Natural variation in the temporal patterning of calling song structure in the field cricket Gryllus pennsylvanicus: effects of temperature, age, mass, time of day, and nearest neighbour

MARK CICERAN AND ANNE-MARIE MURRAY' Department of Biological Sciences, Brock University, St. Catharines, ON L2S 3A1, Canada

AND

GARETH ROWELL Department of Entomology, Texas A&M University, College Station, TX 77843, U.S.A.

Received May 14, 1993 Accepted September 14, 1993

CICERAN, M., MURRAY, A.-M., and ROWELL, G. 1994. Natural variation in the temporal patterning of calling song structure in the field cricket Gryllus pennsylvanicus: effects of temperature, age, mass, time of day, and nearest neighbour. Can. J. Zool. 72: 38-42.

Genetic and environmental sources of variation in the temporal patterning of song structure may be important variables influencing male field cricket reproductive success. Song structure in both field and laboratory populations of Gryllus pennsylvanicus was examined to assess possible sources of variation. Factors examined included temperature, male age, body mass, time of day, and male spacing patterns. Temperature was positively correlated with pulse rate and negatively correlated with interchirp interval for both field and laboratory populations. Temperature was negatively correlated with chirp duration only in the field population. Calling song structure did not vary with male age or mass. Time of day had a significant effect on the song parameters examined, even when data were corrected for temperature differences. Males calling in the morning had faster pulse rates and shorter chirp durations than males recorded at night time. Male spacing patterns also influenced calling; isolated males had longer intervals between consecutive chirps than clumped males. Data are discussed in terms of acoustical competition between males and female choice.

CICERAN, M., MURRAY, A.-M., et ROWELL, G. 1994. Natural variation in the temporal patterning of calling song structure in the field cricket Gryllus pennsylvanicus: effects of temperature, age, mass, time of day, and nearest neighbour. Can. J. Zool. 72 : 38-42.

Les facteurs gCnCtiques et Ccologiques qui entrainent des variations temporelles dans la structure du chant peuvent avoir une grande influence sur le succGs reproducteur des grillons des champs. La structure du chant a CtC CtudiCe chez des populations naturelles et des populations expkrimentales de Gryllus pennsylvanicus et les causes possibles des variations ont

- CtC examinCes, notamment la tempkrature, l'age des miles, la masse corporelle, le moment de la journCe et la distance entre les males. I1 y avait une corrClation positive entre la tempCrature et la frCquence des stridulations et une corrklation nCgative entre la tempCrature et l'intervalle entre les Cmissions de chant chez les deux populations. La temperature Ctait en corrClation nCgative avec la durCe du chant seulement chez la population naturelle. La structure du chant n'Ctait pas fonction de l'age ou de la masse du m8le. Le moment de la journCe influen~ait significativement les variables relikes au chant, meme lorsque les donnCes Ctaient ajustCes pour tenir compte des diffkrences de tempkrature. Les males qui chantaient le matin Cmettaient des stridulations ?I frCquence plus rapide, mais leurs pCriodes de chant Ctaient plus courtes que celles des males qui chantaient la nuit. L'espacement entre les males influen~ait Cgalement 1'Cmission des chants : chez les males isolCs, les intervalles entre les Cmissions de chants Ctaient plus longs que chez les males regroupCs. Les rCsultats sont examinks en fonction de la compCtition acoustique entre les males et en fonction du choix des femelles.

[Traduit par la rCdaction]

Introduction be an important influence on the temporal pattern of song

Male field crickets (Orthoptera: Gryllidae) produce a dis- tinctive species-specific calling song that attracts females for mating (Popov and Shuvalov 1977; Elsner and Popov 1978). However, much variation exists between males in song structure, and females may have the potential to choose between males based on such variation in their calling song. Some work has shown that a male's size or age may be an important determinant of his mating success (Zuk 1987, 1988; Simmons 1988a, 1988b), but it is not clear if information in the calling song can provide reliable cues to females about these characters. The calling song also functions in the maintenance of territories resulting in the regular spacing of calling males in the field (Campbell and Shipp 1979; Cade 1981; Evans 1983; Bailey and Thiele 1983). It might be predicted that male-male competition should be most intense in dense aggregations, and at times when females are most receptive. Changes in the social environment may therefore

'Author to whom all correspondence should be sent.

structure. This study examines several factors that might influence

variation in the calling song of the northern fall field cricket, Gryllus pennsylvanicus. Male age and mass and their influ- ence on calling song parameters were examined in the labora- tory. Field recordings of males at different times of the day and at different densities were also compared to determine how social competition between males affects song structure.

Methods of study The northern fall field cricket, G. pennsylvanicus, is sexually mature

in the Niagara region from mid-July until late October. The species is univoltine and overwinters in the egg stage. All specimens used in this study were captured in the field between 7 September and 14 October 1989.

EfSects of age and mass on song structure Experimental subjects were captured as either adults or late-instar

nymphs. Individuals were isolated in the laboratory and placed in 500-mL plastic containers and provided with purinaB cat chow as food. Water was available in cotton-plugged glass vials. Males were

Printed in Canada / Imprim6 au Canada

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Pulse Chirp Duration

lnterchirp Interval

0.5 Seconds

FIG. 1. A spectrogram produced using the Macintosh IIx speech lab showing the temporal patterning of Gryllus pennsylvanicus song structure.

TABLE 1. The results from linear regressions of temperature and song parameters for both field (n = 74) and laboratory (n = 2 1) populations

Pulse rate Pulses per chirp Interchirp interval Chirp duration

r t P r t P r t P r t P

Field 0.6 6.2 0.0001 -0.12 1.0 0.31 -0.4 3.7 0.0005 -0.6 5.9 0.0001 Laboratory 0.4 2.1 0.05 -0.3 1.3 0.21 -0.6 3.0 0.007 -0.06 0.3 0.80

maintained in the laboratory under a 12 h L : 12 h D cycle and a temperature of 22.1 f 1.2"C. All males were at least 7 days past eclosion prior to testing to ensure reproductive maturity (Solymar and Cade 1990).

Song recordings from individual males were collected using a digi- tal signalling process network (DSPN) developed by the electronics shop at Brock University. The DSPN is equipped with a five channel microphone amplifier module. The inputs to this amplifier module are five microphone elements (ARCHER electret No. 270090PC), each positioned inside a parabolic shell (radius 14 cm). This shell reduces phase shift cancellation by directing the sound to a single point source. Each individual male was placed in a Plexiglas container (50 x 40 mm) with a wire mesh top and ample food and water for the duration of the recording. Each container was placed beneath a microphone in a separate sound recording chamber to eliminate cross- channel interference. The controlling computer program recorded subsequent cricket song using the RC-filtered output of the amplifier module, and measured the duration in time between pulse envelopes. This provided information on pulse rate, number of pulses per chirp, chirp duration, and interchirp interval (see Fig. 1). All DSPN record- ings required at least 10 000 pulses to be included in the analysis. All males were weighed prior to any song recorded using a Mettler electronic balance (model BB240). The effect of age on song structure required initial and final DSPN recordings because most males were field captured adults and only relative age was known. Males were recorded at least twice over their lifetimes. A mean of 14 days sepa- rated initial and final recordings.

males recorded in this study were therefore categorized into two general spacing patterns, clumped and isolated. Clumped was defined as two or more calling males within 10 m of each other. Isolated was defined as a single calling male separated from other callers by a distance greater than 20 m. Three minutes of calling song were recorded for 74 males under either isolated (n = 37) or clumped (n = 37) conditions. Ground air temperatures were taken prior to each recording.

A Macintosh IIx equipped with a GW instruments MacSpeech Lab I1 package was used to analyse field recordings of cricket song. This produces a spectograph of the frequency, amplitude, and durational characteristics of the song emitted by the cricket, displaying the number of pulses per chirp, interchirp interval, and chirp duration. From the field recordings, three 10-s subsamples were chosen at random. Means for pulse rate, number of pulses per chirp, interchirp interval, and chirp duration were then calculated for each male.

Data analysis All data were ln(x) transformed prior to the use of parametric tests

for significance. X 2 tests for normality showed all such transformed variables to be normally distributed. Field collected data were analysed using MANOVA. All four song parameters were entered as variables, with time of day and spacing pattern as factors. Temperature was entered as a covariate. The effect of age on song structure was tested using paired two-tailed t tests. Pearson product-moment correlations examined the relationships between individual song parameters, and between male mass and song structure.

Spatial and temporal efSeects on song structure Results Song recordings in field populations of G. pennsylvanicus were T~~~~~~~~~~ and song structure

collected using a Dan Gibson parabolic microphone (model P200) M~~~ temperature in the laboratory was 2 2 ~ + 1 . 2 0 ~ with connected to a Sony Walkman tape recorder (model WM-F46). All a range of 20.6-240C. Mean temperature in the field was song recordings were collected between 10:OO and 12:OO (n = 24) or between 22:OO and 24:OO (n = 50). The areas sampled were mostly 16.6 + 3.7"C, with a range of 10-24°C. Pulse rate and inter- short-grass fields such as the university campus, school yards, and chip interval were significantly correlated with temperature athletic fields. French et al. (1986) demonstrated that calling male in both laboratory and field ~ o ~ u ~ a t ~ o ~ ~ . rate increased G. penn,yylvanicus in short-grass fields have a nonrandom clumped and interchirp interval decreased with increasing temperature distribution with a mean of 10.3 m separating callers. The sampled (Table 1). Chirp duration was negatively correlated with tem-

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TABLE 2. Comparison of initial and final DSPN song recordings testing the effects of age on the temporal patterning of song structure

Male age

Song parameter Initial Final t P

Pulse rate (no. 1s) 44.3 + 15.7 46.5 f 17.3 -0.4 0.67

Pulses per chirp 3.8 f 0.5 4.0 f 0.7 -1.2 0.23

Interchirp (ms) 667.5 f 141.3 677.3 f 182.4 -0.2 0.85

Chirp duration (ms) 129.0 f 21.4 134.7 f 16.8 -1.0 0.34

NOTE: A mean of 14 days separated initial and final laboratory recordings.

perature, but only for the field population. The number of TABLE 3. Pearson product-moment correlation coefficients for male pulses per chirp did not vary with temperature. body mass against G. pennsylvanicus song parameters; also shown are

the intervariable phenotypic correlation coefficients for both laboratory Male age and song structure (upper) and field (lower) song

Table 2 shows results from 21 males with respect to relative male age and song pattern. There was no significant effect of male age on the four song characters examined.

Body Pulse Pulses Interchirp mass rate per chirp interval

Male mass and song structure The mean mass of the males used in the laboratory was

446.8 f 1 13.3 mg. There were no significant relationships between male mass and any of the song-structure parameters measured (Table 3).

Time of day, male spacing patterns, and song structure Pulse rate and chirp duration varied with time of day (Table 4).

Males had faster pulse rates and shorter chirp durations during the morning hours. Pulses per chirp and interchirp interval were not affected by time of day. Interchirp interval did vary with spacing pattern, with isolated males having greater intervals between chirps. None of the other three parameters were affected by spacing pattern. There was no interaction between time of day and spacing pattern for any of the song parameters.

Intervariable phenotypic correlations Chirp duration was negatively correlated with pulse rate and

positively correlated with number of pulses per chirp, in both field and laboratory populations (Table 3).

Discussion The results presented here show temperature to have a sig-

nificant effect on the calling song of G. pennsylvanicus. Pulse rates increased and interchirp intervals decreased with increasing temperatures, both in the field and in the laboratory. Chirp duration was found to be negatively correlated with increasing temperature in the field. Similar data were reported for another chirping field cricket, G. bimaculatus, where temperature also affected pulse rate and chirp duration, but not the number of pulses per chirp (Doherty and Huber 1983; Doherty 1985). Many studies have reported such temperature dependence in a wide variety of acoustical insects (Walker 1974, 1975; Prestwich and Walker 1981). Temperature will affect the rate at which pulses are produced and thereby to a large extent determine the temporal effects observed in G. pennsylvanicus song structure.

The song parameters studied here did not vary with relative male age. Zuk (1987, 1988) found that older males had greater pairing success than younger males in the field crickets G. veletis and G. pennsylvanicus, and similar results were

Pulse rate -0.02

Pulses per chirp -0.08 -0.26 -0.20

Interchirp -0.36 -0.34 -0.04 -0.22 -0.15

Chirp duration -0.21 -0.79* 0.57* 0.29 -0.68" 0.60" 0.04

found for G. bimaculatus (Simmons and Zuk 1992). The cues that females may use to assess male age in these species are not clear. No variation in song structure parameters was found with increasing male age for G. integer (Souroukis et al. 1992), but in G. bimaculatus the variability in syllable rate within chirps was found to increase with male age. There may be variation, therefore, in the finer structure of male calling song that conveys information related to age (Simmons and Zuk 1992).

Male body mass also had no effect on any of the song parameters examined in this study. Simmons (1988b) reported that larger males of G. bimaculatus had higher intensities and slower chirp repetition rates than smaller males. Laboratory studies demonstrated heritable variation for male body size (Simmons 1987b), and larger males were preferred by females who had increased fecundity and offspring fitness (Simmons 1987a, 1988b). Field-collected data, however, have shown no relationship between male size and pairing success for this species (Simmons and Zuk 1992).

The results from this study did show temporal variation in male calling song structure. Morning time calling males had faster pulse rates and shorter chirp durations than did night- time callers. Pulse rate is significantly negatively correlated with chirp duration in this species, with faster pulse rates resulting in shorter chirps. Since data were corrected for temperature, the increased pulse rate in the morning cannot be explained as a simple temperature effect. Walker (1983) described different patterns of male calling behaviour and hypothesized that males should call at times when females are most receptive to mating. Males might be expected to invest

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TABLE 4. Effects of time of day and male spacing pattern on G. pennsylvanicus song structure in the field

Song parameter

Pulse rate Pulses per chirp Interchirp Chirp duration

1o:oo-12:oo Isolated 38.2 f 7.0 3.3 f 0.6 410.9 f 146.7 87.9 f 27.4 Clumped 36.2 f 4.3 3.5 f 0.1 286.9 f 50.7 97.1 f 9.6

22:OO-24:OO Isolated 32.6 f 5.6 3.5 f 0.4 547.4 f 248.4 107.4f 17.1 Clumped 30.2 f 3.7 3.4 f 0.3 427.6 f 115.0 115.0 f 18.5

Statistical values Time of day 7.03" 0.06 2.34 4.80" Spacing 1.13 0.02 14.5** 1.44 Interaction 0.60 1.96 0.48 1.05

NOTE: Shown are the means f SD for each song parameter, F values, and the level of significance * p < 0.05 ** p < 0.0001

more energy in calling song at these times of peak female acoustic signalling. Females may be biased towards, and mate receptivity. French and Cade (1987) have demonstrated that more frequently with, males having a more energetic and (or) in 6. pen~sylvanicus male calling and mating behaviour are less obscured calling song under such conditions. closely coupled for approximately 3 h around sunrise. Changes in calling song during the morning hours may therefore be associated with increased male' competition during the period of greatest female availability.

Gryllus pennsylvanicus also showed variation in calling song with respect to spacing patterns in the field. Clumped males had shorter intervals between chirps. Calling song not only affects conspecific females but also conspecific males. Several studies have demonstrated the significance of acoustic communication in male spacing patterns in several groups of Orthoptera (Morris 197 1 ; Campbell and Shipp 1979; Bailey and Thiele 1983). Within aggregations, males may try to out- compete or mask the calling songs of neighbouring males and thereby attract more females (Greenfield and Shaw 1983). Such increased energy investment in calling song may be reflected in faster pulse rates or, as is suggested in this study, in shorter interchirp intervals. Males of the katydid Mygalopsis marki showed similar variations in song pattern with social conditions. Aggregated males had shorter interchirp intervals compared with isolated males (Dadour 1989). These varia- tions in certain song parameters may indicate to potential competitors and receptive females the dominance, status, or size of the signaller.

Previous laboratory and field research has shown that in some species of field crickets, females prefer to mate with larger or older males (Simmons 1987b, 1988a; Zuk 1988; Simmons and Zuk 1992). Such preferences may have impor- tant consequences for females, directly or through heritable fitness benefits passed to offspring. However, the results from this study showed that in G. pennsylvanicus, neither male mass nor age had any effect on the song parameters measured. Considerable variation in song pattern in G. pennsylvanicus was revealed, however, with respect to both time of day and male spacing densities. Males exhibited increased energy invest- ment in calling during the morning hours and when in clumped distributions. Moreover, clumped males recorded during the morning hours had the shortest interchirp intervals, supporting the idea that at times of maximum male competition and female availability, males display the greatest expenditure in

Acknowledgements This research was supported by the Natural Sciences and

Engineering Research Council of Canada (grant No. A6174 to William H. Cade), and by Brock University fellowships to A.-M. Murray and G. Rowell. W.H. Cade and W.E. Wagner provided helpful suggestions on previous versions of the manu- script. This research was conducted in partial fulfillment of an Honours B.Sc. thesis by M. Ciceran. The DSPN was designed and built by J. Ross, J. Rustenburg, T. MacDonald, A. Struyk, and G. McDonnell, Department of Technical Services, Brock University.

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