Female communication in anurans: duets, ultrasonic calls and sex-role reversal
Male frogs and toads (anurans) are well known for their calls during the breeding season. Over recent decades a range of vocalisations have been identified in males from advertising calls to territorial and mating calls (Duellman & Trueb, 1986). Female frogs and toads are generally considered to be silent, although an increasing number of research studies have shown that females use calls in a range of contexts. These are usually soft and indistinct since females generally lack or have reduced vocal chords. To date, over 50 species of anurans are known to produce female calls (Boistel & Sueur, 2002). Examples of female calls include: release calls when unwillingly clasped by a male; reproductive calls to attract a male (role-reversal species) and aggressive or territorial vocalisations (summarised in Prieninger et al., 2016). In this article we highlight some examples of female communication within the anurans.
The concave-eared torrent frog (Odorrana tormota) is a tree-dwelling, nocturnal frog living near noisy streams in Huangshan Hot Springs, China. This noisy habitat poses a problem, making vocal communication difficult. Males of this species call to advertise their presence using calls with a high-pitch and frequency. In addition, on rainy nights prior to breeding, females emit ultrasonic calls from the sides of streams. These calls are emitted at a higher frequency and are much shorter than the calls of males. To establish the function of these female calls, Shen et al. (2008) carried out play-back experiments where males were played the call of a female through a speaker. On hearing the call of a female, a male would make large hops towards the speaker with astonishing acuity, rivalling that of a hunting barn owl or dolphin (Shen et al., 2008). Females of O. tormota possess distinct vocal cords, which is unusual. In female O. tormota the vocal cords are bigger and thicker compared to those of the male. The high-frequency and intense mating calls of female O. tormota are therefore exceptional for female anurans and the results of Shen et al. (2008) show that these female calls allow males to accurately detect females in a noisy environment.
The South African clawed frog (Xenopus laevis) is a member of a large genus of totally aquatic frogs from southern Africa (Figure 2). This species inhabits murky ponds and mating occurs at night so visual cues are not possible. Like many other frogs, the African clawed frog relies on auditory cues to detect and select a mate. It has previously been assumed that male African clawed frogs find females by producing long bouts of advertisement calls at night to attract females. It was thought that the male clasps the nearest female and if she is unwilling to mate she utters a clicking release call to inform the male she is not receptive. However, when population densities are high, this method appears costly and time consuming. Tobias et al. (1998) carried out research on the reproductive behaviour in this species and found that unreceptive females swam directly towards a vocalizing male and, on reaching him, produced an unusual rapping call consisting of a rapid series of clicks (Tobias et al., 1998). When a male heard the rapping call, he would intensify his calling and alter its structure as well as moving towards the female. This would lead to a unique duet of calls between the male and female. This example of male-female duetting is very rare amongst amphibians and is more common is birds (reported in over 200 species). In the African clawed frog the initial female rapping call assists in mate localization and the duet enhances mating success (Tobias et al., 1998).
The smooth guardian frog (Limnonectes palavanensis) from Borneo exhibits sex-role reversal where the male carries out all the duties of parental care, depositing eggs in small water bodies (Figure 3). Like many other anurans, males exhibit an advertisement call but does so infrequently from the forest floor. The males are often widely spaced, calling with a soft call, making them hard to locate. However, females have been reported to also utter calls. Goyes Vallejos (2016) carried out further research on the reproductive calling in this species and found that females give a loud call in response to a male advertisement call. When females hear a male calling they will gather around the calling male, calling spontaneously at a higher frequency than the males, a behaviour not previously reported in anurans (Goyes Vallejos, 2016; Goyes Vallejos et al., 2017). Females call 30 times every 10 minutes, while males call just once every 10 minutes (Goyes Vallejos, 2016). It is hypothesised that since the male provides all the parental care and high investment, that the female takes on many of the roles normally carried out by males in courtship e.g. frequent calling and seeking out mates. In addition, Goyes Vallejos (2016) found that females will also initiate calling without a male calling first. When hearing this call, a male will produce a call which is different to the normal advertisement call and aids in locating a receptive mate.
These studies, along with other recent research on calling behaviour in anurans, has led to an increase in the number of reported cases of female calls in courtship. They challenge the notion that in all frogs and toads it is the male which gives the loud advertisement call. Courtship in anurans is often complex and reflects the relative costs of reproduction to males and females as well as environmental and ecological conditions. Further research on less-studied species is likely to further our increase understanding of the role of auditory communication in a range of anuran species.
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