Behavioral Ecology Vol. 13 No. 5: 598-606
© 2002 International Society for Behavioral Ecology
Death comes suddenly to the unprepared: singing crickets, call fragmentation, and parasitoid flies
a Laboratory for Bioacoustics, Institute of Zoology, University of Zürich, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland b School of Biological Sciences, Woodland Road, University of Bristol, Bristol BS8 1UG, UK
Address correspondence to P. Müller. E-mail: piemue{at}zool.unizh.ch.
Received 4 April 2001; revised 5 December 2001; accepted 8 December 2001.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Male field crickets are subject to a delicate dilemma because their songs simultaneously attract mates and acoustic predators. It has been suggested that in response, crickets have modified various temporal song parameters to become less attractive to acoustic predators. We investigated whether crickets with chirping (versus trilling) song structures are less likely to attract acoustically orienting parasitoid flies. Experimentally, we evaluated the phonotactic quest of the parasitoid fly Ormia ochracea in response to broadcast cricket calls, presented both simultaneously (choice paradigm) and sequentially (no-choice paradigm). Flight trajectories were recorded in darkness using three-dimensional active infrared video tracking. The flies showed remarkable phonotactic accuracy by landing directly on the loudspeaker. The introduction of acoustic fragmentation that resembles calls of many chirping crickets altered the flies' phonotactic accuracy only slightly. Our results document differential attraction between trilling and chirping cricket songs and quantitatively demonstrate that chirping songs, if presented alone, do not impair the efficiency (temporal investment and landing accuracy) of the flies' phonotactic quest. This study shows that song fragmentation is no safeguard against acoustic parasitism. We conclude that, in general, a cricket may reduce predation only if its neighbors are acoustically more conspicuous, chiefly by amplitude.
Key words: communication, Gryllus, Ormia, parasitism, phonotactic behavior, trajectory analysis.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Both female field crickets and the larviparous parasitoid flies Ormia ochracea (Diptera, Tachinidae, Ormiini) rely on acoustic cues to detect and find singing male crickets (Cade, 1975
; Robert et al.,
1992; Walker and Wineriter,
1991). Once a fly homes in on her host, she lays her larvae on and
around the cricket. The larvae enter the host, feed, and grow, and after
approximately 7-10 days they emerge and pupate, killing the cricket
(Adamo et al., 1995). Male
crickets are therefore faced with the dilemma of attracting mates on the one
hand and avoiding parasitoids on the other.
Several possibilities have been suggested as to how male crickets could
signal under conditions that reduce the risk of exploitation by acoustic
predators. One such strategy found in some males of Gryllus integer
(Orthoptera, Gryllidae) is to remain silent while staying near callers (Cade,
1975,
1979). These silent males,
called "satellites," intercept females as they move toward callers
and thus avoid both parasitization and the cost of signaling. Another possible
strategy is to shift the seasonal (Burk,
1982) or the diel (Cade et al.,
1996; Zuk et al.,
1993) calling pattern in relation to the phenology and abundance
of parasitoid flies. Greater attention has been directed to the idea that
crickets might have modified various temporal song parameters to become less
attractive to acoustic predators (e.g.,
Bailey and Haythornthwaite,
1998; Lehmann and Heller,
1998; Zuk et al.,
1993,
1998). The idea that
parasitization can be reduced through song modification has found some support
in the finding that female flies show a "preference" for certain
song types (Lehmann and Heller,
1998; Wagner,
1996).
Field studies by Walker
(1986,
1993) have revealed that
gravid females of O. ochracea were attracted in greatest numbers to
the trilling songs of Gryllus rubens. Songs of other candidate hosts
were much less attractive relative to the simultaneous broadcast of a G.
rubens song. It is therefore conceivable that O. ochracea
discriminates between cricket species on the basis of their calling song. By
examining the attractiveness of varied songs in the chirping field cricket
species Gryllus lineaticeps, Wagner
(1996) found that female flies
favor songs with a higher chirp rate, longer chirp duration, and higher chirp
amplitude. This study suggests that O. ochracea may not only
distinguish between potential host species, as found by Walker
(1993), but also displays
differential attraction to certain song variations within a single host
species. Wagner (1996) then
suggested that higher chirp rate and longer chirp duration may be easier for
flies to localize and that ultimately female flies may minimize search costs
by orienting to such songs. Proximately, these search costs should be directly
reflected in the flies' flight behavior in terms of spatial accuracy and
temporal investment.
Thus far, field data on fly phonotaxis have been methodologically confined to choice experiments where alternative stimuli were presented simultaneously. The comparison between stimuli presented at the same time provides a sensitive and adequate measure of differential attraction. Because alternative stimuli may interfere at the perceptual level and possibly mask one another, differential attraction alone does not test whether flies minimize search costs by orienting to one chosen stimulus. Thus, to address the question of search efficiency in response to variable song structures, complementary experiments are desirable. Such experiments may consist in the sequential, no-choice presentation of test stimuli while the flight behavior is documented in standard and reproducible conditions. Differences in flight behavior can then be interpreted as a function of the acoustic parameters modified in the test songs. Such experiments are naturally complementary because, in the field, crickets call simultaneously as well as in sequence. By combining choice experiments with no-choice experiments, more can be learned about the relationship between acoustic signaling and the constraints imposed by eavesdropping parasitoids.
In the present study, we first examined, in the context of choice experiments, whether the trilling song of the primary host (G. rubens) is more attractive than chirping calls. Second, using no-choice experiments, we investigated the flies' phonotactic behavior in terms of their search efficiency (temporal investment and landing accuracy) and structure of flight trajectories. We compared the results from the choice and no-choice paradigms, and we conclude that song fragmentation alone is no safeguard against acoustic parasitism.
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Animals and rearing conditions
The parasitoid flies, O. ochracea, used were reared in the Laboratory of Bioacoustics at the University of Zürich. The founder flies of the colony originated from Gainesville. Florida, courtesy of T. J. Walker. We kept animals at a light regime of 16:8 hr day:night cycle, 26°C, and 60% relative humidity and provided them with nectar (Vita-Rich instant nectar for hummingbirds) and water ad libitum. We performed experiments only on gravid females, as no positive phonotaxis is observed for other sex or age classes.
Experimental arena
We conducted all behavioral experiments in an indoor room (length 6.8 m
x width 4.9 x height 4.0 m) with walls covered with high-frequency
absorbing foam (Maag Technic AG, type 1135). Inside this room, a flight cage
(length 4.5 m x width 2.6 m x height 3.0 m) formed the actual
experimental arena (Figure 1A).
To enhance the fly's contrast against the background for three-dimensional
video tracking, we covered the background uniformly with black cotton sheets.
The only objects placed in the experimental arena were a starting platform,
one or two loudspeakers (each mounted in a cabinet; length 30 cm x width
30 cm x height 8 cm) on the ground and two video cameras protruding
through the roof (Figure
1A).
|
Data acquisition
A single fly was placed on the platform, and placidly stayed there,
motionless, until the test stimulus was presented. As soon as sound was
broadcast through one or both loudspeakers (Radio Shack Super Tweeter, No.
40-1310B, 4 cm diameter), the fly took off and landed on the active
loudspeaker a few seconds later.
Because O. ochracea is crepuscular and nocturnal
(Walker, 1993), and to exclude
visual cues, we conducted all experiments under LED infrared illumination (875
nm peak wavelength), providing light only to the cameras of the tracking
system. We recorded flight trajectories using two infrared-sensitive video
cameras with pan-tilt optics (Sony LSX PT 1;
Figure 1A). Camera tracking and
trajectory data acquisition was achieved using Trackit Stereo software
(Fry et al., 2000). We sampled
the spatial position of the fly every 20 ms. By an additional custom-written
LabVIEW 5.0 (National Instruments) interface, we were able to use the
positional information to control the sound stimulus as a function of the
fly's position in space (Müller and
Robert, 2001). Hence, our set-up allowed us not only to record
flight trajectories as such, but also to perform interactive experiments.
Preliminary experiment
We estimated how short a chirp could be so that a fly could still detect
and locate it. A single chirp is a short series of sound pulses followed by
silence. We then built our chirping cricket calls on the basis of the shortest
possible chirp. To assess the minimal number of sound pulses necessary for the
fly to detect and locate a sound source, we used an interactive paradigm: the
flight space of the fly was separated in two by the introduction of a virtual
plane (Figure 2). The plane was
imaginary but had a dedicated logical function analogous to a light barrier.
The fly was first attracted to the loudspeaker LS 1 by playing a continuous
control trill (Figure 3A). When
the fly crossed the plane, she elicited the switch over from one loudspeaker
(LS 1) to the other (LS 2). As a reaction to the new sound source, the fly
changed her course, turned back, and eventually landed on LS 2
(Figure 2A). We then
systematically reduced the total number of sound pulses in the trill played
from LS 2. Providing the fly with a train of only five sound pulses still
caused a distinct orientation reaction
(Figure 2B). Fewer sound pulses
failed to induce any oriented turn (Figure
2C). Based on this evidence (n = 7), we then constructed
our model songs as described in the following sections.
|
|
Choice experiments
In the choice experiments we exposed 24 female flies to six treatments.
Each treatment was a choice experiment between cricket calls simultaneously
broadcast from two loudspeakers (LS 1 and 2;
Figure 1A). We randomized the
treatments to exclude time and sequence effects.
We presented all pairs of stimuli once to each fly in a randomized order and exchanged the broadcast stimuli between LS 1 and LS 2 to obtain an equal number of presentations per loudspeaker for each treatment. On the basis of the landings on one of the two loudspeaker cabinets, we could determine which of the two stimuli was more attractive. We compared the number of flies successfully attracted to each of the stimuli with a two-tailed binomial test.
Choice experiments encompassed the simultaneous presentation of the control trill with stimulus a, b, or c and, complementarily, of stimuli a, b, and c against each other (Figure 3 and Table 1).
|
Control trill
The natural calling song of G. rubens is a trill in which sound
pulses are repeated at a constant rate and are packaged in long pulse trains
of about 2-30 s (Doherty and Callos,
1991; Walker,
1993). Accordingly, we generated a model calling song using the
program SoundEdit 16 (Macromedia; 16-bit resolution, 44.1 kHz sampling rate).
As in the natural song, the duration of a single pulse was 13 ms, followed by
a gap of silence of 9.2 ms. The carrier frequency was 4.8 kHz. The sound pulse
had a linear onset ramp of 2 ms and a linear offset ramp of 5 ms. We looped
the single pulses so that we obtained a continuous pulse train of 45 pulses/s
(control trill; Figure 3A).
Control trill versus a, b, or c
We simultaneously presented the control trill with stimulus a, b,
or c (Figure 3B and
Table 1). Each of the three
stimuli (Figure 3B) differ in
one acoustical property from the control trill. Stimulus a is also a
continuous trill but only half the intensity of the control (i.e., 6 dB SPL
less). Stimulus b is a chirping call with long chirps but equal
intensity as the control. The chirps had a length of 10 sound pulses followed
by an equal length of silence. Stimulus c was again a chirping call,
but the chirps were shorter (i.e., half the length as in b). As for
the control trill and the other chirping call (b), we adjusted the
sound pressure level to 82 dB SPL.
We measured the intensities of the acoustic stimuli with a TES 1352 sound level meter. The instrument was regularly calibrated with a Brüel & Kjær sound level calibrator (type 4231). We adjusted sound pressure levels (SPL) in decibels (re 20 µPa) at 15 cm above the loudspeaker.
Test stimuli a, b, and c
We constructed a, b, and c by halving either amplitude,
repetition rate, or pulse train length in the control trill. Thus, the overall
acoustic energy of stimuli a, b, and c became equal.
Simultaneous presentation of stimuli a, b, and c against
each other forced the flies to choose between sound stimuli that varied only
in their information content. Therefore, these stimuli allowed us to test the
effects of amplitude (a vs. b and c), repetition
rate (b vs. a and c), and length of pulse train
(c vs. a and b).
Sequential experiments
In the sequential experiments (no-choice), we examined the phonotactic
flight performance of 14 flies in the presence of a single sound stimulus. The
stimuli were broadcast from a single loudspeaker (center cabinet in
Figure 1A). In total, we tested
eight different treatments for each fly
(Figure 3 and
Table 1): the control trill,
the three test stimuli (a, b, and c), and all possible
combinations (ab, ac, bc, and abc). We randomized the
treatments to exclude time and sequence effects. We constructed a
23-factorial design (Bailey,
1995) using one block per fly, each of which contained exactly
eight plots, one for each treatment. The advantage of using this type of
design is that we obtained a broad picture of the effect of each of three song
parameters (amplitude, repetition rate, and pulse train length) in the
different conditions furnished by variations in the other parameters. If the
song parameters were not independent of one another, we collected at once all
the information about the nature of the interaction. Because we were
interested both in the effects on search efficiency and flight behavior, we
chose a set of five descriptors (see below) from each recorded trajectory. The
estimates of each descriptor were subjected to a three-way repeated-measures
ANOVA (von Ende, 1993)
investigating the effects of high versus low amplitude (a), high versus low
repetition rate (b), and long versus short pulse trains (c), both separately
and in different combinations. In the repeated-measures ANOVA, the effect
x fly interaction was used as the error term for the respective
effect.
We examined the following two descriptors to estimate the effects on search
efficiency: (1) landing accuracy—the distance (m) between the landing
position and the center of the active loudspeaker; and (2) flight
duration—the time (s) elapsed between takeoff and landing. Also, we
investigated the flight trajectory alone. One concise approach to doing so is
the analytical technique of finite helix fit
(Crenshaw et al., 2000;
Figure 1B), whereby a
three-dimensional trajectory is completely described by its velocity,
curvature, and torsion. We thus measured (3) speed—the mean magnitude of
flight velocity expressed in m/s; (4) curvature—the average curvature
(rad/m) along the entire flight trajectory; and (5) torsion—the average
torsion (rad/m) along the entire flight trajectory.
We performed all data processing and the according statistical analyses
using the software package R 1.2.2 (General Public License;
http://www.R-project.org)
running on a LINUX platform. The level of significance, 
, was set at
0.05. The significance level for each of the five descriptors (see above) were
adjusted according to the Bonferroni correction (i.e., ' =
/5 = 0.01).
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Choice experiments
In the first series of choice experiments, the goal was to see whether the control trill is more attractive than any one of the modified stimuli a, b, or c. For all pairs of stimuli, we found significant attraction to the control trill (two-tailed binomial tests: control vs. a, 20 out of 24 flies: p = .0015; control vs. b: 22 out of 24 flies, p = .0002; control vs. c: 20 out of 24 flies, p = .0015; Figure 4A). This result demonstrates that the model song of the primary host (G. rubens) is more attractive than any other alternative song (a, b, or c) when broadcast simultaneously.
|
In a second series, we presented test stimuli of equal sound energy per unit of time, but that differed in their informational value (Figure 4B). The data reveal a tendency of higher attraction for amplitude when the flies had the choice between a trill of lower amplitude and a long chirp of high amplitude (a vs. b: two-tailed binomial test; 16 out of 23 flies, p = .0639). Flies were also more attracted to high amplitude when they were given a choice between a trill of low amplitude and a short chirp of high amplitude (a vs. c: two-tailed binomial test, 19 out of 24 flies, p = .0067). Comparing two chirp types, flies clearly showed more attraction to longer chirps (b vs. c: two-tailed binomial test; 17 out of 23 flies, p = .0227).
Altogether, these choice experiments suggest that flies are attracted to songs of higher amplitude. Among chirps of equal amplitude, flies are preferentially attracted to longer chirps.
Sequential experiments
Based on a sample of 14 individuals (112 trajectories), we found that
landing accuracy decreased for low repetition rate, as well as for short pulse
trains (Figure 5A,B and
Table 2). Together, these data
imply that chirping reduces landing accuracy in general. All interaction terms
in the repeated-measures ANOVA were nonsignificant
(Table 2). Hence, the
differences in landing accuracy simply add up if the test song was a
combination of songs b and c. Although the differences in
landing accuracy caused by a change in one of the factors were significant,
they were rather small (Figure
5A,B). The differences in landing accuracy between low and high
levels were only 5.7 cm (SE = 5.2) for factor b and 5.8 cm (SE = 4.9)
for factor c. This is still remarkably precise because the mean path
length between the starting platform to the loud-speaker extended to 3.85 m
(SE = 0.26). Apart from a few outliers (indicated by the circles in the box
plots), all flies landed close to the loudspeaker irrespective of stimulus
condition (Figure 5A,B).
Remarkably, flight duration was not significantly affected by any change of
the song parameters a, b, or c
(Figure 5C and
Table 2).
|
|
Comparing flight trajectories in response to a continuous trill or chirps, we found that flies tend to fly straighter if attracted to chirping cricket calls (Figure 6). Typically, within a flight to a continuous trill, we recognize three phases: a takeoff phase, a cruising phase, and a landing phase. Inspection of the trajectory's three-dimensional representation and its projections reveals that the fly was first gaining altitude and then approached the sound source with a meandering path. Closing in on the sound source, the fly initiated a spiral descent to the loudspeaker. Compared to the control situation, the trajectory to stimulus b did not show such transitions in the flight pattern except for the short takeoff phase. Instead, the fly flew straight to the loudspeaker with less alterations of her flight course. The repeated-measures ANOVA supports the impression obtained from Figure 6. The analysis reveals that both speed and curvature were affected by reducing the number of chirps (Figure 7A,B and Table 3). The flies flew slower, but tended to fly straighter. Hence, we may regard a straight flight path as the flies' behavioral response to the fragmentation of a continuous trill. Similarly to repetition rate, speed was reduced for high amplitudes, whereas curvature and torsion were not affected (Figure 7B and Table 3). The repeated-measures ANOVA yielded no effect on torsion for any change in the factors a, b, or c or for any of the possible interaction (Figure 7C and Table 3).
|
|
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Four main points summarize the results of this study. First, the call of the primary host G. rubens was more attractive than any other alternative stimuli. Second, high intensity was a more attractive song characteristic than trilling. Everything else being equal, flies chose long over short chirps. Third, in no-choice experiments, phonotaxis and search efficiency were altered little in response to substantial fragmentation of the primary host song. Finally, flight trajectories imply that flies coped with the loss of acoustic information due to song fragmentation by keeping their flight direction.
Methodological considerations about choice versus no-choice
experiments
The study of preference by choice experiments presupposes that all stimuli
are perceivable when presented singly or together. Hence, it is useful to
employ both simultaneous (choice) and sequential (no-choice) stimulus
presentation to first establish perceptual capacity for each stimulus
(no-choice) and then highlight differential phonotactic responsiveness
(choice). Moreover, sequential stimulus presentation provides information
about the relationship between call fragmentation and search costs. Field
conditions have promoted choice experiments because they are simple to perform
and require less time to gather a sufficiently large sample. Admittedly,
comparison between stimuli presented at the same time provides sensitive and
adequate information on differential attraction. Yet choice experiments may
not rule out differential perception of the sound stimulus by the animal.
Also, choice experiments present a disadvantage in that they do not unravel
whether a no-preference stimulus is associated with increased search costs. On
the other hand, the no-choice paradigm does not permit one to single out the
part of differential attraction that is due to the specific test song
parameter. Because the attractiveness of a stimulus, as determined from
behavior, may well rely on the animal's evaluation of several properties of
the stimulus, little can be said about the relative attractiveness of any
particular stimulus property (Doherty,
1985). Hence, both methods are clearly complementary; they have
their biological relevance because flies may encounter crickets calling alone
or in aggregations.
Song structure and phonotaxis
In accordance with previous studies
(Cade, 1981;
Gray and Cade, 1999b;
Ramsauer and Robert, 2000;
Wagner, 1996;
Walker, 1993), we found that
female flies are differentially attracted to different song types. Yet
differential attraction alone does not explain the reasons—ultimate and
proximate—for the flies' capacity to distinguish song structures. We see
at least three potential explanations as to why female flies distinguish
different cricket songs. First, songs may convey some information about host
quality that in turn reflects suitability for the flies' offspring. Second,
the flies may find some songs psychoacoustically easier to locate and thus
benefit from a more effective acoustic search. Third, the flies' acoustic
perception may be constrained to specific song types and therefore may be less
sensitive to songs departing from a typical template.
In crickets, it has been suggested that by favoring males that produce more
syllables per chirp, female crickets select males with higher pathogen
resistance ability (Ryder and Siva-Jothy,
2000). Likewise, calling songs could provide parasitoids with
information about host quality. Other parasitoids are known to discriminate
between hosts based on host quality (for review, see
Godfray, 1994). The number of
pulses per trill in male G. integer, the major host for O.
ochracea in Texas, is not related to male size or age
(Gray and Cade, 1999a).
Consequently, Gray and Cade
(1999b) concluded that male
quality is unrelated to the number of pulses per trill. Alternatively, they
suggest that both female crickets and female flies adaptively minimize search
costs by preferring the most common song. This conclusion is intriguing
because the flies are gregarious parasitoids and may deposit a clutch of
larvae on a host even when a host has already been parasitized
(Adamo et al., 1995). In
addition, cricket size seems to influence neither pupal weight nor the flies'
survival to adulthood (Hage,
1998). Hence, the fly's reproductive success is expected to depend
rather on her search efficiency which, in turn, is directly related to her
auditory capacity and to the cricket's acoustic conspicuousness. For crickets,
there is evidence that females search to minimize their search cost by also
reducing predation risk (Hedrick and Dill,
1993). The composition of search costs for parasitoid flies has
not been evaluated. On the basis of choice experiments alone, it is quite
tempting to believe that song preference reflects search costs. Surprisingly,
our data suggests that search costs vary little between different song types.
Hence, other explanations, ultimate and proximate, ought to be considered as
well.
Overall, flies are more attracted to songs with higher amplitudes and longer chirps. In response to a single test stimulus, flies are slightly less efficient in terms of spatial accuracy at low repetition rates and short pulse trains (Figure 5A,B). Because mean flight speed also changes as a function of stimulus properties (i.e., high amplitude and low repetition rate; Figure 7A), it may seem at first glance that overall search efficiency is indeed affected. Yet flight trajectories were highly variable, and the total amount of time elapsed between take-off and landing was not significantly different between treatments. Hence, the introduction of acoustic fragmentation in the cricket's trill alters the flies' phonotactic success little. Providing the flies with only 12.5% of the initial acoustic information of the control trill (control trill vs. stimulus abc; see Figure 3A,C) the flies remain capable of locating the sound source rather precisely. Upon landing, flies proceeded with their phonotactic search by walking straight to the center of the loudspeaker.
The fact that flies tend to keep their flight course in response to song
fragmentation may seem counterintuitive at first but bears significance for
the questions raised here. Earlier studies
(Müller and Robert, 2001)
have shown that the flies' orientation toward the sound source also persists
after complete interruption of the sound stimulus, demonstrating their
remarkable capacity of pursuing a silenced sound source. This most intriguing
persistence in orientation suggests that the flies are endowed with a
behavioral strategy to accommodate the fragmentation (or even the absence) of
acoustic information. Thus, as already pointed out by Walker
(1993), chirping is no
safeguard against acoustic parasitism.
Our data also do not support the ideas that flies show preference for calls
they find easier to locate (Zuk et al.,
1998) and that they spend less time doing so
(Lehmann and Heller, 1998).
Why, then, do Ormia flies show preferential phonotactic behavior when
exposed to alternative songs? Differential attraction to higher intensities
(here for a over both b and c) corroborates
previous field studies (Cade,
1981; Wagner,
1996). In this context, Forrest and Raspet
(1994) developed a model
explaining that differential attraction may solely be based on relative
loudness. Taking into consideration relative loudness and source spacing
(Forrest and Raspet, 1994;
Figure 5A), their model exactly
predicts the relative attraction of 0.83 observed here.
Apart from song amplitude, O. ochracea also shows a comparable
differential attraction for longer chirp duration (i.e., b over
c; Figure 4B), as
found here and in the field (Wagner,
1996). Surprisingly, chirping calls (b and c)
were more attractive when presented simultaneously with a continuous trill of
lower amplitude. We suggest that chirps of high amplitude impose a masking
effect on the low-amplitude trill. Although masking effects have not been
studied in detail in acoustic parasitoids
(Ramsauer and Robert, 2000),
studies in crickets have revealed that auditory masking is an important and
complex issue in insect communication. For example, Römer et al.
(1989) found that the song of
Hemisaga denticulata was suppressed in the presence of the singing
bushcricket Mygalopsis marki. Additionally, song conspicuousness in
M. marki is affected by the competing acoustic activity of
conspecifics (Dadour, 1989).
Clearly, such masking may have negative effects on reproductive success if
one's song becomes less conspicuous to conspecifics. In contrast, the impact
of acoustic predators may favor reduced conspicuousness, which in turn ought
to result in increased survival and reproductive success.
These results show that individual male crickets will benefit from song fragmentation only in some situations. Song fragmentation will reduce conspicuousness only in the presence of acoustic neighbors, conspecific and heterospecific, that are themselves more conspicuous chiefly by way of song amplitude. The flies' behavior highlights how hazardous it is for a keen, but unprepared, cricket to fill up a competitor's acoustic space.
|
ACKNOWLEDGEMENTS |
|---|
We thank Hanni Kohler and Mirjam Müller for rearing the animals; Hansjörg Baumann for his invaluable support in programming LabVIEW applications; and Martin Bichsel, Steven Fry, Helmut Heise, and Stephan Hischier for software and hardware support of the tracking system. Many thanks also go to Wolf Blanckenhorn and two anonymous referees for constructive comments on earlier versions of the manuscript. This research was supported by grants from the Swiss National Science Foundation and the Claraz Donation to D.R.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Adamo SA, Robert D, Perez J, Hoy RR, 1995. The response of an insect parasitoid, Ormia ochracea (Tachinidae), to the uncertainty of larval success during infestation. Behav Ecol Sociobiol 36: 111-118.[Web of Science]
Bailey NTJ, 1995. Statistical methods in biology, 3rd ed. Cambridge: Cambridge University Press.
Bailey WJ, Haythornthwaite S, 1998. Risks of calling by the field cricket Teleogryllus oceanicus; potential predation by Australian longeared bats. J Zool 244: 505-513.
Burk T, 1982. Evolutionary significance of predation on sexually signalling males. Fla Entomol 65: 90-104.
Cade W, 1975. Acoustically orienting parasitoids: fly phonotaxis to cricket song. Science 190: 1312-1313.
Cade WH, 1979. The evolution of alternative male reproductive strategies in field crickets. In: Sexual selection and reproductive competition in insects (Blum MS, Mlum NA, eds). New York: Academic Press; 343-379.
Cade WH, 1981. Field cricket spacing, and the phonotaxis of crickets and parasitoid flies to clumped and isolated cricket song. Z Tierpsychol 55: 365-375.[Web of Science]
Cade WH, Ciceran M, Murray A-M, 1996. Temporal patterns of parasitoid fly (Ormia ochracea) attraction to field cricket song (Gryllus integer). Can J Zool 74: 393-395.
Crenshaw HC, Ciampaglio C, McHenry M, 2000. Analysis of the three-dimensional trajectories of organisms: estimates of velocity, curvature and torsion from positional information. J Exp Biol 203: 961-982.[Abstract]
Dadour IR, 1989. Temporal pattern changes in the calling song of the katydid Mygalopsis marki Baily in response to conspecific song (Orthoptera: Tettigoniidae). J Insect Behav 2: 199-216.
Doherty JA, 1985. Phonotaxis in the cricket, Gryllus bimaculatus DeGeer: comparisons of choice and no-choice paradigms. J Comp Physiol A Sens Neural Behav Physiol 157: 279-289.
Doherty JA, Callos JD, 1991. Acoustic communication in the trilling field cricket, Gryllus rubens, (Orthoptera: Gryllidae). J Insect Behav 4: 67-82.
Forrest TG, Raspet R, 1994. Models of female choice in
acoustic communication. Behav Ecol 5:
293-303.
Fry SN, Bichsel M, Müller P, Robert D, 2000. Tracking of flying insects using pan-tilt cameras. J Neurosci Methods 101: 59-67.[Web of Science][Medline]
Godfray HCJ, 1994. Parasitoids: behavioral and evolutionary ecology. Princeton, New Jersey: Princeton University Press.
Gray DA, Cade WH, 1999a. Quantitative genetics of sexual selection in the field cricket, Gryllus integer. Evolution 53: 848-854.[Web of Science]
Gray DA, Cade WH, 1999b. Sex, death and genetic
variation: natural and sexual selection on cricket song. Proc R Soc
Lond B 266:
707-709.
Hage I, 1998. The importance of body size for the acoustically orienting parasitoid Ormia ochracea (Diptera: Tachinidae): consequences for fitness and phonotaxis in indoor conditions (diploma thesis). Zürich: University of Zürich.
Hedrick AV, Dill LM, 1993. Mate choice by female crickets is influenced by predation risk. Anim Behav 46: 193-196.[Web of Science]
Lehmann GUC, Heller K-G, 1998. Bushcricket song structure and predation by the acoustically orienting parasitoid fly Therobia leonidei (Diptera: Tachinidae: Ormiini). Behav Ecol Sociobiol 43: 239-245.[Web of Science]
Müller P, Robert D, 2001. A shot in the dark: the silent quest of a free-flying phonotactic fly. J Exp Biol 204: 1039-1052.[Abstract]
Ramsauer N, Robert D, 2000. Free-flight phonotaxis in a parasitoid fly: behavioural thresholds, relative attraction and susceptability to noise. Naturwissenschaften 87: 315-319.[Web of Science][Medline]
Robert D, Amoroso J, Hoy RR, 1992. The evolutionary
convergence of hearing in a parasitoid fly and its cricket host.
Science 258:
1135-1136.
Römer H, Bailey W, Dadour I, 1989. Insect hearing in the field. III. Masking by noise. J Comp Physiol A Sens Neural Behav Physiol 164: 609-620.
Ryder JJ, Siva-Jothy MT, 2000. Male calling song provides a reliable signal of immune function in a cricket. Proc R Soc Lond B 267: 1171-1175.[Medline]
von Ende CN, 1993. Repeated-measures analysis: growth and other time-dependant measures. In: Design and analysis of ecological experiments (Scheiner SM, Gurevitch J, eds). New York: Chapman and Hall; 113-137.
Wagner WE, 1996. Convergent song preferences between
female field crickets and acoustically orienting parasitoid flies.
Behav Ecol 7:
279-285.
Walker TJ, 1986. Monitoring the flights of field crickets (Gryllus spp.) and a tachinid fly (Euphasiopterix ochracea) in north Florida. Fla Entomol 69: 678-685.
Walker TJ, 1993. Phonotaxis in female Ormia ochracea (Diptera: Tachinidae), a parasitoid of field crickets. J Insect Behav 6: 389-410.
Walker TJ, Wineriter SA, 1991. Host of a phonotactic parasitoid and levels of parasitism (Diptera: Tachinidae: Ormia ochracea). Fla Entomol 74: 554-559.
Zuk M, Rotenberry JT, Simmons LW, 1998. Calling songs of field crickets (Teleogryllus oceanicus) with and without phonotactic parasitoid infection. Evolution 52: 166-171.[Web of Science]
Zuk M, Simmons LW, Cupp L, 1993. Calling characteristics of parasitized and unparasitized populations of the field cricket Telleogryllus oceanicus. Behav Ecol Sociobiol 33: 339-343.[Web of Science]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  N. Lee, D. O. Elias, and A. C. Mason A precedence effect resolves phantom sound source illusions in the parasitoid fly Ormia ochracea PNAS, April 14, 2009; 106(15): 6357 - 6362. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 X. E. Bernal, A. S. Rand, and M. J. Ryan Acoustic preferences and localization performance of blood-sucking flies (Corethrella Coquillett) to tungara frog calls Behav. Ecol., September 1, 2006; 17(5): 709 - 715. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||