Marine Macrophytes and Plastics Consumed by Green Turtles (Chelonia mydas) in Hong Kong, South China Sea Region
Abstract
This is the first identification of marine macrophytes consumed by green turtles in Hong Kong, South China Sea: 6 red algae species (Pterocladiella tenuis, Gelidium pusillum, Chondrus ocellatus, Gracilaria chorda, Grateloupia filicina, and Amansia glomerata), 1 brown alga species (Lobophora variegata), and 1 sea grass (Halophila ovalis) were identified. Plastics and other foreign materials were also found in the stomach contents of 2 of the 8 individuals sampled.



Of the 7 extant sea turtles species, 5 are found in the South China Sea: green turtle (Chelonia mydas), leatherback turtle (Dermochelys coriacea), olive ridley turtle (Lepidochelys olivacea), loggerhead turtle (Caretta caretta), and hawksbill turtle (Eretmochelys imbricata) (Wang 1993; Chan et al. 2007). The green turtle is the most common turtle recorded in the South China Sea and is the only species that nests in the area, although its nesting population is nearly extinct (Wang 1993; Chan et al. 2007; Wang and Li 2008; Ng et al. 2014). The green turtle, with the exception of the Hawaiian subpopulation, is a globally endangered species (Pilcher et al. 2012) and faces various anthropogenic threats, such as being directly hunted and also as by-catch (Cheng and Chen 1997; Wang and Li 2008), trade pressure (Pilcher et al. 2009; Lam et al. 2011), and habitat degradation of both their nesting and foraging grounds (Wang and Li 2008). A scientific understanding of the complexity and use of their habitat by sea turtles provides a crucial foundation for wildlife conservation and for formulation of effective management plans, e.g., delineation of Marine Protected Areas to properly manage foraging and other vital habitats of the species (Seminoff et al. 2002; Arthur and Balazs 2008; Gaos et al. 2012; Hart et al. 2012). Currently, there are very limited published studies about the diet of green turtles in the South China Sea. This study, therefore, aimed to provide crucially important baseline information to help characterize the ecological niche of green turtles in this region.
Interaction with plastics by marine wildlife, including sea turtles, occurs worldwide and continues to be an emerging threat, including entanglement and accidental ingestion (Wabnitz and Nicholas 2010; Vélez-Rubio et al. 2013). The ingestion of plastics and other anthropogenic debris is likely to cause sublethal effects on sea turtles, namely dietary dilution (McCauley and Bjorndal 1999), interference with energy metabolism or gut function (Lutz 1990), obstruction or displacement of the digestive tract (Bjorndal et al. 1994), and absorption of toxins that may interfere with endocrine function during development and reproduction (Bjorndal 1997; Oehlmann et al. 2009). Although these sublethal effects are difficult to quantify, especially in combination, these effects have conservation implications in that they may result in reduced growth rates, longer developmental periods, and decreased reproductive output and survivorship (McCauley and Bjorndal 1999). This study, therefore, also aimed to identify foreign items found in green turtles in the South China Sea.
Methods
Stranded sea turtles (n = 8) were found by public reports and collected from locations in Hong Kong, in the northern boundary of the South China Sea. Potential causes of stranding were assessed by gross external examination together with circumstantial evidence, personal observations, and interviews with informants. Food items found in the mouth or stomach were retrieved from the stranded green turtles during necropsy performed immediately after the carcass was found and were identified to the lowest taxon possible. Foreign items such as plastics were also visually identified with the naked eye; this study did not consider microplastics or plastic fragments < 5 mm in size (National Oceanic and Atmospheric Administration [NOAA] 2016). Relative volume of each food or foreign item was assessed visually. Seaweeds found in the stomach contents of stranded green turtles were identified morphologically according to Tseng (1983), and their current nomenclature status was checked with Algaebase (Guiry and Guiry 2016). Curved carapace length (CCL), and the sex of each stranded green turtle as determined by external features were also recorded. The following life stages in green turtles defined by carapace length intervals were adopted by making reference to Balazs (1980): a juvenile is a posthatchling individual of up to 67 cm CCL; a subadult is an individual of CCL from 67 to 84 cm; and an adult is a reproductively mature individual of CCL > 84 cm.
Results
All the stranded green turtles were dead when first found (Table 1). The stranded green turtle found on 23 May 2013 was identified to be a subadult male individual, and its death was attributable to fishing net entanglement. Fishing lines were found tangled around its front flippers. Cause of death and sex of the other individuals could not be determined because of severe decomposition of the carcasses. Dietary items found in the stomach or mouth of 8 green turtles (CCL mean = 58 ± 17 cm; range = 34–81 cm) (Table 1; Fig. 1) stranded in Hong Kong were composed mainly of red algae, sea grass, and relatively small amounts of fish, squid, and crab. Foreign materials, such as clear plastic fragments and rope strands, were also found in the stomachs of 2 of the 8 individuals sampled (Table 1). The sea grass Halophila ovalis predominated in quantity along with fish remnants in the diet of 1 juvenile green turtle (CCL 54 cm). Five red algal species were identified: Pterocladiella tenuis, Gelidium pusillum, Chondrus ocellatus, Gracilaria chorda, and Amansia glomerata, along with 1 brown seaweed, Lobophora variegata. Specimens of brown alga L. variegata and red alga P. tenuis, remnants of fish and squid, were observed in 2 of the 8 green turtles sampled.



Citation: Chelonian Conservation and Biology 15, 2; 10.2744/CCB-1210.1
Discussion
Rhodophyta (red algae) are known to predominate in the diet of green turtles in Australia, Hawaii, and Brazil (Fuentes et al. 2006; Russell and Balazs 2009, 2015; Reisser et al. 2013). Perhaps remnants of fish, squid, and crab found in the stomach contents came from fishing gear or from bait discarded by fishers. In this study, juvenile and subadult green turtles stranded in Hong Kong were found to be basically herbivorous, and their major staple food was red algae. We also observed that the red alga Grateloupia filicina was being consumed by green turtles foraging in coastal waters of Vase Rock, Liouciou Island, Taiwan (C.K.Y.N., pers. obs.). These red algae species are widely distributed in the Pacific, including the coasts of mainland China, Taiwan, Korea, Japan, and Southeast Asia (Guiry and Guiry 2016). Red algae can also form low lawns on rocks where they produce an extensive mat-like turf made up of Gelidium pusillum and P. tenuis that green turtles use for food (Russell and Balazs 2009, 2015). The sea grass H. ovalis that was identified in the South China Sea diet also occurs widely in the Indo-Pacific from southern Japan and throughout Southeast Asia and Hawaii (Russell et al. 2003; Short et al. 2010). This study presents the documentation and identification of red algae and sea grass foraged by green turtles in Hong Kong in the South China Sea, which has been underreported.
Ingestion of plastics by sea turtles occurs worldwide and continues to be an emerging threat, including entanglement and accidental ingestion (Russell et al. 2011; Nelms et al. 2015). Schuyler et al. (2013) reported that the probability of green and leatherback turtles ingesting debris is increasing significantly based on 37 studies including data from before 2000 through 2011 and that plastic was the most commonly ingested type of debris. Schuyler et al. (2014) suggested that floating plastic bags might be mistaken for jellyfish, a common natural prey item of some sea turtle species. Plastics were also found in the stomach contents of green turtles in the South China Sea as revealed by the present study. One individual was found to be more severely contaminated with plastics, with its stomach containing plastic fragments as well as a small plastic tissue package. Marine debris pollution is a worldwide problem that should be addressed at scales from the local to the global levels.


Stranding locations of the sampled green turtles (denoted by black points on the large map). The line in the large map outlines the maritime boundary of the Hong Kong Special Administrative Region.
Contributor Notes
Handling Editor: Jeffrey A. Seminoff