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Marine debris is a global problem and has been shown to affect many marine animals (Gall & Thompson 2015). Some previous studies on sea turtles have reported that accidental ingestion of marine debris may prevent survival and growth by causing perforations or blockages of the digestive system (Schuyler et al. 2012), reducing nutrient absorption (McCauley & Bjorndal 1999), and increasing absorption of harmful substances into the body (Teuten et al. 2009). Moreover, it suggests that higher concentrations of plastic items in the gastro-intestinal tract leads to a higher probability of mortality (Wilcox et al. 2018). Therefore, it is important to characterize the current levels of marine debris ingested by sea turtles to formulate an effective conservation plan for these species (Hamann et al. 2010). The extent of marine debris ingestion in sea turtles has been studied in the main islands and Yaeyama Islands in Japan (Kameda & Ishihara 2009; Fukuoka et al. 2016); however, there is a paucity of data from around Okinawa Island. In this study, we dissected the gastrointestinal tracts of stranded, dead sea turtles to determine the extent of marine debris ingestion by sea turtles around Okinawa Island, through analysis of frequency and type of marine debris ingested.

Between October 1990 and July 2019, 383 specimens of green turtles, 63 specimens of hawksbill turtles, and 38 specimens of loggerhead turtles were found on the beaches of Okinawa Island and the small islands at its periphery (Fig. 1). The mean (± SD) for the standard carapace length (SCL) of turtles were measured; the SCL was 572.2 ± 180.6 mm (range: 309-1020 mm) for green turtles, 424.1 ± 161.8 mm (201-800 mm) for hawksbill turtles and 821.3 ± 78.3 mm (655-955 mm) for loggerhead turtles.

Figure 1. A map of Okinawa Island and small islands in its periphery. We collected samples from the islands shaded
gray.

Figure 2. Marine debris ingested by sea turtles; A: Hard plastic, B: Soft plastic, C: Fishing line/rope, D: Styrofoam, E: Fishing hook, F: Rubber. White bars represent 10 mm.

The marine debris found in the gut was removed from all specimens, and classified as hard plastic, soft plastic, Styrofoam, fishing line/rope, fishing hook, rubber, or other (Fig. 2), as described by Fukuoka et al. (2016). The occurrence rate of ingestion (%) for each category of marine debris in each turtle species were calculated using the following equation, as described by Schuyler et al. (2012):

A total of 17.4% (n = 84) of the examined specimens were found to have ingested marine debris. The percentage of specimens with marine debris in their guts was 14.9% for green turtles, 28.6% for hawksbill turtles, and 23.7% for loggerhead turtles (Table 1). The most common categories of ingested debris were soft plastic (54.4%) and fishing line/ rope (36.8%) for green turtles, hard plastic (44.4%) and soft plastic (33.3%) for hawksbill turtles, and hard plastic (44.4%) and Styrofoam (33.3%) for loggerhead turtles (Table 2).

Table 1. Occurrence of marine debris ingestion by sea turtles. N is the number of turtles examined, NTD is the number of turtles found with ingested debris, and occurrence is the percentage of individuals that had ingested marine debris.

Table 2. Number (and percentage) of sea turtles that ingested different categories of debris.

To the best of our knowledge, the present study is the first to provide viable information on marine debris ingested by sea turtles distributed around Okinawa Island. These findings will aid in formulating conservation programs and improving our understanding about the feeding ecology of sea turtles. In particular, approximately 15% to 30% of green turtles, hawksbill turtles, and loggerhead turtles accidentally ingested marine debris. This rate was assessed to be relatively low when compared with other rates worldwide. For example, the frequency of marine debris ingestion is 60.5% for green turtles in southern Brazil (Bugoni et al. 2001), 68.8% for hawksbill turtles in northern Brazil (Macedo et al. 2015), and 79.6% for loggerhead turtles in the Western Mediterranean (Tomas et al. 2002). Some previous studies have reported high ingestion rates of soft plastic and fishing line/ rope in green turtles (Bugoni et al. 2001; Fukuoka et al. 2016). A similar trend was observed among the green turtles of Okinawa Island in this study.

In some previous studies on the main islands of Japan, the occurrence of marine debris in green turtles showed high rates; 100% for the Japan Sea (Kameda & Ishihara 2009) and the Iwate coast (Fukuoka et al. 2016), and 52.3% for Shikoku and Kii (Kameda & Ishihara 2009). However, the occurrence of marine debris ingested by green turtles in the Yaeyama Islands was extremely low (2.8%) (Kameda & Ishihara 2009). The frequency of marine debris in green turtles in Okinawa Island (14.9%) is closest to that of the Yaeyama Islands. Hence, the frequency of marine debris in green turtles was lower in the southern region, including around Okinawa Island and Yaeyama Islands, and higher in the northern region, including the main islands of Japan. Such differences between regions in Japan could be attributed to differences in feeding ecology, and feeding preferences may also affect the types of debris that turtles encounter (Schuyler et al. 2014).

Foraging green turtles are distributed around the Yaeyama Islands in a small area between their feeding grounds and a neighboring rest point (Okuyama et al. 2013). Kameda et al. (2013) reported that during a foraging period, green turtles were distributed in a narrow area of approximately 16.3 km2 near the Yaeyama Islands, based on a mark-recapture method. On Okinawa Island, additional studies using the mark-recapture method have recorded some migrations between the east and west coasts of Okinawa Island (Hayashi & Nishizawa 2015; Nakanishi et al. 2017). In contrast, green turtles found in the Iwate Coast visit to forage during summer only, when they seasonally migrate a few hundred kilometers (Fukuoka et al. 2015). Fukuoka et al. (2016) demonstrated that green turtles confuse marine debris with gelatinous prey near the water surface during long-term migrations. Consequently, we suggest that the migration area for foraging has an effect on the encounter and ingestion rates of marine debris within sea turtle populations. These findings support the hypothesis that pelagic and neritic sea turtles exhibit significant differences in their likelihood of ingesting debris (Schuyler et al. 2012).

The gut contents of loggerhead turtles in Japanese Pacific temperate waters were recently studied by Fukuoka et al. (2016). Fukuoka and colleagues reported that 11 of the 13 loggerhead turtles found off the coast of Iwate of mainland Japan had marine debris. In contrast, 23.7% of the loggerhead turtles from Okinawa Islands had marine debris in their guts. Such variation in the occurrence of marine debris in gut contents might be explained by the difference in sexual maturity and appetite of loggerheads. Adult sea turtles reduce food intake during the reproductive season (Bjorndal 1985). The loggerhead turtles captured in Okinawa waters (nesting area) were mostly mature (Kawazu et al. 2013), while those in Iwate (foraging area) were immature (Fukuoka et al. 2016). Hence, we suggest that the frequency of marine debris ingestion is driven by appetite, which is related to sexual maturity.

We evaluated the levels of marine debris ingested by sea turtles distributed around Okinawa Island. This rate was assessed to be relatively low compared to certain other regions Japan and around the world. In recent years, ocean contamination by microplastics has become an increasingly global concern (Caron et al. 2018), requiring further study to improve our understanding of marine debris impacts on sea turtles.

Acknowledgments. Field sampling was financially supported by the members of the Okinawa Churashima Research Center and the Okinawa Churaumi Aquarium. Special thanks to T. Fukuoka of The University of Tokyo for his great assistance and discussions. And finally, we thank two anonymous reviewers for their detailed comments on the manuscript.

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