Home The prevalence of helminth parasites in Pelophylax nigromaculatus (Anura: Ranidae) from Shanghai, China
Article
Licensed
Unlicensed Requires Authentication

The prevalence of helminth parasites in Pelophylax nigromaculatus (Anura: Ranidae) from Shanghai, China

  • Qifei Men , Hongyu Han , Qiping Zhao , Weili Xia , Hui Dong , Shunhai Zhu , Ziwen Wang , Cong Li , Xuelong Zhu and Bing Huang EMAIL logo
Published/Copyright: October 24, 2016
Become an author with De Gruyter Brill

Abstract

Parasites are ubiquitous members of biotic communities. To investigate the infective status of helminth parasites in Pelophylax nigromaculatus from Shanghai, 90 frogs were collected from July 2013 to July 2014 and examined for the presence of internal parasites. Of these, 86.67% (78/90) of frogs were infected with parasites, the total helminth intensity within infected frogs ranged from 1 to 367, and the mean intensity was 28.49. The infection rates and intensities were 78.89% and 22.89 for trematodes, 50.00% and 5.24 for nematodes, 13.33% and 3.92 for cestodes, and 41.11% and 8.49 for acanthocephalas, respectively. The majority (60.04%) of parasites were parasitic in the intestine, followed by urinary bladder (24.8%) and lungs (7.38%). Based on morphological features, 13 different species of helminth, including 9 undetermined species, were identified. The infective status of different species was significantly different. The most prevalent species were Diplodiscus nigromaculati (64.44%), Diplodiscus sp. (37.78%), Pomphorhynchus sp. (35.56%), Strongyloides sp. (33.33%). The mean infection intensity of Diplorchis nigromaculatus (139.25) was higher than the others’ species ranged from 3.57-14.63. This is the first reported discovery of Pomphorhynchus sp. (Pomphorhynchidae Yamaguti, 1939) in frogs from China. These data provide the foundation for further analyses of parasites in this and other species of amphibians.

References

Adamson M.L., Caira J.N. 1994. Evolutionary factors influencing the nature of parasite specificity. Parasitology, 109, 85-95. DOI 10.1017/S003118200008513Search in Google Scholar

Amin O.M., Ha N.V., Heckmann R.A. 2009. New and already known Acanthocephalans from amphibians and reptiles in Vietnam, with keys to species of Pseudoacanthocephalus Petrochenko, 1956 (Echinorhynchidae) and Sphaerechinorhynchus John-ston and Deland, 1929 (Plagiorhynchidae). Journal of Parasitology, 94, 181-189. 10.1645/GE-1288.1Search in Google Scholar PubMed

Biserkov V.Y., Yildirimhan H.S., Buchvarov G., Ugurtas I.H. 2001. Polystoma macrocnemis n. sp. (Monogenea: Polystomatidae) from the Iranian longlegged wood frog Rana macrocnemis (Ranidae) in Turkey. Systematic Parasitology, 48, 61-66. 10.1023/A:1026524324272.Search in Google Scholar

Bray R.A., Gibson D.I., Jones A. (Eds). 2008. Keys to the Trematoda, Volume 3, CABI Publishing, Wallingford, UK and the Natural History Museum, London, pp. 51710.1079/9780851995885.0000Search in Google Scholar

Bursey C.R., Vrcibradic D., Hatano F.H., Rocha C.F. 2006. New genus, new species of Acanthocephala (Echinorhynchidae) from the Brazilian frog Hylodes phyllodes (Anura: Leptodactylidae). Journal of Parasitology, 92, 353-356. 10.1645/GE-3518.1Search in Google Scholar PubMed

Chen J. 2012. A case of Sparganum mansoni infection induced by eating live frogs. Chinese Journal of Schistosomiasis Control,24, 639-644. (In Chinese)Search in Google Scholar

Chin D.H. 1963. Three new species of trematodes of the family Gorgoderidae from Kweiyang. Acta Zoologica Sinica, 15, 397402. (In Chinese)Search in Google Scholar

Churchill H.M. 1955. Survival of frog lung flukes, Haematoloechus sp in certain artificial media. Journal of Parasitology, 41, 329-329. 10.2307/3274229Search in Google Scholar

Deng Y., Liu C.J., Chen W.Q., Zhou R.M., He L.J., Lin X.M. 2012. Investigation on prevalence of Spirometra mansoni sparganum infection in frogs from Henan Province. Chinese Jour-nal of Schistosomiasis Control, 24, 82-84. (In Chinese)Search in Google Scholar

DuĹźen S., Oguz M.C. 2008. Occurence of Pomphorhynchus laevis (Acanthocephala) in the marsh frog (Rana ridibunda Pallas, 1771), from Turkey. Helminthologia, 45, 154-156. 10.2478/s11687-008-0031-2Search in Google Scholar

Fan L.X., Li J.H., He Z.Y. 2008. A new species of the genus Polystoma (Polystomatidae, Monogenwa) parasitic in the host Rhacophorus Carvirostris Guenther. Acta Zootaxonomica Sinica, 33, 340-343. (In Chinese)Search in Google Scholar

Fan L.X., Wang C.L., Xu H.J. 2007. A new species of the genus Polystoma (Polystomatidae, Monogenwa) parasitic in Rana Grahami Boulenges. Acta Zootaxonomica Sinica, 32, 182-185. (In Chinese)Search in Google Scholar

Fu R.J., Lv G., Zhong S.F., Gan X.F., Liang P. 2015. Preliminary survey of spirometra plerocercoid infection in wild frogs from Ding’an County. Journal of Hainan Medical University, 21, 289-295. (In Chinese)Search in Google Scholar

Ganaie H. A., Nazir M.N.A.S., Muzaffar G., Chishti M.Z. 2012. Prevalence studies of parasite Pomphorhynchus kashmirensis in local fish species Schizothorax. European Scientific Journal, 8, 197-209Search in Google Scholar

Gao P.R., Zhang L.P. 2014. Research on parasitic trematodes from amphibians in Yunnan Province. Journal of Yunnan University of Nationalities, 23, 181-185. (In Chinese)Search in Google Scholar

Hamann M.I., González C.E., Kehr A.I. 2006. Helminth community structure of the oven frog Leptodactylus latinasus (Anura, Leptodactylidae) from Corrientes, Argentina. Acta Parasitologica, 51, 294-299. 10.2478/s11686-006-0045-1Search in Google Scholar

He X. 2012. Phylogenetic analysis of the two gastrointestinal nematodes in frogs. MS Thesis, Hunan Agricultural University, China. (In Chinese)Search in Google Scholar

Jiang P.Z., Sun X.D. 1983. Report on some trematodes from am-phibians and reptiles in Zhoushan Island. Journal of Hangzhou Normal University, 1, 106-112. (In Chinese)Search in Google Scholar

Johnson P.T.J., Lunde K.B., Haight R.W., Bowerman J., Blaustein, A.R. 2001. Ribeiroia ondatrae (Trematoda Digenea) infection induces severe limb malformations in western toads (Bufo boreas). Canadian Journal of Zoology, 79, 370-379. 10.1139/cjz-79-3-370Search in Google Scholar

Johnson P.T.J., Lunde K.B., Ritchie E.G., Launer A.E. 1999. The effect of trematode infection on amphibian limb development and survivorship. Science, 284, 802-804. 10.1126/science. 284.5415.802Search in Google Scholar

Kong F.Y. (Ed.). 2000. Veterinary parasitology, Press of China Agricultural University, Beijing, pp. 99 (In Chinese)Search in Google Scholar

Koprivnikar J., Baker R.L., Forbes M.R. 2006. Environmental factors influencing trematode prevalence in grey tree frog (Hyla versicolor) tadpoles in southern Ontario. Journal of Parasitol ogy, 92, 997-1001. 10.1645/GE-771R.1Search in Google Scholar

Krull W.H. 1933. Studies on the life history of a frog lung fluke, Haematoloechus complexus (Seely, 1906) Krull, N. Comb. Parasitology Research, 6, 192-206. 10.1007/BF02122063Search in Google Scholar

Li L., Hasegawa H., Roca V., Xu Z., Guo Y.N., Sato A., Zhang L.P. 2014. Morphology, ultrastructure and molecular characterisation of Spiroxys japonica Morishita, 1926 (Spirurida: Gnathostomatidae) from Pelophylax nigromaculatus (Hallowell) (Amphibia: Ranidae). Parasitology Research, 113, 893-901. 10.1007/s00436-013-3720-9Search in Google Scholar

Li L.S., Zhou X.N., Lin J.X., Zhang Y., Cheng Y.Z., Zhang R.Y., Fang Y.Y., Lin C.X., Chen B.J., Li Y.S. 2006. Discovery of the new hosts for six species of Angiostrongy cantonensis and investigation on the epidemic foci in Fujian province. Chinese Journal of Zoonoses. 22, 533-537. (In Chinese)Search in Google Scholar

Li M.M., Gu C.D. 1978. Report of some digenetic trematodes from frogs and toads of China. Acta Zoologica Sinica, 24, 163-169. (In Chinese)Search in Google Scholar

Li M.W., Song H.Q., Li C., Lin H.Y., Xie W.T., Lin R.Q., Zhu X.Q. 2011. Sparganosis in mainland China. International Journal of Infectious Diseases, 15, e154-e156. 10.1016/j.ijid.2010.10.001Search in Google Scholar

Li Z., Cai F.K., Liu F.X., Piao Z.J. 2011. The case of Chinese wood frog (Rana chensinensis) infected by lung worm (nematode parasites) in Changbai Mountain. Journal of Beihua University(Natural Science), 12, 575-577. (In Chinese)Search in Google Scholar

Liu F.X., Cai F.K., Li Z., Niu L.J., Piao Z.J. 2011. Investigation on Chinese wood frog (Rana chensinensis) infected by parasites in Changbai Mountain. Journal of Beihua University(Natural Science), 12, 704-707. (In Chinese)Search in Google Scholar

Liu J.Y., Lang S. 1988. On the life cycle of Diplorchis nigromaculatus. Acta Zoologica Sinica, 34, 271-277. (In Chinese)Search in Google Scholar

Liu Z., Chen M.S., Li L. 1978. New species and new records of some trematodes from wood frogs in Jilin. Journal of Jilin University (Medicine Edtion), 4, 16-22. (In Chinese)Search in Google Scholar

Mueller J.F., Coulston F. 1941. Experimental human infection with the sparganum larva of Spirometra mansonoides (Mueller, 1935). American Journal of Tropical Medicine and Hygiene, 1, 399-42510.4269/ajtmh.1941.s1-21.399Search in Google Scholar

Nabi S., Tanveer S., Ahmed S.G., Ahad S., Niyaz U., Abdullah I. 2015. Acanthocephalan infestation in fishes-A review. Journal of Zoology Studies, 2, 33-38Search in Google Scholar

Oshima T., Kliks M. 1987. Effects of marine mammal parasites on human health. International Journal for Parasitology, 17, 415-421. 10.1016/0020-7519(87)90117-2Search in Google Scholar

Smales L.R. 2007. Acanthocephala in amphibians (Anura) and reptiles (Squamata) from Brazil and Paraguay with description of a new species. Journal of Parasitology, 93, 392-398. 10.1645/GE-937R.1Search in Google Scholar

Song L., Xiao Z., Ding X.J. 2008. A new species of the genus Diplorchis (Monogenea, Polystomatidae) parasitic in Rana livida Blyth, 1855 from Hainan Island, China. Acta Zootaxonomica Sinica, 33, 733-736. (In Chinese)Search in Google Scholar

Stromberg B.E. 1997. Environmental factors influencing transmission. Veterinary Parasitology, 72, 247-264. 10.1016/ S0304-4017(97)00100-3Search in Google Scholar

Sun X.D., Jiang P.Z. 1985. Research on parasitic trematodes from amphibians in Zhejiang Province. Journal of Hangzhou Normal University, 1, 29-35. (In Chinese)Search in Google Scholar

Tang Z.Z., Tang C.T. (Eds). 2009. Human and animal nematology, Press of Science, Beijing, pp. 406 (In Chinese)Search in Google Scholar

Tang, A.F. 2009. Production technology of the Fasciola hepatica slide specimen. Shandong Journal of Animal Science and Veterinary Medicine, 3, 9-11. (In Chinese)Search in Google Scholar

Ugbomoiko U.S., Ariza L., Heukelbach J. 2008. Parasites of importance for human health in Nigerian dogs: high prevalence and limited knowledge of pet owners. BMC Veterinary Research, 4, 1-9. 10.1186/1746-6148-4-49Search in Google Scholar PubMed PubMed Central

Wang P.Q. 1980. Report on some trematodes from amphibians and reptiles in Fujian, South China. Journal of Fujian Normal University, 1, 81-92. (In Chinese)Search in Google Scholar

Wang P.Q., Wang Y.Y. 1992. Synopsis of trematodes and nematodes of amphibians and reptiles from China. Wuyi Science Journal, 49-65. (In Chinese)Search in Google Scholar

Wang X.Y., Zhou J.Y., 1993. Jiangxi Fauna-Human and Animal Trematoda, Jiangxi Science and Technology Press, Nanchang, pp. 59 (In Chinese)Search in Google Scholar

Wang Y.Y., Wang P.Q. 1998. Notes on Acanthocephala from Fujian with description of three new species. Journal of Fujian Teachers University(Natural Science), 3: 80-86. (In Chinese)Search in Google Scholar

Whitehouse C.A. 2002. A study of the frog lung fluke Haematoloechus (Trematoda: Haematoloechidae) collected from areas of Kentucky and Indiana. Indiana Academy of Science,111, 77-94Search in Google Scholar

Wiwanitkit V. 2005. A review of human sparganosis in Thailand. International Journal of Infectious Diseases, 9, 312-316. 10.1016/j.ijid.2004.08.003Search in Google Scholar PubMed

Xie W.H., Wang X.P., Li J.L. 2004. Survey on Pelophylax nigromaculatus infected by sparganum of Spirometra mansoni in spring of Yulin. Journal of Yulin Normal University, 25, 63-64. (In Chinese)Search in Google Scholar

Yamaguti S. 1963. Systema helminthum.Volume V. Acanthocephala, Interscience Publications, New York. pp. 423Search in Google Scholar

Yang Y.H., Zhang D.X., Li Y.M. 2004. Mitochondrial DNA diversity and preliminary biogeographic inference of the evolutionary history of the black-spotted pond frog Pelophylax nigromaculatus populations in China. Acta Zootaxonomica Sinica, 50, 193-201. (In Chinese)Search in Google Scholar

Zamparo D., Ferrao A., Brooks D.R., Bettaso J., Mata-LĂłpez R. 2011. New species of Haematoloechus (Digenea: Plagiorchidae) in the lung of the foothill yellow-legged frog Rana boylii (Anura), from Humboldt County, California, USA. Revista Mexicana de Biodiversidad, 82, 445-451. (In Spanish)10.22201/ib.20078706e.2011.2.498Search in Google Scholar

Zeng X.J., Jiang W.S., Chen H.G., Lv S., Ge J., Lan W.M., Xie F., Dai K.J., Zhou X.N. 2011. Distribution of natural epidemic foci of Angiostrongylus cantonensis in Jiangxi province. Chinese Journal of Zoonoses, 27, 459-463. (In Chinese)Search in Google Scholar

Zhang S.Y., Lang S. 1990. Tegument of Diplorchis Hangzhouensis (Monogenea: Polystomatidae) in various stages of life cycle. Current Zoology, 36, 217-221. (In Chinese)Search in Google Scholar

Zhang T.F., Sha G.R. 1986. A new species of the genus Rauschiella from Tibet Autonomous Region. Acta Zootaxonomica Sinica, 11, 25-27. (In Chinese)Search in Google Scholar

Zhang, T.F., 1996. Some trematodes from amphibians and reptiles in Sichuan province, with description of a new species (Trematoda: Digenea). Sichuan Journal of Zoology, 15, 141-143. (In Chinese)Search in Google Scholar

Received: 2016-1-28
Revised: 2016-7-1
Accepted: 2016-7-8
Published Online: 2016-10-24
Published in Print: 2016-12-1

© 2016 W. Stefański Institute of Parasitology, PAS

Articles in the same Issue

  1. Review
  2. Internal parasitic fauna of elk (Alces alces) in Poland
  3. Research Article
  4. First report of mixed Entamoeba polecki (ST 1) and E. suis infection in piglets shedding abnormalfeces by histopathological and molecular surveys
  5. Research Article
  6. Genotyping of Cryptosporidium spp. in environmental water in Turkey
  7. Research Article
  8. Tranmission pattern differences of miracidia and cercariae larval stages of digenetic trematode parasites
  9. Research Article
  10. Characteristics, behaviors and association between Human African Trypanosomiasis and HIV seropositivity among volunteer blood donors in a semi-rural area: A survey from Kikwit, the Democratic Republic of Congo
  11. Research Article
  12. Comparison of indirect fluorescent antibody test and the modified agglutination test for the detection of Toxoplasma gondii antibodies in stray dogs from Southern Brazil
  13. Research Article
  14. Critical analysis of vector-borne infections in dogs: Babesia vogeli, Babesia gibsoni, Ehrlichia canis and Hepatozoon canis in Punjab, India
  15. Research Article
  16. A new species of Trichodina Ehrenberg, 1830 (Ciliophora: Trichodinidae) from Rhamdia quelen (Siluriformes: Heptapteridae) and Gymnotus sp. (Teleostei: Gymnotidae) in Brazil
  17. Research Article
  18. Monocotyle luquei n. sp. (Monogenea: Monocotylidae), from the gills of diamond stingray Dasyatis dipterura (Jordan and Gilbert, 1880) (Myliobatiformes: Dasyatidae), in the South Pacific
  19. Research Article
  20. First record of Hammerschmidtiella diesingi (Hammerschmidt, 1838) (Oxyuridomorpha: Thelastomatidae) parasite of Periplaneta americana (Linnaeus, 1758) (Blattodea: Blattidae) in Japan, morphological and molecular characterization
  21. Research Article
  22. The genus Ixodes (Acari: Ixodidae) in China with three new record species
  23. Research Article
  24. First insights into indoor and outdoor Culicoides activity related to the risk period for Bluetongue virus transmission in Eastern Slovakia
  25. Research Article
  26. Detection of Theileria lestoquardi cross infection in cattle with clinical theileriosis in Iran
  27. Research Article
  28. Prevalence of Toxoplasma gondii and Neospora caninum in red foxes in Slovakia
  29. Research Article
  30. Epidemiological survey on Leishmania infection in red foxes (Vulpes vulpes) and hunting dogs sharing the same rural area in Southern Italy
  31. Research Article
  32. Fasciola hepatica infection in humans: overcoming problems for the diagnosis
  33. Research Article
  34. Isolation and molecular characterization of Acanthamoeba genotypes isolated from soil sources of public and recreational areas in Iran
  35. Research Article
  36. A genetic structure of novel population of Fascioloides magna from Poland, Podkarpackie Province, indicates an expanding second European natural focus of fascioloidosis
  37. Research Article
  38. Genotyping of clinical isolates of Acanthamoeba genus in Venezuela
  39. Research Article
  40. The prevalence of helminth parasites in Pelophylax nigromaculatus (Anura: Ranidae) from Shanghai, China
  41. Research Article
  42. Ocular symptoms reported by patients infested with Demodex mites
  43. Research Article
  44. Norway rat (Rattus norvegicus) as a potential reservoir for Echinococcus granulosus: A public health implication
  45. Research Article
  46. Redescription of Rhabdochona papuanensis (Nematoda: Thelazioidea), a parasite of rainbow fishes (Melanotaenia spp.); the first record of the species of Rhabdochona in Australia
  47. Research Article
  48. Development of a rapid and reliable assay for in vitro determination of compound cidality against the asexual stages of Plasmodium falciparum
  49. Research Article
  50. A case of persisting massive infection of Scomberomorus commerson, a commercially exploited scombrid fish, with Cybicola armatus (Copepoda: Siphonostomatoida: Pseudocycnidae)
  51. Research Article
  52. The PCR and nested PCR detection of Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum and Babesia microti in Dermacentor reticulatus F. collected in a new location in Poland (Trzciel, Western Poland)
  53. Research Article
  54. Cutaneous leishmaniasis caused by Leishmania infantum in Southern Israel
  55. Research Note
  56. A morphological study of Diplodiscus subclavatus (Pallas, 1760) (Trematoda: Diplodiscidae) adults from the accidental host, Viviparus contectus (Millet, 1813) (Caenogastropoda: Viviparidae)
Downloaded on 15.9.2025 from https://www.degruyterbrill.com/document/doi/10.1515/ap-2016-0111/html
Scroll to top button