Methods

This study was conducted in the southwestern area of Iriomote Island, Japan (lat 24°17′N, long 123°53′E). For detailed experimental protocol, see Okuyama et al. (2013). Briefly, we caught a green turtle (straight carapace length [SCL]: 54.3 cm, body weight: 24.1 kg, sex: unknown, CM5 in Okuyama et al. 2013), which is regarded as immature according to the data of the minimum size of nesting turtles on Iriomote Island (91.2 cm SCL; Nishizawa et al. unpubl. data, 2013) and the mature size of green turtles in other populations (Limpus and Chaloupka 1997). The turtle was deployed with a package of data loggers attached to the carapace, including a video logger (GoPro HD®; Woodman Labs, CA) in a custom-made waterproof case with a programmable recording system and an extra-battery (Logical Product Co, Fukuoka, Japan). A Fast-loc Global Positioning System tag and depth tag (Mk10-F; Wildlife Computers, WA) were also included in the package along with the video logger to monitor the vertical and horizontal movements of the turtle. The turtle equipped with the package was released very close to the initial capture point. To retrieve the data loggers from the released turtle, the package of data loggers was equipped with a float made of copolymer foam (Nichiyu Giken Kogyo, Saitama, Japan) in which a Very High Frequency transmitter (130 BB; Advanced Telemetry Systems, Isanti, MN) and a time-scheduled release mechanism (Little Leonardo Co, Tokyo, Japan) were embedded. The time-scheduled release mechanism was programmed to activate 120 hrs after release, at which time an electric charge would incise the plastic cable that was holding the data logger package to the turtle's carapace. The logger unit would then detach from the turtle and float to the sea surface.

Results

The immature turtle deployed with the data logger package encountered an adult male turtle at 1925 hrs local time on 31 July 2011, which was about 32 hrs after the release. This time of year coincides with the middle of the green turtle nesting season in Iriomote Island. The place of encounter was at the reef edge in the southern part of Iriomote Island, approximately 300 m from the shore; the water depth was 13.1 m, which was 2.5 km away from the release point. The male turtle appeared in front of the immature turtle and was observed approaching (Fig. 1a), circling (Fig. 1b), getting behind, and then mounting the immature turtle (Fig. 1c). Once mounted, the male attempted to hook his fore-flipper claws over the anterior rim of the immature turtle carapace and to repeatedly bite at its neck (Fig. 1d). However, the immature turtle countered these advances by attempting to spin out from under the male. After an approximately 5-min interaction, the male turtle departed the vicinity of the immature turtle.

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Discussion

The male turtle showed the typical sequence of behaviors during courtship: approaching, circling, mounting, and biting (Dodd 1988; Alvarado and Figueroa 1989; Frick et al. 2000; Schofield et al. 2006); this indicated that the male turtle would attempt to court and mate with the immature turtle. Sea turtles have sensory abilities of vision, hearing, and chemoreception (Bartol and Musick 2003). If males use the cues, such as olfactory stimuli, specific to mature females (as do other chelonians; see Miller and Dinkelacker 2008), then they would never attempt to court immature turtles. Hence, our observation suggests that male turtles may not distinguish mature females from immature turtles. Also, our result indicates the possibility that mate-searching strategy is completely different between sea turtles and other chelonians.

How then do adult male turtles find a mating partner? Male turtles do not seem to have an ability to distinguish a mature female turtle from human swimmers, skin divers, or scuba divers; indeed, mature male turtles have occasionally approached and attempted copulation with humans during mating season (Booth and Peters 1972; Bowen 2007; J. Okuyama, pers. comm., June 2012). This occurs despite the fact that humans are unlikely to emit the cues similar to the smells or sounds that sea turtles specifically do. Moreover, it has been reported that male turtles mounted a wooden disk, barrel, or decoy in the water as a potential mate (Bowen 2007). On the other hand, it is still unclear whether they have an ability to discriminate other males. It has been reported that males occasionally attempted courtship with another male (Booth and Peters 1972), and also that an attendant male mounted a copulating pair to form a threesome (Green 1999), which may indicate that males cannot distinguish between females and other males. Aggressive behaviors toward a mating pair by attendant males, such as biting the tail of the copulating male in a presumed effort to dislodge him, have been observed (Alvarado and Figueroa 1989; Schofield et al. 2006). This indicates that males may correctly identify other males mounting on the female. Based on these facts, one of the most robust hypotheses is that males discriminate a mating partner mainly using a visual cue, but without high acuity, so that they can distinguish the size of mature turtles from that of immature turtles. This is supported by the fact that loggerhead turtles (Caretta caretta) generally use vision to distinguish prey (Narazaki et al. 2013). However, it is undeniable that they might find a mating partner by using other cues, such as the smell emitted from animal or human or the noise generated by animal or human's locomotion.

Although we reported a single case of observation, if our hypothesis is true, male turtles may judge the objects moving underwater that have the similar size to a mature female turtle as a mating partner and consequently randomly attempt to court turtles of that size, including both immature and mature turtles. The probability of male-to-female encounters would therefore mainly depend on the population density at the breeding site. Sea turtles mate in waters adjacent to the nesting beach after long-distance natal homing (Limpus 1993; Plotkin et al. 1996; Frick et al. 2000; James et al. 2005), although other previous studies suggest the possibility that turtles do not mate in these areas (Pritchard 1982; Eckert and Eckert 1988). In evolutionary terms, natal homing presumably arose in sea turtles because individuals that returned to their natal areas to nest produced more surviving offspring than did those that tried to nest elsewhere (Lohmann et al. 2013). For male turtles, however, it also would be effective strategy to maximize chances of encountering females of the right age, reproductive status, and species in the extensive ocean.

There have been numerous documented cases of hybridization among species in the family Cheloniidae (Karl et al. 1995; Bowen and Karl 2007). The indiscriminate mating behavior of males as observed in this study may be one of the significant factors that facilitates the hybridization among this species (Bowen and Karl 2007).