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Acoustic Evolution in Crickets: Need for Phylogenetic Study and a Reappraisal of Signal Effectiveness

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Acoustic Evolution in Crickets: Need for Phylogenetic Study and a Reappraisal of Signal Effectiveness Anais da Academia Brasileira de Ciências (2004) 76(2): 301-315 (Annals of the Brazilian Academy of Sciences) ISSN 0001-3765 www.scielo.br/aabc Acoustic evolution in crickets: need for phylogenetic study and a reappraisal of signal effectiveness LAURE DESUTTER-GRANDCOLAS and TONY ROBILLARD Muséum National d’Histoire Naturelle, Département Systématique et Evolution USM601 MNHN & FRE2695 CNRS, Case Postale 50 (Entomologie), 75231 Paris Cedex 05, France Manuscript received on January 15, 2004; accepted for publication on February 5, 2004. ABSTRACT Cricket stridulums and calls are highly stereotyped, except those with greatly modified tegmina and/or vena- tion, or ‘‘unusual’’ frequency, duration and/or intensity. This acoustic diversity remained unsuspected until recently, and current models of acoustic evolution in crickets erroneously consider this clade homogeneous for acoustic features. The few phylogenetic studies analyzing acoustic evolution in crickets demonstrated that acoustic behavior could be particularly labile in some clades. The ensuing pattern for cricket evolution is consequently extremely complex. We argue that: (1) phylogeny should always be considered when analyz- ing acoustic evolution, whatever characters are considered (signals, stridulums or behaviors). Consequently, future studies should be devoted to entire clades, and not consider isolated taxa; character and character state definitions should allow significant reconstructions of character evolutionary transformations; and homolo- gies should be carefully defined for all characters, including behavior. (2) The factors responsible for song effectiveness should be reconsidered and hypotheses on their potential influence on signal evolution tested jointly by phylogenies (for example, to assess correlated transformations of acoustic and ecological features), and population studies (for example, to correlate call range and population structure, or test the predation risk associated with a signal structure). Better understanding these points should help clarifying acoustic evolution in crickets. Key words: acoustic communication, evolution, phylogeny, calling song effectiveness, crickets. INTRODUCTION phylum. Sound production is most often achieved by stridulation and the emitted sounds are usually Acoustic communication occurs in vertebrates and considered highly stereotyped compared to those of arthropods, and both groups possess specific organs vertebrates (Dumortier 1963a, Fletcher 1992). for the emission and reception of acoustic signals. In crickets, the stridulatory apparatus is located These organs are constrained by the basic morpho- on the forewings (FWs), and crickets sing by rubbing anatomical features of each phylum, and this in turn their raised FWs together. Sound is produced when determines the main characteristics of the signals the right file hits the left plectrum during FW closure that each phylum is able to emit (Fletcher 1992). and is radiated by the mechanical resonator made of In arthropods, acoustic designs are shaped by the enlarged areas of both FWs (Michelsen and Nocke hard exoskeleton, one of the characteristics of this 1974, Sismondo 1979). Cricket songs are com- Correspondence to: Laure Desutter-Grandcolas monly characterized by their carrier frequency, in- E-mail: [email protected] An Acad Bras Cienc (2004) 76 (2) 302 LAURE DESUTTER-GRANDCOLAS and TONY ROBILLARD tensity and temporal structure (Bennet-Clark 1989). ied of all cricket songs, is considered here for sake The carrier frequency corresponds to the resonant of comparison. frequency of the tegminal resonator and the calling Cricket songs are loud pure tones emitted re- song is most often a loud pure tone (Michelsen peatedly during a limited period of time and charac- 1998). terized by their frequency, amplitude and temporal Crickets are usually considered a homoge- structure (Bennet-Clark 1999). However, an unsus- neous and well-known group and their acoustic evo- pected amount of variation (Fig. 1) has been docu- lution has previously been thought to be relatively mented. straightforward, involving limited possibilities of Cricket calling frequencies usually range be- evolutionary changes from an a priori determined tween 2 and 8 kHz, with one clear dominant fre- ancestral condition (Alexander 1962, Bailey 1991, quency corresponding to the resonance frequency Otte 1992). of FW resonator (Leroy 1966). Frequency varia- However, recent studies have revealed an un- tion may occur in the form of bandwidth, the occur- suspected diversity for all the characters involved rence of broad modulation, or extreme frequency in acoustic communication, stridulums, signals and values. The former parameter has been implicitly associated behaviors (Huber et al. 1989, Desutter- acknowledged since a long time, even though its Grandcolas 1995a, 1997a, 1998a, b, Preston- significance in term of signal propagation has not Mafham 2000, Bailey et al. 2001, Desutter- been clarified yet. Only recently have frequencies Grandcolas and Bland 2003), and they brought new beyond 12 kHz been recorded in the calls of several information on the behavioral ecology of diverse Eneopterinae (Desutter-Grandcolas 1997a, 1998a, cricket species not considered to date in current Robillard and Desutter-Grandcolas in prep.). Fur- cricket studies and literature. In the same time, ther, broad frequency modulations, considered im- phylogenetic analyses have resulted in unexpected probable in cricket songs (Alexander 1962, Dumor- evolutionary patterns that contradict current models tier 1963b), occurred convergently in eneopterines of cricket acoustic evolution (Desutter-Grandcolas and phalangopsids (Desutter-Grandcolas 1998a). 1997b, c, Huang et al. 2000, Shaw and Herlihy Cricket songs are most often very loud (Du- 2000, Desutter-Grandcolas and Robillard 2003, mortier 1963b, Leroy 1966, Bennet-Clark 1989). As Robillard and Desutter-Grandcolas 2004). stated by Alexander (1962, p. 450), ‘‘All modern Here we first draw a general picture of cricket stridulating species – except for a few obviously de- acoustic diversity, contrasting for each attribute cur- generate species – produce this intense, clear sounds rent ideas with recent discoveries. We then present a that only crickets among all animals are able to pro- short reappraisal of current model for acoustic evo- duce with a stridulatory device.’’ (emphasis ours). lution in crickets. Finally, we present promising However soft calls have been recorded in nemobi- cues for cricket evolutionary studies, phylogeny use ines (Bennet-Clark 1989), eneopterines (Desut- and effectiveness investigation. ter-Grandcolas 1997a) and phalangopsids (Desutter- Grandcolas 1998b). Calls with amplitude modu- DIVERSITY OF ACOUSTIC FEATURES IN CRICKETS lation of the carrier frequency (buzzing sounds, Gerhardt 1998), have also been described in 1. Signals hapithine Podoscirtidae (Desutter-Grandcolas and Only male crickets sing, mostly in the frame of Bland 2003). reproduction, and a cricket repertoire may include Temporal parameters are the most variable fea- many different songs (Alexander 1962, Boake 1983, tures of calling songs. A cricket call commonly Desutter-Grandcolas 1998c, Su and Rentz 2000). comprises pulses (or syllables) that are emitted dur- Only calling, the most widespread and the best stud- ing each wing closure. The pulses are either emit- An Acad Bras Cienc (2004) 76 (2) ACOUSTIC COMMUNICATION IN CRICKETS 303 kHz dB kHz -45 -50 dB 20 -50-55 -60 B A -65 -70 -75 -80 10 -85 -90 -95 -100-100 -105 0 2 4 6 8 10 12 14 16 18 20 kHzkHz 0.2 0.4 Time (s) 0 10 20 dB -35 20 kHz -40 dB -40-45 -50 -55 D C -60 -65 10 -70 -75 -80-80 -85 -90 -95 kHz 0 2 4 6 8 10 12 14 16 18 20 kHz 0.5 1 Time (s) 0 510 kHz dB 20 -55 -60-60 -65 -70 F E -75 -80 10 -85 -90-90 -95 -100 -105 -110 0 2 4 6 8 10 12 14 16 18 20 kHz kHz 0.5 1 1.5 0 Time (s) dB 10 20 kHz 6 H G 3 0 kHz 260 520 780 Time (ms) kHz 6 dB J I 3 kH 0 800 1600 Time (ms) z Fig. 1 – Diversity of cricket advertisement signals. Spectrogram and power spectrum of Eneoptera surinamensis (A, B), Xenogryllus marmoratus (C, D), Agnotecous yahoue (E, F), Paragryllodes campanella (G, H) (modified from Desutter-Grandcolas 1998b), and Orocharis fulvescens (I, J) (modified from Desutter-Grandcolas and Bland 2003). ted continuously (trills) or discontinuously (chirps); This short enumeration of peculiar features chirps in turn vary indefinitely, with regular or ir- shows that the cricket clade emits more diversified regular pulse period and rate. Maximal impulse du- songs than previously thought. It is unclear how this ration has been assessed on the basis of efficiency variability affects the song effectiveness. criteria and estimated at less than 50 ms (Bennet- Clark 1989). Similarly, an optimal duration of 30 to 2. Cricket Stridulum: Structural 60 ms has been hypothesized (Otte 1992). However, and Functional Diversity syllables 3 to 6 times longer are emitted by various The diversity of cricket stridulum should be ana- cricket species (Desutter-Grandcolas 1998b). lyzed from a structural and a functional point of An Acad Bras Cienc (2004) 76 (2) 304 LAURE DESUTTER-GRANDCOLAS and TONY ROBILLARD view, because the vibratory properties of a stridu- tic resonator in Gryllus campestris (Nocke 1971, lum are directly related to FW morphology and ul- Michelsen and Nocke 1974), but other radiating trastructure (Michelsen and Nocke 1974). Struc- cells are known in Oecanthus spp. (Sismondo 1979) turally, a cricket stridulum comprises modified FW or have been hypothesized in modulating
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