Introduction

Observing copulatory activity of bats under natural conditions is difficult mainly because they live in inaccessible sites such as caves, crevices and tree holes. Among the 1100 species of bats, copulatory activity has been described for less than ten including the hammer-headed bat Hypsignathus monstrosus [1], the Indian flying fox Pteropus giganteus [2], [3], the Australian flying fox P. poliocephalus [4], the little brown bat Myotis lucifugus [5], the Brazilian free-tailed bat Tadarida brasiliensis [6], the common vampire bat Desmodus rotundus [7], and the short-nosed fruit bat Cynopterus sphinx [8]. Observations of social organization [9] including behavioural repertoire and copulation [2], [3] of P. giganteus is less difficult, mainly because the majority of individuals roost in trees. Our preliminary observations showed that during the breeding season, P. giganteus males follow females during courtship while females move away. Similarly, female black flying foxes P. alecto [10] move away when males approach them. When the females stop moving, the males begin to sniff and lick their uro-genital regions. Female C. sphinx licks the penis of males during copulation (fellatio) [8]. These observations on P. alecto and C. sphinx led us to assess whether individuals of P. giganteus exhibit any such behaviour associated with copulation. Our subsequent observations revealed that males exhibit cunnilingus (licking vagina of females). We describe these behaviours and their influence on copulation.

Materials and Methods

We conducted the study from July 2010 to July 2011 near the village of Nallachampatti (9°58′N, 77°47′E), approximately 32 km west of Madurai Kamaraj University campus. A colony of about 420 P. giganteus occupied a single Ficus religiosa tree (Family: Moraceae), situated adjacent to private agricultural land. We recorded the timings of emergence and returning flights, behaviours observable during daytime such as copulation together with the influence of ambient temperature, humidity and rain. These observations were made twice a month by using binoculars (Balileo 20×50 gross feld) from 0230 h (day 1) to 2330 h (day 2) for a total of 1170 hours. Copulation occurred during the morning (0700–0930 h) between July and January. In addition to visual observations, we made videographs (Sony handycam DCR-SR47) and photographs (Nikon D3000 with 18–200 mm lens) of the bats from which to prepare illustrations and supporting documents. Humidity and temperature in the study area were 68.5±2.2% and 28.7±0.7°C (n = 26 for both), respectively. Because movement of people was common in the area, we presumed that our presence did not disturb the bats.

Results and Discussion

We observed a total of 57 copulations, all between 07.00 h and 09.30 h from July 2010 to July 2011. More copulations occurred during October and November. Initially a male groomed its genital organ, which led to erection of the penis. Afterwards, the male moved towards a nearby female with gentle wing flapping and touched with its wing (Video S1). In 57 out of 69 observations, the female moved away and the male followed. After 12–75 s, the female stopped moving and the male craned its neck to reach the female’s vagina and started licking it (Video S1). The female was alert and let the male exhibit cunnilingus for 50.5±2.12 s (n = 57). The male then mounted the female (Video S1). The act of copulation lasted 14.9±0.38 s, (n = 57). Afterwards, the male dismounted and resumed cunnilingus (Video S1) in all the observations (n = 57). The female did not show any movement during this post-copulatory cunnilingus (Video S1), which was always longer (146.4±4.0 s; n = 57) than that before copulation occurred. Although prolonged rituals and competition between males occurred in the remaining 12 observations, we could not follow them as it was beyond the capacity of our visual observation. We found a positive relationship between the duration of pre-copulatory cunnilingus and copulation (Pearson correlation: r₆ = 0.91, P<0.05; Fig. 1). Thus the duration of pre-copulatory cunnilingus was related to increase in the duration of copulation. Whereas, we found a negative relationship between the duration of pre- and post-copulatory cunnilingus (Pearson correlation: r₆ = 0.79, P<0.05; Fig. 2).

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Figure 1. Relationship between duration of pre-copulatory cunnilingus and copulation.

Circles and numbers indicate average duration of copulation and n value, respectively.

https://doi.org/10.1371/journal.pone.0059743.g001

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Figure 2. Relationship between duration of pre- and post-copulatory cunnilingus.

Circles and numbers indicate average duration of cunnilingus and n value, respectively.

https://doi.org/10.1371/journal.pone.0059743.g002

Our observations suggest that cunnilingus is an important prerequisite for male P. giganteus making the female receptive for copulation. The positive correlation between the duration of pre-copulatory cunnilingus and copulation is consistent with this suggestion. Pre-copulatory cunnilingus may enhance the arousal and lubrication of the female as suggested for fellatio in C. sphinx [8]. Thus, the longer the duration of cunnilingus the greater the duration of copulation. Markus [10] reported that male P. alecto also exhibits courtship display by sniffing and licking the female’s genital organ before copulation, but she did not quantify the duration of copulation. At the completion of the initial copulation, unlike P. alecto [10], P. giganteus males never attempted to resume copulation. Male P. alecto never repeated vaginal licking after the initial copulation. Instead, they began to groom or lick their own penis [10]. We never observed P. giganteus grooming its penis after copulation. The longer duration of post-copulatory cunnilingus in P. giganteus compared to that observed before copulation in all cases may be due mainly to the fact that females made no movements after copulation.

A possible functional explanation for the association of cunnilingus with copulation may be sperm competition. Before copulation, P. giganteus males lick females’ genitals to remove sperm from males that might have mated with her earlier, as occurs in ‘cloaca pecking’ by dunnocks, Prunella modularis [11]. However, whether several P. giganteus males mate with the same female over a short time period is not known. The positive relationship between the duration of pre-copulatory cunnilingus and copulation supports the sperm competition hypothesis (lick for longer and copulate for longer increases the chances of paternity). In this context, cunnilingus would be maladaptive after mating as there is a risk of removing the male’s own sperm. Observation at close-range is needed to find out whether the male’s tongue enters the vagina or not. Nevertheless, the negative relationship between the duration of pre- and post-copulatory cunnilingus suggests the possibility of sperm competition. Thus, the male removes the sperm of competitors but apparently not its own – lick for longer before but less after copulation, if paternity uncertainty is high. Hosken [12] suggested that the risk of sperm competition among pteropodids increases with group size, testes mass and conspecific proximity. Further study on the association between cunnilingus and copulation with reference to group size and testes mass will likely lead to greater understanding of sperm competition in P. giganteus.

Ours is the first evidence for cunnilingus occurring both before and after copulation in bats under natural conditions. Oral sex was observed in C. sphinx under captive conditions, in which females lick the male’s penis during dorsoventral copulation [8]. Fellatio in C. sphinx occurs simultaneously with copulation, whereas cunnilingus takes place in P. giganteus both before and after copulation. It appears that male P. giganteus and P. alecto [10] and female C. sphinx [8] employ oral sex as a pre-requisite for successful copulation. Similar studies should be carried out on other bat species, especially pteropodids, to establish whether oral sex, in association with copulation, is common in this group.

Supporting Information

Acknowledgments

We are grateful to Karuppu, the land owner for permitting us to carry out the study. We thank Sathiskumar and Vinod for their assistance. We thank P.A. Racey for critically reading the revised version of the manuscript. We are grateful to an anonymous reviewer for valuable comments. We thank M. Ramesh for help in editing the video sequences.