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Annanogammarus) Fluvialis As an Intermediate Host in a Stream of the Lake Biwa Basin, Central Japan

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Annanogammarus) Fluvialis As an Intermediate Host in a Stream of the Lake Biwa Basin, Central Japan Species Diversity 20: 191–197 25 November 2015 DOI: 10.12782/sd.20.2.191 Pseudorhadinorhynchus samegaiensis (Acanthocephala: Echinorhynchida: Illiosentidae) 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 Pseudorhadinorhynchus 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 genus 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, fish parasite, life cycle, Jesogammarus (Annanogam- marus) fluvialis, Amphipoda, 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 (Palaeacanthocephala: Echinorhynchida) currently com- these cystacanths and acanthellae. prise 18 valid species (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 worms 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.
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