[go: up one dir, main page]
More Web Proxy on the site http://driver.im/ Skip to main content

Advertisement

Log in

Gigantobilharzia melanoidis n.sp. (Trematoda: Schistosomatidae) from Melanoides tuberculata (Gastropoda: Thiaridae) in the United Arab Emirates

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Delicate filamentous schistosomatids detected in the intestinal veins of experimentally infected chickens are here described as a new parasite species, Gigantobilharzia melanoidis, and details of its life cycle are given. It is the first complete description of a schistosome species that uses Melanoides tuberculata as an intermediate host. Apharyngeate ocellate brevifurcate cercariae found in 65 out of 950 M. tuberculata collected in a pond in Al Aweer, United Arab Emirates were used as infection material. The new species can be distinguished from the other species of the genus by the following combination of characters: caecal reunion in males situated anterior to seminal vesicle, a very short gynecophoric canal (gynecophoric canal length/body length ratio lower than 0.05) supported by 12–14 thickened bands. Cercariae of G. melanoidis can be distinguished from other Gigantobilharzia cercariae described in the literature based on the combination of these characters: flame cell formula 2[3 + 3 + (1)] = 14 and relatively longer tail stem in relation to body (tail stem length/body length ratio = 2). Under laboratory conditions at a temperature between 24 and 26 °C, M. tuberculata started to shed cercariae 7 weeks after exposure to miracidia. The prepatent period of G. melanoidis in experimentally infected chicken lasted between 43 and 49 days. The parasite inhabits the blood vessels mainly of the small intestine. Sections of adult worms and eggs were also found in histocuts of parenchymatous organs. Results of phylogenetic analysis corroborated that G. melanoidis is a distinct species; however, they also confirmed that the genus Gigantobilharzia is in need of revision and in future might be split into several genera.

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

Access this article

Subscribe and save

Springer+ Basic
£29.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Notes

  1. Both species were synonymised by Farley (1971), and this opinion is shared also by Khalifa (1974) and Aldhoun et al. (2012).

  2. Oral sucker is well developed in both male and females of G. gyrauli (Brackett 1940). It is present only in the male of G. monocotylea (Szidat 1930) and week in both sexes of G. tantali (Fain 1955).

  3. There are several descriptions of cercariae of G. sturniae. They obviously deal with multiple species, as they state two different flame cell formulas, and the isolates also differ considerably in their dimensions (for details see Aldhoun et al. 2012). However, G. melanoidis differs from all these isolates.

  4. This species was synonymised with G. aegypti by Omran et al. (1976), but there are differences between the two species (e.g. presence of a structure that appears to be a ventral sucker in females of Gigantobilharzia sp., different size and shape of eggs, etc.); therefore, we regard these findings as two different species.

References

  • Akramova FD, Azimov DA, Shakarboev EB (2010) The morphology and biology of the trematode Gigantobilharzia acotylea (Digenea, Schistosomatidae). Vestnik Zool 44:403–412

    Google Scholar 

  • Aldhoun JA, Faltýnková A, Karvonen A, Horák P (2009a) Bird schistosomes in the North: a unique finding from a prosobranch snail using molecular tools. Parasitol Int 58:314–317

    Article  CAS  PubMed  Google Scholar 

  • Aldhoun JA, Kolářová L, Horák P, Skírnisson K (2009b) Bird schistosome diversity in Iceland: molecular approach. J Helminthol 83:173–180

    Article  CAS  PubMed  Google Scholar 

  • Aldhoun JA, Podhorský M, Holická M, Horák P (2012) Bird schistosomes in planorbid snails in the Czech Republic. Parasitol Int 61:250–259

    Article  PubMed  Google Scholar 

  • Brackett S (1940) Five new species of avian schistosomes from Wisconsin and Michigan with the life cycle of Gigantobilharzia gyrauli (Brackett, 1940). J Parasitol 28:25–42

    Article  Google Scholar 

  • Brant SV (2007) The occurrence of the avian schistosome Allobilharzia visceralis Kolářová, Rudolfová, Hampl et Skírnisson, 2006 (Schistosomatidae) in the tundra swan, Cygnus columbianus (Anatidae), from North America. Folia Parasitol 54:99–104

    Article  CAS  PubMed  Google Scholar 

  • Brant SV, Loker ES (2009) Schistosomes in the Southwest United States and their potential for causing cercarial dermatitis or “swimmer's itch”. J Helminthol 83:191–198

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brant SV, Morgan JA, Mkoji GM, Snzder SD, Rajapakse RP, Loker ES (2006) An approach to revealing blood fluke life cycles, taxonomy, and diversity: provision of key reference data including DNA sequence from single life cycle stages. J Parasitol 92:77–88

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brant SV, Cohen AN, James D, Hui L, Hom A, Loker ES (2010) Cercarial dermatitis transmitted by exotic marine snail. Emerging Infect Dis 16:1357–1365

    Article  PubMed  Google Scholar 

  • Dönges J (1964) Gigantobilharzia suebica n. sp. (Trematoda), ein Dermatitiserreger beim Menschen. Parasitol Res 24:65–75

    Google Scholar 

  • Dvořák J, Vanácová Š, Hampl V, Flegr J, Horák P (2002) Comparison of European Trichobilharzia species based on ITS1 and ITS2 sequences. Parasitology 124:307–313

    PubMed  Google Scholar 

  • Fahmy MAM, Mandour AM, Arafa MS, Omran LAM (1976) Gigantobilharzia sp. recovered from chicken experimentally infected with cercariae from Melanoides tuberculata in Egypt. Acta Parasitol Polonica 24:11–18

    Google Scholar 

  • Fain A (1955) Étude sur le schistosomes d'oiseaux au Ruanda-Urundi (Congo Belge) un nouveau schistosome du tantale ibis (Ibis ibis Lin) Gigantobilharzia tantali n.sp. Ann Parasitol Hum Comp 30:321–328

    Google Scholar 

  • Farahnak A, Setodeh S, Mobedi I (2005) A faunistic survey of cercariae isolated from Melanoides tuberculata and their role in transmission diseases. Arch Razi Inst 59:113–119

    Google Scholar 

  • Farley J (1971) A review of the family Schistosomatidae: excluding the genus Schistosoma from mammals. J Helminthol 45:289–320

    Article  CAS  PubMed  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Huyse T, Webster BL, Geldof S, Stothard JR, Diaw OT, Polman K, Rollinson D (2009) Bidirectional introgressive hybridization between a cattle and human schistosome species. PloS Pathogens 5:e1000571

    Article  PubMed Central  PubMed  Google Scholar 

  • Johnston DA, Kane RA, Rollinson D (1993) Small subunit (18S) ribosomal RNA gene divergence in the genus Schistosoma. Parasitology 107:147–156

    Article  CAS  PubMed  Google Scholar 

  • Karamian M, Aldhoun JA, Maraghi S, Hatam G, Farhangmehr B, Sadjjadi SM (2011) Parasitological and molecular study of the furcocercariae from Melanoides tuberculata as a probable agent of cercarial dermatitis. Parasitol Res 108:955–962

    Article  PubMed  Google Scholar 

  • Khalifa R (1974) Studies on Schistosomatidae Looss, 1899 (Trematoda) of aquatic birds of Poland. II. Gigantobilharzia mazuriana sp. n., with a discussion of the subfamily Gigantobilharziinae Mehra, 1940. Acta Parasitol Polonica 22:265–284

    Google Scholar 

  • Khalil KF (2002) Family Schistosomatidae Stiles & Hassall, 1898. In Gibson DI, Jones A & Bray RA (eds) Keys to the Trematoda, vol. 1. CAB International and the Natural History Museum, London, pp 419-432

  • Kolářová L, Rudolfová J, Hampl V, Skírnisson K (2006) Allobilharzia visceralis gen. nov., sp. nov. (Schistosomatidae-Trematoda) from Cygnus cygnus (L.) (Anatidae). Parasitol Int 55:179–186

    Article  PubMed  Google Scholar 

  • Leigh WH (1955) The morphology of Gigantobilharzia huttoni (Leigh, 1953) an avian schistosome with marine dermatitis producing larvae. J Parasitol 4:262–269

    Article  Google Scholar 

  • Lockyer AE, Olson PD, Ostergaard P, Rollinson D, Johnston DA, Attwood SW, Southgate VR, Horak P, Snyder SD, Le TH, Agatsuma T, McManus DP, Carmichael AC, Naem S, Littlewood DTJ (2003) The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126:203–224

    Article  CAS  PubMed  Google Scholar 

  • Morgan JA, DeJong RJ, Kayibwe F, Mkoji GM, Loker ES (2003) A newly-identified lineage of Schistosoma. Int J Parasitol 33:977–985

    Article  PubMed  Google Scholar 

  • Naim SI, Arif AMS (1991) Larval stages of Melanoides tuberculata (Muller, 1774) (Gastropoda: Prosobranchia) in a brackish spring, United Arab Emirates). Jap J Parasitol 40:157–169

    Google Scholar 

  • Najim AT (1956) Life history of Gigantobilharzia huronensis Najim, 1950. A dermatitis-producing bird-blood fluke (Trematoda-Schistosomatidae). Parasitology 46:443–469

    Article  CAS  PubMed  Google Scholar 

  • Odhner T (1910) Gigantobilharzia acotylea n. g. n. sp., ein mit Bilharzien verwandter Blutparasit von enormer Länge. Zool Anz 35:380–385

    Google Scholar 

  • Omran LA, El-Naffar MK, Mandour AM (1976) Gigantobilharzia aegypti sp. nov. in the domestic sparrow, Passer domesticus. J EgyptVet Med Assoc 36:75–87

    Google Scholar 

  • Pinto AA, De Melo AL (2011) A checklist of trematodes (Platyhelminthes) transmitted by Melanoides tuberculata (Mollusca: Thiaridae). Zootaxa 2799:15–28

    Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  CAS  PubMed  Google Scholar 

  • Rudolfová J, Hampl V, Bayssade-Dufour C, Lockyer AE, Littlewood DTJ, Horák P (2005) Validity reassessment of Trichobilharzia species using Lymnaea stagnalis as the intermediate host. Parasitol Res 95:79–89

    Article  PubMed  Google Scholar 

  • Rudolfová J, Littlewood DTJ, Sitko J, Horák P (2007) Bird schistosomes of wildfowl in the Czech Republic and Poland. Folia Parasitol 54:88–93

    Article  PubMed  Google Scholar 

  • Snyder SD (2004) Phylogeny and paraphyly among tetrapod blood flukes (Digenea: Schistosomatidae and Spirorchiidae). Intern J Parasitol 34:1385–1392

    Article  CAS  Google Scholar 

  • Szidat L (1930) Gigantobilharzia monocotylea n. sp., ein neuer Blutparasit aus ostpreussischen Wasservögeln. Parasitol Res 2:583–588

    Google Scholar 

  • Waeschenbach A, Webster BL, Bray RA, Littlewood DTJ (2007) Added resolution among ordinal level relationships of tapeworms (Platyhelminthes: Cestoda) with complete small and large subunit nuclear ribosomal RNA genes. Mol Phylogenet Evol 45:311–325

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Dr. J. Kinne and his colleagues from the Department of Pathology of the Central Veterinary Research Laboratory for processing the samples and preparing the histological cuts. Our thanks go also to Thilakaratna Samarasingha from Wadi Al Safa Wildlife Centre and to Manie Grobler from Al Ajban farm for the snail collection.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rolf K. Schuster.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schuster, R.K., Aldhoun, J.A. & O’Donovan, D. Gigantobilharzia melanoidis n.sp. (Trematoda: Schistosomatidae) from Melanoides tuberculata (Gastropoda: Thiaridae) in the United Arab Emirates. Parasitol Res 113, 959–972 (2014). https://doi.org/10.1007/s00436-013-3728-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-013-3728-1

Keywords

Navigation