Occurrence of Hysterothylacium and Anisakis nematodes (Ascaridida: Ascaridoidea) in the tanaka’s snailfish Liparis tanakae (Gilbert & Burke) (Scorpaeniformes: Liparidae)

Parasitology Research - Tập 113 - Trang 1289-1300 - 2014
Yan-Ning Guo1, Zhen Xu2, Lu-Ping Zhang1, Yong-Hong Hu1, Liang Li1
1Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology of Hebei Province, College of Life Science, Hebei Normal University, Shijiazhuang, China
2Medical College, Hebei University of Engineering, Handan, China

Tóm tắt

The tanaka’s snailfish Liparis tanakae (Gilbert & Burke) (Scorpaeniformes: Liparidae) is an economically important marine fish species in China. However, the helminth parasites of this fish are still poorly known. During a helminthological survey of Chinese marine fishes from 2011 to 2012, we revealed that L. tanakae was heavily infected with third-stage larvae and adults of ascaridoid nematodes (total prevalence 100 % and mean intensity 82.3 nematodes per fish). Four species of third-stage larvae Hysterothylacium liparis Li, Xu & Zhang, 2007, H. aduncum (Rudolphi, 1802), Hysterothylacium fabri (Rudolphi, 1819), and Anisakis pegreffii (Campana-Rouget & Biocca, 1955) and a single species of adults H. liparis were differentiated and identified by morphological and molecular methods. The detailed morphology of the four species of third-stage larvae was also studied using light microscopy and scanning electron microscopy. The morphological and molecular characterization of the third-stage larvae of H. liparis was reported. Liparis tanakae represents a new host record for A. pegreffii and H. fabri. In addition, a new name, Hysterothylacium zhoushanense nom. nov. was also given to Hysterothylacium zhoushanensis Li, Liu & Zhang, 2012 to make the latinized specific epithet agree with this neuter generic name.

Tài liệu tham khảo

Abe N, Ohya N, Yanagiguchi R (2005) Molecular characterization of Anisakis pegreffii larvae in Pacific cod in Japan. J Helminthol 79:303–306 Amor N, Farjallah S, Merella P, Said K, Slimane BB (2011) Molecular characterization of Hysterothylacium aduncum (Nematoda: Raphidascaridae) from different fish caught off the Tunisian caught off the Tunisian coast based on nuclear ribosomal DNA sequences. Parasitol Res 109:1429–1437 Andersen K (1993) Hysterothylacium aduncum (Rudolphi, 1862) infection in cod from the Oslofjord: seasonal occurrence of third- and fourth-stage larvae as well as adult worms. Parasitol Res 79:67–72 Balbuena JA, Karlsbakk E, Saksvik M, Kvenseth AM, Nylund A (1998) New data on the early development of Hysterothylacium aduncum (Nematoda, Anisakidae). J Parasitol 84:615–617 Balbuena JA, Karlsbakk E, Kvenseth AM, Saksvik M, Nylund A (2000) Growth and emigration of third-stage larvae of Hysterothylacium aduncum (Nematoda: Anisakidae) in larval herring Clupea harengus. J Parasitol 86:1271–1275 Borges JN, Cunha LFG, Santos HLC, Monteiro-Neto C, Santos CP (2012) Morphological and molecular diagnosis of anisakid nematode larvae from cutlassfish (Trichiurus lepturus) off the Coast of Rio de Janeiro, Brazil. PLoS One 7:1–14 Cannon LRG (1977) Some larval ascaridoids from south-eastern Queensland marine fishes. Int J Parasitol 7:233–243 Chai J-Y, Chu Y-M, Sohn W-M, Lee S-H (1986) Larval anisakids collected from the Yellow Corvina in Korea. Korean J Parasitol 24:1–11 Du C-X, Zhang L-P, Shi M-Q, Ming Z, Hu M, Gasser RB (2010) Elucidating the identity of Anisakis larvae from a broad range of marine fishes from the Yellow Sea, China, using a combined electrophoretic-sequencing approach. Electrophoresis 31:654–658 Garbin L, Mattiucci S, Paoletti M, González-Acuña D, Nascetti G (2011) Genetic and morphological evidences for the existence of a new species of Contracaecum (Nematoda: Anisakidae) parasite of Phalacrocorax brasilianus (Gmelin) from Chile and its genetic relationships with congeners from fish-eating birds. J Parasitol 97:476–492 Gasser RB (2006) Molecular tools—advances, opportunities and prospects. Vet Parasitol 136:69–89 González L (1998) The life cycle of Hysterothylacium aduncum (Nematoda: Anisakidae) in Chilean marine farms. Aquaculture 162:173–186 Hartwich G (1975) Schlauchwürmer, Nemathelminthes, Rund-oder Fadenwürmer, Nematoda parasitische Rundwürmer von Wirbeltieren: I. Rhabditida und Ascaridida. Tierwelt Deutschl 62:1–256 Iglesias L, Valero A, Galvez L, Benitez R, Adroher FJ (2002) In vitro cultivation of Hysterothylacium aduncum (Nematoda: Anisakidae) from 3rd-stage larvae to egg-laying adults. Parasitology 125:467–475 Jabbar A, Fong RWJ, KoK KX, Lopata AL, Gasser RB, Beveridge I (2013) Molecular characterization of anisakid nematode larvae from 13 species of fish from Western Australia. Int J Food Microbiol 161:247–253 Kalay M, Dönmez AE, Koyuncu CE, Genc E, Sahin G (2009) Seasonal variation of Hysterothylacium aduncum (Nematoda: Raphidascarididae) infestation in sparid fishes in the Northeast Mediterranean Sea. Turk J Vet Anim Sci 33:517–523 Klimpel S, Rückert S (2005) Life cycle strategy of Hysterothylacium aduncum to become the most abundant anisakid fish nematode in the North Sea. Parasitol Res 97:141–149 Klimpel S, Kleinertz S, Hanel R, Ruckert S (2007) Genetic variability in Hysterothylacium aduncum, a raphidascarid nematode isolated from spat (Sprattus sprattus) of different geographicl reas of the northeastern Atlantic. Parasitol Res 101:1425–1430 Koie M, (1993) Aspects of the life-cycle and morphology of Hysterothylacium aduncum (Rudolphi, 1802) (Nematoda, Ascaridoidea, Anisakidae). Can J Zool 71:1289–1296 Kuhn T, Garcia-Marquez J, Klimpel S (2011) Adaptive radiation within marine anisakid nematodes: a zoogeographical modeling of cosmopolitan, zoonotic parasites. PLoS One 6:1–6 Li L, Xu Z, Zhang L-P (2007) A new species of genus Hysterothylacium Ward et Magath, 1917 (Nematoda, Anisakidae) from Liparis tanakae (Scorpaeniformes, Liparidae) from the Yellow Sea, China. Acta Parasitol 52:371–375 Li L, Xu Z, Zhang L-P (2008a) Redescription of three species of Hysterothylacium (Nematoda: Anisakidae) from marine fishes from the Yellow Sea, China, with the synonymy of Hysterothylacium muraenesoxin (Luo, 1999). Zootaxa 1878:55–67 Li L, Xu Z, Zhang L-P (2008b) Investigation of nematodes in fishes from the Yellow Sea. Fish Sci 27:283–285 Li L, Xu Z, Zhang L-P (2012a) Goezia nankingensis Hsü, 1933 (Nematoda: Raphidascarididae) from the critically endangered Chinese paddlefish Psephurus gladius (Martens) (Acipenseriformes: Polyodontidae). Syst Parasitol 82:39–48 Li L, Liu Y-Y, Zhang L-P (2012b) Morphological and molecular identification of Hysterothylacium longilabrum sp. nov. and larvae of different stages (Nematoda: Anisakidae) from marine fishes in the South China Sea. Parasitol Res 111:767–777 Li L, Liu Y-Y, Zhang L-P (2012c) Morphological and genetic characterization of Hysterothylacium zhoushanensis sp. nov. (Ascaridida: Anisakidae) from the flatfish Pseudorhombus oligodon (Bleeker) (Pleuronectiformes: Paralichthyidae) in the East China Sea. Parasitol Res 111:2393–2401 Li L, Gibson DI, Liu Y-Y, Zhang L-P (2012d) Morphological and molecular study of the poorly known species Pseudanisakis rajae (Yamaguti, 1941) (Nematoda: Acanthocheilidae) from elasmobranchs in the Yellow Sea and Taiwan Strait off the coast of China. Syst Parasitol 81:115–123 Li L, Zhang L-P, Liu Y-Y (2013) Hysterothylacium simile n. sp. (Nematoda: Raphidascarididae) and H. aduncum (Rudolphi, 1802) from marine fishes in the Bohai and Yellow Sea, China, with comments on the record of H. paralichthydis (Yamaguti, 1941) in the Chinese waters. Syst Parasitol 84:57–69 Liu Y-Y, Xu Z, Zhang L-P, Li L (2013) Redescription and genetic characterization of Hysterothylacium thalassini Bruce, 1990 (Nematoda: Anisakidae) from marine fishes in the South China Sea. J Parasitol 99:655–661 Martín-Sánchez J, Díaz M, Artacho ME, Valero A (2003) Molecular arguments for considering Hysterothylacium fabri (Nematoda: Anisakidae) a complex of sibling species. Parasitol Res 89:214–220 Mašová Š, Moravec F, Baruš V, Seifertová M (2010) Redescription, systematic status and molecular characterization of Multicaecum heterotis Petter, Vassiliadès et Marchand, 1979 (Nematoda: Heterocheilidae), an intestinal parasite of Heterotis niloticus (Osteichthyes: Arapaimidae) in Africa. Fol Parasitol 57:280–288 Mattiucci S, Nascetti G (2006) Molecular systematics, phylogeny and ecology of anisakid nematodes of the genus Anisakis Dujardin, 1845: an update. Parasite 13:99–113 Moravec F (1994) Parasitic nematodes of freshwater fishes of Europe. Academia, Prague, 473 pp Moravec F (1998) Nematodes of freshwater fishes of the Neotropical Region. Academia, Praha, 464 pp Moravec F, Nagasawa K (2000) Some anisakid nematodes from marine fishes of Japan and the North Pacific Ocean. J Nat Hist 34:1555–1574 Moravec F, Nagasawa K, Urawa S (1985) Some fish nematodes from fresh water in Hokkaido, Japan. Fol Parasitol 32:305–316 Moravec F, Urawa S, Coria CO (1997) Hysterothylacium patagonense n. sp. (Nematoda: Anisakidae) from freshwater fishes in Patagonia, Argentina, with a key to the species of Hysterothylacium in American freshwater fishes. Syst Parasitol 36:31–38 Pekmezci GZ, Bolukbas CS, Gurler AT, Onuk EE (2013) Occurrence and molecular characterization of Hysterothylacium aduncum (Nematoda: Anisakidae) from Merlangius merlangus euxinus and Trachurus trachurus off the Turkish coast of Black Sea. Parasitol Res 112:1031–1037 Petter AJ, Maillard C (1987) Ascarides de poissons de Méditerranée occidentale. Bull Mus Hist Nat 9:773–798 Petter AJ, Radujkovic BM (1986) Nematodes parasites de poisons de la mer Adriatique. Bull Mus Hist Nat 8:489–499 Petter AJ, Lébre C, Radujkovic BM (1984) Nématodes parasites de poissons osteichthyens de l’Adriatique méridionale. Acta Adriat 25:205–221 Quiazon KMA, Yoshinaga T, Ogawa K (2011) Distribution of Anisakis species larvae from fishes of the Japanese waters. Parasitol Int 60:223–226 Setyobudi E, Jeon C-H, Choi K, Lee S II, Lee C II, Kim J-H (2013) Molecular identification of anisakid nematodes third stage larvae isolated from common squid (Todarodes pacificus) in Korea. Ocean Sci J 48:197–205 Shamsi S, Norman R, Gasser RB, Beveridge I (2009) Redescription and genetic characterization of selected Contracaecum spp. (Nematoda: Anisakidae) from various hosts in Australia. Parasitol Res 104:1507–1525 Shamsi S, Eisenbarth A, Saptarshi S, Beveridge I, Gasser RB, Lopata AL (2011) Occurrence and abundance of anisakid nematode larvae in five species of fish from southern Australian waters. Parasitol Res 108:927–934 Shamsi S, Gasser RB, Beveridge I (2012) Genetic characterisation and taxonomy of species of Anisakis (Nematoda: Anisakidae) parasitic in Australian marine mammals. Invertebr Syst 26:204–212 Shamsi S, Gasser RB, Beveridge I (2013) Description and genetic characterisation of Hysterothylacium (Nematoda: Raphidascarididae) larvae parasitic in Australian marine fishes. Parasitol Int 62:320–328 Shih HH, Jeng MS (2002) Hysterothylacium aduncum (Nematoda: -Anisakidae) infecting a herbivorous fish, Siganus fuscescens, off the Taiwanese coast of the northwest Pacific. Zool Stud 41:185–189 Silva JP, Melo FTV, Silva LCN, Gonçalves EC, Giese EG, Furtado AP, Santos JN (2013) Morphological and molecular characterization of Ortleppascaris sp. larvae, parasites of the cane toad Rhinella marina from eastern Amazonia. J Parasitol 99:118–123 Smrzlic IV, Valic D, Kapetanovic D, Kurtovic B, Teskeredzic E (2012) Molecular characterisation of Anisakidae larvae from fish in Adriatic Sea. Parasitol Res 111:2385–2391 Soleim O, Berland B (1981) The morphology of Thynnascaris adunca (Rudolphi) (Nematoda, Ascaridoidea). Zool Scr 10:167–182 Testini G, Papini R, Lia RP, Parisi A, Dantas-Torres F, Traversa D, Otranto D (2011) New insights into the morphology, molecular characterization and identification of Baylisascaris transfuga (Ascaridida, Ascarididae). Vet Parasitol 175:97–102 Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680 Torres P, Andrade P, Silva R (1998) On a new species of Hysterothylacium (Nematoda: Anisakidae) from Cauque mauleanum (Pisces: Atherinidae) by brightfield and scanning electron microscopy. Mem I Oswaldo Cruz 93:745–752 Umehara A, Kawakami Y, Matsui T, Araki J, Uchida A (2006) Molecular identification of Anisakis simplex sensu stricto and Anisakis pegreffii (Nematoda: Anisakidae) from fish and cetacean in Japanese waters. Parasitol Int 55:267–271 Umehara A, Kawakami Y, Ooi HK, Uchida A, Ohmae H, Sugiyama H (2010) Molecular identification of Anisakis type I larvae isolated from hairtail fish off the coasts of Taiwan and Japan. Int J Food Microbiol 143:161–165 Xu Z, Zhang L-P, Liu B-C, Li L (2012) Morphological and molecular characterization of Raphidascaris (Ichthyascaris) lophii (Wu, 1949) (Nematoda, Anisakidae) from marine fishes from China, with a key to the species of the subgenus Ichthyascaris. Acta Parasitol 57:316–322 Xue Y, Xu B-D, Gao T-X, Qiu T-L, Lin L-S (2010) Preliminary study on feeding ecology of Liparis tanakae in north Yellow Sea. J Fish Sci Chin 17:1066–1074 Yamada U, Shirai S, Irie T, Tokimura M, Deng S, Zheng Y, Li C, Kim YU, Kim YS (1995) Names and illustrations of fishes from the East China Sea and the Yellow Sea. Overseas Fishery Cooperation Foundation, Tokyo, Japan, 288 pp Yoshinaga T, Ogawa K, Wakabayashi K (1987) Experimental life cycle of Hysterothylacium aduncum Nematoda: Anisakidae in freshwater. Fish Pathol 22:243–251 Zhang B, Jin X-S, Dai F-Q (2011) Feeding habits and their variation of seasnail (Liparis tanakae) in the central and southern Yellow Sea. J Fish Sci Chin 35:1199–1207 Zhang L-P, Hu M, Shamsi S, Beveridge I, Li H-M, Xu Z, Li L, Cantacessi C, Gasser RB (2007) The specific identification of anisakid larvae from fishes from the Yellow Sea, China, using mutation scanning-coupled sequence analysis of nuclear ribosomal DNA. Mol Cell Probe 21:386–390 Zhang L-P, Du X-J, An R-Y, Li L, Gasser RB (2013) Identification and genetic characterization of Anisakis larvae from marine fishes in the South China Sea using an electrophoretic-guided approach. Electrophoresis 34:888–894 Zhou Z-P, Jin X-S, Shan X-J, Li Z-L, Dai F-Q (2012) Seasonal variations in distribution and biological characteristics of snailfish Liparis tanakae in the central and southern Yellow Sea. Acta Ecol Sin 32:5550–5561 Zhu X-Q, Podolska M, Liu J-S, Yu H-Q, Chen H-H, Lin Z-X, Luo C-B, Song H-Q, Lin R-Q (2007) Identification of anisakid nematodes with zoonotic potential from Europe and China by single-strand conformation polymorphism analysis of nuclear ribosomal DNA. Parasitol Res 101:1703–1707