Species Diversity 20: 191–197 25 November 2015 DOI: 10.12782/sd.20.2.191

Pseudorhadinorhynchus samegaiensis (: : ) Uses the Amphipod Jesogammarus (Annanogammarus) fluvialis as an Intermediate Host in a Stream of the Lake Biwa Basin, Central Japan

Kazuya Nagasawa1,4 and Yasuhiro Fujioka2,3 1 Graduate School of Biosphere Science, Hiroshima University, 1-4-4 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8528, Japan E-mail: [email protected] 2 Lake Biwa Museum, 1091 Oroshimo, Kusatsu, Shiga 525-0001, Japan 3 Shiga Prefecture Fisheries Experiment Station, 2138-3 Hassaka, Hikone, Shiga 522-0057, Japan E-mail: [email protected] 4 Corresponding author (Received 28 July 2015; Accepted 27 October 2015)

Cystacanths and acanthellae of the illiosentid acanthocephalan samegaiensis Nakajima and Egusa, 1975 are described from the anisogammarid amphipod Jesogammarus (Annanogammarus) fluvialis Morino, 1985 in a stream at the Samegai Trout Experimental Station, the type locality of the acanthocephalan, in the Lake Biwa basin, Shiga Prefecture, west-central Japan. This amphipod is herein regarded as an intermediate host of P. samegaiensis. This is the first description of developmental stages of any member of the Pseudorhadinorhynchus Achmerov and Dombrovskaja- Achmerova, 1941. Since J. (A.) fluvialis does not occur in the Lake Biwa proper but two other congeners, J. (A.) annandalei (Tattersall, 1922) and J. (A.) naritai Morino, 1985, inhabit the lake, it is suggested that P. samegaiensis uses one or both of the latter two amphipods as its intermediate host(s) in the lake. Key Words: Pseudorhadinorhynchus samegaiensis, Acanthocephala, parasite, life cycle, Jesogammarus (Annanogam- marus) fluvialis, , Lake Biwa basin, Japan.

Recently, individuals of the amphipod Jesogammarus Introduction (Annanogammarus) fluvialis Morino, 1985 (Gammaroidea: Anisogammaridae) collected at the Samegai Trout Experi- Acanthocephalans of the illiosentid genus Pseudorhadino- mental Station were found to be infected with cystacanths rhynchus Achmerov and Dombrovskaja-Achmerova, 1941 and acanthellae of P. samegaiensis. In this paper, we describe (: Echinorhynchida) currently com- these cystacanths and acanthellae. prise 18 valid (Amin 2013). They are found in the intestine of fish, but no life cycle is known for any species of this genus. Two species of the genus occur in Japan: P. s a - Materials and Methods megaiensis Nakajima and Egusa, 1975 (Nakajima et al. 1975; Nakajima and Egusa 1975b; Grygier 2004, 2013; Amin et al. Specimens of J. (A.) fluvialis were sampled twice using a 2007; Nagasawa and Grygier 2011) and P. leuciscus (Krotov hand net in a stream along the Nyuu River flowing through and Petrochenko, 1956) (Machida and Araki 1982; Araki the Samegai Trout Experimental Station (35°17′57″N, and Machida 1987; Hashimoto 2000). The former species 136°20′19″E), the type locality of P. samegaiensis (Nakajima was originally described by Nakajima and Egusa (1975b) and Egusa 1975b), at Kami-nyuu, Maibara, Shiga Prefecture, based on specimens from rainbow trout Oncorhynchus west-central Japan. The first lot of specimens (their number mykiss (Walbaum, 1729) (as Salmo gairdnerii irideus Gib- was not counted) was collected on 20 June 2012 from the bons, 1885) (Salmoniformes: Salmonidae) at the Samegai downstream section of the stream and brought alive to the Trout Experimental Station, Shiga Prefecture, west-central laboratory at the Lake Biwa Museum, Kusatsu, Shiga Prefec- Japan. This station is located on the Nyuu River within the ture, where only infected amphipods (n=10) were dissect- watershed of Lake Biwa, which is the largest (640 km2) and ed for acanthocephalan larvae. The second lot (n=123 in oldest (over four million years old) lake in Japan (Horie total) was collected on 10 October 2014 from the upstream 1984), and the acanthocephalan has so far been reported (n=58) and downstream (n=65) sections of the stream and only from Lake Biwa and its watershed (Grygier 2004, 2013; transported alive to the laboratory at Hiroshima University, Amin et al. 2007; Nagasawa and Nitta 2015). Higashi-Hiroshima, Hiroshima Prefecture, where all speci-

© 2015 The Japanese Society of Systematic Zoology 192 K. Nagasawa and Y. Fujioka mens were dissected after being measured for body length (18.7%) of the 123 amphipods collected on 10 October 2014 (BL). On both occasions, acanthocephalan larvae removed harbored a total of 30 larvae, consisting of 29 cystacanths from the amphipods were flattened between slides and cover (12 males, 17 females) and one acanthella (one male). The glasses with slight pressure, fixed in 70% ethanol, stained sex ratio of these larvae was 0.87 : 1 (26 males to 30 females). in alum carmine or Heidenhain’s iron hematoxylin, dehy- The cystacanths (n=54) were further divided into two stag- drated through a graded ethanol series, cleared in xylene, es, i.e., early (n=13) and fully developed (=infective, n=41) and mounted in Canada balsam. When the larvae were cystacanths. flattened, the proboscis and copulatory bursa of some in- The presence of an infective cystacanth in the hemocoel dividuals were partially or fully everted. The stained speci- was recognized as a faint orange spot (Fig. 1A), and the live mens were used for measurements and counts, and some infective and early cystacanths dissected free from the am- live specimens were also observed. All measurements in phipods were faint orange and white in body coloration, re- the text are given in millimeters as the range followed by spectively (Fig. 1B). Infective cystacanths were surrounded the mean in parentheses. Drawings were made with the aid by a thin membranous envelope in the hemocoel. of a drawing tube fitted on an Olympus BX 51 compound Prevalence and intensity of infection. Intensity of lar- microscope. Five slides of developmental stages of P. s a - val P. samegaiensis in amphipods (BL not measured) collect- megaiensis collected on 10 October 2014 are deposited in ed on 20 June 2012 ranged from one to five (mean intensity: the Aschelminthes (As) collection of the National Museum 2.6), but no data on their prevalence of infection were taken of Nature and Science, Tsukuba, Ibaraki Prefecture, Japan because only infected amphipods were dissected. In con- (NSMT–As 4296). Prevalence, intensity, mean intensity, and trast, on 10 October 2014 there was a significant difference mean abundance of infection are as defined by Bush et al. in prevalence and mean abundance of larval P. samegaiensis (1997). Amphipods were identified based on Morino (1985) in amphipods between the two sampling sites, the upstream and Tomikawa and Morino (2012). The scientific names of and downstream sections of the stream, although mean in- fish, amphipods, and isopods used in this paper follow those tensity did not differ significantly between the two sites recommended by Nakabo (2013), Tomikawa and Morino (Table 1). (2012), and Matsumoto (1973), respectively. Of the 33 infected amphipods, more than half (63.6%) harbored a single larva, but seven (21.2%), one (3.0%), two (6.1%), and two (6.1%) carried two, three, four, and five lar- Results vae, respectively (Fig. 1). Description of acanthella. Based on a male specimen In total, 54 cystacanths and two acanthellae of P. s a - (Fig. 2A), 1.67 long by 0.48 wide. Body fusiform. Proboscis megaiensis were found in the hemocoel of J. (A.) fluvialis. receptacle distinct, with apical nuclei at anterior extremity, Twenty-six larvae were collected from the 10 infected am- posterior proboscis nuclei at mid-length, and cerebral gan- phipods on 20 June 2012, consisting of 25 cystacanths (12 glion at base. Lemniscal giant nuclei located around mid- males, 13 females) and one acanthella (one male), and 23 length of proboscis receptacle. Giant subcuticular nuclei

Fig. 1. Jesogammarus (Annanogammarus) fluvialis infected with two fully developed cystacanths (a, b) and one early cystacanth (c) of Pseudorhadinorhynchus samegaiensis. A, Lateral view of amphipod harboring three cystacanths in hemocoel; B, three cystacanths dissected free from amphipod. Note faint orange spots (a, b) in amphipod’s hemocoel (A) and faint orange body surface of cystacanths (B). Scale bars: A, 2 mm; B, 1 mm. Life cycle of a fish acanthocephalan 193

Table 1. Comparison between infection level of larval Pseudorhadinorhynchus samegaiensis in amphipods Jesogammarus (Annanogamma- rus) fluvialis from the upstream and downstream sections of a stream flowing through the Samegai Trout Experimental Station on 10 Octo- ber 2014.

No. of amphipods examimed Body length (mean) in mm Prevalence (%) Intensity (total) Mean intensity Mean abundance Upstream section 58 5.5–9.5 (mean 7.0) 31.0 1–3 (24) 1.33 0.41 Downstream section 65 6.5–10.5 (mean 8.0) 7.7 1–2 (6) 1.20 0.09 P<0.01* P>0.05** P<0.01** * Chi-square test. ** Student’s t-test. fragmenting. Reproductive system differentiated: testes, ce- genus. ment glands, and copulatory bursa distinct. The proboscis armament (13–14 rows of 9–11 hooks Description of early cystacanth. Based on two male each) of the fully developed cystacanths collected in this and two female specimens with fully everted proboscis, study agrees with that in the original description (14 rows of 3.25–3.63 (3.44) long by 0.64–0.67 (0.66) wide and 2.30– 9–11 hooks each) of adult P. samegaiensis by Nakajima and 2.88 (2.59) long by 0.41–0.57 (0.49) wide, respectively; a Egusa (1975b) from the Samegai Trout Experimental Station male specimen with partially everted proboscis (Fig. 2B), and the subsequent brief description (13–14 rows of 9–10 2.83 long, excluding everted copulatory bursa, by 0.70 wide; hooks each) of adult by Amin et al. (2007) from and two female specimens with inverted proboscis (Fig. Lake Biwa and several of its inflowing rivers, including a site 2C), 2.87–3.75 (3.31) long by 0.71–0.82 (0.77) wide. Body downstream from the station in the Nyuu River. cylindrical with anterior part of trunk covered with cuticu- lar spines. Proboscis inverted but eversible with almost fully developed hooks. Proboscis receptacle double-walled with Discussion cerebral ganglion near base. Lemnisci distinct, longer than proboscis receptacle. Development of reproductive system Two species of acanthocephalan are known to parasitize nearly completed: copulatory bursa eversible in male; ovar- the fish cultured at the Samegai Trout Experimental Station, ian balls in a mass in female. Genital pore terminal. where the amphipods were sampled in this study: one is P. Description of fully developed (=infective) cysta- samegaiensis and the other is opsariich- canth. Based on three male and three female specimens thydis Yamaguti, 1935 (Echinorhynchida: Echinorhynchi- with fully everted proboscis (Fig. 2D–E), 2.78–3.13 (2.99) dae) (Ito 1959; Nakajima et al. 1975; Nakajima and Egusa long by 0.92–1.01 (0.96) wide and 3.78–4.28 (4.06) long by 1975a, 1975b). Another potential intermediate host of P. 0.85–1.03 (0.95) wide, respectively; and a male and three fe- samegaiensis, the isopod Asellus hilgendorfii Bovallius, 1886 male specimens with inverted proboscis, 1.93 long by 0.70 (Aselloidea: Asellidae), also occurs at this location (Ito 1959; wide and 2.38–2.80 (2.59) long by 0.81–2.80 (0.98) wide, Nagasawa and Fujioka unpublished). In fact, Ito (1959) re- respectively. Body of inverted cystacanths lemon-shaped ported larval acanthocephalans, identified as Acanthocepha- (Fig. 1B); trunk of everted cystacanths consisting of ante- lus sp. (misspelled as Acanthocepharus sp.) from A. hilgen- rior cylindrical and posterior fusiform portions. Trunk with dorfii (as A. nipponensis Nicholas, 1929) and the amphipod cuticular spines in anterior portion but only some spines in Gammarus sp. (misspelled as Gonmarus sp. and Ganmarus anterior part of posterior portion. Proboscis inverted but sp.) (Gammaroidea: Gammaridae). This amphipod was eversible, cylindrical, slightly bulbous near base, armed with very likely J. (A.) fluvialis because only this species has been hooks arranged in 13–14 longitudinal rows of 9–11 hooks confirmed to occur in streams at the Samegai Trout Experi- each (Fig. 2F). Largest hooks, 0.057–0.065 (0.061) long in mental Station and its adjacent region (Kusano 2009). No male (n=4) and 0.073–0.079 (0.076) long in female (n=4), specimen of J. (A.) fluvialis examined in the present study third or fourth from apex; basal hooks smallest. Neck short. harbored any larvae of Acanthocephalus opsariichthydis, Proboscis receptacle double-walled with cerebral ganglion which indicates that only P. samegaiensis uses J. (A.) fluvialis near base, extending into anterior portion of trunk in evert- as its intermediate host at this location. To confirm whether ed specimens. Lemnisci much longer than proboscis recep- Asellus hilgendorfii also serves as an intermediate host for P. tacle. Reproductive system completely developed, but ovar- samegaiensis there, it is necessary to examine individuals of ian balls still in a mass. Genital pore terminal. A. hilgendorfii from this location for larval acanthocepha- Remarks. Aquatic amphipods have been reported to lans. serve as intermediate hosts for acanthocephalans of the fam- Sixteen nominal and some unidentified species of acan- ily Illiosentidae Golvan, 1960 (Buckner et al. 1978; Orecchia thocephalan have been reported from freshwater fish in et al. 1978; see also Schmidt 1985), in which the genus Pseu- Japan (Shimazu 1999; Amin 2005) but their life cycles and dorhadinorhynchus is placed, but to date there has no pub- intermediate hosts are poorly understood. Three species lished information on life cycles and developmental stages of aquatic crustacean (one isopod and two amphipods) of acanthocephalans of this genus. This paper is the first are known to serve as intermediate hosts for four nominal description of developmental stages of any member of the and two unidentified acanthocephalans: the isopod Asellus 194 K. Nagasawa and Y. Fujioka

Fig. 2. Developmental stages of Pseudorhadinorhynchus samegaiensis. A, Male acanthella; B, early male cystacanth with part of proboscis and copulatory bursa everted, same individual as “c” in Fig. 1B; C, early female cystacanth; D, fully developed male cystacanth with everted proboscis; E, fully developed female cystacanth with everted proboscis; F, everted proboscis of fully developed female cystacanth (E). Scale bars: A, 300 µm; B–E, 500 µm; F, 200 µm. Life cycle of a fish acanthocephalan 195 hilgendorfii for Acanthocephalus acerbus Van Cleave, 1931 stream of the stream flowing through the Samegai Trout (Nakai and Koumi 1932), A. minor Yamaguti, 1935 (Awa­ Experimental Station (Table 1). This is probably due to the kura 1972; Nagasawa et al. 1982), A. opsariichthydis (Naga- fact that adult rainbow trout Oncorhynchus mykiss were sawa et al. 1983), and Acanthocephalus spp. (Mayama 1989, abundantly cultured near the former site. They have been 1990; Ohtaka et al. 2002; Kakizaki et al. 2003); and the two reported to suffer heavy acanthocephalan infection at this amphipods Sternomoera japonica (Tattersall, 1922) [as Par- station (Ito 1959; Nakajima et al. 1975), and the eggs of P. amoera japonica in Nagasawa and Egusa (1981)] (Gamma- samegaiensis passed from such fish may be abundantly sup- roidea: Pontogeneiidae) and Jesogammarus (Annanogamma- plied to the site, where the amphipods can easily become in- rus) naritai Morino, 1985 [as J. naritai in Shimazu (1999)] fected. (Gammaroidea: Anisogammaridae) for cotti It is well known that amphipods infected with acantho- Yamaguti, 1935 (Nagasawa and Egusa 1981; Shimazu 1999). cephalan cystacanths may exhibit altered behavior and More work is needed on the life cycles of acanthocephalans body pigmentation (e.g., Holmes and Bethel 1972; Nickol that infect freshwater fish in Japan. 1985; Moore 2002). In this study, up to five larvae of P. s a - Pseudorhadinorhynchus samegaiensis occurs in fish in megaiensis were found infecting a single J. (A.) fluvialis, but Lake Biwa proper and several of its inflowing rivers (Amin our preliminary observations indicate no color alteration et al. 2007) as well as at the present sampling location (Na- of the hosts, although they had faint orange spot(s) in the kajima et al. 1975; Nakajima and Egusa 1975b). Jesogamma- hemocoel (Fig. 1A). Detailed examination and experiments rus (A.) fluvialis is found in the eastern part of Shiga Pre- with the cystacanth of P. samegaiensis in J. (A.) fluvialis are fecture including the sampling location but does not occur needed to assess the impact of this acanthocephalan on the in Lake Biwa proper (Kusano 2009). Instead, four other spe- behavior and pigmentation of the amphipod. cies of amphipod, viz., Jesogammarus (Annanogammarus) annandalei (Tattersall, 1922), J. (A.) naritai [as J. naritai in Kusano (2009)] (Gammaroidea: Anisogammaridae), Ka- Acknowledgments maka biwae Uéno, 1943 (Gammaroidea: Kamakidae), and Crangonyx floridanus Bousfield, 1963 (Gammaroidea: Cran- We thank Mark J. Grygier, Lake Biwa Museum (LBM), gonyctidae), occur in Lake Biwa (Narita 1976; Morino 1985, for arranging permission to use his museum’s laboratory fa- 1994; Tomikawa et al. 2007; Kusano 2009; Nishino 2012). cilities, and Masato Nitta, Graduate School of Biosphere Sci- The former three species are endemic to Lake Biwa (Nishino ence, Hiroshima University, for staining the specimens. We 2011a, 2011b, 2011c, 2012 [as J. annandalei and J. naritai in are also grateful to two anonymous reviewers and Mark J. Nishino (2011b, 2001c)]) but the fourth species was only re- Grygier, LBM, for valuable comments to improve the manu- cently recorded from it as an alien invasive species (Nishino script. 2007; Kaneko et al. 2012). In particular, both J. (A.) nari- tai and J. (A.) annandalei (as Anisogammarus annandalei in Narita [1976]; J. annandalei in Trevorrow and Tanaka References [1997], Ishikawa and Urabe [2002], Godo and Ban [2007], Jiao et al. [2015]) are found in coastal and offshore waters Amin, O. M. 2005. Occurrence of the subgenus Acanthosentis Verma & of the lake, respectively (Narita 1976; Trevorrow and Tanaka Datta, 1929 (Acanthocephala: Quadrigyridae) in Japan, with the 1997; Ishikawa and Urabe 2002; Godo and Ban 2007; Jiao description of Acanthogyrus (Acanthosentis) alternatspinus n. sp. and A. (A.) parareceptaclis n. sp. from Lake Biwa drainage et al. 2015), and we suggest that P. samegaiensis most like- and a key to the species of the subgenus. Systematic Parasitology ly uses one or both of these amphipods as its intermediate 60: 125–137. host(s) in Lake Biwa, although the Red Data Book of Japan Amin, O. M. 2013. Classification of the Acanthocephala. Folia Parasito- lists the amphipods (as J. naritai and J. annandalei in Mori- logica 60: 273–305. no [2014a, b]) as near threatened species (Morino 2014a, b). Amin, O. M., Nagasawa, K., and Grygier, M. J. 2007. Host and - Recently, Nagasawa and Nitta (2015) suggested that P. s a - sonal distribution of fish acanthocephalans from Lake Biwa basin, megaiensis is not endemic to the Lake Biwa basin but also Japan. Comparative Parasitology 74: 244–253. occurs in other areas of Japan, under the assumption that Araki, J. and Machida, M. 1987. Some acanthocephalans from marine a widely distributed cyprinid, the big-scaled redfin Tribolo- fishes of northern Japan, with descriptions of two new species, don hakonensis (Günther, 1877), is its usual definitive host, Acanthocephaloides ichiharai and A. claviformis. Bulletin of the National Science Museum, Tokyo, Series A 13: 1–11. as Amin et al.’s (2007) data on the occurrence of mature fe- Awakura, T. 1972. 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Para- sitology meets ecology on its own terms: Margolis et al. revisited. the upstream part than in those from the farther down- 196 K. Nagasawa and Y. Fujioka

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