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Ambient temperature and sound power of

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Tibicina)

Article in Physiological Entomology · December 2003

DOI: 10.1111/j.1365-3032.2003.00345.x

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Physiological Entomology (2003) 28, 340–343

SHORT COMMUNICATION

Ambient temperature and sound power of cicada

calling songs (Hemiptera: Cicadidae: Tibicina)
J É R Ô M E S U E U R and A L L E N F . S A N B O R N *
École Pratique des Hautes Études, Biologie et Évolution des Insectes, Muséum National d’Histoire Naturelle, Paris, France
and *School of Natural and Health Sciences, Barry University, Miami Shores, FL, U.S.A.

Abstract. Male cicadas produce a loud calling song that attracts females at long
range. In some cases, ambient temperature has been shown to have an effect on
the temporal structure of this acoustic signal. Here, a positive correlation is
reported for the first time between the ambient temperature and the sound
power of the calling song. This relationship is illustrated in three species of the
Palaearctic genus Tibicina: Tibicina corsica fairmairei Boulard, Tibicina garricola
Boulard and Tibicina tomentosa Olivier. It is suggested that the males thermo-
regulate behaviourally. The minimal ambient temperature range that the Tibicina
species need to call is 22–24
C. The effect of ambient temperature on calling song
power is assumed to be the result of thermal effects in the response of the acoustic
system (i.e. muscle activity of the acoustic system being temperature-dependent).
Inter-individual and interspecific differences in calling song power are interpreted
in the general context of the Tibicina sound behaviour.
Key words. Acoustic communication, cicada, France, sound power, sound pres-
sure level, thermoregulation.

Introduction studies specifically dealing with sound pressure levels in

During the adult part of their life, the main activity of male
cicada consists of producing an acoustic sexual signal. This
calling song constitutes the first step of pair formation,
attracting females at long distance (Alexander et al., 1997).
The signal is produced by the repetitive buckling of a pair of
abdominal timbals (Pringle, 1954). The sound can be modi-
fied by different parts of the body such as the abdomen
(Bennet-Clark & Young, 1992). The initial sound source,
buckling of the timbal, is due to the action of large abdom-
inal muscles that insert on the dorsal plate of the timbals. A
smaller muscle, the tensor muscle, can also regulate the
tension of the timbal and modify the signal structure.
Although the temporal and frequency characteristics of
the calling song of nearly 300 species have already been
described (Sueur, 2001, 2003), there are only two previous
Correspondence: Dr Jérôme Sueur, École Pratique des Hautes
Études, Biologie et Évolution des Insectes, Muséum National
d’Histoire Naturelle, 45 rue Buffon, F-75005 Paris, France. Tel:
þ33 1 40 79 37 04; fax: þ33 1 40 79 36 99; e-mail: sueur@mnhn.fr
cicadas: one in South African species (Villet, 1987) and
one in North American species (Sanborn & Phillips, 1995).
Except for the detailed laboratory study on the sound
radiation of Tympanistalna gastrica by Michelsen &
Fonseca (2000), no measurements of sound pressure level
have been reported for Mediterranean species. In particular,
the sound pressure level of the seven Tibicina species occur-
ring in France has never been analysed. This lack of sound
pressure data is probably due to the difficulty of observing
cicadas in the field and of approaching them sufficiently
close to record the intensity of their calling song. This is
especially true in the case of Tibicina males, which are often
observed calling in the canopy.
Cicada activity is dependent on the daily fluctuations in
ambient temperature (ta) (Sanborn, 2002). In particular, ta
can modify timbal muscle tension and thus modify timbal
activity. Previous studies of sound pressure level in cicadas
have focused on the absolute values of the calls in each
species but did not relate sound pressure level to ta (Villet,
1987; Sanborn & Phillips, 1995). We present the first illus-
tration of a possible correlation between sound pressure
level and ta in three Tibicina species recorded in France.

340 # 2003 The Royal Entomological Society


Materials and methods
Three Tibicina taxa were investigated in France from the 23
June 2000 to 18 July 2000, and from 6 to 14 July 2001.
Tibicina corsica fairmairei Boulard and Tibicina tomentosa
Olivier were studied in the same site in the Département of
Hérault. The habitat was an open grassland where the main
plant species were Bituminaria bituminosa, Foeniculum
vulgare and Thymus vulgaris. The third species, Tibicina
garricola Boulard, was studied in Domazan (Département
of Gard). The site corresponded to a closed high shrubland,
where the dominant plant species was Quercus coccifera.
Males of the Tibicina species can produce four main
categories of acoustic signals. The calling song attracts
conspecific males and females at long range, whereas the
courtship song attracts females at short-range. Males raise
their abdomen and lift up their wings above their abdomen
throughout the calling song sequence and this behaviour is
exhibited only during a part of the courtship song. The
rivalry song is produced when two males compete for a
calling perch, and the distress song is produced when
males are seized by a predator. The intensity measurements
presented here were made during calling song production.
The differences between acoustic behaviours and signal
structures were so obvious that there could be no confusion
between the four types of signals.
Sound pressure level was measured (in dB) with a Bruël
and Kjaer Sound Level Meter Type 2203, equipped with a
microphone Type 4145, a microphone extension rod Type
UA 0196 and a wind screen Type UA 0207 (Bruël & Kjaer,
Nærum, Denmark). The microphone was calibrated with a
Bruël and Kjaer portable sound pressure calibrator Type
4230. Measurements were made on a unweighted scale and
with a slow setting that averaged the sound pressure level
over a period of approximately 0.5 s. Calling songs pro-
duced by Tibicina species are continuous and emitted at a
regular pulse rate (Sueur & Aubin, 2003). Quiet periods
between groups of pulses or changes in pulse rate were
not considered to have significant effects on mean values.
Measurement procedures follow those previously reported
by Villet (1987) and Sanborn & Phillips (1995). Briefly, it
consisted of placing the microphone medially and dorsally
to the insect at a constant distance of 0.5 m. Measurements
were therefore always made in the far field and in the same
orientation to the animal, avoiding near field complex
pressure affects (Michelsen & Fonseca, 2000). In addition,
morphological and mechanical symmetries between left and
right timbals in Tibicina suggest minor asymmetries in
sound radiation (Sueur & Aubin, 2003). There were no
obstacles between the calling male and the microphone.
Tibicina calling songs are continuous (duration > 7 s), and
comprise a regular succession of groups of pulses. Measure-
ments were therefore made approximately in the middle of
the signal. If a cicada was disturbed by placement of the
instrumentation, a reading was made only after the normal
calling pattern had been re-established by the insect.
Measurements were obtained at different times of the day.
There was no wind and the level of background noise was
# 2003 The Royal Entomological Society, Physiological Entomology, 28, 340–343
Ambient temperature and sound power of cicada song 341
at least 15 dB below that of the calling songs. For each
measurement, ta was recorded in the shade with a digital
thermometer ( 1
C), 1 m above the ground.
Because sound pressure level is measured on a logarithmic
scale, measurements in decibels were converted to power
levels (W). This conversion followed the equation:
Q ¼ 4
r2I0  10SPL/10, where Q ¼ sound power (W),
r ¼ distance from source (0.5 m), I0 ¼ reference intensity
(1012 W/m2) and SPL ¼ sound pressure level (dB). The
mean power output was then used to calculate mean
sound pressure level at 0.5 m for each species.
The correlation between ta and sound power was tested
with Spearman’s nonparametric rank correlation to avoid
any hypothesis related to linearity. In addition, sound
powers were compared between each species with the non-
parametric Kolmogorov–Smirnov test. Statistical defin-
itions follow those previously described by Scherrer (1984).
Results and discussion
The sound power of the three Tibicina calling songs studied
here showed a positive correlation with the ta (Fig. 1). The
Spearman rank test showed that this correlation was statistic-
ally significant for each Tibicina taxon (Table 1). Previous
studies on the effect of ta on call parameters have given
contradictory results in cicadas. The call temporal para-
meters of some species exhibit a relationship with ta whereas
the temporal parameters of other species are independent of
ta (Popov, 1975; Gogala et al., 1996; Popov et al., 1997;
Quartau et al., 2000; Sanborn & Maté, 2000; Fonseca &
Revez, 2002). To our knowledge, this is the first report of a
possible influence of ta on cicada calling song intensity.
Body temperature (tb) has been shown to regulate acous-
tic behaviour in cicadas. tb has been shown to affect when
the cicadas are able to call, as well as altering the activity of
the sound production system (Sanborn, 2002). The changes
in sound power with changes in ta observed here are prob-
ably the result of thermal affects in the response of the
acoustic system. Song intensity was shown to correlate
with tb in the endothermic cicada Lyristes winnemanna
(Sanborn, 1997, 2000). It was also shown that timbal muscle
temperature increased during the changes in acoustic
activity in L. winnemanna until the full song was produced,
and that timbal muscle tension increased with increasing
muscle temperature (Sanborn, 2001). It is likely that a
similar phenomenon occurs in the Tibicina species studied
here.
The three Tibicina species studied produced minimal
sound power at ta 22–24
C. At this ta range, males were
observed basking, turning their backs to the sun. The spe-
cies stopped calling each time any clouds appeared or when
wind velocities increased. By contrast, males were observed
to orientate their ventral surface perpendicular to the sun at
elevated ta; such behaviour would decrease the radiant heat
load. These behaviours suggest that Tibicina species could
regulate their body temperature by modifying their behav-
iour in relation to environmental conditions.
342 J. Sueur and A. F. Sanborn

T. corsica fairmairei produced at higher muscle temperatures in cicadas will lead

1.20 to louder calls (Josephson & Young, 1979; Josephson, 1981;
1.00
Young & Josephson, 1983; Josephson & Young, 1985;
Sanborn, 2001). In addition, the timbal tensor muscle will
0.80 also produce greater tension at higher temperature. The
timbal tensor muscle has been shown to influence the inten-
0.60 sity of cicada calls (Hennig et al., 1994). The apparent
0.40
plateau of maximal sound power in the Tibicina species,
except T. corsica fairmairei (which was only encountered
0.20 over a limited ta range), suggests that the changes in sound
power are due to thermally induced changes in the activity
0.00
20 22 24 26 28 30 32 34 of the sound production system.
In addition, our observations report inter-individual dif-
T. garricola ferences in song power at the same ta. These differences are
0.18
probably due to differences in calling postures or in micro-
0.16
climatic conditions that we were unable to identify in the
Sound Power (mW)

0.14
field. When emitting their calling signal, Tibicina males
0.12 typically raised their abdomen and lifted up their wings
0.10 upon their body. Raising the abdomen exposes the tym-
0.08 pana, and probably enhances sound radiation through the
0.06 tympana, as demonstrated in other cicada species (Young,
0.04 1990). In addition, the wing position over the abdomen may
0.02 facilitate sound radiation. Therefore, males that raise their
0.00 abdomen and lift up their wings to a greater degree should
20 22 24 26 28 30 32 34 produce louder calls. Furthermore, these inter-individual
differences could support mate selection by females, as
T. tomentosa
0.25 already suggested and discussed by Sueur (2003).
The data illustrate differences between the three species.
0.20 However, the difference is significant only between the
sound power of T. corsica fairmairei and T. garricola
0.15 (Kolmogoro-Smirnov test, P < 0.01). The similarity in the
results is probably due to the high morphological homo-
0.10 geneity in the genus Tibicina. Even if the difference of the
means is not statistically significant, we note that males of
0.05 T. corsica fairmairei produce louder calls than males of
T. tomentosa. This observation confirms our previous
0.00 hypothesis explaining differences in minimum intermale
20 22 24 26 28 30 32 34
distance between males of T. c. fairmairei and males of
Ambient temperature (°C) T. tomentosa (Sueur, 2003). Inter-individual distance is
estimated most likely through calling song intensity and,
Fig. 1. Correlation between ambient temperature and sound
as a result, males of T. corsica fairmairei defend a larger
power of the calling song in three species of Tibicina.
individual territory than males of T. tomentosa.
Taking into account the ta may help to explain the calling
The 22–24
C ta range appears to be the minimum ta at behaviour of a related group of cicadas. Further behav-
which the Tibicina males can produce a calling song. As ta, ioural and physiological observations and experiments are
and presumably tb, increases, the temperature of the sound needed to examine in more detail the role of temperature in
producing muscles will also increase. The increased tension calling Tibicina species. In particular, Tibicina species

Table 1. Sound pressure levels, sound power (Q) and correlation between sound power and ambient temperature (ta) in three Tibicina species.

Sound Sound Regression line between Spearman

pressure Range power Sample sound power (Q) and rank
Taxa level (dB) (dB) (mW) size ambient temperature (ta) coefficient
T. c. fairmairei 79.3 71.0–84.5 0.27 19 Q ¼ 3.138 þ 0.138(ta) 0.77**
T. garricola 73.5 64.0–77.0 0.07 15 Q ¼ 0.236 þ 0.011(ta) 0.61*
T. tomentosa 75.8 69.5–78.5 0.12 8 Q ¼ 0.335 þ 0.017(ta) 0.90**

Correlation was tested using the Spearman rank test (*P < 0.05, **P < 0.001).

# 2003 The Royal Entomological Society, Physiological Entomology, 28, 340–343


occurring in France have been documented to occupy dif-
ferent habitats and/or show divergence in their emergence
period (Sueur & Puissant, 2002). Consequently, specific
thermoregulatory conditions could be analysed and
compared in relation to the ecological conditions of each
species.
Acknowledgements
We thank Claude Bercy for the loan of the Sound Level
Meter and Stéphane Puissant for help during field
observations. This study was partly conducted in the
‘Harmas de Jean-Henri Fabre’ (Muséum National
d’Histoire Naturelle, France). We also thank two anonym-
ous referees for their comments leading to improvement of
the manuscript.
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Accepted 17 June 2003