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Acoustic Adaptations of Periodical Cicadas (Hemiptera: Magicicada)

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Blackwell Publishing LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066© 2006 The Linnean Society of London? 2006 90? 1524 Original Article PERIODICAL CICADAS U. OBERDÖRSTER and P. R. GRANT Biological Journal of the Linnean Society, 2007, 90, 15–24. With 1 figure Acoustic adaptations of periodical cicadas (Hemiptera: Magicicada) UTA OBERDÖRSTER† and PETER R. GRANT* Department of Ecology and Evolutionary Biology, Princeton University, Princeton NJ, 08544-1003, USA Received 14 March 2005; accepted for publication 15 January 2006 We studied the trade-off between traits that function in mate attraction and those that function in enemy avoidance by contrasting features of acoustic communication in cicadas differentially at risk to predators in the same envi- ronment. Two genera of North American cicadas were studied: Magicicada and Tibicen. Magicicada species of peri- odical cicadas, with 17-year life cycles, seek mates in dense aggregations of calling males that are made possible by the relative ineffectiveness of predators to control their numbers. During the breeding season, Magicicada are so abundant that they satiate their predators. From their relative freedom from predation, it is to be expected that traits for attracting mates are emphasized in Magicicada compared with the more solitary genus Tibicen, which reproduce at much lower densities. Males of solitary species are expected to sing more loudly and at low pitch because both features enhance long-distance transmission. These two features were confirmed by measurement. Magicicada septendecim appears to be the most divergent species, evolutionarily, in terms of an unusually sharply tuned sound resonating system, low resonant frequency, and quietness of its song that cannot be entirely explained by body size. These characteristics represent adaptations to the problem of communicating unambiguously to females at close range in a loud and heterogeneous sound environment. Sensitivity to predators, parasitoids, and congeneric species may also have shaped the evolution of their communication systems. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 90, 15–24. ADDITIONAL KEYWORDS: Helmholtz equation – mate acquisition – predation risk – quiet songs – resonant frequency – sharp tuning – Tibicen – tympani. INTRODUCTION cicadas can reach to over 3.5 million per hectare (Dybas & Davis, 1962; Leonard, 1964), and such abun- Advertising or searching for mates is usually accom- dance makes per capita risk of predation extremely panied by a risk of attracting predators and parasi- low (Karban, 1982). These densely aggregated species toids (Gwynne, 1987; Zuk & Kolluru, 1998; Cooley, are expected to have traits that are advantageous in 2001); therefore, a trade-off is expected between traits mate attraction relatively unmodified by risk of pre- that function in mate attraction and those that func- dation, whereas solitary species in the same environ- tion in enemy avoidance. The trade-off is likely to vary ment, such as Tibicen species, should display among related species that are differentially at risk. adaptations that reduce the risk of being eaten or par- North American cicadas are interesting in this regard asitized. One set of traits in the periodical cicada spe- because adult cicadas in the genus Magicicada, cies (Magicicada) has been identified and labelled emerging at 13- or 17-year intervals, are so abundant ‘predator foolhardy’ (Lloyd & Dybas, 1966). All mem- in their 4–6-week breeding season (Dybas & Davis, bers of the genus fly slowly and are easily approached 1962; Dybas & Lloyd, 1974) that they satiate their on the vegetation (White et al., 1983). Lack of wari- predators (Lloyd & Dybas, 1966; Karban, 1982; Will- ness and insensitivity to disturbance may be advanta- iams & Simon, 1995). Densities of emerging periodical geous during the frequent interactions that occur during mate seeking and courtship (Lloyd & Dybas, 1966; Grant, 2005). Tibicen, on the other hand, and *Corresponding author. E-mail: [email protected] †Current address: School of Law, Vanderbilt University, other nonperiodical cicada species are far more wary Nashville, TN 37235, USA. and fly faster (Oberdörster & Grant, 2006a). © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 90, 15–24 15 16 U. OBERDÖRSTER and P. R. GRANT In the present study, we ask whether features of has been described as an energy storage mechanism acoustic advertising reflect the altered trade-off that releases energy as the ribs buckle inwards between attracting mates and avoiding enemies. We sequentially upon tymbal muscle contraction (Bennet- do so by contrasting two species of gregarious Magici- Clark, 1997). Buckling causes pressure changes in the cada species with two species of solitary Tibicen spe- abdominal cavity, and sound leaves the cavity through cies living in the same environment. a pair of tympani. Tensor muscles modulate the ampli- Individual Magicicada males gain a collective tude (Hennig et al., 1994), as does the opening and advantage in long-distance transmission by calling closing of the opercula overlying the tympani through simultaneously in dense aggregations. Visual cues changes in the posture of the abdomen (Young, 1990; also stimulate mating, but songs are more critical Bennet-Clark & Young, 1992). (Dybas, 1969). Being physically close to other males, The abdominal cavity and tymbals act as a coupled cicadas experience strong competition for mates. This Helmholtz resonator, radiating sound through the competition has been studied in male Magicicada acoustically transparent tympani (Bennet-Clark & septendecim. Males acoustically interfere with other Young, 1992). Two measurable properties are of value approaching males while courting females (Marshall when comparing species. The first is the resonant fre- & Cooley, 2000; Cooley & Marshall, 2001, 2004). quency (f0). This is related to the volume (V) of the cav- Three species of the genus Magicicada, members of ity and the area (A) and length (L) of the aperture the -decula, -decim, and -cassini groups, are synchro- (tympani) by the general equation: nous and coextensive over the majority of their fc0 =( /2p ). ( ALV / . ) (1) respective geographical ranges in North America (Alexander & Moore, 1962; Williams & Simon, 1995; The symbol c is the speed of sound in the fluid, taken Marshall & Cooley, 2000; Cooley & Marshall, 2001). as 340 m/s. For two tympani, as in cicadas, A is the They overlap broadly in the use of habitat, although combined area of the two tympani and L is 1.7 times some degree of habitat partitioning occurs by tree spe- the radius of one of them (Bennet-Clark & Young, cies, soil type, and oviposition site (Dybas & Lloyd, 1992). The second property is a so-called quality factor, 1974; White, 1980). Given loud chorusing at the same Q. This measures the effective increase in the ampli- time from the same vegetation, there should be a tude of the vibration at resonance and the rapidity selective advantage for males broadcasting unambig- with which it changes. It is given by the formula: uous signals to females against a loud and heteroge- 33 neous background. Ambiguity would be minimized QLVA=2p ( / ) (2) and effectiveness maximized if songs have a species- Q is a measure of the sharpness of its tuning, and is specific fundamental frequency (Alexander & Moore, equal to the resonant frequency divided by the band- 1958; Simmons, Wever & Pylcka, 1971a; Huber et al., width at 3 dB below maximum (Bennet-Clark & 1990; Hennig et al., 1994; Marshall & Cooley, 2000; Young, 1994). A sharply tuned resonator has a high Q. Cooley et al., 2001) produced from sharply tuned res- It does not scale with body size and is a constant of the onators (Bennet-Clark & Young, 1992, 1994). Calling resonator design. A similar sharpness of tuning is songs of three species of Magicicada are known to dif- potentially available to all species (Bennet-Clark & fer in frequency, length, and temporal patterning Young, 1994); therefore, differences among species in (Alexander & Moore, 1958; Simmons et al., 1971a; Q-values can be interpreted as different evolutionary Cooley & Marshall, 2001). Songs of males of the soli- solutions to problems of communication. tary Tibicen species in the same environment are sim- Resonant frequency (f0) increases with area of the ilarly differentiated. In addition, they are expected to tympani and decreases with volume cavity and hence sing more loudly and at low pitch because both fea- with abdomen size. Since area (L2) increases more tures enhance long-distance transmission and com- slowly with body size than does volume (L3), the net munication with potential mates (MacNally & Young, effect of an increase in body size is a decrease in fre- 1981). quency. Bennet-Clark & Young (1994) confirmed the expected relationship with data from 17 species. The correlation between dominant frequency and body ACOUSTIC FEATURES OF CICADAS length as an index of body size was 0.857. The inter- The mechanics of a male cicada’s loud song have been specific comparison assumes that sound-producing extensively investigated (Pringle, 1954; Young & structures are similar in all species, and this appears Josephson, 1983; Young, 1990; Bennet-Clark & Young, to be true (Bennet-Clark & Young, 1994; Fonseca & 1992, 1994; Fonseca & Popov, 1994; Hennig et al., Popov, 1997). It also assumes a constant relationship 1994; Young & Bennet-Clark, 1995; Fonseca & Hen- between tympani and abdominal cavities, so that nig, 1996; Bennet-Clark, 1997). Sound is produced by tympanum size can be ignored when relating song a pair of ribbed tymbals on the abdomen. The tymbal frequency to body size. However, data provided by © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 90, 15–24 PERIODICAL CICADAS 17 Bennet-Clark & Young (1992; tables 1, 3) show that body length of M. cassini on the basis of their relative this is not correct. The present study was designed to proboscis lengths given by Dybas & Lloyd (1974). Call- investigate the relationship between tympani and ing songs (N = 1) of all four species, as well as body size, and f0 and Q-values.
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