Crustacean Research 2019 Vol.48: 99–103 ©Carcinological Society of . doi: 10.18353/crustacea.48.0_99 Survival of Argulus japonicus (Branchiura: Argulidae) on a cyprinid in drought-induced brackish waters in a Japanese lake

Kazuya Nagasawa

Abstract.―Two specimens of a freshwater fish parasite Argulus japonicus Thiele, 1900 were found to be mixed in a sample of over 600 specimens of a brackish-water fish parasite Caligus orientalis Gusev, 1951 in a glass vial kept at Hiroshima Univer- sity. These specimens were all collected in September 1973 from the body surface of a moribund Japanese white crucian carp, Carassius cuvieri Temminck & Schlegel, 1846, in drought-induced brackish waters of Lake Shinji, , Japan. This collection indicates that A. japonicus can survive in brackish waters under un- usual climate conditions.

Key words: fish parasite, Caligus orientalis, concurrent infection, salinity tolerance, Lake Shinji

Argulus japonicus Thiele, 1900 is an ecto- sawa, 2004). Based on a specimen label, all of parasite of freshwater fishes (Poly, 2008; these specimens were collected from the body Neethuling & Avenant-Oldewage, 2016). This surface of a moribund Japanese white crucian species was originally described using material carp, Carassius cuvieri Temminck & Schlegel, from Japan (Thiele, 1900), where it has been 1846 (written as “kawachi-buna” in Japanese) reported from cyprinids in inland waters and (body size unknown), by Hiroya Suzumoto almost exclusively those fishes reared at fish (Mitoya Inland Branch, Shimane Prefectural ponds and aquaria (Nagasawa, 2011a, 2011b, Fisheries Experimental Station) on 11 Septem- 2017, 2018; Nagasawa et al., 2010, 2012, ber 1973 in brackish waters of Lake Shinji, 2013, 2018; Yamauchi & Shimizu, 2013; Na- Shimane Prefecture, Japan. gasawa & Sato, 2014; Nagasawa & Miyajima, Lake Shinji (79.1 km2, 6.4 m in maximum 2018; see Nagasawa, 2009 for the earlier litera- depth, 35°27′01″N, 132°56′58″E at its center) ture). Nevertheless, Yamauchi et al. (2011) col- is connected to the Sea of Japan through a lected A. japonicus from an aquarium-held fish brackish-water lake and two short channels. In reared in brackish waters (salinity: 1–7‰). the summer of 1973, there was a serious This collection is interesting because A. japoni- drought around the lake, which caused a cus had never been recorded from salt waters. marked increase in lake water salinity up to In this paper, I report on my observation to 12.7‰ at the surface and 16.3‰ near the bot- support Yamauchi et al.’s finding on the surviv- tom [Suzumoto, 1974; chlorinity values (C) re- al of A. japonicus in brackish waters. ported by this author are here transferred to sa- Recently, I found two specimens of A. japon- linity values (S, ‰) using an equation: S＝ icus and 605 specimens of copepod Caligus 0.030＋1.8050×C]. Under such unusual con- orientalis Gusev, 1951 (Siphonostomatoida: ditions, marine and brackish-water fishes from Caligidae) in a glass vial kept at the Laboratory the nearby brackish-water lake and the Sea of of Aquatic Pathology, Hiroshima University, Japan invaded Lake Shinji, where the co-in- Higashi-Hiroshima, Japan. The latter species is vading parasite C. orientalis reproduced and known as a brackish-water fish parasite (Naga- heavily parasitized Carassius cuvieri (reported

Received: 14 June 2019. Accepted: 3 Sept 2019. Published online: 30 Sept 2019. 99 KAZUYA NAGASAWA

Fig. 1. Argulus japonicus, male (A) and female (B), NSMT-Cr 26691, ventral view, from the body surface of Carassius cuvieri in brackish waters of Lake Shinji, Shimane Prefecture, Japan, on 11 September 1973. Ethanol-preserved specimens. Scale bars: A–B, 1 mm. as Carassius auratus) in the brackish-water re- able features to characterize A. coregoni (To- gion (Suzumoto, 1974). Suzumoto (1974) ex- kioka, 1936; Yamaguti, 1937). In Lake Shinji, amined those fish and reported on the heavy in- A. japonicus was previously collected from fection of C. orientalis but did not state the common carp, Cyprinus carpio Linnaeus, 1758 concurrent infection with A. japonicus. He (Nagasawa et al., 2009). probably overlooked the two specimens of A. The present finding of A. japonicus from the japonicus mixed in the sample of over 600 fish in the drought-induced brackish waters of specimens of C. orientalis. Lake Shinji indicates that A. japonicus can sur- The specimens of A. japonicus consisted of vive in such salt waters, as previously observed one male and one female, measuring 4.0× in an aquarium (Yamauchi et al., 2011). The 2.5 mm and 4.8×3.1 mm, respectively (Fig. 1). salinity of Lake Shinji strikingly increased in They were damaged, probably due to rough re- July 1973 (Suzumoto, 1974), and the parasite moval from the host fish and/or infection in specimens were sampled on 11 September brackish waters. Thus, their detailed morpho- 1973. Thus, A. japonicus most likely could sur- logical features were not observed well, but vive for about two months in brackish waters. they correspond to A. japonicus described by In other words, the species is able to tolerate Tokioka (1936) and Yamaguti (1937). The salinity change for a certain period. male specimen somewhat resembles that of Ar- Carassius cuvieri is endemic to gulus coregoni Thorell, 1864 but has not a and the Yodo River system, central Japan, and digitiform process on the dorso-posterior mar- has been introduced to many Japanese rivers gin of the second leg, which is one of the reli- and lakes, including Lake Shinji. The Hii River

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flows into the western end of Lake Shinji, and ■ Literature Cited the salinity of the lake increases from the west- ern coast towards the eastern area (Date et al., Causey, D., 1960. “Creepin, blastit wonner” or on 1989). While C. cuvieri is generally regarded the misidentification of common Argulus of as a freshwater species, it is actually euryhaline freshwater fish. Turtox News, 38: 70–75. as it is known to occur even in the brackish Cressey, R. F., 1972. The genus Argulus (Crusta- lower reaches of the Nagara River, a big river cea: Branchiura) of the United States. Biota in central Japan (Suzuki & Kimura, 1977, of Freshwater Ecosystems. Identification 1978). In Lake Shinji and its adjacent region, Manual 2. 14 pp. Environmental Protection C. cuvieri usually occurs in the lower reaches Agency, Washington, DC. of the Hii River and the western (freshwater) Date, Y., Hashitani, H., Seike, y., Kondo, K., area of the lake (Koshikawa, 1985), where the Okumura, M., & Fujinaga, K., 1989. Water quality of Lake and Lake Shinji as individual of C. cuvieri examined by Suzumoto seen from the results of monthly observation (1974) perhaps became infected by A. japoni- for 12 years̶seasonal variation, secular cus. Moreover, because of its salt tolerance, variation and typical value̶. Studies of the this individual is considered to have survived San’in Region, 5: 89–102. (In Japanese with along with A. japonicus in the drought-induced English abstract) brackish waters. Koshikawa, T., 1985. Pisces of Lake Shinji. Argulus flavescens Wilson, 1916 and A. ko- Freshwater fish: Annual Bulletin of the sus Avenant-Oldewage, 1994 are known to oc- Freshwater Fish Protection Association, 11: cur in both fresh and salt waters in North 10–14. (In Japanese with English title) America (Causey, 1960; Cressey, 1972; Nagasawa, K., 2004. Sea lice, Lepeophtheirus Suárez-Morales et al., 1998) and South Africa salmonis and Caligus orientalis (Copepoda: (Van As et al., 1999), respectively. These spe- Caligidae), of wild and farmed fish in sea cies are completely separated from A. japoni- and brackish waters of Japan and adjacent cus in their geographical distribution, and, regions: A review. Zoological Studies, 43: most probably, their euryhaline characteristic 173–178. has evolved independently. For understanding Nagasawa, K., 2009. Synopsis of branchiurans of their occurrence and host utilization within the genus Argulus (Crustacea, Argulidae), their distributional range, it is desirable to ex- ectoparasites of freshwater and marine fish- perimentally access their tolerance to various es, in Japan (1900–2009). Bulletin of the salinities. Biogeographical Society of Japan, 64: 135– The specimens of A. japonicus are deposited 148. (In Japanese with English abstract) in the Crustacea collection of the National Mu- Nagasawa, K., 2011a. The biology of Argulus seum of Nature and Science, Tsukuba, Ibaraki spp. (Branchiura, Argulidae) in Japan: A re- Prefecture, Japan (NSMT-Cr 26691). view. In: A. Asakura et al., (eds.), New Frontiers in Crustacean Biology, Proceed- ings of the TCS Summer Meeting, Tokyo, ■ Acknowledgments 20–24 September 2009. Crustaceana Mono- graph, 15: 15–21. I thank the staff of the Laboratory of Aquatic Nagasawa, K., 2011b. Branchiura. In: O. A. Ti- Pathology, Hiroshima University, for giving moshkin, (ed.), Index of Animal Species In- me the opportunity to examine the specimens. habiting Lake Baikal and its Catchment Area: Volume II. Basins and Channels in the South of East Siberia and North Mongolia,

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tematic Parasitology, 43: 75–80. Yamauchi, T., Nakano, H., & Nagasawa, K., Yamaguti, S., 1937. On two species of Argulus 2011. Infection with Argulus japonicus on from Japan. In: R.-E. S. Schulz, & M. P. Amur catfish Silurus asotus in an aquarium. Gnyedina, (eds.), Papers on Helminthology Japanese Journal of Limnology, 72: 211– Published in Commemoration of the 30 Year 214. (In Japanese with English abstract) Jubileum of the Scientific, Educational and Social Activities of the Honoured Worker of Addresses Science K. J. Skrjabin, M. Ac. Sci. and of (KN) Graduate School of Integrated Sciences the 15th Anniversary of All-Union Institute for Life, Hiroshima University, 1–4–4 Kagami- of Helminthology, Lenin All-Union Acade- yama, Higashi-Hiroshima, Hiroshima 739– my of Agricultural Science, Moscow, pp. 8528, Japan; present address: Aquaparasitology 781–784. Laboratory, 365–61 Kusanagi, Shizuoka 424– Yamauchi, T., & Shimizu, M., 2013. New and 0886, Japan. distribution records for the freshwater fish ectoparasite Argulus japonicus (Crustacea: Branchiura: Argulidae). Comparative Parasi- tology, 80: 136–137. E-mail address of corresponding author (KN) [email protected]

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