環境毒性学会誌 (Jpn. J. Environ. Toxicol.), 24, 12–25, 2021 Research Articles Effect of ontogenetic changes of feeding habits on total mercury level in red stingray, Hemitrygon akajei Teerapong DUANGDEE1, *, Wachirah JAINGAM2, Jun KOBAYASHI3 and Hiroaki TSUTSUMI3 1 Graduate School of Environmental and Symbiotic Sciences, Prefectural University of Kumamoto/3–1–100 Tsukide, Higashi-ku, Kumamoto 862–8502, Japan 2 Faculty of Fisheries, Kasetsart University/50 Ngam Wong Wan Rd, Lad Yao, Chatuchak, Bangkok, 10900, Thailand 3 Faculty of Environmental and Symbiotic Sciences, Prefectural University of Kumamoto/3–1–100 Tsukide, Higashi-ku, Kumamoto 862–8502, Japan ABSTRACT In Isahaya Bay, Kyushu, Japan, one of the edible ray species, red stingray, Hemitrygon akajei tends to acceleratedly accumulate total mercury (THg) that was released from Mt. Unzen beside the bay as it grows. In this study, we collected 20 individuals of the female ray with wide variety of body sizes (16 to 65 cm in disc size, 140 to 9,540 gww in body wet weight), and aimed to clarify its mechanism. The stomach content anal- ysis revealed ontogenetic changes of feeding habits among the immature females, females in transitional maturity, and mature females in its long life of 10 to 15 years or more. Immature females favor to preying on epifaunal macro-benthic animals such as shrimps, which are classied as “Low THg content group” of the secondary consum- ers, while mature ones mainly feed on short-neck clam, Ruditapes philippinarum, and polychaete, Nectoneanthes ijimai, which are “High THg content group” of the primary consumers. Therefore, mature females with larger bodies tend to acceleratedly accu- mulate THg and reached a max. 1,370 ng g−1 dw, although the stable isotope analysis of carbon and nitrogen of the muscles of the mature females indicates the descent of the trophic position to the immature ones in the food web system. Key words: biomagnication, feeding habits, Hemitrygon akajei, mercury, ontogenetic changes, red stingray, Ruditapes phillipinarum 1. INTRODUCTION and has brought serious negative impacts on Bioaccumulation of hazardous substances the health of not only the wildlife located at the such as heavy metals, polychlorinated bi- higher trophic positions in the food chain3, 10), phenyls, dioxin, etc. has been reported from but also humans through dietary intake11, 12). various aquatic ecosystems in lakes1–3), coastal Among these harmful substances, our research waters4–7) and oceans8, 9) throughout the world, has focused on the bioaccumulation process- *Corresponding author, Email: [email protected]; Tel: 096–321–6715; Fax: 096–384–6765 Received: 28 July 2020; Accepted: 28 December 2020 — 12 — Teerapong Duangdee et al. es of mercury to the animals occurring in the in the sediment in several times higher levels coastal water, since 7,400 tons of mercury to the organic particles derived from the dead per year is still being emitted into the envi- bodies of phytoplankton, since the organic ronment throughout the world not only from particles deposited on the sea oor tends to anthropogenic sources but also natural ones be decomposed by bacteria, but the mercury including volcanos13), which are among the contained in the particles is apt to remain in basic geographical components in the Japa- the sediment. The THg concentrated in the nese Archipelago. In Japan, the majority of the sediment is transferred to infaunal macro-ben- mercury emitted to the environment is nally thic animals such as clams and deposit-feed- discharged to the coastal waters, where over ing polychaetes that burrow in the sediment 1,879,000 tons of sh and shellsh has been through their feeding activities directly or caught to obtain seafood14). Careful intake of indirectly, while epifaunal macro-benthic ani- naturally contaminated mercury in seafoods mals such as amphipods and mussel occurring is, therefore, needed for the people living in on the surface of the sediment are apt to be Japan because of its negative impact on human much less exposed to the mercury accumulat- health. ed in the sediment. Consequently, although In the aquatic ecosystem, the mercury con- they were located at the same trophic position taminated in water tends to be absorbed by in the food web system in the bay as primary phytoplankton or aquatic animals such as sh consumers, the former infaunal consumers (through their respiratory activities), which contained 101±23 ng g−1 of THg, which were is referred to as “bioconcentration”. It is apt referred to as “High THg content group”, while to be further biologically concentrated on the the THg contents of the latter epifaunal ones body tissues of animals in higher trophic lev- were about one fourth of “High THg content els linked together with a food chain by their group”, 25.2±8.5 ng g−1, which were referred to predation, which is referred to as “biomag- as “Low THg content group”16). In the benthic nication”15). In the previous studies on the ecosystem, these two dierent levels of THg bioaccumulation, a process in which a mercury contained in the muscles of primary consumers is absorbed in an organism by all routes of are transferred to the secondary consumers in exposure as occurs in the aquatic ecosystem, the prey and predator relationship. Therefore, which includes its bioconcentration process by “High” and “Low” THg content groups were phytoplankton and biomagnication by preda- also found among carnivorous benthic animals. tory animals, most have described the discon- THg contents of crabs and sea stars which prey tinuous increase of mercury in the body tissues on infaunal macro-benthic animals were sever- of the organisms linked together with a food al times higher than those of carnivorous poly- chain in the pelagic water2, 5, 6, 8). chaete and shrimp which depended on diets to Jaingam et al.16) found another characteristic the epifaunal ones. bioaccumulation process of mercury through Jaingam et al.17) found a further curious bio- the benthic ecosystem in the eld surveys in a magnication process of THg between the mac- bay, Isahaya Bay, located beside an active vol- ro-benthic animals and carnivorous bentho- cano, Mt. Unzen, in Kyushu, Japan. The dead pelagic sh, red stingray (Hemitrygon akajei), bodies of phytoplankton that absorbed mercury in Isahaya Bay. The results of stable isotope from the surrounding water easily deposits on analysis of carbon and nitrogen of the muscles the sea oor of the shallow water of less than of red stingray indicate that its juvenile was 10 m in depth, and the mercury accumulates classied as one of the intermediate consumers — 13 — Eect of feeding habits on total mercury level in red stingray (very close to the tertiary one), but its trophic position in the benthic food web system de- scended to the level of an almost secondary consumer as it grew to an adult. Nevertheless, the THg contents of the adult increased to ex- tremely high levels, 670 to 3,700 ng g−1, which far exceeded the THg contents of the tertiary consumers of shes (about 250 to 270 ng g−1) oc- curring in the pelagic system of the same bay. Fig. 1. Study area, Isahaya Bay located in the Our study has focused on this biomagni- inner parts of Ariake Bay, Kyushu, western cation process of THg to the muscles of H. Japan. akajei. It is an endemic species of stingray that is distributed in a wide area of Pacic Ocean and an average depth of 10 m (Fig. 1). An ac- between northwestern part, Japan, Russia, tive volcano, Mt. Unzen, is located in the center China, Thailand, Malaysia, and Indonesia18, 19). of Shimabara Peninsula, it is one of the major In Japan, it has been used as a popular sea natural sources of discharging mercury into the food item for a long time, and 113 tons of its bay21, 22), since this peninsula is located beside catch as sea food was recorded in 2006 accord- the southern side of Isahaya Bay. According to ing the catch statistics in Ariake Bay20). We the most recent record of volcanic eruptions, need to know the detailed mechanisms of how Mt. Unzen erupted for 1928 days between 1990 this species accumulates to such extremely and 1995, and emitted 2.95 metric tons of mer- high levels of THg in its muscles, although it cury into the surrounding environment22, 23). is located at the trophic level close to the sec- ondary consumer in the food web system of the 2.2 Red stingray collection bay. In total, 22 red stingray individuals were In this study, we caught 22 red stingray in- captured from Isahaya Bay with a longline dividuals with a wide variety of body size in eet on 27 April 2019 and a gill net on 15 Isahaya. We examined the stomach contents of May 2019. The specimens were weighed with these specimens to identify its main food items, a digital balance, and their disc widths were determined their stable isotope ratios of carbon measured with a measuring tape. The gender and nitrogen to describe their trophic positions was determined by the presence or absence in the food web system, and determined the of claspers. According to Furumitsu et al.20), THg content in the muscle of the stingray. We the individuals whose disc widths were larger clarify the mechanisms of the magnication of than 56 cm in females and 35 cm in males were extremely high levels of THg in the muscles of regarded as sexually mature ones, the females the adult, and discuss the characteristics of the with the disc width between 45 and 55 cm were bioaccumulation process of THg in the benthic treated as ones in transitional maturity, and system in the coastal shallow water.