Rapping, a female receptive call, initiates male–female duets in the South African clawed frog

Abstract

Finding a sexually receptive partner of the opposite sex is a challenge; one solution is to advertise. That advertising is usually the province of males has shaped scenarios for sexual selection, especially the ardent active male courting the passive but choosy female. Herein we consider an unusual case in which constraints on reproduction may have led to fertility advertisement by female frogs. When oviposition is imminent, female South African clawed frogs swim to an advertising male and produce an aphrodisiac call, rapping, that stimulates both male vocalization and approach. Males respond to rapping with a distinctive answer call. The rapping-answer interaction thus forms a duet between partners of a receptive pair.In most vertebrates, perhaps due to the greater investment of females in gametes and offspring (1), it is the male that competes for receptive conspecific females (2, 3). Many males find mates by advertising; prominent examples are mating leks and the songs of birds and frogs. This simple solution works well when the responding female can be identified by the signaling male. However, if the signaling environment is noisy or if population density is high, it may be difficult for the signaler to distinguish the responder. Under these conditions, we might expect a reciprocal signaling system involving both sexes. Herein we present evidence for a system of auditory recognition-receptive duets-in the South African clawed frog.We have studied male-female courtship vocalizations in Xenopus laevis, a member of a large genus of totally aquatic frogs from southern Africa (4). Xenopus inhabit murky ponds and mating occurs at night so that few if any visual cues are available to identify potential mates. Instead, it is believed that Xenopus, like other frogs (5), relies on auditory cues to broadcast receptivity and location. At the time we began our studies, two courtship vocalizations had been examined in this species. The advertisement or mating call (6) given only by sexually receptive males (7) is loud and prolonged with distinct fast and slow trill phases (7,8). Sexually receptive females display positive phonotaxis to tapes of advertisement calling (8). Ticking (6), given by sexually unreceptive females (9), is a quiet, slow, and monotonous trill (10) believed to function as a release call (6, 11).It has been assumed that male Xenopus find females by producing prolonged bouts of advertisement calling to which females are attracted; the male then clasps the nearest moving animal, releasing those that tick (12). The natural breeding conditions for Xenopus, high population density and low visibility, suggest that finding a mate may not be this simple. Unless the calling male could isolate himself from the rest of the group, clasping every animal in his vicinity would be disadvantageous; how then does he discriminate a responder?We have examined populations of Xenopus near Cape Town during the prolonged breeding season (about 6 months). Most (88%) adult males taken from these ponds were sexually rec...

Male Phonotropism and Answer Calls Elicited by Female Vocalizations in the African Clawed Frog, Xenopus laevis

“…African Clawed Frogs belong to a restricted group of anuran species in which females produce a fertility call (Emerson and Boyd, 1999;Cui et al, 2010) resulting in courtship duets between partners (Tobias et al, 1998). As shown in Figure 1, natural female rapping calls differed from natural female ticking calls in terms of repetitive click rhythms, intensities of sounds (or amplitudes of waveforms), durations of pulses, and frequency structures.…”

“…The advertisement call type is produced mainly during duets with females producing receptive (i.e., rapping) calls (Wetzel and Kelley, 1983;Watson and Kelley, 1992;Tobias et al, 1998). Other calls produced by Xenopus males include amplectant, ticking, chirping, and growling calls; however, these calls are not considered in this study.…”

“…The fast trills can be intensity modulated (i.e., there is a progressive increase in click volume). Females produce rapping calls (11-12 Hz click rate), which indicate sexual receptivity and increase male vocal activity, and ticking calls (click rate of 4 Hz), which depress male vocal activity (Tobias et al, 1998). Male answer calls are similar to male advertisement calls, although the duration of the fast trill is increased, the slow trill duration is decreased, and fast trill intensity modulation is more pronounced.…”

Current research in amphibians: Studies integrating endocrinology, behavior, and neurobiology

“…Sexually receptive behavior in female amphibians includes approaching an advertising male (Schmidt, 1984(Schmidt, , 1985Zerani and Gobbetti, 1993), emitting a vocalization in some species (Tobias et al, 1998), or inhibiting release calls or leg extensions (Diakow and Nemiroff, 1981;Kelley, 1982). Early studies found that female American toads (Bufo americanus) will approach a conspecific mate signal when injected with a variety of peptide or steroid hormones, such as human chorionic gonadotropin (HCG) or prostaglandin (Schmidt, 1984(Schmidt, , 1985Weintraub et al, 1985).…”

“…Early studies found that female American toads (Bufo americanus) will approach a conspecific mate signal when injected with a variety of peptide or steroid hormones, such as human chorionic gonadotropin (HCG) or prostaglandin (Schmidt, 1984(Schmidt, , 1985Weintraub et al, 1985). In anuran species in which the female is able to vocalize, call production occurs when the female has mature eggs (Roy et al, 1995;Bush, 1997;Tobias et al, 1998), which is the same period when gonadal steroids are elevated (Harvey et al, 1997;Gobbetti and Zerani, 1999). Surprisingly, until recently, there have been few attempts to relate female behavior to estrogens.…”