Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Structure of the Parasite Infracommunity of Hoplobatrachus tigerinus Daudin, 1803 from YSR Kadapa District, Andhra Pradesh, India

  • 11 Accesses


Three hundred specimens of Hoplobatrachus tigerinus (Daudin, 1803), 133 females and 167 males, collected in YSR Kadapa district, Andhra Pradesh, India, from 2013 to 2015, were examined for the presence of metazoan parasites. One hundred seventy-two (57.3%) frogs were parasitized by at least one or more metazoan parasite species. Nine species of parasites were collected: 6 digeneans, 1 cestode and 2 nematodes. All the recovered parasites are satellite species with less than 33% prevalence. Digeneans are the most abundant group of parasites accounting for 89.9% of total parasites. Hoplobatrachus tigerinus is a new host record for Paracephalogonimus minutum. Paracephalogonimus minutum is the dominant species followed by Tremiorchis ranarum. The metazoan parasite species of H. tigerinus showed the typical aggregated pattern of distribution of most parasite systems. Only Cosmocercoides variabilisOswaldocruzia filiformis (0.23), Paracephalogonimus minutumOphiotaenia tigrina (0.13), Diplodiscus amphichrusOhiotaenia tigrina (0.13), Cosmocercoides variabilisMehraorchis ranarum (0.11) and Ganeo tigrnumDiplodiscus amphichrus (0.11) showed significant interspecific associations while the other pairs showed very less to no association. There was a very negligible influence of host snout-vent length on the parasitism however; there is no influence of host sex on the parasitic abundance.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3


  1. Aho, J.M. 1990. Helminth communities of amphibians and reptiles: comparative approaches to understanding patterns and processes. In Parasite communities: patterns and processes, ed. G.W. Esch, A.O. Bush, and J.M. Aho, 157–195. New York: Chapman and Hall.

  2. Akani, G.C., L. Luiselli, C.C. Amuzie, and G.N. Wokem. 2011. Helminth community structure and diet of three Afrotropical anuran species: a test of the interactive-versus-isolationist parasite communities’ hypothesis. Web Ecology 11: 11–19.

  3. Anderson, R.C. 2000. Nematode parasites of vertebrates. Their development and transmission, 650. Wallingford: CABI Publishing.

  4. Anderson, R.C., A.G. Chabaud, and S. Willmott. 2009. Keys to nematode parasites of vertebrates, 1–449. Wallingford: CABI Publishing.

  5. Anderson, R.M., and R.M. May. 1979. Population biology of infectious: part-1. Nature 280: 361–367.

  6. Ataur-Rahim, M. 1981. Occurrence of helminth parasites of brown trout in the river Alyn, North Wales. Pakistan Journal of Zoology 13: 169–177.

  7. Baker, M.R. 1987. Synopsis of the nematode parasitic in amphibians and reptiles. Memorial University of Newfoundland Occasional Papers in Biology 11: 1–325.

  8. Barton, D.P. 1999. Ecology of helminth communities in tropical Australian amphibians. International Journal for Parasitology 29: 921–926.

  9. Begum, A., and N. Banu. 2012. Sex, organal and seasonal differences of helmintho-fauna of Toad, Bufo melanostictus (Schneider, 1799). Bangladesh Journal of Zoology 40: 155–164.

  10. Bolek, M.G., and J.R. Coggins. 2003. Helminth community structure of sympatric eastern American toad, Bufo americanus americanus, northern leopard frog, Rana pipiens, and blue-spotted salamander, Ambystoma laterale, from southeastern Wisconsin. Journal of Parasitology 89: 673–680.

  11. Bray, R.A., D.I. Gibson, and A. Jones. 2002. Keys to the trematoda, vol. 1. Wallingford and London: CABI Publishing and The Natural History Museum.

  12. Burn, P.R. 1980. The parasites of smooth flounder, Liopsetta putnami (Gill), from the Great Bay Estuary, New Hampshire. The Journal of Parasitology 66: 532–541.

  13. Bursey, C.R., and S.R. Goldberg. 2001. Falcaustra lowei n. sp. and other helminths from the Tarahumara frog, Rana tarahumarae (Anura: Ranidae), from Sonora, Mexico. The Journal of Parasitology 87: 340–344.

  14. Bush, A.O., and J.C. Holmes. 1986. Intestinal helminths of lesser scaup ducks: An interactive community. Canadian Journal of Zoology 64: 142–152.

  15. Bush, A.O., K.D. Lafferty, J.M. Lotz, and A.W. Shostak. 1997. Parasitology meets ecology on its own terms: Margolis et al., revisited. Journal of Parasitology 83: 575–583.

  16. Campiao, K.M., R.J. da Silva, and V.L. Ferreira. 2009. Helminth parasites of Leptodactylus podicipinus (Anura: Leptodactylidae) from southeastern Pantanal, State of Mato Grosso do Sul, Brazil. Journal of Helminthology 83: 345–349.

  17. Campos, A., and E. Carbonell. 1994. Parasite community diversity in two Mediterranean labrid fishes, Symphodus tinca and Labrus merula. Journal of Fish Biology 44: 409–413.

  18. Cannon, L.R.G. 1977. Some ecological relationships of larval ascaridoids from south-eastern Queensland marine fishes. International Journal for Parasitology 7: 227–232.

  19. Chandra, P., and N. Gupta. 2007. Habitat preference and seasonal fluctuations in the helmintho fauna of amphibian hosts of Rohilkhand zone, India. Asian Journal of Experimental Science 21: 69–78.

  20. Cloutman, D.G. 1975. Parasite community structure of largemouth bass, and bluegill in Lake Fort Smith, Arkansas. Transactions of the American Fisheries Society 104: 277–283.

  21. Comas, M., A. Ribas, C. Mialzzo, E. Sperone, and S. Tripepi. 2014. High levels of prevalence related to age and body condition: host-parasite interaction in a water frog, Pelophylaxkl hispanicus. Acta Herpetologica 9: 25–31.

  22. Dambacher, J.M. 2002. Relevance of community structure in assessing indeterminacy of ecological predictions. Ecology 83: 1372–1385.

  23. Dare, O.K., and M.R. Forbes. 2008. Rates of development in male and female wood frogs and patterns of parasitism by lung nematodes. Parasitology 135: 385–393.

  24. Dare, O.K., and M.R. Forbes. 2009a. Patterns of trematode and nematode lungworm infections in northern leopard frogs and wood frogs from Ontario, Canada. Journal of Helminthology 83: 339–343.

  25. Dare, O.K., and M.R. Forbes. 2009b. Patterns of infection by lungworms, Rhabdias ranae and Haematoloechus spp., in Northern leopard frogs, a relationship between sex and parasitism. Journal of Parasitology 95: 275–280.

  26. Dogiel, V.A. 1970. Ecology of the parasites of freshwater fishes. In Parasitology of fishes, ed. V.A. Dogiel, G.K. Petrushevsky, and Y.I. Polyanski, 1–47. Hong Kong: T.F.H. Publications, Inc. Ltd.

  27. Esch, G.W., and J.C. Fernandez. 1993. A functional biology parasitism. London: Chapmann and Hall.

  28. Esch, G.W., A.W. Shostak, D.J. Marcogliese, and T.M. Goater. 1990. Patterns, and processes in helminth parasite communities: an overview. In Parasite communities: patterns and processes, ed. G.W. Esch, A.O. Bush, and J. Aho, 1–9. New York: Chapman and Hall.

  29. Folstad, I., and A.J. Karter. 1992. Parasites, bright males, and the immune competence handicap. The American Naturalist 139: 603–622.

  30. Garvin, M.C., J.P. Basbaum, R.M. Ducore, and K.E. Bell. 2003. Patterns of Haemoproteus beckeri parasitism in the gray catbird (Dumetella carolinensis) during the breeding season. Journal of wildlife Diseases 39: 582–587.

  31. Gonzalez, C.E., and M.I. Hamann. 2012. Seasonal occurrence of Cosmocerca podicipinus (Nematoda: Cosmocercidae) in Pseudopaludicola boliviana (Anura: Leiuperidae) from natural environments in Corrientes Province, Argentina and aspects of its population structure. Parasitology Research 111: 1923–1928.

  32. Grabda-Kazubski, B., B. Baturo-Warsza-wska, and T. Pojmanska. 1987. Dynamics of parasite infestations of fishes in Lakes Dgal Wielki and Warnaik in connection with introduction of phytophagous species. Acta Parasitologica Polonica 32: 1–28.

  33. Guidelli, G.M., A. Isaac, R.M. Takemoto, and G.C. Pavanelli. 2003. Endoparasite infracommunities of hemisorubim platyrhynchos (valenciennes, 1840) (pisces: pimelodidae) of the baia river, upper parana river floodplain, brazil: specific composition and ecological aspects. Brazilian Journal of Biology 63: 261–268.

  34. Hamann, M.I., A.I. Kehr, and C.E. Gonzalez. 2010. Helminth community structure of Scinax nasicus (Anura: Hylidae) from a South American subtropical area. Diseases of Aquatic Organisms 93: 71–82.

  35. Hamann, M.I., C.E. Gonzalez, and A.I. Kehr. 2006. Helminth community of Leptodactylus latinasus (Anura: Leptodactylidae) in two contrasting environments from northeastern Argentina. Journal of Parasitology 92: 1171–1179.

  36. Hamann, M.I., A.I. Kehr, and C.E. Gonzalez. 2012. Community structure of helminth parasites of Leptodactylus bufonius (Anura: Leptodactylidae) from Northeastern Argentina. Zoological Studies 51: 1454–1463.

  37. Hamann, M.I., A.I. Kehr, and C.E. Gonzalez. 2013. Helminth communities in the burrowing toad, Rhinella fernandezae, from northeastern Argentina. Biologia 68: 1155–1162.

  38. Hamann, M.I., A.I. Kehr, and C.E. Gonzalez. 2014. Helminth community structure in the Argentinean bufonid Melanophryniscus klappenbachi: importance of habitat use and season. Parasitology Research 113:3639–3649.

  39. Hamann, M.I., A.I. Kehr, and C.E. Gonzalez. 2015. Helminth parasites in the toad Rhinella major (Bufonidae) from Chaco region, Argentina. Acta Herpetologica 10: 93–101.

  40. Hasselquist, D., O. Ostman, J. Waldenstrom, and S. Bensch. 2007. Temporal patterns of occurrence and transmission of the blood parasite Haemoproteus payevskyi in the great reed warbler (Acrocephalus arundinaceus). Journal of Ornithology 148: 401–409.

  41. Hemalatha, M., S.C. Kalyan, and V. Anuprasanna. 2015. Seasonal Occurrence and infectivity of Nematode parasites in the Indian bull frog, Hoplobatrachus tigerinus Daudin, 1803 (Anura: Dicroglossidae) of YSR Kadapa District, Andhra Pradesh, India. The Journal of Advances in Parasitology 2: 34–39.

  42. Hiware, C.J., B.V. Jadhav, and A.D. Mohekar. 2003. Applied Parasitology. A practical manual. Jaipur: Mangaldeep publications.

  43. Holland, C.V. 2009. Predisposition to ascariasis: patterns, mechanisms and implications. Parasitology 136: 1537–1547.

  44. Holmes, J.C. 1961. Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephalan) general effects and comparison with crowding. Journal of Parasitology 47: 209–216.

  45. Holmes, J.C. 1962. Effects of concurrent infections on Hymenolepis diminuta (cestoda) and Moniliformis dubius (Acanthocephalus) II. Effects on growth. The Journal of parasitology 48: 87–96.

  46. Holmes, J.C., and P.W. Price. 1986. Communities of parasites in J. Kikkawa. Community ecology: pattern and process, 187–213. Melbourne: Blackwell Scientific.

  47. Ibrahim, M.M.I. 2008. Helminth infracommunities of the maculated toad Amietophrynus regularis (Anura: Bufonidae) from Ismailiam, Egypt. Diseases of Aquatic Organisms 82: 19–26.

  48. Jones, A., R.A. Bray, and D.I. Gibson. 2005. Keys to the trematoda, vol. 2. Wallingford and London: CABI Publishing and The Natural History Museum.

  49. Khalil, L.F., A. Jones, and R. A. Bray. 1994. Keys to the cestode parasites of Vertebrates. xiii+751pp.

  50. Kuperman, B.I. (1973). Tapeworms of the Genus Triaenophorus. Parasites of Fishes. Nauka Publishers Leningrad Section, Leningrad (English translation 1981 Amerind Publishing Co. Pvt. Ltd, New Delhi).

  51. Lawrence, J.L. 1970. Effects of season, host age, and sex on endohelminths of Catostomus commersoni. Journal of Parasitology 56: 567–571.

  52. Lizama, M., L.A. De, R.M. Takemoto, and G.C. Pavanelli. 2005. Influence of host sex and age on infracommunities of metazoan parasites of Prochilodus lineatus (Valenciennes 1836) (Prochilodontidae) of Upper Parana River floodplain, Brazil. Parasite 12: 299–304.

  53. Luque, J.L., J.F.R. Amato, and R.M. Takemoto. 1996. Comparative analysis of the communities of metazoan parasites of Orthopristis rubber and Haemulon steindachneri (Osteichthyes: Haemulidae) from the Southeastern Brazilian littoral: I. Structure and influence of size and sex of the hosts. Revista Brasileira de Biologia 56: 279–299.

  54. Luque, J.L., A.N. Martins, and L.E.R. Tavares. 2005. Community structure of metazoan parasites of the yellow Cururu toad, Bufo ictericus (Anura: Bufonidae) from Rio de Janeiro, Brazil. Acta Parasitology 50: 215–220.

  55. Madhavi, R., C. Vijayalakshmi, and K. Shyamasundari. 2007. Collection, staining and identification of different helminth parasites. A manual of the workshop on fish parasites—Taxonomy Capacity Building. Visakhapatnam: Andhra University Press.

  56. Margolis, L., G.W. Esch, J.C. Holmes, A.M. Kuris, and G.A. Shad. 1982. The use of ecological terms in parasitology. (Report of an Ad Hoc Committee of American Society of Parasitology). Journal of Parasitology 68: 131–133.

  57. McAllister, C.T., C.R. Bursey, and P.S. Freed. 2010. Helminth parasites of selected amphibians and reptiles from the Republic of Ecuador. Comparative Parasitology 77: 52–66.

  58. McAlpine, D.F. 1997. Helminth communities in bullfrogs (Rana catesbeiana), green frogs (Rana clamitans) and leopard frogs (Rana pipiens) from New Brunswick, Canada. Canadian Journal of Zoology 75: 1883–1890.

  59. Michael, W.J., A.N. Patrick, and A.T. Dick. 2004. Structuring mechanisms of yellow perch (Perca flavescens) parasite communities: host age, diet and local factors. Canadian Journal of Zoology 82: 1291–1301.

  60. Moser, M., and J. Hseih. 1992. Biological tags for stock separation in Pacific herring Clupea harengus pallasi in California. Journal of Parasitology 78: 54–60.

  61. Noble, G.K. 1930. The biology of the amphibia, 433–441. New York: Dover Publications Inc.

  62. Pearson, J.C. 1968. Observations on the morphology and life-cycle of Paucivitellosus fragilis Coil, Reid and Kuntz, 1965 (Trematoda: Bivesiculidae). Parasitology 58: 769–788.

  63. Poulin, R. 1996. Helminth growth in vertebrate hosts: does host sex matter? International Journal for Parasitology 26: 1311–1315.

  64. Poulin, R. 2001. Interactions between the species and the structure of helminth communities. Parasitology 122: S3–S11.

  65. Poulin, R., and J.L. Luque. 2003. A general test of the interactive isolationist continuum in gastrointestinal parasite communities of fish. International Journal for Parasitology 33: 1623–1630.

  66. Price, P.W., and K.M. Clancy. 1983. Patterns in number of helminth parasite species in freshwater fishes. Journal of Parasitology 69: 449–454.

  67. Raffel, T.R., R.P. LeGros, B.C. Love, J.R. Rohr, and P.J. Hudson. 2009. Parasite age-intensity relationships in red-spotted newts: Does immune memory influence salamander disease dynamics? International Journal for Parasitology 39: 231–241.

  68. Reichenbach-klinke, H., and E. Elken. 1965. The principle of lower vertebrates. Diseases of Amphibians. London: Academic press.

  69. Sanchis, V., J.M. Roig, M.A. Carretero, V. Roca, and G.A. Llorente. 2000. Host-parasite relationships of Zootoca vivipara (Sauria: Lacertidae) in the Pyrenees (North Spain). Folia Parasitologica 47: 118–122.

  70. Santos, V.G.T., and S.B. Amato. 2010. Helminth fauna of Rhinella fernandezae (Anura: Bufonidae) from the Rio Grande do Sul Coastland, Brazil: Analysis the parasite community. Journal of Parasitology 96: 823–826.

  71. Santos, V.G.T., S.B. Amato, and M. Marcio Borges. 2013. Community structure of helminth parasites of the “Cururu” toad, Rhinella icterica (Anura: Bufonidae) from southern Brazil. Parasitology Research 112: 1097–1103.

  72. Scott, J.S. 1982. Digenean parasite communities in flatfishes of the Scotia Shelf and southern Gulf of St. Lawrence. Canadian Journal of Zoology 60: 2804–2811.

  73. Shannon, C.E., and W. Weaver. 1949. The mathematical theory of communication. Urbana: University of Illions Press.

  74. Sluys, M.V., G.M. Schittini, R.V. Marra, A.R.M. Azevedo, J.J. Vincente, and D. Vrcibradic. 2006. Body size, diet and endoparasites of the Microhyalid frog, Chiasmocleius capixaba in an Atlantic forest area of Southern Bahia state, Brazil. Brazilian Journal of Biology 66(1A): 167–173.

  75. Sousa, W.P. 1994. Patterns and processes in communities of helminth parasites. Trends in Ecology & Evolution 9: 52–57.

  76. Sulieman, Y., A. Afifi, M.H. Awad, and T. Pengsakul. 2015. Helminth parasites of the subdesert toad, Amietophrynus (Bufo) xeros (Anura: Bufonidae). International Journal of Research–Granthaalayah 3(10): 75–83.

  77. Takemoto, R.M., and G.C. Pavanelli. 2000. Aspects of the ecology of proteocephalid cestodes parasites of Sorbium lima (Pimelodidae) of the Upper Parana river, Brazil. Structure and influence of host’s size and sex. Brazilian Journal of Biology 60: 577–584.

  78. Telfer, S., R. Birtles, M. Bennet, X. Lambin, S. Paterson, and M. Begon. 2008. Parasite interactions in natural populations: insights from longitudinal data. Parasitology 135: 767–781.

  79. Tinsley, R., L. Stott, J. York, A. Everard, S. Chapple, J. Jackson, Vinev Ma, and M.C. Tinsley. 2012. Acquired immunity protects against helminth infection in a natural host population: long-term field and laboratory evidence. International Journal for Parasitology 42: 931–938.

  80. Ulmer, M.J. 1970. Studies on the helminth fauna of Iowa I. Trematodes of amphibians. American Midland. Naturalist 83: 38–64.

  81. Williams, H.M., and A. Jones. 1994. Parasitic worms of fish, 563. London: Taylor & Francis.

  82. Yamaguti, S. 1958. Systema helminthum, Vol. I. The digenetic trematodes of vertebrates. New York: Interscience Publishers Inc.

  83. Yamaguti, S. 1959. Systema helminthum, vol II. The cestodes of vertebrates, 699. New York: Interscience Publishers Inc.

  84. Yamaguti, S. 1961. Systema helminthum, Vol. III. Nematoda. New York: Interscience Publishers Inc.

  85. Yamaguti, S. 1971. Synopsis of digenetic trematodes of vertebrates, Vol. I., part-I & II. Tokyo: Kigaku Publ. Co.

  86. Yoder, H.R., and J.R. Coggins. 2007. Helminth communities in five species of sympatric amphibians from three adjacent ephemeral ponds in southeastern Wisconsin. Journal of Parasitology 93: 755–760.

  87. Zar, J.H. 1996. Biostatistical analysis. 3rd ed. Upper Saddle River: Prentice Hall Inc.

  88. Zelmer, D.A., and H.P. Arai. 1998. The contributions of host age and size to the aggregated distribution of parasites in yellow perch, Perca flavescens, from Garner Lake, Alberta, Canada. The Journal of Parasitology 84: 24–29.

Download references


The First author, Mannela Hemalatha is grateful to University Grants Commission for providing the financial assistance as JRF and SRF under Rajiv Gandhi National fellowship (RGNF Award No. 2011-12/RGNF-SC-AND-5015, dt.01.06.2012).

Author information

The first and second author, Mannela Hemalatha and C. Srinivasa kalyan were involved in collecting the host samples and parasites, literature survey, statistical analysis and writing the manuscript while the third author, Anu prasanna Vankara was the research supervisor who guided in drafting the manuscript.

Correspondence to Anu Prasanna Vankara.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest related to the work.

Significance statement

This study shows that the community structure of parasites in the amphibian host, Hoplobatrachus tigerinus is less diverse, non-interactive, isolationist and depauperate. Many factors such as temperature, seasons, host age, sex, length, weight, food and feeding habits are very crucial in shaping the parasitic communities in a host. This study would also help the young researchers to analyze the parasitic community structure of other amphibians in a very classy mode.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Mannela, H., Chadamala, S.K. & Vankara, A.P. Structure of the Parasite Infracommunity of Hoplobatrachus tigerinus Daudin, 1803 from YSR Kadapa District, Andhra Pradesh, India. Proc Zool Soc 73, 46–58 (2020). https://doi.org/10.1007/s12595-019-00297-3

Download citation


  • Hoplobatrachus tigerinus
  • Metazoan parasites
  • Community structure