Skip to main content
SpringerLink
Log in

Compatibility of Schistosoma japonicum from the hilly region and Oncomelania hupensis hupensis from the marshland region within Anhui, China

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

Abstract

Schistosome japonicum remains one main public concern in China. This is exemplified in the hilly region in Anhui Province, where rodents have served as reservoirs for the parasite and no effective intervention could target such wild animals. The closer relationship between the hilly region and the near marshland induces the worry of spread of the hill parasite to the marshland region. Therefore, the level of snail-parasite compatibility between the hill parasite and snail populations from the Yangtze River valley was investigated. The results of this study demonstrated that both the hill (Shitai, Anhui) and the marshland (Wuxi, Jiangsu) strains of parasite were more infective to the marshland strains of snail (Zongyang and Hexian, Anhui) than to the hill strain of snail (Shitai, Anhui). When snails were individually exposed to one single miracidium, the longest prepatent period for cercarial development was observed in the combination of Shitai schistosome/Shitai snail. A nocturnal cercarial emergence pattern was observed for the hill parasite, either harbored in the hill or the marshland strain of snails. The results suggested a high compatibility between the marshland strains of snail and both the hill and the marshland strains of parasite. This would have practical implications. Moreover, the fact of the lower compatible relationship between the hill parasite and its local intermediate hosts warranted more studies.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abou-El-Naga IF (2014) Meta-analysis indicates lack of local adaptation of Schistosoma mansoni to Biomphalaria alexandrina in Egypt. Parasitol Res 113:1185–1194

    Article  PubMed  Google Scholar 

  • Boissier J, Morand S, Mone H (1999) A review of performance and pathogenicity of male and female Schistosoma mansoni during the life-cycle. Parasitology 119(Pt 5):447–454

    Article  PubMed  Google Scholar 

  • Cao SQ, Wu MY (2004) An investigation of ourbreak of acute schistosomiasis in Shitai county of Anhui Province. Tropical Diseases and Parasitology 1:67–68

    Google Scholar 

  • Chen MG, Zheng F (1999) Schistosomiasis control in China. Parasitol Int 48:11–19

    Article  Google Scholar 

  • Chen XF, Chu CZ, Du YF, Gao FH (2010) Snail distribution in Shitai county of Anhui province. Journal of Tropical Diseases and Parasitology 8:88–90

    Google Scholar 

  • Claveria FG, Etges FJ (1987) Differential susceptibility of male and female Oncomelania hupensis quadrasi infected with Schistosoma japonicum. Int J Parasitol 17:1273–1277

    Article  CAS  PubMed  Google Scholar 

  • Cross JH, Zaraspe G, Lu SK, Chiu KM, Hung HK (1984) Susceptibility of Oncomelania hupensis subspecies to infection with geographic strains of Schistosoma japonicum. Southeast Asian J Trop Med Public Health 15:155–160

    CAS  PubMed  Google Scholar 

  • Gandon S, Capowiez Y, Dubois Y, Michalakis Y, Olivieri I (1996) Local adaptation and gene-for-gene coevolution in a metapopulation model. Proc R Soc B 263:1003–1009

    Article  Google Scholar 

  • Gryseels B, Polman K, Clerinx J, Kestens L (2006) Human schistosomiasis. Lancet 368:1106–1118

    Article  PubMed  Google Scholar 

  • He YX, Guo YH, Ni CH, Xia F, Liu HX, Yu QF, Hu YQ (1991) Compatibility between Oncomelania hupensis and different isolates of Schistosoma japonicum in China. Southeast Asian J Trop Med Public Health 22:245–248

    CAS  PubMed  Google Scholar 

  • He YX, Salafsky B, Ramaswamy K (2001) Host-parasite relationships of Schistosoma japonicum in mammalian hosts. Trends Parasitol 17:320–324

    Article  CAS  PubMed  Google Scholar 

  • Ibikounle M, Mouahid G, Mintsa Nguema R, Sakiti NG, Kinde-Gasard D, Massougbodji A, Mone H (2012) Life-history traits indicate local adaptation of the schistosome parasite, Schistosoma mansoni, to its snail host, Biomphalaria pfeifferi. Exp Parasitol 132:501–507

    Article  CAS  PubMed  Google Scholar 

  • Jiang YJ, Xi WP, Sun QQ (1997) The observation of mixed mud fodder for snail raising. Chin J Schistoso Control 1:46–47

    Google Scholar 

  • Lepesant JM, Boissier J, Climent D, Cosseau C, Grunau C (2013) Female biased sex-ratio in Schistosoma mansoni after exposure to an allopatric intermediate host strain of Biomphalaria glabrata. Exp Parasitol 135:350–356

    Article  PubMed  Google Scholar 

  • Li SZ et al (2013) Endemic status of schistosomiasis in People’s Rupublic of China in 2012. Chin J Schisto Control 25:557–563

    Google Scholar 

  • Li SZ et al (2014) Reduction patterns of acute schistosomiasis in the People’s Republic of China. PLoS Negl Trop Dis 8:e2849

    Article  PubMed Central  PubMed  Google Scholar 

  • Lin Q, Du YF, Wu MY, Xu YX (2004) Acute schistosomiasis in Shitai county, China from 1998 to 2003. Chin J Schisto Control 16:475

    Google Scholar 

  • Liu XP et al (2013) Infection status of sources of schistosomiasis japonica in marshland and hilly regions. Journal of Pathogen Biology 8(445–447):410

    CAS  Google Scholar 

  • Lu DB, Wang TP, Rudge JW, Donnelly CA, Fang GR, Webster JP (2009) Evolution in a multi-host parasite: chronobiological circadian rhythm and population genetics of Schistosoma japonicum cercariae indicates contrasting definitive host reservoirs by habitat. Int J Parasitol 39:1581–1588

    Article  PubMed  Google Scholar 

  • Lu DB, Wang TP, Rudge JW, Donnelly CA, Fang GR, Webster JP (2010) Contrasting reservoirs for Schistosoma japonicum between marshland and hilly regions in Anhui, China—a two-year longitudinal parasitological survey. Parasitology 137:99–110

    Article  PubMed  Google Scholar 

  • Manning SD, Woolhouse ME, Ndamba J (1995) Geographic compatibility of the freshwater snail Bulinus globosus and schistosomes from the Zimbabwe highveld. Int J Parasitol 25:37–42 doi:0020-7519(94)00097-8 [pii]

  • Mao SP (1990) Schistosome biology and control of schistosomiasis. Publishing House of People's Health, Beijing

    Google Scholar 

  • McManus DP et al (2010) Schistosomiasis in the People’s Republic of China: the era of the Three Gorges Dam. Clin Microbiol Rev 23:442–466

    Article  PubMed Central  PubMed  Google Scholar 

  • Mouahid A, Combes C (1987) Genetic variability of Schistosoma bovis cercarial production according to miracidial dose. J Helminthol 61:89–94

    Article  CAS  PubMed  Google Scholar 

  • Norton A, Rollinson D, Richards L, Webster J (2008) Simultaneous infection of Schistosoma mansoni and S. rodhaini in Biomphalaria glabrata: impact on chronobiology and cercarial behaviour. Parasites and Vectors 1:43

    Article  PubMed Central  PubMed  Google Scholar 

  • Ohmae H, Iwanaga Y, Nara T, Matsuda H, Yasuraoka K (2003) Biological characteristics and control of intermediate snail host of Schistosoma japonicum. Parasitol Int 52:409–417

    Article  PubMed  Google Scholar 

  • Pesigan TP, Hairston NG, Jauregui JJ, Garcia EG, Santos AT, Santos BC, Besa AA (1958) Studies on Schistosoma japonicum infection in the Philippines. 2. The molluscan host. Bull World Health Organ 18:481–578

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shi HP, Lu DB, Shen L, Shi T, Gu J (2014) Single- or mixed-sex Schistosoma japonicum infections of intermediate host snails in hilly areas of Anhui, China. Parasitol Res 113:717–721

    Article  PubMed  Google Scholar 

  • Steinauer ML (2009) The sex lives of parasites: investigating the mating system and mechanisms of sexual selection of the human pathogen Schistosoma mansoni. Int J Parasitol 39:1157–1163

    Article  PubMed Central  PubMed  Google Scholar 

  • Su J, Zhou F, Lu DB (2013) A circular analysis of chronobiology of Schistosoma japonicum cercarial emergence from hilly areas of Anhui, China. Exp Parasitol 135:421–425

    Article  PubMed  Google Scholar 

  • Theron A (1989) Hybrids between Schistosoma mansoni and S. rodhaini: characterization by cercarial emergence rhythms. Parasitology 99:225–228

    Article  PubMed  Google Scholar 

  • Theron A, Combes C (1988) Genetic analysis of cercarial emergence rhythms of Schistosoma mansoni. Behav Genet 18:201–209

    Article  CAS  PubMed  Google Scholar 

  • Theron A, Pages JR, Rognon A (1997) Schistosoma mansoni: distribution patterns of miracidia among Biomphalaria glabrata snail as related to host susceptibility and sporocyst regulatory processes. Exp Parasitol 85:1–9

    Article  CAS  PubMed  Google Scholar 

  • Theron A, Coustau C, Rognon A, Gourbiere S, Blouin MS (2008) Effects of laboratory culture on compatibility between snails and schistosomes. Parasitology 135:1179–1188

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Liang YS, Hong QB, Dai JR (2013) African schistosomiasis in mainland China: risk of transmission and countermeasures to tackle the risk. Parasit Vectors 6:249

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wilke T, Davis GM, Cui EC, Xiao-Nung Z, Xiao Peng Z, Yi Z, Spolsky CM (2000) Oncomelania hupensis (Gastropoda: rissooidea) in eastern China: molecular phylogeny, population structure, and ecology. Acta Trop 77:215–227

    Article  CAS  PubMed  Google Scholar 

  • Yang GJ, Utzinger J, Sun LP, Hong QB, Vounatsou P, Tanner M, Zhou XN (2007) Effect of temperature on the development of Schistosoma japonicum within Oncomelania hupensis, and hibernation of O. hupensis. Parasitol Res 100:695–700

    Article  PubMed  Google Scholar 

  • Zavodna M, Sandland GJ, Minchella DJ (2008) Effects of intermediate host genetic background on parasite transmission dynamics: a case study using Schistosoma mansoni. Exp Parasitol 120:57–61

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhou XN et al (2005) The public health significance and control of schistosomiasis in China—then and now. Acta Trop 96:97–105

    Article  PubMed  Google Scholar 

  • Zhou XN et al (2007) Potential risks for transmission of schistosomiasis caused by mobile population in Shanghai. Chin J Parasit Dis Con 25:180–184

    Google Scholar 

  • Zhou XN et al (2008) Potential impact of climate change on schistosomiasis transmission in China. Am J Trop Med Hyg 78:188–194

    PubMed  Google Scholar 

Download references

Acknowledgments

This work was funded by the Soochow University for Training Programs of Innovation and Entrepreneurship of Undergraduates (2013) and the National Sciences Foundation of China (No. 81273141).

Author information

Authors and Affiliations

  1. Department of Epidemiology and Statistics, School of Public Health, Soochow University, 215123, Suzhou, China

    Chen-Zhong Wang, Da-Bing Lu, Cheng-Xiang Guo, Yuan-Meng Gao, Chao-Rong Bian & Jing Su

  2. School of Biology and Basic Medical Sciences, Soochow University, 215123, Suzhou, China

    Ying Li

Authors
  1. Chen-Zhong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Da-Bing Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cheng-Xiang Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ying Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuan-Meng Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chao-Rong Bian
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jing Su
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Da-Bing Lu.

Additional information

Chen-Zhong Wang and Da-Bing Lu contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, CZ., Lu, DB., Guo, CX. et al. Compatibility of Schistosoma japonicum from the hilly region and Oncomelania hupensis hupensis from the marshland region within Anhui, China. Parasitol Res 113, 4477–4484 (2014). https://doi.org/10.1007/s00436-014-4133-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-014-4133-0

Keywords

Search

Navigation