further record of pontobdella macrothela (hirudinida

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Biogeography 23.

Further record of Pontobdella macrothela (Hirudinida: Piscicolidae),an ectoparasite of elasmobranchs, from Japan, with an updated list of its hosts and

collection localities in Japan

Kazuya Nagasawa 1,2*, Hikaru Nakano 3, and Ryosuke Ichikawa 4

1 Graduate School of Integrated Sciences for Life, Hiroshima University, 1–4–4 Kagamiyama,Higashi-Hiroshima, Hiroshima 739–8528, Japan

2 Present address: Aquaparasitology Laboratory, 365–61 Kusanagi, Shizuoka 424–0886, Japan3 Fukui Prefecture Inland Waters Fisheries Cooperative Association, 34–10 Nakanogo-cho, Fukui 910–0816, Japan

4 Hino Store, Kakujo Gyorui, 271–1 Kawabe-Horinouchi, Hino, Tokyo 191–0015, Japan

Abstract: Eight individuals of the piscicolid leech Pontobdella macrothela Schmarda, 1861 were collected from the buccal cavity of a Japanese bullhead shark, Heterodontus japonicus Miklouho-Maclay & Macleay, 1884 (Elasmobranchii: Heterodontidae), in Okada Port, Izu-Oshima Island (the northwestern Pacific), central Japan. This collection represents the first record of P. macrothela from wild Japanese bullhead shark. This paper also provides an updated list of the known hosts and collection localities of P. macrothela in Japan, based on the literature published between 1910 and 2021. Seven nominal species of elasmobranchs have been reported as the hosts of P. macrothela from Japan, where the species is found in coastal waters affected by two warm currents, the Kuroshio, and its branch, the Tsushima Current. Coastal rocky reefs and lagoons may be important sites for infestation of bottom-associated elasmobranchs by P. macrothela.

Key words: fish parasite, marine leech, elasmobranchs, Pontobdella macrothela, Japanese bullhead shark, Heterodontus japonicus, host list

Introduction

The piscicolid leech Pontobdella macrothela Schmarda, 1861 is a parasite of elasmobranchs worldwide (Llewellyn, 1966; Sawyer et al., 1975; Burreson & Passarelli, 2015; Burreson, 2020). In Japan, the species was originally described by Oka (1910a) as Pontobdella bimaculata. As its original description was very short, the same author (Oka, 1927a) later reported its external morphology in detail. During the 20th century, the species was reported as P. bimaculata in various publications in Japan (Oka, 1910b, 1927c, 1935, 1947b; Iijima, 1918; Oka & Nagao, 1965a; Nishimura & Suzuki, 1971; Honma & Kitami, 1978; Suzuki, 1979; Yamashita, 1980; Imajima, 1983, 1997; Nishimura, 1992; Anonymous, 1997). A different generic name (Pontobdellina) was also used for the species (Ono, 1998). Subsequently, Pontobdella bimaculata was relegated to a junior synonym of Stibarobdella macrothela (Furiness et al., 2007), and the latter name was commonly used during the late 2000s and early 2010s (Yamauchi et al., 2008; Nagasawa & Hagiwara, 2008; Nagasawa et al., 2008, 2009; Nagasawa & Toda, 2010). Currently, however, Stibarobdella has been synonymized with

Pontobdella (Burreson & Passarelli, 2015), and P. macrothela is used as a valid name of the species in this paper.

In 2019, we collected specimens of P. macrothela from a Japanese bullhead shark, Heterodontus japonicus Miklouho-Maclay & Macleay, 1884, at Izu-Oshima Island, central Japan. These specimens are reported herein as the first record of P. macrothela from wild Japanese bullhead shark. Previously, Yamauchi et al. (2008) compiled a list of the elasmobranch hosts of P. macrothela from Japan and other countries. The present paper also provides an updated list of the Japanese elasmobranch hosts and collection localities, based on the literature published between 1910 and 2021.

Materials and Methods

An individual of Japanese bullhead shark was collected by the one of the authors (RI) with hook and line using fish bait on 5 November 2019 in Okada Port (34°47’32.4”N, 139°23’20.4”E), Izu-Oshima Island (the northwestern Pacific), central Japan. When the fish was dissected in a fresh condition by the second author (HN) for anatomical study, leeches were found in the buccal cavity of the fish, collected, and then kept frozen. These leeches were transported to the Aquaparasitology Laboratory, Shizuoka Prefecture, where

−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−*Corresponding author: [email protected]

15–21. Sep. 20, 2021

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Pontobdella macrothela, a parasite of elasmobranchs

they were thawed and examined for their morphology and coloration using an Olympus SZX10 stereo microscope. They were measured for body length (from the anterior end of the oral sucker to the posterior end of the caudal sucker), body width (maximum width in the urosome), and sucker width (maximum width in the oral and caudal suckers). Voucher specimens of P. macrothela preserved in 70% ethanol have been deposited in the Annelida (An) collection of the National Museum of Nature and Science, Tsukuba, Ibaraki Prefecture, Japan (NSMT-An 631). The scientifi c and common names of fi shes mentioned in this paper follow those recommended in FishBase (Froese & Pauly, 2021).

Results

Genus Pontobdella Leach, 1815(Synonym: Stibarobdella Leigh-Sharpe, 1925,

based on Burreson & Passarelli, 2015)[Japanese name: Umibiru-zoku, based on Iijima, 1918,

see Nagasawa et al., 2008]

Pontobdella macrothela Schmarda, 1861[Japanese name: Akame-umibiru, based on Oka, 1927c]

(Fig. 1)

Synonyms (restricted to the records from Japan)Pontobdella bimaculata Oka, 1910: p. 171; Oka, 1910b: p. 17;

Iijima, 1918: p. 430, fi g. 515B; Oka, 1927a: pp. 90–93, fi g. 1; Oka, 1927c: p. 1599, fi g. 3062; Oka, 1935: p. 240; Oka, 1947b: p. 1387, fig. 3928 (encyclopedia); Oka & Nagao, 1965a: p. 570, unnumbered fi g. (encyclopedia); Nishimura & Suzuki, 1971: p. 52, fig. 9 (encyclopedia); Honma & Kitami, 1978: p. 37; Suzuki, 1979: p. 134; Imajima, 1983: pp. 89 (original photograph), 191 (encyclopedia); Nishimura, 1992: p. 378, pl. 72–12, fig. 19–8C (original photograph) (encyclopedia); Anonymous, 1997: p. 46; Imajima, 1997: p. 114, unnumbered fig. (original photograph) (encyclopedia).

Pontobdellina macrothela (Schmarda, 1861): Ono, 1998: p. 48 (checklist).

Stibarobdella macrothela (Schmarda, 1861): Llewellyn, 1966: p. 410; Furiness et al., 2007: pp. 880–881, fi g. 13; Yamauchi

Fig. 1. Pontobdella macrothela, NSMT-An 631. A, leeches attached to the buccal cavity wall, near the posterior teeth, of a Japanese bullhead shark, Heterodontus japonicus. Five leeches (1–5) are seen; B, largest leech, 50.1 mm long, dorsal view; C, oral suck-er with a pair of crown-shaped eyespots (arrowheads) and four pairs of papillae (1–4), dorsal view; D, oral sucker and anterior half of trachelosome, dorsal view; E, middle part of urosome, dorsal view; F, posterior part of urosome, and caudal sucker, dorsal view. A, fresh specimens; B–F, frozen-thawed specimen. Abbreviations: cs, caudal sucker; os, oral sucker; pt, posterior teeth; tr, trachelosome; tu, tubercle; ur, urosome. Scale bars: A, 20 mm; B, 10 mm; C, 1 mm; D, F, 2 mm; E, 4 mm.

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Kazuya Nagasawa, Hikaru Nakano and Ryosuke Ichikawa

et al., 2008: pp. 53–57, figs. 1–4; Nagasawa & Hagiwara, 2008: pp. 2–3 (review), fig. 1 (original photograph); Nagasawa et al., 2008: pp. 160–161 (checklist); Nagasawa et al., 2009: pp. 38–39, fig. 1 (review); Nagasawa & Toda, 2010: pp. 34–37, figs. 1–2.

Occurrence on the host. Eight individuals of P. macrothela were found attached together using their caudal sucker to the buccal cavity wall, near the posterior teeth, of the Japanese bullhead shark examined (96.3 cm in total length) (Fig. 1A). The frozen-thawed, relaxed individuals show a wide variation in body length, measuring 28.1 to 50.1 (mean= 37.3, n=8) mm. Their body width ranges from 3.8 to 5.0 (mean=4.2, n=8) mm.

Description. Body cylindrical, slightly tapering towards suckers (Fig. 1B). Oral sucker, 1.6–3.4 mm (mean=2.1, n=8) wide, eccentrically attached, with a pair of crown-shaped brown eyespots and four pairs of papillae on dorsal surface (Fig. 1C). Caudal sucker, 2.5–4.1 mm (mean=3.1, n=8) wide, not cupped, centrally attached, larger than oral sucker with ratio of oral to caudal sucker diameter varying from 1:1.2 to 1:1.7 (mean, 1:1.5, n=8) (Fig. 1B, F). Tubercles on middle (a2) annulus of urosome square and much larger than those on a2 annulus of trachelosome (Fig. 1D–F). In frozen-thawed specimens, oral sucker and trachelosome yellowish brown (Fig. 1B–D) but urosome and caudal sucker light brown (Fig. 1E, F). Most of tubercles on a2 annulus of trachelosome dark brown but some of those white (Fig. 1D–F).

Remarks. Pontobdella macrothela is characterized by two distinct “trumpet-shaped” eyespots on the oral sucker, large square tubercles on the a2 annulus of the urosome, and a relatively large caudal sucker (Llewellyn, 1966; Furiness et al., 2007; Buresson, 2020). The leech specimens collected in this study show the same external morphology and are identified as P. macrothela. The eyespots of these specimens are crown-shaped (Fig. 1C, arrowheads), but different expressions have been used for the shape of the eyespots of the species: “coronet-shaped (ocular?)” (Llewellyn, 1966), “trumpet-shaped” (Furiness et al., 2007; Yamauchi et al., 2008), “trapezoid-shaped” (Daly et al., 2019a), and “circular” (Daly et al., 2019b). Despite such differences in the expression, the presence of two large eyespots on the oral sucker is the most important morphological character of P. macrothela and has been used for its identification (e.g., Furiness et al., 2007; Yamauchi et al., 2008; Daly et al., 2019a, b).

The caudal sucker is also an important character of the species and larger than the oral sucker. Llewellyn (1966) stated that the caudal sucker was “between two and three times the size of the” oral sucker in his specimens, but the ratios of both suckers in the specimens examined in the present study range

from 1:1.2 to 1:1.7, which are similar to those previously reported from the Japanese specimens (1:1.5 to 1:2, Furiness et al., 2007).

Moreover, an Australian specimen has a cupped caudal sucker (Burreson, 2020: fig. 15E), but the Japanese specimens reported in the previous and present papers have weakly cupped or flattened caudal sucker (Furiness et al., 2007: fig. 13; Yamauchi et al., 2008: fig. 2; Nagasawa et al., 2009: fig. 1; Nagasawa & Toda, 2010: fig. 1B; this paper: Fig. 1B, F).

Pontobdella macrothela occurs in tropical to subtropical waters of the Atlantic, Pacific, and Indian oceans (Llewellyn, 1966; Sawyer et al., 1975; Burreson & Passarelli, 2015; Burreson, 2020). In the western Pacific, the species has been reported from China (Llewellyn, 1966; Yamashita, 1980; Zheng et al., 2012), Micronesia (Yamauchi & Ota, 2012), Singapore (Silva & Fernando, 1965), Indonesia (Blanchard, 1897), and Australia (Goddard, 1909; Llewellyn, 1966; Burreson, 2020) as well as Japan. It may also occur in Brunei (Sawyer et al., 1982). In Japan, some collection localities extend to the temperate region (see the second paragraph of the Discussion below).

In addition to P. macrothela, another congeneric species, Pontobdella moorei Oka, 1910, is known to parasitize Japanese elasmobranchs (Oka, 1910a, b, 1927b, 1947a; Oka & Nagao, 1965b, 1979; Nishimura, 1992; Furiness et al., 2007, reported as Stibarobdella moorei; Nagasawa et al., 2008, 2009, as S. moorei). Pontobdella macrothela is distinguished from P. moorei by having two large crown-shaped eyespots on the oral sucker (Fig. 1C, D) and a large caudal sucker (Fig. 1B, F). In P. moorei, the oral sucker has a marginal fringe but no eyespots, and the caudal sucker is small and deeply cupped (Furiness et al., 2007; Burreson, 2020).

Pontobdella macrothela is not a site-specific parasite: it has been found from various body sites of Japanese elasmo-branchs, including the skin at the base of the pectoral fin, the clasper, the caudal peduncle, and the wall of the buccal cavity (Furiness et al., 2007; Yamauchi et al., 2008; Nagasawa & Toda, 2010; this paper).

Two reviews regarding the leeches of Japanese elasmo-branchs, including P. macrothela, are available (Nagasawa & Hagiwara, 2008; Nagasawa et al., 2009). One and some specimens of P. macrothela from Japan have been deposited, respectively, in the National Museum of Natural History, Paris, France (MNHN 18VV, Furiness et al., 2007) and the National Museum of Nature and Science, Tsukuba, Japan (NSMT-An 352–357, Furiness et al., 2007; NSMT-An 385–387, Yamauchi et al., 2008; NSMT-An 413, Nagasawa & Toda, 2010; NSMT-An 631, this paper).

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Discussion

Based on the literature published between 1910 and 2021, P. macrothela has been reported from seven nominal species of elasmobranchs in Japan, including five species of sharks in five families of two orders and two species of rays in two families of two orders (Table 1). Although the Japanese bullhead shark is among these hosts, P. macrothela was not collected previously from wild-caught individuals of the shark species. Thus, the present paper represents the first record of P. macrothela from a wild population of the Japanese bullhead shark.

In Japan, P. macrothela has been found from coastal waters of Honshu, one of the four major islands of Japan, and the Ryukyu Islands, which are affected by two warm currents, the Kuroshio, and its branch, the Tsushima Current (Fig. 2). The species occurs in the northwestern Pacific (localities 1–7), the East China Sea (locality 8), and the Sea of Japan (localities 9 and 10) around the Japanese Archipelago. The leech was also reported to “occur in coastal waters of Kyushu and Shikoku”, two major islands of southwestern Japan (Oka, 1927b, 1947b; Oka & Nagao, 1965b), but there are no published records to support it. As stated above, the coastal waters of Honshu (localities 1–5, 9 and 10) are influenced by the warm currents, but these waters are not located in the subtropical region, which shows that the species can occur in the temperate region as well. Both Sado Island and Nezugaseki (localities 9 and 10) are the known northernmost localities in the northwestern

Pacific. Interestingly, three individuals of P. macrothela were

collected with bottom trawl nets each at three sites in shallow waters (36–40 m deep) of the Yellow Sea off China

Table 1. Hosts and collection localities of Pontobdella macrothela in Japan. The scientific names of the host fishes follow Froese & Pauly (2021).

Fig. 2. Map of the Japanese Archipelago, showing the collection localities (closed circles) of Pontobdella macrothela. 1, Coast at Tateyama; 2, Sagami Bay off Arasaki; 3, Coast of Kanagawa; 4, Suruga Bay off Heta; 5, Izu-Oshima Island; 6, off Chi-nen, Okinawa-jima Island; 7, off Ishigaki-jima Island; 8, off Yomitan, Okinawa-jima Island; 9, Sado Island; 10, Nezugaseki. The routes of two warm currents, the Kuroshio, and its branch, the Tsushima Current, are also shown.

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(Yamashita, 1980). These individuals most probably detached from their elasmobranch hosts in the nets during fishing operations. The Yellow Sea is influenced by a warm current, the Yellow Sea Warm Current, a branch of the Tsushima Current (Ichikawa & Beardsley, 2002).

In this study, eight individuals of P. macrothela were collected from a single Japanese bullhead shark. This number follows 33 and 10 individuals of the same leech species recorded from, respectively, a round ribbontail ray, Taeniura meyeni (Müller & Henle, 1841), in Micronesia (Yamauchi & Ota, 2012) and a nurse shark, Ginglymostoma cirratum (Bonnaterre, 1788), in Puerto Rico and adjacent waters (Williams, 1988). Since the specimens of P. macrothela collected in this study show a wide body-length variation (28.1–50.0 mm), the host fish may have acquired repeated infestations.

Recently, Daly et al. (2019b) have suggested that the occurrence of P. macrothela on elasmobranch hosts is associated with both host behavioral and environmental factors. Although elasmobranch-infesting leeches including P. macrothela have not been clarified for their life cycles, some of piscicolid leeches are known to detach from their fish hosts for reproduction and then deposit cocoons on hard substrates. For example, Notostomum cyclostomum (Johansson, 1898) utilizes, on the soft bottom of the deep seas, the exoskeletons of crabs (Sloan et al., 1984; Nagasawa & Fujiwara, 2008) and the shells of gastropods (Epshtein & Utevski, 1996; Nagasawa & Ueda, 2013) as substrates for cocoon attachment. The two hosts of P. macrothela, i.e., the Japanese bullhead shark and the blotchy swell shark, Cephaloscyllium umbratile Jordan & Fowler, 1903 (see Table 1), inhabit coastal rocky reefs (Froese & Pauly, 2021), where P. macrothela most probably can utilize various hard substrates (e.g., rocks) for cocoon deposition and its juveniles that hatch out the cocoons are inferred to infest these bottom-associated sharks. The tiger shark, Galeocerdo cuvier Péron & Lesueur, 1822, also serves as a host for P. macrothela in Japan (see Table 1) and is known to frequently migrate into inshore areas, such as lagoons (Froese & Pauly, 2021), where individuals of the shark may get infested by juvenile leeches. Since P. macrothela infests aquarium-held elasmobranchs (Furiness et al., 2007; Nagasawa et al., 2009), it is desirable to study the life cycle of the species and conduct experimental infestations in tanks using various species of elasmobranchs of different swimming speeds and behaviors for clarifying its host utilization in the wild.

Acknowledgments

We thank Eugene M. Buresson, School of Marine Science, Virginia Institute of Marine Science, Gloucester Point, and

Tamaki Shimose, Fisheries Resources Institute, Japan Fisheries Research and Education Agency, Nagasaki, for their assistance with literature. We are also grateful to an anonymous reviewer for useful comments to improve the manuscript.

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Zheng, F.-w., Lin, J.-h. & Shin, P., 2012. Phylum Annelida. Pp. 278–400. In: Huang, Z. & Lin, M. (Eds.), The Living Species and Their Illustrations in China’s Seas (Part II), An Illustrated Guide to Species in China’s Seas, Vol. 3, Animalia (1). China Ocean Press, Beijing. (In Chinese and English).

(Received May 18, 2021; Accepted June 29, 2021)

further record of pontobdella macrothela (hirudinida

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