redescription of camallanus hypophthalmichthys

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The light and scanning electron microscopical examination made it possible to study in detail ... lanus Railliet and Henry, 1915 were collected from the cyprinid.

J. Parasitol., 90(6), 2004, pp. 1463–1467 q American Society of Parasitologists 2004

REDESCRIPTION OF CAMALLANUS HYPOPHTHALMICHTHYS DOGEL AND AKHMEROV, 1959 (NEMATODA: CAMALLANIDAE) AND ITS FIRST RECORD FROM FISHES IN CHINA Frantisˇek Moravec, Pin Nie*, and Guitang Wang* ˇ eske´ Budeˇjovice 370 05, Czech Republic. e-mail: Institute of Parasitology, Academy of Sciences of the Czech Republic, Branisˇovska´ 31, C [email protected] ABSTRACT: The nematode Camallanus hypophthalmichthys Dogel and Akhmerov, 1959 is redescribed from specimens collected from the intestine of the bighead carp Aristichthys nobilis, from Liangzihu Lake (Yangtze River basin), Hubei Province, central China. The light and scanning electron microscopical examination made it possible to study in detail the morphology of this so far little-known species and to confirm its validity. The main specific features of C. hypophthalmichthys distinguishing it from the most similar Camallanus spp. is the presence of 3 small caudal processes on the male tail tip, 13–16 longitudinal ridges on the inner surface of the valve of the buccal capsule, and the arrangement of preanal and postanal genital papillae in the male. This finding represents a new host record, the first record of this parasite in the Yangtze River basin, and the first documented record of C. hypophthalmichthys from China. Camallanus hypophthalmichthys is considered a specific intestinal parasite of fishes of the cyprinid Hypophthalmichthyinae.

In September 2002, during investigations into the helminth parasites of fishes in central China, carried out by the Chinese– Czech research team in central China (see also Moravec and Nie, 2002; Moravec and Wang, 2002; Moravec et al., 2003, 2003a, 2003b), numerous specimens of the nematode Camallanus Railliet and Henry, 1915 were collected from the cyprinid fish Aristichthys nobilis (Richardson, 1844) from Liangzihu Lake near Wuchan. These were identified as C. hypophthalmichthys Dogel and Akhmerov, 1959, a species described from the Amur River basin in eastern Russia (Dogel and Akhmerov, 1959). This material made possible a detailed study (including scanning electron microscopy) and redescription of this inadequately known parasite and a comparison with related congeneric species. The results obtained are presented in this study. MATERIALS AND METHODS The recovered nematodes were washed in physiological saline and then fixed in hot 4% formaldehyde solution. For light microscopical examination, the nematodes were cleared with glycerin. Drawings were made with the aid of a Zeiss drawing attachment. Specimens used for scanning electron microscopy (SEM) were postfixed in 1% osmium tetroxide, dehydrated through a graded ethanol series, critical point dried, and sputter coated with gold; they were examined using a JEOL JSM-6300 scanning electron microscope at an accelerating voltage of 15 kV. All measurements are in micrometers unless otherwise stated. The scientific names of fishes follow Froese and Pauly (2003).

REDESCRIPTION

Camallanus hypophthalmichthys Dogel and Akhmerov, 1959 (Figs. 1–3) Description: Medium-sized nematodes with thick, transversely striated cuticle and large, orange-brown capsule typical of genus. Body of large females reddish (brownish after fixation), with distinct dark-brown intestine; body of small specimens whitish. Mouth aperture slit shaped, dorsoventrally elongated, surrounded by 4 submedian cephalic papillae, pair of small lateral amphids, and 4 large sublateral sclerotized plates Received 2 February 2003; revised 1 April 2004; accepted 1 April 2004. * State Key Laboratory of Freshwater Ecology and Biotechnology and Laboratory of Fish Diseases, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, Hubei Province, People’s Republic of China.

extending posteriorly to about third of length of buccal capsule (Figs. 1C, D, 3A). Valves of buccal capsule roughly pentagonal in lateral view, internally bearing 13–16 smooth longitudinal ridges (some of them incomplete) not reaching posteriorly basal ring; some incomplete ridges with 1–3 interruptions (Fig. 1C, D); anterior end of each valve with fairly wide membranous margin. Narrow, sclerotized ring present at bottom of capsule, provided with 3 distinct, posteriorly protruding swellings (Fig. 1C, D). Tridents large, only moderately surpassing posterior border of buccal capsule (Fig. 1A–E). Excretory pore just posterior to level of nerve ring (Fig. 1A). Deirids very small, located at about three fourths of muscular esophagus (Fig. 1B). Intestine dark-brown, fairly narrow, equally broad almost throughout its length. Male (8 specimens): Length of body 4.65–6.64 mm, maximum width 218–272. Buccal capsule including basal ring 90– 96 long, maximum width 81–84; basal ring 9–12 long, 54–58 wide; length of tridents 69–78. Each valve of capsule strengthened internally by 13–15 longitudinal ridges, 4–8 of them being incomplete. Muscular esophagus 449–558 long, 72–96 wide; glandular esophagus 612–748 long, 75–102 wide; length ratio of both parts of esophagus 1:1.3–1.4. Nerve ring, excretory pore, and deirids 177–216, 210–300, and 399–450, respectively, from anterior extremity. Testis reaching anteriorly nearly to anterior end of glandular esophagus (Fig. 1A). Posterior end of body with vesiculate caudal alae supported by pedunculate papillae; latter difficult to observe because of densely granular structure of alae; caudal alae interconnected anteriorly by somewhat elevated transverse mound (Fig. 3D). Body markedly narrowed in region anterior to anterior end of caudal alae. Caudal papillae: 7 pairs of preanal and 6 pairs of postanal pedunculate papillae present (Figs. 1F, G, 2B, C, 3B, D, E). Preanal papillae: 6 pairs of subventral, equally spaced papillae, and 1 pair of lateral papillae situated at about level of last subventrals. Postanal papillae: 5 pairs of subventral and 1 pair of lateral papillae present; lateral pair just posterior to last but 1 subventral pair. Cloacal opening surrounded by 2 transverse mounds, forming laterally 2 pairs of additional, sessile papillae (Figs. 2B, 3B, E). Spicules unequal, simple, with sharply pointed distal ends (Fig. 2D, E). Large (right) spicule well sclerotized, 147–162 long; small (left) spicule weakly sclerotized, 108–126 long; length ratio of spicules 1:1.29–1.44. Tail conical, 90–111 long, with 3 minute, sometimes indistinct caudal projections at tip (Fig. 2B, C, H).

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Site of infection: Intestine (its posterior and middle sections). Locality: Liangzihu Lake (308059–308189N, 1148219– 1148399E; Yangtze River basin), Jiangxia District, Hubei Province, central China (collected 9 September 2002). Prevalence and intensity: In all, 3 specimens of A. nobilis examined; 4–39 (mean 17) nematodes per fish. Deposition of specimens: Helminthological collection of the Institute of Parasitology, Academy of Sciences of the Czech ˇ eske´ Budeˇjovice (cat. no. N-810) and in the InRepublic, in C stitute of Hydrobiology, Chinese Academy of Sciences, in Wuhan. DISCUSSION

FIGURE 1. Camallanus hypophthalmichthys. A–B. Anterior end of male, lateral, and dorsoventral views. C–D. Buccal capsule of male and gravid female, respectively, lateral views. E. Cephalic end of male, dorsoventral view. F–G. Caudal end of male, lateral and ventral views. H. Vulva, lateral view. I. Larva from uterus. Scale bars in millimeters.

Female (5 specimens with larvae; measurements of 2 specimens with eggs in parentheses): Body length 8.87–12.49 mm (7.71–7.97 mm), maximum width 449–585 (299–449). Buccal capsule including basal ring 117–126 (120) long, maximum width 114–123 (111–120); basal ring 21 (18) long, 75–87 (69– 78) wide; length of tridents 105–120 (105–120). Each valve of capsule with 14–16 (14–16) longitudinal ridges, 4–7 (4–6) of them being incomplete. Muscular esophagus 666–721 (558– 571) long, 105–120 (108–114) wide; glandular esophagus 884– 1,047 (762–843) long, 78–114 (90–111) wide; length ratio of both parts of esophagus 1:1.3–1.5 (1:1.4–1.5). Nerve ring, excretory pore, and deirids 240–272 (204–237), 270–313 (267– 270), and 693–720 (not located), respectively, from anterior extremity. Vulva near middle of body (slightly pre- or postequatorial), 3.77–8.77 mm (3.56–4.33 mm) from anterior extremity (at 42–53% [46–54%] of body length), with elevated anterior vulvar lip (Fig. 1H). Vagina muscular, directed posteriorly from vulva. Uterus filled with numerous larvae, not reaching posteriorly rectum. Larvae about 350 long and 18 wide, with rounded anterior and sharply pointed posterior ends (Fig. 1I). Tail conical, 435–571 (367–394) long (3.4–4.9% [4.8–4.9%] of body length), with 3 small (3 [3–5] long) conical caudal projections at tip (Fig. 2F, G). Two lateral phasmids present short distance anterior to caudal extremity (Figs. 2A, 3F). Taxonomic summary Host: Bighead carp, A. nobilis (Richardson, 1844) (Cyprinidae, Cypriniformes).

Camallanus hypophthalmichthys was described originally by Dogel and Akhmerov (1959) from the intestine of the cyprinid fish (silver carp) Hypophthalmichthys molitrix (Valenciennes) from the Amur River in the Russian Far East; the authors found it in about 25% of H. molitrix examined. However, the description is poor, not providing data on many taxonomically important features. According to information of Dr. Akhmerov provided to the first author of this paper (F.M.) in 1967, the type specimens of C. hypophthalmichthys were not deposited. This species has been cited erroneously as C. hypophthalmichthys Akhmerov, 1954 in the review of the Camallanidae by Ivashkin et al. (1971). Later, this species was recorded from the Amur River basin in eastern Russia by Roytman (1963) from H. molitrix from the Zeya River and by Finogenova (1971), reporting it from the intestine of H. molitrix and black carp Mylopharyngodon piceus (Richardson) from the region of Lake Bolon; the latter author gave the prevalence in H. molitrix to be 40%, with the intensity 1–4 nematodes per fish, whereas she considered the occurrence of C. hypophthalmichthys in M. piceus as accidental. Finogenova (1971) somewhat supplemented the original description and gave a few additional illustrations, but again this description remained very incomplete. Her data were later repeated by Vismanis et al. (1987). As far as the authors of this study know, this species has not been recorded since. Pan et al. (1990) and Zhang et al. (1999) mention C. hypophthalmichthys as 1 of the 3 Camallanus spp. parasitizing freshwater fishes in China, but this information is evidently based on data in Dogel and Akhmerov (1959) on the occurrence of this parasite in the Amur River, a major part of which forms the border between northeastern China and Russia. Wang et al. (1978) listed Camallanus sp. from A. nobilis from South China; their nematodes might be conspecific with C. hypophthalmichthys. Because the existing descriptions of C. hypophthalmichthys are poor and the type specimens were not deposited, the identification of nematodes of the present material is based on their morphological and biometrical similarity to this species, the fact that their host is closely related with those of C. hypophthalmichthys (all belong to the Hypophthalmichthyinae), and that they were collected from the nearby region. Dogel and Akhmerov (1959) wrote that females of C. hypophthalmichthys were up to 14 mm long, with the buccal capsule 0.13 mm long and 0.12 mm wide; this corresponds, more or less, with the present data. Neither Dogel and Akhmerov (1959) nor Finogenova (1971) reported on the number of ridges on the valve of the buccal capsule and, apparently, they did not

MORAVEC ET AL.—REDESCRIPTION OF C. HYPOPHTHALMICHTHYS

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FIGURE 2. Camallanus hypophthalmichthys. A. Tail of female, largest female, lateral view. B–C. Tail of male, ventral and lateral views. D. Large (right) spicule. E. Small (left) spicule. F–G. Tip of female tail, lateral views. H. Tip of male tail, ventral view. Scale bars in millimeters.

pay attention to this feature. They provided drawings of the buccal capsule, where they illustrated considerably different numbers (30 and 10, respectively) of only complete, noninterrupted ridges. However, their drawings are only schematic, not detailed, and it is apparent that the illustrated ridges were to show rather the character of the ornamentation of the valve than to give their exact number and forms. The specimens of the material in this study show that, in this species, the number of ridges on the valve ranges between 13–16 and that some ridges are incomplete, not extending along the entire length of the valve, or they are 1–3 times interrupted; none of the ridges reaches posteriorly the anterior border of the basal ring of the capsule. The character of ridges on the buccal capsule somewhat resembles that in C. hampalae Moravec and Scholz, 1991 described from a cyprinid fish in Laos (Moravec and Scholz, 1991). The length of the large (right) spicule in C. hypophthalmichthys was reported by Dogel and Akhmerov (1959) to be 0.12 mm, but they failed to give the length of the small (left) spicule; the length of the small spicule (0.10 mm) was given by Vismanis et al. (1987), who had probably derived it from the drawing of the male posterior end in the article by Finogenova (1971). In this case, the length ratio of spicules would be 1:1.2.

Although both spicules were slightly longer in the specimens in this study, their length ratio was very similar (1:1.29–1.44). In the original description of C. hypophthalmichthys, Dogel and Akhmerov (1959) reported 4–5 pairs of preanal and 4 pairs of postanal papillae in the male. Finogenova (1971) did not mention the number of male genital papillae, but her drawing of the male caudal end shows the presence of 5 preanal papillae on one side of the body and 4 papillae on the opposite side, and 6 pairs of postanal papillae. However, the male caudal alae in this species have a densely granular structure, which obscures the papillae, so that they are very difficult to observe. The SEM examination shows the presence of 7 preanal and 6 postanal pairs, which is typical of some other congeneric species. However, the lateral situation of the last but 1 pair of preanals and the location of the first 3 pairs of postanals seem to be specific characters of this species. The presence of 2 transverse mounds surrounding the cloacal aperture, each with 2 flat papillae, not reported previously for C. hypophthalmichthys, is also characteristic of some other Camallanus spp. (e.g., Moravec, 1973; Moravec and Scholz, 1991; Moravec et al., 2003a). The female tail tip of some Camallanus spp. is provided with 3 small conical processes, as in C. hypophthalmichthys, which is considered to be an important taxonomic feature (Moravec,

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FIGURE 3. Camallanus hypophthalmichthys, SEM micrographs. A. Cephalic end, apical view (arrow shows position of poorly visible amphid). B. Tail of male, subventral view. C. Cephalic end with distinctly visible trident of buccal capsule below cuticle, dorsoventral view. D. Caudal end of male, sublateral view. E. Tail of male (another specimen), subventral view. F. End of female tail with distinct phasmid, lateral view.

MORAVEC ET AL.—REDESCRIPTION OF C. HYPOPHTHALMICHTHYS

1973). However, C. hypophthalmichthys is the only Camallanus species in which such processes are present also in the male; these are reported in the male of this species for the first time. By its general morphology, especially the relatively short tridents on the buccal capsule, relatively short, conical female tail with 3 small processes at the tip, and measurements of the spicules, C. hypophthalmichthys resembles C. lacustris (Zoega, 1776), a Palearctic species parasitic mainly in perchlike fishes. Vismanis et al. (1987) tried to distinguish both species on the basis of the length of the buccal capsule, but, in fact, the length of the buccal capsule of C. lacustris (see Vismanis et al., 1987; Moravec, 1994) is very similar to that of C. hypophthalmichthys, and these dimensions overlap considerably in them. This study shows that C. hypophthalmichthys distinctly differs from C. lacustris in a smaller number of ridges on the buccal capsule valve (13–16 vs. 16–25 in the latter, see Moravec, 1994), in that the ridges do not reach posteriorly the anterior border of the basal ring and some of them are 1–3 times inrerrupted, in the presence of 3 small conical processes on the male tail tip, and in the distribution of some caudal papillae in the male (last but 1 pair of preanals lateral, almost at the same level as the last 1 vs. last 2 pairs of preanals subventral; first 3 pairs of postanals not close to each other vs. first 3 pairs of postanals close to each other). Both species also differ in their preferred hosts (percids vs. cyprinids) and their sites in the host (posterior and middle portions of intestine vs. mainly pyloric ceca and the anterior portion of intestine). In addition to the widely distributed species C. cotti Fujita, 1927, Pan et al. (1990) and Zhang et al. (1999) reported C. zacconis Li, 1941 to be the parasite of some cyprinid and other fishes in China; apparently, this information was based on data of some previous authors (e.g., Wang and Lin, 1975; Wang, 1984). However, according to Moravec (1973), C. zacconis is a junior synonym of C. cotti (see also Moravec et al., 2003a). Consequently, to date only 2 species of Camallanus, C. cotti and C. hypophthalmichthys, are known to occur in freshwater fishes in China. The former differs from the latter mainly in having a conspicuously long tail without caudal processes in the gravid female (Moravec et al., 2003a). The finding in this study of C. hypophthalmichthys in A. nobilis represents a new host record, the first record of this parasite in the Yangtze River drainage system, and its first documented record from China. ACKNOWLEDGMENTS Thanks are due to the staff of the Laboratory of Electron Microscopy of the Institute of Parasitology, ASCR, for their technical assistance and to Irena Husa´kova´ of the Department of Helminthology from the same institute for her help with the preparation of illustrations. This study was supported by the grant ME 424 from the Ministry of Education, Youth and Sports of the Czech Republic and by the grant 30025035 from the National Natural Science Foundation of China.

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LITERATURE CITED DOGEL, V. A., AND A. KH. AKHMEROV. 1959. Nematodes of fishes of the Amur River. Acta Hydrobiologica Sinica 3: 272–304. [In Chinese and Russian.] FINOGENOVA, S. P. 1971. Round worms of fishes of the Amur River basin. Parazitologicheskiy Sbornik, Trudy Zoologicheskogo Instituta Akademii Nauk USSR 25: 140–164. [In Russian.] FROESE, R., AND D. PAULY. 2003. FishBase. Available from: www.fishbase.org. Accessed on 26 January 2004. IVASHKIN, V. M., A. A. SOBOLEV, AND L. A. KHROMOVA. 1971. Camallanata of animals and man and the diseases caused by them. Osnovy nematodologii 22. Nauka, Moscow, Russia, 388 p. [In Russian.] MORAVEC, F. 1973. On the nematode Camallanus longicaudatus sp. n. from the Nile fish, Labeo horie Heck. Revue de Zoologie et de Botanique Africaines 87: 165–173. ———. 1994. Parasitic nematodes of freshwater fishes of Europe. Academia and Kluwer Academic Publishers, Dordrecht, The Netherlands, 473 p. ———, AND P. NIE. 2002. Observations on two species of phyllodistomes (Trematoda: Gorgoderidae) from fishes of the Hubei Province, central China, with an erection of Neophyllodistomum gen. n. Helminthologia 39: 221–225. ———, ———, T. SCHOLZ, AND G. WANG. 2003. Some trematodes and cestodes of fishes mainly from Hubei Province, central China. Acta Societatis Zoologicae Bohemicae 67: 161–174. ———, ———, AND G. WANG. 2003a. Some nematodes of fishes from central China, with the redescription of Procamallanus (Spirocamallanus) fulvidraconis (Camallanidae). Folia Parasitologica 50: 220–230. ———, ———, AND ———. 2003b. Observations on some acanthocephalans of fishes from Hubei Province, central China. Acta Societatis Zoologicae Bohemicae 67: 213–224. ———, AND T. SCHOLZ. 1991. Observations on some nematodes parasitic in freshwater fishes in Laos. Folia Parasitologica 38: 163–178. ———, AND G. WANG. 2002. Dentiphilometra monopteri n. gen., n. sp. (Nematoda: Philometridae) from the abdominal cavity of the ricefield eel Monopterus albus in China. Journal of Parasitology 88: 961–966. PAN, J. H., J. Y. ZHANG, AND Z. C. LI, EDITORS. 1990. Fish parasitology. Science Press, Beijing, 443 p. [In Chinese.] ROYTMAN, V. A. 1963. Nematodes of fishes of the Zeya River basin. Trudy GELAN 13: 253–300. [In Russian.] VISMANIS, K. O., V. V. LOMAKIN, V. A. ROYTMAN, M. K. SEMENOVA, AND V. YA. TROFIMENKO. 1987. Nemathelminthes. In Key to parasites of freshwater fishes of the USSR fauna, vol. 3. Parasitic metazoans, part 2, O. N. Bauer (ed.). Nauka, Leningrad, Russia, p. 187– 310. [In Russian.] WANG, P. Q. 1984: Descriptions of three new species and a list of parasitic nematodes from vertebrates in Fujian Province. Wuyi Science Journal 4: 113–132. [In Chinese, English summary.] ———, AND X. M. LIN. 1975. Some nematodes of the suborder Camallanata from Fujian Province, with notes on their life histories. Acta Zoologica Sinica 21: 350–358. [In Chinese, English summary.] ———, Y. R. ZHAO, AND C. C. CHEN. 1978. On some nematodes from vertebrates in South China. Fujian Shida Xuebao 2: 75–90. [In Chinese.] ZHANG, J. Y., Z. Z. QIU, AND X. J. DING. 1999. Parasites and parasitic diseases of fishes. Science Press, Beijing, 735 p. [In Chinese.]