Female crickets are driven to fight by the male courting and calling songs

Animal Behaviour 77 (2009) 737–742

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Female crickets are driven to fight by the male courting and calling songs Jan Rillich, Edgar Buhl, Klaus Schildberger, Paul A. Stevenson*,1 ¨t Leipzig Biologie II, Universita

a r t i c l e i n f o Article history: Received 5 July 2008 Initial acceptance 15 September 2008 Final acceptance 7 December 2008 Published online 18 January 2009 MS. number: 08-00430R Keywords: aggression agonistic behaviour competition cricket Gryllus campestris polyandry resources sexual selection

Crickets have traditional sex roles, where males compete aggressively for access to selective polyandrous females. However, in a laboratory experiment, we found that normally nonaggressive female Gryllus campestris fought each other vigorously in the presence of a courting male, resulting in a dominant female that gained a greater probability of receiving the spermatophore. Female–female fights included the same series of characteristic actions known from male–male fights, which demonstrates that the females can perform the full repertoire of agonistic actions except for the production of the aggressive rival song. Since females remained nonaggressive towards each other in the vicinity of a muted male, but were induced to fight each other in the complete absence of a male by the auditory experience of the courtship song, this song is both sufficient and necessary to induce female competition for males. Calling song was as effective as courtship song at inducing female aggression, whereas rival song was least effective. We therefore speculate that the calling and courtship songs may signal a male’s resource value. Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

While in most species males compete aggressively for access to females, it is unusual for females to compete for males (Andersson 1994). Although females are known to interact aggressively during the breeding season or when they are highly receptive (red-winged blackbirds, Agelaius phoeniceus: Hurly & Robertson 1984; bonobos, Pan paniscus: Hohmann & Fruth 2003; red deer, Cervus elaphus: Bebie´ & McElligott 2006), it is mostly unclear whether they compete for food or territories (reviewed in Rosenqvist & Berglund 1992; Jennions & Petrie 1997) or mating opportunities (lion tamarins, Leontopithecus rosalia: French & Inglett 1989; green poisondart frog, Dendrobates auratus: Summers 1989; cichlid fish, Lamprologus ocellatus: Walter & Trillmich 1994; capuchin monkey, Cebus apella: Linn et al. 1995). Most studies of female contests have focused on ‘sex role-reversed’ systems, where male parental investment is comparatively high (reviewed in Gwynne 1991; katydids, Anigozanthos manglesii: Gwynne & Simmons 1990; blenny, Salaria pavo: Almada et al. 1995; sand goby, Pomatoschistus minutus: Forsgren et al. 1996). More recent studies, however, have addressed the consequence of female aggression for reproductive success in animals with conventional sex roles (reviewed in Cunningham & Birkhead 1998; birds: Slagsvold & Lifjeld 1994;

* Correspondence: P. A. Stevenson, Universita¨t Leipzig, Biologie-II, Talstr. 33, D-04103 Leipzig, Germany. E-mail address: [email protected] (P.A. Stevenson). 1 P. A. S. is the leading writer.

European starling, Sturnus vulgaris: Sandell & Smith 1997; pipefish, Syngnathus typhle: Berglund & Rosenqvist 2001; prairie vole, Microtus ochrogaster: Bowler et al. 2002). Such investigations suggest that females should compete for males not only when the operational sex ratio is female biased or when males have similar parental investments, but also when winning secures mating opportunities with high-quality, high-ranking males (reviewed in Berglund et al. 1993; European lobster, Homarus gammarus: Debuse et al. 1999; chacma baboon, Papio cynocephalus ursinus: Palombit et al. 2001). Thus, female contests for males should be far more common than has been documented. We evaluated female aggression in the cricket Gryllus campestris. These crickets have conventional sex roles whereby males produce the calling song to attract females (Zuk & Simmons 1997), which are choosy (Hedrick 1986; Bateman et al. 2001), and fight with other males to secure and guard them (Simmons 1986; Wynn & Vahed 2004). Females are mute but, like males, may occupy burrows and ‘defend them against conspecifics’ (Hissmann 1990). Females are not, however, known to compete aggressively for mates in the field (see also Rost & Honegger 1987; Ritz & Ko¨hler 2007). Under laboratory conditions, female crickets, in contrast to males, rarely interact and usually avoid contact, but will compete aggressively for food when starved (Adamo & Hoy 1995; Nosil 2002). Even so, the agonistic behavioural repertoire of females seems more limited than males: Adamo & Hoy (1995) did not observe mandible spreading, mandible interlocking or grappling in

0003-3472/$38.00 Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2008.12.009

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a detailed videotape analysis of Gryllus bimaculatus. Although animal contest structure need not always be the same in the two genders (see e.g. Draud et al. 2004 on cichlids Herichthys cyanoguttatum), the observation that drugs, such as the opiate antagonist naloxone, dramatically increase the incidence of mandible spreading in G. bimaculatus females (Dyakonova et al. 2002) indicates that there may be natural circumstances where female crickets show the same agonistic traits as males. Since the aggressive motivation of an animal can be elevated by the presence of a valuable resource (Enquist & Leimar 1987), such as food in crickets, we speculated that female crickets may also be induced to compete aggressively by the presence of a male, a potential mate and provider of a nutritious spermatophore (Simmons 1988a, b). We therefore compared interactions between weight-matched adult females in an arena in the absence and presence of a mature adult male, noting in particular the frequency of mandible spreading and physical fighting. Since male crickets may signal their quality by singing (e.g. Wagner & Reiser 2000), we also evaluated female aggressiveness in the presence of a muted male and with playback recordings of the three male songs: the calling song, which attracts females by evoking phonotaxis, the courtship song, which guides the female and triggers mounting, and the aggressive rival song, which is produced when the male confronts, and defeats, a conspecific male (Huber 1962). METHODS Experimental Animals Male and female G. campestris were collected in their last nymphal stage from south-facing sloping grassland west of Leipzig city, Saxony, Germany, during April. The sexes were kept physically and acoustically separated in plastic containers (25  40 cm and 28 cm high), with at most 30 animals in each, at Leipzig University under standard conditions (22–24  C, 40–60% relative humidity, 12:12 h light:dark regime, see Staudacher & Schildberger 1998). The experimental animals were returned to their natural habitat after the experiment. All experimental procedures are in accord with animal welfare regulations in Germany. Evaluation of Aggression We staged all interactions in an equilateral triangular arena fashioned from clear Perspex (each side 25 cm long and 7 cm high) and with a sand-covered floor. A centrally positioned, ‘Y’-shaped door, constructed from three individually removable squares (65  65 mm) of grey opaque plastic, served to divide the arena into three corners of equal area. We placed pairs of previously isolated, weight-matched, adult females in separate corners, and, when required, a male in the third corner, and left the animals for 5 min to adapt to the new surroundings. The doors were then opened manually and interactions between the animals were noted and videotaped (Sony DCR-TRV 130 Digital8 Camcorder) for a continuous observation period of 5 min, using focal animal sampling and continuous event-sampling rules. As a measure of female aggressiveness we noted the frequency of occurrence of the following key agonistic behaviours (see Stevenson et al. 2000), defined as the percentage of contests in which they occurred at least once. Nonaggressive: after initial antennal contact no further interaction occurred. Antennal fencing: after initial antennal contact the two females turned towards each other and lashed their antennae while maintaining a raised body posture. Mandible spreading: the two crickets faced each other and one or both broadly spread its mandibles. Physical fighting: the two females interlocked their mandibles, pushed and occasionally bit

the opponent. These aggressive behavioural acts are not mutually exclusive and can be reliably identified even by inexperienced observers. In our experiment the scores of two independent observers were in full agreement. Experimental Groups For all interactions, we used mature adults, taken 7–28 days after the final moult and transferred to individual glass jars at least 24 h before the interactions by which time influences of prior social contact on aggression are extinguished (Adamo & Hoy 1995; Hofmann & Stevenson 2000; Stevenson et al. 2005). Supporting this, a comparison of the aggressiveness of females that had no previous contact with a male with that of females that had had social contact with a male on the previous day revealed no significant differences in the frequency of occurrence of the evaluated elements of aggression (Fisher’s exact test: N ¼ 47, P ¼ 1.0 for antennal fencing, 0.76 for mandible spreading, 0.72 for physical fighting). Data from these two female categories were thus pooled. In total we analysed the fighting behaviour of 282 adult female and 66 adult male crickets. In some cases a female was used in more than one interaction, but never on the same day, and never against a previous contestant, as a further precaution against influences of previous agonistic experience. The two contestants were always matched for weight (weight difference < 5%) and their interactions were recorded in the arena under the following experimental conditions. (1) Control: females in the absence of males or the male song (N ¼ 36 pairs). (2) Male: females in the presence of a courting male (N ¼ 47 pairs). (3) Mute: females in the presence of a courting male that was prevented from producing the courtship song by sticking the forewings together with a water-soluble adhesive, which was later removed (N ¼ 36 pairs). (4) Mute þ song: females in the presence of a muted courting male and a played-back recording of a male cricket’s courtship song (N ¼ 27 pairs). For the latter, long uninterrupted bouts of courtship songs were recorded from a randomly selected singing male with a high-fidelity microphone (ECM MS 907, Sony) on a tape recorder (WM-D6C, Sony) and replayed through a tweeter loudspeaker (Conrad Electronics, Wernberg, Germany) placed 15 cm from the arena (70–80 dB). The same methods were used to record and present the male’s rival song and calling song (see below). (5) Courtship song: females presented with the played-back recording of a male’s courtship song, in the absence of a male (N ¼ 26 pairs). (6) Rival song: females presented with a played-back recording of a male’s rival song, in the absence of a male (N ¼ 42 pairs). (7) Calling song: females presented with a played-back recording of a male’s calling song, in the absence of a male (N ¼ 25 pairs). (8) White noise: as an acoustic control, this group of females (N ¼ 21 pairs) were presented with cyclically repeated bursts of white noise (200 ms on, 800 ms off), generated electronically using standard software (peak 3.2, bias sound creative, Bias Inc., Petaluma, CA, U.S.A.). (9) Male–male: for comparative purposes, we also evaluated the aggressive interactions of weight-matched adult male crickets (N ¼ 33 pairs). Statistics and Data Analysis For statistical tests we used the software package Prism 5 (GraphPad Software Inc., San Diego, CA, U.S.A.). The Fisher’s exact probability test was used to obtain the significance level of the

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differences in the frequency of occurrence of behavioural acts. The Mann–Whitney U test for unpaired data was used to determine the significance of differences in the total duration of aggressive encounters. RESULTS Female–Female Aggression: Control The control interactions between weight-matched females in the test arena within the 5 min observation period were typified by brief antennal contact without aggression (nonaggressive: 78%, N ¼ 36; Fig. 1). Antennal fencing, the key releasing stimulus for male aggression (Hofmann & Schildberger 2001), was observed only occasionally (22%), and this was followed by mandible spreading, which is regarded as a threat display in male interactions (Rillich et al. 2007), in only 17% of cases. Physical fighting, in which both females interlock their mandibles and push each other, was observed only once (3%). Effect of Male Presence More complex interactions were observed when two females were placed in the arena together with a single sexually mature male. In response to a brief contact with either female the male typically produced the characteristic courtship song by stridulating its forewings after which the females turned towards the courting male. In some cases one female mounted the male before coming into contact with the other female, although in most cases (81%, of N ¼ 47) the two females encountered each other before mounting occurred. Females showed elements of aggressive behaviour significantly more frequently towards each other when a male was present than when a male was absent (antennal fencing: 58%; P ¼ 0.002; mandible spreading: 41%; P ¼ 0.029; physical fighting: 21%; P ¼ 0.019; P values from Fisher’s exact test against control, N ¼ 83; Fig. 1). Female aggression towards the male was never observed under these circumstances. In 58% of the female–female contacts in the presence of a male, a clear subordinate loser was established, which avoided further

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contact with the winning, dominant female. In such cases, the winning female copulated and received the male’s spermatophore significantly more frequently than losers (winners: 78%; losers: 15%; Fisher’s exact test: N ¼ 54, P < 0.001). In 7% of cases neither female gained a spermatophore. Muting the males by fixing their forewings appeared to have no detrimental effect on the behaviour of the male towards the females, but the behaviour of the females was now different in that 33% (N ¼ 72 individuals) responded aggressively towards the muted male compared to none towards a singing male (Fisher’s exact test: N ¼ 166 individuals, P < 0.001). With respect to female–female aggression in the presence of a mute male, the frequency of agonistic actions did not differ significantly from that in female–female encounters in the absence of a male (antennal fencing: 42%; P ¼ 0.13; mandible spreading: 22%; P ¼ 0.77; physical fighting: 6%; P ¼ 1.0; P values from Fisher’s exact test against control, N ¼ 72; Fig. 1). Compared to this, females fought significantly more aggressively in the presence of a muted male when a recording of the courtship song was played from an adjacent loudspeaker (antennal fencing: 85%; mandible spreading: 85%; physical fighting: 63%; Fisher’s exact tests against control: N ¼ 63, P < 0.001 in each case; Fig. 1). When the recorded courtship song was played, none of the females responded aggressively towards the muted male, and the incidence of mounting attempts increased significantly from 42% without song to 89% with song (Fisher’s exact test: N ¼ 63, P < 0.001), which is not significantly different to the frequency of female mounting attempts in the intact, singing male group (82%; Fisher’s exact test: N ¼ 74, P ¼ 0.74). Furthermore, in terms of the frequency of occurrence of the key elements of aggressive behaviour, the female fights in the presence of a mute male and song playback were not significantly different to those between males (antennal fencing: 93%; P ¼ 0.69; mandible spreading: 90%; P ¼ 1.0; physical fighting: 66%; P ¼ 1.0; P values from Fisher’s exact test against mute þ song, N ¼ 60; Fig. 1). The total duration of aggressive female–female contests in the presence of a mute male and song playback lasted some 4 s (median, interquartile range, IQR 2–13), which was also in the range of fights between males (median duration 8 s, IQR 5–14; U test: U ¼ 327.0, N1 ¼ 27, N2 ¼ 33, P ¼ 0.079).

100 ***

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Frequency (%)

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Antennal fencing

Mandible spreading

Physical fighting

Behavioural elements Figure 1. The influence of a courting male on female–female aggression. Bars depict female–female interactions for the following conditions: male absence (white bars; control condition, N ¼ 36); presence of a courting male (stippled bars; N ¼ 27); presence of a muted male (hatched bars; N ¼ 36); presence of a muted male and a recorded courtship song (black bars; N ¼ 27). Data for male–male interactions are included for comparison (grey bars; N ¼ 33). Statistically significant differences between control and test groups (Fisher’s exact test) are indicated by asterisks: *P < 0.05; **P < 0.01; ***P < 0.001.

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usually interact aggressively (G. bimaculatus: Adamo & Hoy 1995; Acheta domestica: Nosil 2002). This situation, however, changed dramatically in the presence of a courting male, where female G. campestris then fought vigorously (Fig. 1) and showed the same stereotyped agonistic behaviours that characterize male–male aggression, including antennal fencing, mandible spreading and grappling (Stevenson et al. 2000, 2005; Rillich et al. 2007). Aggression is generally regarded as a behavioural strategy for asserting a claim to a limited resource (Archer 1987) to increase individual fitness and reproductive success (reviewed in Cunningham & Birkhead 1998). Female crickets are known to interact aggressively in the presence of food when hungry (Adamo & Hoy 1995; Nosil 2002), although these interactions did not involve grappling and were hence clearly less aggressive than observed here when competing for a male. We therefore suggest that females fight to secure some resource of potential value in the male’s possession. For example, by driving her rival away, the dominant female was significantly more likely to acquire the courting male’s spermatophore. That some of the winners were unsuccessful in this respect is probably due partly to the confinements of the arena, in which displaced losers could still make contact and mate with the male. The spermatophore of field crickets, although nutritious, is smaller than that of bush crickets, Ephippiger ephippiger, and has accordingly less value (Wedell & Ritchie 2004). Although field crickets are not known to benefit from consuming a single spermatophore, an increase in egg-hatching success can none the less be accrued throughout a female’s sexual life from multiple mates (Simmons 1988a). Similarly, other benefits from polyandry, such as a better chance of receiving sperm from superior sires (Sakaluk et al. 2002), or a reduced risk of gaining incompatible sperm from inbreeding (Rodriguez-Munoz et al. 2008), may also contribute to the value of a male cricket as a resource for which females are willing to compete. Although it can be assumed that all the courting males in this study had a spermatophore, since they had had no sexual interaction for a day and spermatophores are replenished within hours of being spent, the females had no way of telling this as far as we know. This prompts the question as to which attributes signal male resource value and cause aggressive behaviour to become overt in females? Fighting in males is triggered even in the absence of resources by pheromonal (Rence & Loher 1977; Tregenza & Wedell

Effect of Song in Male Absence The females showed no increase in aggressiveness in the absence of a male when presented with regular bursts of white noise from the loudspeakers (antennal fencing: 24%; P ¼ 1.0; mandible spreading: 10%; P ¼ 0.24; physical fighting: 0%; P ¼ 1.0; P values from Fisher’s exact tests against control, N ¼ 57; Fig. 2). However, when a recording of the male courtship song was played through a nearby loudspeaker, the females became highly aggressive towards each other in the absence of a male (antennal fencing: 81%; P < 0.001; mandible spreading: 69%; P < 0.001; physical fighting: 39%; P ¼ 0.001; P values from Fisher’s exact tests against white noise, N ¼ 47; Fig. 2). Similarly, the calling song, which otherwise induces female phonotaxis (Huber 1962), effectively enhanced female aggression (antennal fencing: 84%; P < 0.001; mandible spreading: 80%; P < 0.001; physical fighting: 20%; P ¼ 0.054; P values from Fisher’s exact test against white noise, N ¼ 46; Fig. 2). The rival song, produced by males during aggressive interactions, however, led only to an increased incidence of antennal fencing and was thus far less effective at inducing female fighting (antennal fencing: 57%, P ¼ 0.007; mandible spreading: 24%, P ¼ 0.083; physical fighting: 14%, P ¼ 0.16; P values from Fisher’s exact tests, N ¼ 63; values for mandible spreading and physical fighting were also significantly different to courtship song: P ¼ 0.003, 0.038, respectively, N ¼ 68; Fig. 2). Continuous presentation of courtship song was necessary to keep the females fighting. When we turned it off at the moment of antennal contact, most of the females (N ¼ 24 pairs) did not escalate further than antennal fencing (75%; mandible spreading: 17%; physical fighting: 0%) and broke off without establishing a clear winner or loser. When we turned the song back on, the same females then became significantly more aggressive (mandible spreading: 67%; physical fighting: 29%; Fisher’s exact tests: P ¼ 0.001, 0.009, respectively, N ¼ 48). DISCUSSION Our laboratory observation that confrontations between female G. campestris are normally typified by avoidance behaviour conforms to findings in related species that female crickets do not

100 *** ***

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Nonaggressive

Antennal fencing

Mandible spreading

Physical fighting

Behavioural elements Figure 2. The influence of male cricket song on female–female aggression in the absence of a male. Bars depict female–female interactions in the presence of the following auditory stimuli: patterned white noise (white bars; N ¼ 21); courtship song (black bars; N ¼ 26); calling song (grey bars; N ¼ 25); rival song (stippled bars; N ¼ 42). Statistically significant differences between control (white noise) and test groups (Fisher’s exact test) are indicated by asterisks: *P < 0.05; **P < 0.01; ***P < 0.001.

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1997) and tactile (Adamo & Hoy 1995) information from the antennae, and their ablation produces males that retreat from or court conspecific males (Hofmann & Schildberger 2001). However, whereas female antennal cues can suppress male escape behaviour during copulation (Killian et al. 2006) and also enhance male–male aggression (Otte & Cade 1976), they are alone insufficient to induce female–female aggression. In respect to mate selection at least, female crickets assess male value from multiple cues, including age and novelty of the partner, body scent, size, condition and symmetry, and song quality (Hedrick 1986; Simmons 1992, 1995; Simmons & Ritchie 1996; Bateman 1998; Wagner & Reiser 2000; Holzer et al. 2003; Ivy et al. 2005; Kortet & Hedrick 2005). We found that females remained nonaggressive towards each other in the vicinity of a muted male (Fig. 1), but started fighting in response to a played-back recording of the male courtship song (Fig. 2). We thus conclude that male visual, tactile and olfactory cues are not essential for inducing female competition for males in G. campestris. Female fights were more intense in the presence of a mute male and song playback than in the presence of a naturally singing male. We suspect that this occurred because males stop singing when mounted. Supporting this, when song playback was halted, the females immediately ceased fighting. Thus, the male song can be regarded as a driving, rather than a simple releasing, stimulus. The calling song is significantly less costly to produce than the courtship song (Hack 1998), but is none the less a reliable measure of male quality. In Gryllus integer, females choose males that generate longer calling song bouts (Hedrick 1986) and this song accelerates egg development in Gryllodes sigillatus (Bateman et al. 2005). Similarly, female Gryllus lineaticeps receive fecundity and fertility benefits from, and prefer to mate with, males with higher chirp rates (Wagner & Basolo 2007). In G. bimaculatus, calling song may predict a male’s immune competence (Rantala & Kortet 2003; Teleogryllus sp.: Simmons et al. 2005; Tregenza et al. 2006a), whereas immune challenge reduces daily calling rates (Jacot et al. 2004). In G. campestris, song calling rate and chirp rate increase with food quality (Scheuber et al. 2003) and better fed males secure more females (Holzer et al. 2003). In our experiment, the calling song was as effective as the courtship song at inducing female– female aggression, whereas the aggressive rival song proved far less so (Fig. 2). The latter result is perhaps surprising, considering that rival song is produced more frequently by potentially superior, dominant males (Alexander 1961). In cockroaches, females may mate preferentially with subordinate males to reduce costs resulting from manipulation by dominant mates (Moore & Moore 1999; Moore et al. 2001, 2003), a general concept of current debate (see Stewart et al. 2005; reviewed in Hosken & Tregenza 2005; Tregenza et al. 2006b). Whether female crickets are less attracted to hyperaggressive males for similar reasons, or adopt this tactic simply to avoid being bitten, must be investigated. We conclude that the calling and courtship songs of G. campestris, as reliable predictors of a male’s potential resource value, are sufficient and necessary signals for inducing female competition for males. Although aggressive female competition for a male has not yet been observed in the field (Rost & Honegger 1987; Hissmann 1990; Ritz & Ko¨hler 2007), we predict that it may occur under favourable ecological conditions, for example at high female/ male ratios, when encounters of multiple females with a single courting male are more likely. Acknowledgments We thank Stefanie Schapp, Leipzig University, and two anonymous referees for helpful comments on the manuscript.

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