0.7 cm, stem length 24.2±2.2 cm). For comparative reasons resonance was tested for single brussels sprouts (Brassica oleracea var. gemmifera L), turnip cabbage (Brassica oleracea var. caulorapa L) and tomato (Lycopersicon esculentum Mill.) as well as for two cyperus (Cyperus alternifolius L), broccoli (Brassica oleracea var. italica L), strawberry (Fragaria chiloensis L) and cauliflower (Brassica oleracea var. botrytis L) plants.
Induction and recording of vibrations in plants and loudspeaker membrane
Plant vibrations were induced naturally by females of a Slovene population,
singing on the dorsal surface of a bean leaf 13 cm from the insertion
to the stalk. Bugs were triggered to sing by a male who was presented to a
female over the air and removed immediately after the first emitted female
calls. Spectra were determined from signals of four females, each singing on a
different plant.
Plant vibrations were induced artificially by a magnet glued to the upper surface of a bean leaf at the place from where females are usually calling. The magnet weight of 26 mgcorresponded approximately to the weight of adult females. The magnet was vibrated by an electromagnet positioned 0.51.0 cm away. Stimulus sequences were synthesized from loudspeaker-recorded calling songs of N. viridula females of Slovene and French populations. Stimulus pulse trains of both populations differed in their mean dominant frequency (83±1 Hz, N=10 and 102±4 Hz, N=10 for the Slovene and French population, respectively), pulse train duration (1962±125 ms, N=10 for the Slovene and 988±72 ms, N=10 for the French population) and repetition time (5379±117 ms, N=10 for the Slovene and 3732±174 ms, N=10 for the French population). Each stimulus song was composed of 10 pulse trains.
Airborne sound stimuli (380 Hz, 5 s duration, random repetition rate) were
used to induce resonance of a loudspeaker membrane (2r=10 cm, 406000 Hz
frequency response, impedance 8 , #WS 13 BF, Visaton, Germany) or
plants. Acoustic stimuli were synthesized using Sound Forge (Sonic Foundry,
Madison, WI, USA) software, amplified over an amplifier (PM 5175, Philips,
Holland) and applied by a middle-tone loudspeaker positioned 12 cm from
the investigated substrate. Sound evoked vibrations of velocity values of 18
mm s1 in a loudspeaker membrane and between 0.2 and 4.1 mm
s1 in leaves, 0.1 and 1.9 mm s1 in stalks
and between 0.1 and 2.5 mm s1 in the bean stems.
Substrate vibrations were recorded using a laser vibrometer (Polytec, Waldbronn, Germany; OFV-353 sensor head and OFV-2200 controller). Two identical laser vibrometers were used for simultaneous recording from different points. Recorded signals were stored directly on a computer for later analyses by Cool EditPro (Adobe Systems Incorporate, San Jose, CA, USA) and Sound Forge software. To obtain better reflection small reflective flags (ca. 1 mm2) were attached to plant surfaces at a measuring point and small areas (ca. 1 mm2) on the bug surface were painted using white correction fluid (Tipp-Ex).
Naturally emitted signals were recorded simultaneously with the reference laser vibrometer from the pronotum of a singing bug and with the measuring one from (a) the leaf immediately below, (b) from ipsi- or (c) contralateral stalks 1 cm from the crossing with the stem, or (d) from the middle of the stem. Artificially induced vibrations were measured simultaneously on the bean with the reference laser vibrometer from the ipsilateral stalk about 0.5 cm from the junction with the leaf and about 1 cm from the vibration source, and with the measuring laser vibrometer from (a) ipsi- and (b) contralateral stalks about 1 cm from the crossing with the stem, (c) at the distal end of the contralateral stalk as well as (d) on the stem about 1 cm below the crossing or (e) approximately at stem middle. Sound-induced vibrations were recorded from the surface of a loudspeaker membrane or from plant leaves, stalks and stem.
Terminology and statistics
Pulses are defined as unitary homogeneous parcels of sound waves of finite
duration, and pulse trains as repeatable and temporally distinct groups of
pulses (Broughton, 1963). In
spectra of vibratory-induced vibrations the positions of the dominant and
subdominant peaks were determined together with relative amplitude, as the
difference between amplitudes of the dominant (0 dB) and subdominant peaks.
Position and amplitude values were calculated for peaks whose amplitudes were
at least 15 dB above the resonant spectra baseline. Values of spectral peak
positions and amplitudes were averaged in frequency ranges of 50100 Hz,
100150 Hz, 150250 Hz and 250400 Hz. Two-tailed Student's
t-test and analysis of variance (ANOVA) were used for statistical
data processing.
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Results |
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Spectra of signals recorded on different parts of a plant differ. Comparing only spectra of body- and leaf-recorded signals (Fig. 1F), we could find no significant difference in the position of the dominant and subdominant spectral peaks. By contrast, spectra of leaf-recorded signals show a significant (P<0.05) amplitude decrease of subdominant peaks and a general damping of frequencies below 70 Hz (Fig. 1F). The amplitude difference between the dominant and 4050 Hzsubdominant peaks increased from 8±3 dB (N=20) as measured in body-recorded signals to 28±4 dB (N=20) in signals recorded on the leaf. Mean subdominant peak frequencies between 150 and 250 Hz are not the double of mean dominant frequencies, indicating that they do not represent their first harmonics.
Spectral properties of artificially induced vibratory signals
Spectra of loudspeaker-recorded stimulus songs differ from spectra of
plant-recorded signals (Figs
1E,
2). Mean dominant frequencies
of plant-recorded signals were about 1 Hz above the mean value (83±1
Hz, N=10) of the stimulus song of the Slovene population; the
difference was significant (P<0.05) only for signals recorded on
the ipsilateral stalk.
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The mean dominant frequency of the French population stimulus song (102±4 Hz, N=10) ranged in plant-recorded signals between 101±11 Hz (N=11) and 110±2 Hz (N=16); a significant (P<0.05) difference between stimulus song and plant-recorded signals could be shown only on the ipsilateral stalk. Spectra of artificially induced vibrations lack peaks above 250 Hz and the main subdominant peak of the Slovene population stimulus song at 169±3 Hz (N=10) does not differ significantly from values of plant-recorded signals. The corresponding subdominant peak in plant-recorded French female calling-song signals could be shown only in spectra of signals recorded on the ipsilateral stalk and stem close to the crossing (Fig. 2A,C). Subdominant spectral peaks not characteristic for the stimulus songs appear in plant-recorded signals in the frequency range below 150 Hz (Fig. 2). Their peak position corresponds to values measured for naturally emitted signals in frequency ranges below 100 Hz and between 100 and 150 Hz (Figs 1, 2). Mean values differ significantly (P<0.05) between populations and between recordings from different points on a plant within each frequency range, except for the Slovene female calling-song signals in the 100150 Hz frequency range.
Resonant properties of plants
Spectra of loudspeaker- or plant-recorded environmental noise contained
peaks around 15, 50, 150 and 250 Hz (Fig.
3). Velocity of sound-induced vibrations of a loudspeaker membrane
or plant was comparable with values of signals recorded on the surface of a
singing bug. Resonant peaks could be shown in spectra of vibrations recorded
from plants (Fig. 3A) but not
from the loudspeaker (Fig. 3B).
The main resonant peak of leaf-recorded signals in 10 different bean plants
was 194±33 Hz and subdominant peaks were detected around 81 Hz, 118 and
290 Hz (Table 1). No
significant difference could be shown for the position of resonant peaks in
spectra of signals recorded from leaves and stalks. By contrast, significantly
different (P<0.05) values were measured for resonant peaks of
stem-recorded vibrations in the frequency range 100150 Hz. In the
frequency ranges below 100 and above 150 Hz the plant resonant peaks
correspond to the spectral peaks of naturally emitted female calling-song
signals recorded on the body or the plant
(Fig. 3C). Comparable spectral
peak values of naturally and artificially induced signals were recorded in the
frequency range 150250 Hz (Figs
1F,
2;
Table 1). For comparative
reasons we tested resonant properties in other N. viridula host
plants. Resonant spectra are similar to those of bean
(Fig. 4), with the dominant
peak for leaf-recorded vibrations at 201±31 Hz (N=2) for
cyperus, 189±30 Hz (N=2) for strawberry, 174±23 Hz
(N=2) for cauliflower, 170±13 Hz (N=2) for broccoli, 190 Hz
for brussels sprouts and turnip/cabbage and 160 Hz for tomato.
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Discussion |
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Loudspeaker-recorded vibratory signals reflect characteristics of body
vibrations without any feed-back from the substrate. This recording technique
is relevant for comparison of spectral properties of different songs or
species, but does not reveal anything about the possible effect of substrate
vibration on the spectral properties of transmitted signals. Panizzi
(1997) summarized data on
plants on which polyphagous stink bugs feed and mate; no special plants
preferred for mating have been identified. N. viridula, for example,
concentrates in Paraná on soybean plants during summer but is also
found on common bean P. vulgaris. During autumn, adults feed,
reproduce and complete the fourth generation on wild legumes but also move to
wild hosts like star bristle and castor bean to feed. During late fall and
early winter the species is found on radish, mustards and wheat. During spring
a sixth generation is completed on Siberian motherwort. Although polyphagous,
N. viridula prefers legumes and brassicas in Brazil, pods of green
bean P. vulgaris in India, individuals from United States prefer pods
of soybean G. max, and nymphs from South Carolina but not those from
Florida survive on Cassia fasciculata L. At the North Adriatic coast
N. viridula feeds and reproduces during spring and summer on
different legumes and brassicas but in autumn it gathers on Clematis
plants, upon which reproduction was not observed. Green bean P.
vulgaris is one of the common host plants of N. viridula on
which feeding and reproduction was observed in nature.
The mechanical properties of plants as transmission channels for vibratory
signals have been studied in the context of communication in insects
(Michelsen et al., 1982) and
spiders (Barth, 2002
).
Arthropods communicating through plants use bending waves, and in standing
wave conditions it would not be a good strategy to use pure tone vibratory
signals for communication (Michelsen et
al., 1982
). In fact pure tone vibratory signals are not emitted by
arthropods and broad-band stridulatory together with narrow band low frequency
components are characteristic for signals of some insect groups like
planthoppers, leafhoppers and cydnide bugs
(Gogala, 1984
;
Claridge, 1985
;
okl and Virant-Doberlet,
2003
). On the other hand several spider and insect species
communicate successfully via plants using only low frequency and
narrow band signals. The frequency spectrum of male wandering spider
Cupiennius salei (Keyserling) opisthosomal signals has its prominent
peak between 75 and 100 Hz and the main frequency components of female
vibrations are at ca. 2040 Hz
(Barth, 2002
). Stink bugs emit
only low frequency narrow band songs
(
okl and Virant-Doberlet,
2003
). Even in combined low frequency and broad-band stridulatory
signals the main energy is emitted at the lower frequencies of the
substrate-borne component. For example, the vibration component of Euides
speciosa Boh. signals shows its maximum between 150 and 200 Hz, whereas
the maximum for airborne sound is at about 550 Hz
(Traue, 1978
). The main energy
emitted by cydnide bugs is in most cases below 500 Hz, although sound energy
extends in some species at least to 12 kHz
(Gogala et al., 1974
).
The mean dominant frequency of the N. viridula female calling song
was only occasionally measured below 90 Hz in bugs singing on a loudspeaker
membrane. In our experiments the mean dominant frequency value was regularly
below 90 Hz in spectra of signals recorded from bugs singing on a plant.
Although one cannot exclude the possibility that the 8090 Hz dominant
frequency in the latter case can be attributed to inter-individual
differences, several data indicate that the position of the dominant frequency
peak is potentially determined by the resonant properties of plants. The
8090 Hz component dominates in spectra of naturally emitted signals
recorded on both body and plant, and represents one of the resonant peaks in
the frequency range below 100 Hz. The mean dominant frequency of
plant-recorded song varies by just 1 Hz when the song with 83 Hz dominant
frequency was used to induce vibrations and by almost 10 Hz in the case of
stimulus song of higher dominant frequency. Early experiments on transmission
of N. viridula male calling song through cyperus
(okl, 1988
)
demonstrated that increasing the distance from the source results in a
decrease of the amount of spectral components above 200 Hz and shift of the
dominant frequency to values around 90 Hz. The 8090 Hz peak also
becomes prominent in spectra of stem-recorded vibrations that were
artificially induced by 124 Hz pure tone signals.
Spectra of plant-recorded female calling songs differ in some respect when induced naturally by singing females or artificially by electromagnetic vibration of a magnet glued to the upper surface of the leaf. The dominant frequency of the French female stimulus calling song did not fall below 90 Hz in plant-recorded signals and no peaks above 250 Hz could be recorded. We have no explanation for differences in naturally emitted signals except that vibrations in the latter case are transferred from the body to the substrate over spatially separated legs and that loading of a plant even with a light magnet potentially modifies its mechanical properties. The stimulation technique using a magnet glued to the plant surface needs a critical application when used to mimic natural conditions.
Spectra of loudspeaker-recorded vibratory signals differ among different species, sex and song types, mainly in the number of higher harmonics and in the amounts of frequency modulation. In this respect the female calling song of N. viridula represents a simple example with narrow dominant and first harmonic spectral peaks, without any pronounced frequency modulation. Spectra of body- and plant-recorded signals contain subdominant peaks that are not present in loudspeaker-recorded vibrations. The dominant resonant peak of bean between 180 and 200 Hz corresponds to the subdominant spectral peak of laser-recorded songs from the pronotum or different parts of a plant. The new added peaks outside the range of the first harmonic support the hypothesis that spectral properties of signals transmitted through plant are at least partly determined by feed-back from vibrated plants.
Similar resonant properties of different plants indicate that frequency
filtering of transmitted vibratory signals is of a rather similar nature. The
propagation velocity at a particular frequency is largely independent of a
plant's mechanical properties (Michelsen
et al., 1982). Attenuation of only 0.3 dB cm1
was measured for 75 Hz signals transmitted in the banana leaf and signals of
frequencies around 100 Hz show amplification (and not attenuation) when
recorded at a distance of several cm from the source on Thesium
bavarum Schrank (Michelsen et al.,
1982
). N. viridula mates were observed to alternate at a
distance above 2 m through different cyperus stems in mechanical contact only
by their roots and surrounding earth, and the naturally emitted female calling
song of the species was attenuated for less than 5 dB at a distance of 1 m
from the source on a cyperus stem (A.
okl, unpublished). Such low
attenuation can be explained by signals tuned with the plant resonance.
Plant resonant peaks that determine spectra of transmitted signals fit well
with tuning of leg vibratory receptors in N. viridula
(okl, 1983
). The middle
frequency receptor cell of the subgenual organ responds with highest
sensitivity and with prolonged responses to frequencies around 200 Hz
(
okl, 1983
). In the
frequency range above 200 Hz the sensitivity of the subgenual middle frequency
receptor cell decreases but that of the high frequency receptor cell
increases, so that spectral components above 250 Hz can be detected
efficiently. Low frequency receptor cells show best sensitivity around 70 Hz
and the shift of the signal dominant frequency below 100 Hz enables better
cycle-by-cycle analysis of time of arrival differences as the peripheral
neuronal basis for male-expressed vibratory directionality.
We can conclude that efficient substrate-borne communication of stink bugs is based on optimal tuning between frequency characteristics of vibratory songs, frequency sensitivity of vibratory sensory organs and resonant properties of green plants. Experimental data on the efficiency of transmission of broad-band stridulatory signals through plants is needed to determine their role in vibratory communication between insects.
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Acknowledgments |
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