Animal Behaviour 82 (2011) 1175e1183

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Animal Behaviour
journal homepage: www.elsevier.com/locate/anbehav

Silent singers are not safe: selective response of a parasitoid to substrate-borne

vibratory signals of stink bugs

Raúl A. Laumanna, *, Andrej Coklb,1
, Ana P. S. Lopesa, Jonatas B. C. Fereiraa, Maria C. B. Moraesa,
Miguel Borgesa
a
Embrapa Recursos Genéticos e Biotecnologia, Brasília, DF, Brazil
b
National Institute of Biology, Ljubljana, Slovenia

a r t i c l e i n f o
The egg parasitoid Telenomus podisi Ashmead (Hymenoptera: Scelionidae) can eavesdrop on vibratory
Article history: signals of adult stink bugs. Here, we tested the hypothesis that the parasitoid can selectively respond to
Received 2 May 2011 the sex- and species-specific songs of different stink bugs. Two-choice plant bioassays were performed
Initial acceptance 20 June 2011 using dried bean plants with two expanded opposite leaves that were vibrated with played-back signals
Final acceptance 4 August 2011 or with naturally produced signals from live insects placed on plants. Each leaf was vibrated with signals
Available online 13 September 2011 of the host Euschistus heros Fabricius (Hemiptera: Pentatomidae), the alternative host Piezodorus guildinii
MS. number: A11-00360R (Westwood) or the nonhost Chinavia impicticornis (Stål) (played back). Parasitoid females showed
a selective response to the female songs of E. heros when these songs were tested against male songs or
Keywords: maleefemale duets. Telenomus podisi females also preferred E. heros female songs to female songs of the
foraging behaviour
other pentatomid bugs tested. Our results show that T. podisi females respond selectively to female songs
parasitoid eavesdropping
of their preferred host (E. heros); this behaviour may have relevant adaptive significance for the para-
Scelionidae
stink bug
sitoid, allowing it to forage in microhabitats with increased probability of finding host eggs. We discuss
Telenomus podisi the ecological significance of the use of vibratory signals and interactions with other (chemical) cues
vibratory communication during the host-searching behaviour of T. podisi.
Ó 2011 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Many phytophagous insects communicate by vibratory signals
transmitted through plants (Greenfield 2002; Cokl & Virant-Doberlet
2003). Vibratory signals carry diverse information, including species,

sex and location of partners (Cokl & Virant-Doberlet 2003). Vibratory
signals are also used by insects in social and mutualistic interactions
(Travassos & Pierce 2000; Cocroft 2001, 2003; Cocroft & Rodríguez
2005). In addition, vibratory cues produced by movement or
feeding of insects may be used by predators/parasitoids to locate
prey/host (Pfannenstiel et al. 1995; Meyhöfer et al. 1997; Wäckers
et al. 1998; Meyhöfer & Casas 1999; Broad & Quicke 2000;
Vilhelmsen et al. 2001). On the other hand, vibratory cues
produced by predators’/parasitoids’ locomotion may warn their prey
or hosts to avoid attack (Cocroft & Rodríguez 2005; Castellanos &
Barbosa 2006).
Insects that use vibratory communication are called ‘silent
singers’ because these signals can be detected by other insects only
* Correspondence: R. A. Laumann, Embrapa Recursos Genéticos e Biotecnologia,
Núcleo de Controle Biológico, Laboratório de Semioquímicos, PqEb W5 Norte
(Final), Caixa Postal 02372, CEP: 70770-917, Brasília, DF, Brazil.
E-mail address: laumann@cenargen.embrapa.br (R. A. Laumann).
 
1
A. Cokl is at the National Institute of Biology, Ve
cna pot 111, SI-1000, Ljubljana,
Slovenia.
after they have arrived on the plants or on other substrates where
the signals are being propagated. Silent singers have the selective
advantage of avoiding detection by predators that forage using
more conspicuous signals from their hosts such as sound propa-
gated by air, chemicals or light (Belwood & Morris 1987).
Cocroft & Rodríguez (2005) presented the hypothesis that,
considering the diversity of predators/parasitoids, the probability
of a successful exploitation of insect vibratory signals by a natural
enemy could be high. This hypothesis gained support after the
demonstration that the egg parasitoid Telenomus podisi Ashmead
(Hymenoptera: Scelionidae) is attracted by vibratory signals of the
Neotropical brown stink bug, Euschistus heros Fabricius (Hemiptera:
Pentatomidae) (Laumann et al. 2007). This in turn suggested that
specialized natural enemies (such as scelionid parasitoids in stink
bug eggs) can evolve mechanisms to use this signal while searching
for a host.
Stink bugs communicate with substrate-borne vibratory signals
during mating. Plant-restricted vibratory communication is part of
a multimodal communication that uses pheromones as long-range
signals (Borges et al. 1987; Aldrich 1995). Vibrational communica-

tion has been described for several species of stink bugs (Cokl &
Virant-Doberlet 2003; Gogala 2006; Cokl 2008), including the
neotropicals Chinavia impicticornis (Stål) (¼Acrosternum impicticone),

0003-3472/$38.00 Ó 2011 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.anbehav.2011.08.017
1176 R. A. Laumann et al. / Animal Behaviour 82 (2011) 1175e1183

E. heros, Piezodorus guildinii (Westwood) and Thyanta perditor (Fab-
ricius), and these signals are species- and sex-specific (Moraes et al.
2005a). In general, different vibratory signals have specific roles
during mating behaviour and may be classified as calling signals (to
attract mates), courtship signals (to stimulate pairs to copulate),
copulation signals (produced by males during copulation) or
rivalry signals (competition between males for females) (Cokl  &
Virant-Doberlet 2003).
The vibratory songs of different species and sexes of stink bugs
differ in their spectral (dominant frequency, bandwidth, frequency
modulation) and temporal (pulse duration, repetition time) char-
acteristics. In the present study, we conducted experiments with
naturally produced and played-back vibratory signals on plants to
test the response preferences of the parasitoid to signals from
different stink bug species and sexes. We tested two hypotheses:
(1) T. podisi can discriminate between signals from adults (males
and females) of E. heros, responding preferentially to females’
signals and (2) T. podisi can recognize and discriminate signals from
different species of stink bug, showing preference for signals from
the preferred host E. heros (Sujii et al. 2002).
METHODS
Insects
Euschistus heros nymphs and adults collected near the Embrapa
Genetic Resources and Biotechnology Laboratory in Brasilia, DF,
Brazil (15 470 S; 47 550 W) were reared on seed of sunflower, Heli-
anthus annuus (L.), soybean, Glycine max (L.) Merrill and raw
peanut, Arachis hypogaea (L.), and green beans pods, Phaseolus
vulgaris (L.). Nymphs and adults were reared in separate 8-litre
plastic containers (200 nymphs and 100 pairs/container). Stink
bug eggs were collected daily and separated in petri dishes for
hatching. The parasitoids were obtained from a laboratory colony
maintained on E. heros egg masses, initiated in our laboratory
2 years prior to the experiments, and started from parasitized stink
bug egg masses of different species collected in the same area of the
stink bugs. The T. podisi colony was maintained in an environmental
chamber in plastic cages (25 cm2 angled neck tissue culture flasks,
ICN Biomedicals, Irvine, CA, U.S.A.) and adult parasitoids were fed
with pure bee honey. Host (E. heros) eggs were exposed to female
parasitoids for 24 h and then removed and placed in glass tubes
(7.5  1.3 cm) for incubation. After emerging, adult parasitoids
were kept for 24e48 h in plastic cages for mating, and afterwards,
females were transferred to cages with host eggs. Environmental
rearing conditions for the insects were 14:10 h light:dark cycle,
26.0  1  C and 65  10% relative humidity.
Vibratory Signals
Naturally produced vibratory songs of E. heros, P. guildinii and
C. impicticornis were previously recorded and played back in our
experiments following methodologies described in Moraes et al.
(2005a) and Laumann et al. (2007). The choice of these stink bug
species’ signals was based on the host preference established by
Sujii et al. (2002). The authors showed that T. podisi preferentially
parasitize eggs of E. heros and can use P. guildinii as an alternative
host. However, they do not parasitize eggs of Chinavia asseada
(formerly Acrosternum asseadum) or eggs of the other two species
of this genus. It was thus possible to test signals of a preferred host,
of a nonpreferred host and of a nonhost.
We analysed vibratory signals using Sound Forge 4.5 (Sonic
Foundry, www.sonicfoundry.com) software. Terminology and
definitions of vibratory signals follow Cokl  & Virant-Doberlet
(2003). We identified (1) ‘pulses’ as unitary and homogeneous
parcels of sound waves of finite duration, (2) ‘pulse trains’ as
repeatable and temporally distinct groups of pulses and (3) ‘song’
as a sequence of pulses and/or pulse trains with a distinct beginning
and end. We characterized pulses/or pulse trains by the dominant
frequency value and the temporal characteristics using pulse/or
pulse train duration and repetition time (Table 1, Fig. 1).
Details of spectral and temporal characteristics of the selected
test songs and their behavioural context are described in Moraes
et al. (2005a). Songs were classified according to their order of
appearance in a duetting pair, thus: female songs 1 and 2 (FS-1 and
FS-2) and male songs 1, 2 and 3 (MS-1, MS-2 and MS-3). For the
experiments, we used the first female song (FS-1), the first male
song (MS-1) and the duet song (DS, composed of FS-1, FS-2, MS-1
and MS-2) of E. heros and the first female song of the other
selected species. FS-1 and MS-1 are characterized as calling songs
and FS-2 and MS-2 are normally produced during courtship
behaviour (Moraes et al. 2005a; Cokl 2008).
To test the hypotheses described above, we used the FS-1, MS-1
and DS of E. heros (hypothesis 1) in two sets of experiments
(naturally produced and played-back signal experiments) and we
used FS-1 of E. heros, P. guildinii and C. impicticornis (hypothesis 2)

Table 1
Temporal and spectral parameters of the songs used as stimuli in bioassays

Species Song Duration (ms) Repetition time (ms) Dominant frequency (Hz)
E. heros FS-1 P 1298272 (18) 30881017 (14) 1325 (18)
F4,13¼0.48, P¼0.75 F4,9¼0.36, P¼0.83 F4,13¼0.44, P¼0.78
FS-2 PT 4254930 (32) d 1459 (32)
F5,25¼1.18, P¼0.35 F5,25¼1.09, P¼0.395
MS-1 P 1502676 (13) 39643257 (10) 1720.8 (13)
F2,10¼1.05, P¼0.0.39 F2,8¼0.09, P¼0.92 F2,10¼0.52, P¼0.61
MS-2 PT 45501531 (21) d 1743 (21)
F4,16¼0.64, P¼0.29 F4,16¼0.64, P¼0.64
P. guildinii FS-1 P 5007179 (12) d 1291 (12)
F4,11¼1.09, P¼0.41 F4,11¼1.36, P¼0.31
C. impicticornis FS-1 PT 838125 (19) 2385186 (18) d
F4,14¼0.48, P¼0.74 F4,14¼1.81, P¼0.18
SP 17054 (20) d 927 (20)
F4,15¼0.50, P¼0.74 F4,15¼0.19, P¼0.94
LP 61095 (20) d 1157 (20)
F4,15¼1.76, P¼0.19 F4,15¼0.21, P¼0.93

Values are means  SD. All parameters were estimated from records of five individuals of each sex/species; numbers of pulses used for the parameter estimation are given in
parentheses. FS: female song; MS: male song; P: pulse; SP: short pulse; LP: long pulse; PT: pulse train. Values not determined are from long pulses with irregular repetition
time. Variations of temporal and spectral characteristics of each song from different individuals were compared using ANOVA. All parameters measured were within the
ranges determined by Moraes et al. (2005a).
 R. A. Laumann et al. / Animal Behaviour 82 (2011) 1175e1183
MP
LP
Figure 1. Typical oscillograms of Euschistus heros, Piezodorus guildinii and Chinavia impicticornis vibratory signals used in the bioassays. FS-1: female calling song; MS-1: male calling
song; DS: duet song (pulses of FS-1, FS-2, MS-1, MS-2); MP: male pulse; FP: female pulse; FMP: female and male pulses superimposed; LP: long pulse; SP: short pulse.
in another set. All records and bioassays were conducted at the
Embrapa Genetic Resources and Biotechnology Laboratory in
Brasilia, DF, Brazil, in a soundproof room with artificial illumination
(4 fluorescent lamps 40 W) at 26  1  C and a relative humidity of
65  10%, between 0800 and 1700 hours. For experiments with live
insects, we used songs from 10 different individuals for each song
type, and for experiments with played-back signals, we used five
recordings of each song from different individuals.
Bioassays Design and Parasitoid General Pattern of Searching
Behaviour
Bioassays were performed using bean plants (Phaseolus vulgaris
L.) that were 20e30 cm high with two completely expanded
opposite leaves. The plants were divided into three areas: left
treatment area (vibrated left leaf þ petiole), right treatment area
(vibrated right leaf þ petiole) and stem (area below the petiole)
(Fig. 2).
To test the influence of vibrations (naturally produced or played
back), in each bioassay, we released a naïve T. podisi female,
24e48 h old, onto the stem just above the hypocotyls (w5 cm from
soil) and observed her behaviour for 10 min. We recorded the initial
choice (the first treated area where the insect entered and
remained for more than 10 s) and the residence time (time that an
insect spent in each area of plant, expressed as the percentage of
total bioassay time). Insects that did not move from the release area
or that did not choose the treatment or control areas after 5 min
were considered unresponsive and were excluded from the
analyses.
To test the general patterns of searching behaviour of the
parasitoid on plants and the existence of any bias in the
1177
Euschistus heros FS-1
1s
Euschistus heros MS-1
1s
FP FMP
Euschistus heros DS
1s
Piezodorus guildinii FS-1
1s
SP
Chinavia impicticornis FS-1
1s
experimental design, we performed bioassays with no signals on
either leaf (N ¼ 40).
Bioassays to Test Preference for Naturally Produced E. heros signals
To study the response of T. podisi to E. heros signals in a natural
context, we performed bioassays with E. heros signals produced
naturally on the same plant. To do this, we placed sexually mature
adults of E. heros from the laboratory colony (10e15 days after the
final moult) on the leaf of a bean plant with the characteristics
described above.
The emission of vibratory signals was monitored with
a device described in Laumann et al. (2007) (Fig. 2). One end of
a fine steel-carbon wire (5 cm  0.5 mm diameter) was intro-
duced into the stem of the plant, just below the point where the
parasitoids were released, and the other end was attached with
an adhesive paper strip to a nonresonant 10 cm diameter low-
emidrange loudspeaker (40e6000 Hz frequency response,
impedance 8 U, RadioShack, Taiwan). Vibrations produced by
insects were amplified by the home-made operational amplifier
TL081CN, (www.mouser.com), digitized (Aardvark-Direct Pro
24/96, Aardvark Computer Systems, WA, U.S.A.) and monitored in
real time by headphones and oscillogram plots created by the
software CoolEdit Pro (Syntrillium Software 2001, Fort Wayne,
IN, U.S.A.). After transmission on plants, vibratory signals show
spectral distortions from the naturally produced signals (Cokl 
2008), making the device useful only for monitoring the
signals, not for recording and analysing them. However, the
temporal parameters and characteristic oscillograms, as well as
the behaviour of the insects, permit identification of the signaller
and the signaller’s song type.
1178 R. A. Laumann et al. / Animal Behaviour 82 (2011) 1175e1183
Left treatment area
Petiole
Insect
decision
area
Stem
Insect
release
point
Figure 2. General design for bioassays using vibratory cues from live insects and from playback. For bioassays with live insects, only the arrangement of plants was used.
To test the influence of FS-1 or MS-1 on the parasitoid’s
behaviour, we placed a female or a male of E. heros on one of the
plant leaves. After being placed on the adaxial side of a leaf, female
E. heros spontaneously produced FS-1. A male placed on the plant in
the same position was stimulated to produce MS-1 using playback
of prerecorded FS-1 (for playback methodology see below). With
these procedures it was possible to test the behaviour of T. podisi in
the absence of other signals because the opposite leaf on each plant
was maintained as a control (not directly vibrated).
To test the preference of T. podisi females for FS-1 or MS-1 when
these signals were vibrated simultaneously on a plant, we placed
a female and a male E. heros on the same plant (opposite leaves) and
performed bioassays only when the insects were singing an FS-1
and MS-1 duet. In some pairs, and after some minutes of signal
production, males moved along the plant towards the females, as
described by Cokl et al. (1999), and when this happened the
bioassays were interrupted and started again using a new pair of
E. heros on the plant.
To test the influence of courtship songs on parasitoid behaviour,
we placed a female and a male on the same leaf of the plant and
performed the bioassays when the insects displayed courtship
behaviour (Borges et al. 1987) and produced duet songs (DS)
(Moraes et al. 2005a; Laumann et al. 2007). After courtship
behaviour, most of the pairs mated and interrupted the signal
production; in these situations the bioassays were stopped and
reinitiated with a new pair of E. heros.
Finally, to test whether the presence of insects on plants could
interfere with the parasitoid’s behaviour, we performed bioassays
following the same procedures and treatment combinations
described above except that we used silent E. heros males and
females.
For each combination of treatments, we performed 25 bioassays
following the methodologies described above for Bioassays Design
and Parasitoid General Pattern of Searching Behaviour.
To avoid the influence of E. heros adults and the positions of the
vibrated and nonvibrated leaves (in bioassays with a single insect)
or the positions of the insects (in bioassays with two insects), we
changed the position of the insects on the plant every three to five
bioassays and we changed bean plants every 5e10 bioassays. Stink
Right treatment area
Amplifier
Computer for signal
reproduction
bugs were changed every one or two bioassays because live insects
singing alone ceased calling after 10e20 min, and pairs attempted
to copulate or move towards each other on a plant. The same
insects were used in another bioassays after at least a 2 h delay, and
to avoid pseudoreplication, the same pair was not used again (i.e.
female 1 was paired with different males, and the same procedures
were followed with the other females and males).
Played-back Signal Bioassays
General procedures
We performed these bioassays to test the response of the
parasitoid to vibratory signals of stink bugs in the absence of other
stimuli (chemical, visual, vibration from insect movements) that
might be present when insects were on plants. All bioassays were
conducted following the methodology described in Laumann et al.
(2007). The parasitoids were stimulated using different (sex or
species) stink bug vibratory signals applied to bean plants (Fig. 2).
The range of temporal and spectral characteristics of signals
used in the playback experiments did not differ significantly from
the natural range for each species (Table 1), which allowed us to
perform bioassays with a homogeneous set of vibratory signals
within the range of each species, as determined by Moraes et al.
(2005a).
The vibration signals were transmitted to the leaf through
a plastic cone (automatic pipette tip, 50 mm high  5.5 mm base)
whose opposite end was glued with instant adhesive to the middle
of a loudspeaker membrane (4 inch (10.2 cm), 40e6000 Hz
frequency response, impedance 8 U, FE103, RadioShack). The
plastic cone was placed in contact with the treatment leaf by
touching its tip to the leaf (Fig. 2). This general arrangement proved
to be efficient in reproducing the stink bugs’ vibratory signals
(Laumann et al. 2007). The intensity of stimulation was adjusted to
the level of stink bugs’ signal production, using a home-made
operational amplifier (TL081CN, www.mouser.com). The signals
were played continuously throughout the 10 min bioassay. Proce-
dures for releasing and monitoring the behaviour of the parasitoids
were the same as those described above for Bioassays Design and
Parasitoid General Pattern of Searching Behaviour.
 R. A. Laumann et al. / Animal Behaviour 82 (2011) 1175e1183 1179

Bioassays to Test Preference for Intraspecific Played-back Signals Bioassays to Test Preference for Naturally Produced Signals of
E. heros
We conducted these bioassays to test whether T. podisi can
recognize and discriminate between artificially induced male, female In the set of experiments with stink bugs vibrating on plants, the
and duet songs of E. heros. Using the general procedures described parasitoid’s initial choice was clearly influenced by female songs. In
above, we performed bioassays with contrasting pairs of FS-1, MS-1 all bioassays where females were singing (FS-1 or FS-2), the para-
and DS. The signals were played back and transmitted to the dried sitoid showed a preference for plant areas where females were
bean leaves, one signal from the contrasting pair on each leaf, singing (Fig. 3). The presence of males did not interfere with
throughout the bioassay time (10 min for each replicate). We changed parasitoid response, evidenced by the fact that in bioassays with
the position (right or left side) of each stimulus (song) on the plants calling songs (FS-1 and MS-1) or courtship songs (DS), T. podisi
every three replicates to avoid positional bias, and we changed the females preferred areas of the plant that vibrated with female
combination of treatments every six to nine bioassays. The signals of signals (Fig. 3). In bioassays with silent E. heros females on plants,
different insects were randomly combined (i.e. FS-1 of female 1 was T. podisi showed no preference for leaves occupied by females, but
tested with MS-1 of all males, and the same was done for the other the difference from control leaves was marginally nonsignificant
signals), and each combination was used in one or two bioassays. We (Wald test: c21 ¼ 3.62, P ¼ 0.057; Fig. 3).
performed 30e40 replicates for each combination of songs. Female T. podisi spent more time searching on leaves of bean
plants vibrated with FS-1 (GLM: z ¼ 2.45, P ¼ 0.01) or DS (z ¼ 4.17,
Bioassays to Test Preference for Interspecific Played-back Signals P < 0.001) than they did on control leaves (opposite, nondirectly
vibrated leaves; Fig. 3). When females and males were singing on
We performed these bioassays to evaluate whether T. podisi can different leaves (both producing song 1), the residence time on
discriminate between songs of different stink bug species and
whether they show a preference for the songs of their preferred
host, E. heros. Following the same procedure as described above, we
(a)
performed the bioassays using contrasting female songs of E. heros,
P. guildinii and C. impicticornis (Table 1). We conducted 50e55 F+MNS
NV 25 (4)
replicates of each combination of songs using T. podisi females in
the same physiological conditions as described above and NV 25 (16) *** F+MS
recording the same variables. We also used the same procedures FNS
MNS 25 (6)
described above to avoid positional bias and to apply treatments.
MS 25 (14) * FS
Statistical Analyses
NV 25 (12) MNS
We analysed the choices made by the parasitoids in the bioas- NV 25 (13) MS
says using logistic regression, and determined the parasitoid’s
probability of choosing one of the signals tested. The fitted model NV 25 (9) FNS
contained a factor for the side (left or right) on which the songs
NV 25 (10) * FS
were presented to control for this variable. We tested the hypoth-
esis of no preference (50% first choice to each vibratory signal) 1 0.8 0.6 0.4 0.2 0 0.2 0.4 0.6 0.8 1
using a chi-square Wald test. The proportion of the total bioassay Initial choice (proportion of response)
time spent in each vibrated area (residence time) was analysed by (b)
generalized linear models (GLM) with binomial distribution of NV F+MNS
errors and logit link function, using maximum likelihood estima-
NV F+MS
tion. All tests were conducted using the R programming language ***
(R Development Core Team 2008). MNS FNS
MS
RESULTS FS
NV MNS
Bioassays Design and Parasitoid General Pattern of Searching
Behaviour NV MS

In the absence of stimulus (nonsignal experiments), the NV FNS

**
behaviour of the parasitoid was similar to that described by
NV FS
Laumann et al. (2007), and thus, there was no evidence that the *
experimental design influenced the parasitoid’s movements. Tele- 50 40 30 20 10 0 10 20 30 40 50
nomus podisi females showed no preference for different areas of Residence time (%)
the plant: 19 females chose the left side and 21 females chose the
right side of the plant (c21 ¼ 0.1, P ¼ 0.75). In addition, the parasitoid Figure 3. (a) Initial choice (mean þ 95% confidence interval) and (b) residence time
(mean þ SE) of T. podisi females when stimulated with different combinations of
females showed no significant difference in residence time in
E. heros vibratory signals produced by live insects placed on bean plants. NV: non-
different areas (left ¼ 24.27  5.46% of total bioassay time; vibrated leaf; MNS: male alone on a plant and not singing; F þ MNS: female and male
right ¼ 25.82  5.58% of total bioassay time; GLM: z ¼ 0.16, on a plant (same leaf) and not singing; F þ MS: female and male on a plant (same leaf)
P ¼ 0.87). Additionally, the percentages of time spent moving and singing; FNS: female alone on a plant and not singing; FS: female alone on a plant
(46.11  3.96%, N ¼ 40) and of showing typical search behaviour and singing (producing FS-1); MS: male alone on a plant and singing (producing
MS-1). In (a), numbers beside bars indicate the total repetitions used for statistical
with substrate antennation (Colazza et al. 1999; Borges et al. 2003) analyses of each combination; numbers in parentheses indicate the number of insects
were similar to the mean values estimated for data of all bioassays evaluated that did not respond to treatment (did not make a choice after 5 min).
with different stimuli (50.30  3.29%, N ¼ 233). *P < 0.05; **P < 0.01; ***P < 0.001.
1180 R. A. Laumann et al. / Animal Behaviour 82 (2011) 1175e1183

leaves vibrated with singing females was higher but not statistically (a)
significant (GLM: z ¼ 1.26, P ¼ 0.21; Fig. 3). Similarly to that
Eh
observed for the initial choice, the residence time on leaves with
nonsinging females was higher than on leaves without vibratory Pg
47 (8)
signals (GLM: z ¼ 2.69, P ¼ 0.007; Fig. 3). Ci
The percentage of parasitoids that did not respond to treatments
(i.e. that did not move during the first 5 min or that left the plant
without making a choice) was higher in bioassays with signals from
48 (5)
live stink bugs (42%) than in bioassays with played-back signals
(16%) (Figs 3, 4, 5). Parasitoids also spent less time exploring plants
vibrated with naturally produced stink bug signals than they did
plants vibrated with artificially induced played-back signals (total
residence time on plants: 36.41  8.22% and 76.66  13.66% of total 47 (8)
bioassay time (600 s) for bioassays with stink bug or played-back
signals, respectively).
Parasitoid females showed two different behaviours after they 1 0.8 0.6 0.4 0.2 0 0.2 0.4 0.6 0.8 1
reached the leaves with live insects. In most of the observations Initial choice (proportion of response)
(74.41% of the females that made a choice), the parasitoids walked (b)
on the abaxial surface of the leaves just below the female or male
stink bug(s), and after a few seconds, some of the females stopped
and remained at rest. After a brief period (10e30 s), they either
∗∗

(a)

FS-1 ∗
31 (5) MS-1
DS

∗∗∗

30 (7)
100 80 60 40 20 0 20 40 60 80 100
Residence time (%)

Figure 5. (a) Initial choice (mean þ 95% confidence interval) and (b) residence time
28 (5) (mean þ SE) of T. podisi females when stimulated with different combinations of stink
∗
∗∗ bug vibratory signals on bean plants. Eh: Euschistus heros FS-1; Pg: Piezodorus guildinii
FS-1; Ci: Chinavia impicticornis FS-1. In (a), numbers beside bars indicate the total
repetitions used for statistical analyses of each combination; numbers in parentheses
1 0.8 0.6 0.4 0.2 0 0.2 0.4 0.6 0.8 indicate the number of insects evaluated that did not respond to treatment (did not
Initial choice (proportion of response) make a choice after 5 min). *P < 0.05; **P < 0.01; ***P < 0.001.

(b)
proceeded to search actively, moving to the adaxial side of the leaf,
or they flew away. When the parasitoid females went to the upper
side of leaves (25.25% of females that made a choice and most of
females that initially chose the abaxial surface) with the stink bugs,
they walked around the insects, then stopped and stayed near
them. In three cases, E. heros females made physical contact with
the parasitoids and then showed defensive behaviour, kicking the
parasitoid females with their hindlegs. If insects stopped singing for
a few seconds, T. podisi females also stopped moving and only
resumed movement when the stink bugs start to produce vibratory
signals again.

∗∗∗ Bioassays to Test Preference for Intraspecific Played-back Signals

100 80 60 40 20 0 20 40 60 80 100 Telenomus podisi females showed a clear preference for E. heros
FS-1 over E. heros MS-1. The initial choice for the plant area with
Residence time (%)
female songs was significantly higher than that for the area
Figure 4. (a) Initial choice (mean þ 95% confidence interval) and (b) residence time vibrated with E. heros male songs (c21 ¼ 5.14, P ¼ 0.02; Fig. 4). In
(mean þ SE) of T. podisi females when stimulated with different combinations of a similar way, parasitoid females spent more time in the female-
E. heros vibratory signals on bean plants. FS-1: female calling song; MS-1: male calling vibrated area (residence time comparison, GLM: z ¼ 3.76,
song; DS: duet song. In (a), numbers beside bars indicate the total repetitions used for
statistical analyses of each combination; numbers in parentheses indicate the number
P < 0.001; Fig. 4). Parasitoid females showed no significant
of insects evaluated that did not respond to treatment (did not make a choice after response to other treatment combinations (female song versus
5 min). ***P < 0.001. duet song, male song versus duet song; Fig. 4).
 R. A. Laumann et al. / Animal Behaviour 82 (2011) 1175e1183
Bioassays to Test Preference for Interspecific Played-back Signals
When female songs of different stink bugs species were con-
trasted, T. podisi showed no significant difference in its initial choice
(Fig. 5). In contrast, the residence time of T. podisi was higher in the
plant area vibrated with E. heros FS-1 than in the plant area vibrated
with C. impicticornis FS-1 (GLM: z ¼ 3.28, P < 0.001) or P. guildinii
FS-1 (z ¼ 2.23, P ¼ 0.03; Fig. 5). When we compared residence
times in areas of the plant vibrated with C. impicticornis and
P. guildinii female songs, the parasitoid spent more time in areas of
the plant vibrated with C. impicticornis song (GLM: z ¼ 2.73,
P ¼ 0.006; Fig. 5).
DISCUSSION
Our results show that T. podisi females respond selectively to
female songs of their preferred host E. heros. Bean plant leaves that
were vibrated using naturally or artificially induced female songs of
E. heros were significantly more likely to attract and retain T. podisi
than were nonvibrated leaves or than those vibrated with E. heros
male songs.
These findings suggest that taxic (attraction) and kinetic
(retention) components of the searching behaviour of T. podisi
females are triggered (influenced) by vibratory signals of E. heros
females. Simultaneously presented E. heros male songs or female
calling songs of P. guildinii or C. impicticornis did not interfere with
the parasitoid’s preferred orientation response to the E. heros
female song source. The only exception was the experiment with
played-back E. heros DS against MS-1, in which male song was
vibrated on both sides of the experimental plants, suggesting that
this might have interfered with the parasitoid’s response.
Our results are in agreement with the previous observation that
T. podisi females show directional movement towards E. heros FS-1
(Laumann et al. 2007). In that work, bioassays were performed
without contrasting female and male songs, so the results
Herbivore-induced synomones
(1,2,3)
Telenomus podisi
female searching
for a host
Host allomones or sex
pheromones (4,5,6)
Long range
(habitat location)
Figure 6. Theoretical model for the principal behavioural steps and cues, including stink bug vibratory signals, used by Telenomus podisi when searching for hosts (eggs of Pen-
tatomidae). Squares indicate cues that stimulate directional movements (taxic cues) to the parasitoid. Circles indicate cues that stimulate kinetic movements or increase resting
behaviour. Numbers indicate references for each behavioural step and the stimuli associated with each step: 1: Moraes et al. (2005b); 2: Moraes et al. (2008); 3: Michereff et al.
(2011); 4: Borges et al. (1999); 5: Silva et al. (2006); 6: Laumann et al. (2009); 7: Borges et al. (2003); 8: Conti et al. (2010).
1181
presented here clearly show that T. podisi respond selectively to
female songs of E. heros.
Several species of scelionid wasps search for pentatomid eggs;
although they are oligophagous or polyphagous, they show a pref-
erence for certain species (Orr 1988). Our results suggest that the
preferential use of E. heros female songs by T. podisi could be
directly related to the parasitoid’s preference for this stink bug
species, which has also been observed in the laboratory (Sujii et al.
2002) and in the field (Corrêa-Ferreira & Moscardi 1995; Medeiros
et al. 1997, 1998; Pacheco & Corrêa-Ferreira 2000).
In scelionid wasps, the process of host location is also influenced
by semiochemicals from hosts or plants (Aldrich 1985, 1995;
Mattiacci et al. 1993; Borges & Aldrich 1994; Borges et al. 1998,
1999, 2003; Bruni et al. 2000; Colazza et al. 2004; Moraes et al.
2005b, 2008; Silva et al. 2006). The use of semiochemicals (for
example, sex pheromones, allomones or cairomones from foot-
prints) shows a specificity related to the time of hosteparasitoid
associations and to the gender or physiological stage of the
preferred host species (Conti et al. 2004; Salerno et al. 2006;
Colazza et al. 2007; Laumann et al. 2009). Our results are also
consistent with some patterns of semiochemical use by scelionid
wasps and could indicate a similar behavioural response mecha-
nism to different cues.
Telenomus podisi females tested in our experiments were reared
on the same host and had no previous contact with vibratory
signals of stink bugs, so the responses observed appear to have an
innate component. Therefore, T. podisi’s innate response to vibra-
tory signals and its specificity for songs of preferred hosts is
consistent with the predictions of infochemical use in relation to
dietary specialization in carnivorous arthropods (Steidle & van Loon
2003), suggesting a similar selection mechanism for responses to
specific semiochemicals and vibratory signals.
Telenomus podisi females found the leaves with silent E. heros
females by chance, but they remained on these leaves. This finding
supports the hypothesis that searching behaviour on a plant may be
Stink bugs vibratory
signals Host footprints (7)
Visual cues ? Host
Short-range
herbivore-induced
Random search
synomones ? (8)
1st step 2nd step
On a plant
(host location)
1182 R. A. Laumann et al. / Animal Behaviour 82 (2011) 1175e1183
mediated multimodally. Vibratory signals stimulate directional
movements of the parasitoid, and once the parasitoid reaches the
vibration source on the leaf, it shows arrestment behaviour typical
of scelionid wasps in response to the host’s footprint on the leaf
surface (Colazza et al. 1999; Borges et al. 2003; Conti et al. 2004;
Peri et al. 2006) or in response to induced short-range syno-
mones (Conti et al. 2010). Vibrations resulting from the host’s
movement on the plant could also provide another cue that influ-
ences the parasitoid’s behaviour.
Parasitoids pass through sequential steps from habitat detection
to host selection, and the use of multimodal cues could be inter-
preted as the use of the more reliable and/or detectable signal in
each step (Vinson 1998; Steidle & van Loon 2003). Considering this,
we propose a putative model for the interaction of different cues
used by T. podisi during host-searching behaviour and their
ecological significance (Fig. 6). First, T. podisi moves directionally to
habitat occupied by their host, using plant semiochemicals or host
pheromones or allomones. When it is on the plant, the parasitoid
probably passes through two different steps of searching behaviour.
The initial searching behaviour on a plant could be random or may
show vibrational directionality mediated by the stink bug’s vibra-
tory signals. Then the second phase of the search on plants could
involve T. podisi using the host’s footprint or short-range herbivore-
induced synomones to find the places where it is most likely to find
eggs. At very close range the parasitoid could use vision to make
physical contact with the egg masses.
Searching behaviour based on the use of indirect information
(i.e. information not directly originated from the host: eggs) needs
to be related to higher probabilities of finding egg masses. This
might be feasible if adults feed and mate in the field in the same
place that they lay their eggs. This hypothesis needs to be tested
with field observations of stink bug behaviour, but the pattern of
aggregate distribution of nymphs and adults of stink bugs in the
field (Higuchi 1992; Roggia 2009; Tillman et al. 2009) lends support
to these considerations.
The species’ selectivity and the mechanisms underlying vibra-
tional directionality of parasitoids mediated by stink bug host
vibratory signals are not yet clear. Stink bugs’ vibratory signals are
characterized by narrow low-frequency peaks (70e150 Hz)

(McBrien et al. 2002; Cokl et al. 2005; Moraes et al. 2005a) that are
tuned to the resonant properties of herbaceous plants and are
transmitted with little attenuation through the plant (Cokl  2008).
Signal species’ specificity of pentatomine vibratory emissions lies in
their temporal characteristics (Cokl  2008), which may change
during transmission through green plants to the extent that they
influence song recognition (Miklas et al. 2001). In our study, we
used naturally and artificially induced stink bug vibratory signals of
similar frequency but different time characteristics. The hypothesis
that parasitoids discriminate between signals on the basis of signal
duration and/or repetition time needs further experimental
confirmation.
Other parameters of vibratory signals, as duty cycles and
intensity, could influence the parasitoid recognition and respon-
siveness towards specific vibratory signals. In our experimental
conditions, parasitoids showed stronger responses (higher proba-
bility of response) to playback of FS-1 signals than to naturally
produced signals. This differential response may have been influ-
enced by different duty cycles caused by continuous reproduction
of the played-back signal, and production of signals with irregular
patterns of repetition time by live females on the plant. The infor-
mational value of stink bug song parameters that mediate T. podisi
response need to be investigated in a specific study oriented to
evaluate responses to artificially synthesized signals of various
temporal, spectral and amplitude characteristics in artificial and
natural conditions. In the latter case, the transmission properties of
the substrate (plants) and the mechanism involved in the parasit-
oid’s reception and processing of the information need to be
considered.
The tendency of parasitoids to move preferentially to female
song is not surprising because female stink bugs usually call from

the same place for up to 20e30 min (Cokl & Virant-Doberlet 2003),
and their songs are produced autonomously and with steady time
characteristics. As such, the vibrational directionality of the female
is optimally mediated on a plant, as shown in Nezara viridula
and other stink bug species (Ota & Cokl  
1991; Cokl et al. 1999;

Virant-Doberlet et al. 2006; Cokl 2008).
Our results show that, when eavesdropping on stink bugs’
vibratory communication, the parasitoid T. podisi responds selec-
tively to the E. heros female’s song. This behaviour may have rele-
vant adaptive significance for the parasitoid because it may allow
the parasitoid to forage in microhabitats with increased probability
of finding the host eggs. For a more comprehensive understanding
of this phenomenon, some aspects of the mechanisms of T. podisi’s
response to vibratory signals, their evolution and ecological
significance need to be studied.
Acknowledgments
We thank Hélio Moreira dos Santos and Diva Tiburcio for
helping with the fieldwork and laboratory rearing of the insects
used in this study. We also thank Dr Mark Horn, an International
Consultant at Embrapa, for the English revision of the manuscript.
Two anonymous referees made helpful comments on an earlier
version of the manuscript. This investigation was supported by
Embrapa, the Brazilian Council for Scientific and Technological
Development (CNPq) (476619/2010-6 research project and Bilateral
Cooperation Project CNPq (Brazil)-MHEST (Slovenia)), Distrito
Federal Research Foundation (FAP-DF) and by a CNPq-PIBIC grant to
Ana Paula Silva Lopes.
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