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The effect of temperature on the development of Angiostrongylus cantonensis (Chen 1935) in Pomacea canaliculata (Lamarck 1822)

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Abstract

Angiostrongyliasis cantonensis, clinically presented as eosinophilic meningitis, is a snail-borne parasitic disease. We studied the effects of different temperatures on the larval development of Angiostrongylus cantonensis in the freshwater snail Pomacea canaliculata. Six groups of snails were infected and each group was cultured under different temperature conditions. At predefined intervals, four snails from each group were dissected to examine the larval development. The development–time curve of each group was drawn according to the fraction of third-stage larvae present. The developmental time was defined as the time needed until 50% of the first-stage larvae developed into third-stage larvae. A linear regression model was established based on the time (D; in days) and the corresponding temperature (T; in degrees Celsius): \( DT = 15 \times D + 262.5 \). The threshold temperature for larval development was 15.04°C and the thermal constant was 262.53 degree-days. These parameters could be helpful in estimating the number of parasite generations in a year and the impact of climate change on the distribution of A. cantonensis.

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References

  • Arnold CY (1959) The development and significance of the base temperature in a linear heat unit system. Proc Am Soc Hortic Sci 74:430–445

    Google Scholar 

  • Barçante JM, Barçante TA, Dias SR, Vieira LQ, Lima WS, Negrão-Corrêa D (2003) A method to obtain axenic Angiostrongylus vasorum first-stage larvae from dog feces. Parasitol Res 89:89–93

    Article  PubMed  Google Scholar 

  • Carlsson NOL, Lacoursière JO (2005) Herbivory on aquatic vascular plants by the introduced golden apple snail (Pomacea canaliculata) in Lao PDR. Biol Invasions 7:233–241

    Article  Google Scholar 

  • Chen HT (1933) A preliminary report on a survey of animal parasites of Canton China rats. Lingnan Sci J 12:65–74

    Google Scholar 

  • Chen XG, Li H, Lun ZR (2005) Angiostrongyliasis, mainland China. Emerg Infect Dis 11:1645–1647

    PubMed  Google Scholar 

  • Cramer JS (2004) The early origins of the logit model. Stud Hist Philos Biol Biomed Sci 35:613–626

    Article  Google Scholar 

  • el-Shazly AM, el-Hamshary EM, el-Shewy KM, Rifaat MM, el-Sharkawy IM (2002) Incidence of Parastrongylus cantonensis larvae in different fresh water snails in Dakahlia Governorate. J Egypt Soc Parasitol 32:579–588

    PubMed  CAS  Google Scholar 

  • Estebenet AL, Martín PR (2002) Pomacea canaliculata (Gastropoda: Ampullariidae): life-history traits and their plasticity. Biocell 26:83–89

    PubMed  Google Scholar 

  • Halvorsen O, Skorping A (1982) The influence of temperature on growth and development of the nematode Elaphostrongylus rangiferi in the gastropods Arianta arbustorum and Euconulus fulvus. Oikos 38:285–290

    Article  Google Scholar 

  • Hata H, Kojima S (1990) Angiostrongylus cantonensis: in vitro cultivation from the first-stage to infective third-stage larvae. Exp Parasitol 70:476–482

    Article  PubMed  CAS  Google Scholar 

  • He JZ (1982) Angiostrongylus spp. related to human diseases. J Guangzhou Med Coll 10:73–81 (in Chinese)

    Google Scholar 

  • He JZ, Zhu SH, Yang SQ, Yu BW, Chen YS, Hu GX, Wang XB, Wang L (1984) Discovery of the first human angiostrongyliasis case in mainland China by detecting worms in the cerebrospinal fluid. J Guangzhou Med Coll 12:1–4 (in Chinese)

    CAS  Google Scholar 

  • Houghton JT, Jenkins GJ, Ephraums JJ (1990) Scientific assessment of climate change. Report of Working Group I of the Intergovernmental Panel on Climate Change (IPCC). Cambridge University Press, UK

    Google Scholar 

  • Hu ZQ, Hu QJ (1991) The morphology and structure of Ampullaria gigas. Chin J Zool 26:4–6

    Google Scholar 

  • Ikemoto T, Takai K (2000) A new linearized formula for the law of total effective temperature and the evaluation of line-fitting methods with both variables subject to error. Environ Entomol 29:671–682

    Article  Google Scholar 

  • Ishii AI (1984) Effects of temperature on the larval development of Angiostrongylus cantonensis in the intermediate host, Biomphalaria glabrata. Z Parasitenkd 70:375–379

    Article  PubMed  CAS  Google Scholar 

  • Kim DY, Stewart TB, Bauer RW, Mitchell M (2002) Parastrongylus (=Angiostrongylus) cantonensis now endemic in Louisiana wildlife. J Parasitol 88:1024–1026

    PubMed  CAS  Google Scholar 

  • Kliks MM, Palumbo NE (1992) Eosinophilic meningitis beyond the Pacific Basin: the global dispersal of a peridomestic zoonosis caused by Angiostrongylus cantonensis, the nematode lungworm of rats. Soc Sci Med 34:199–212

    Article  PubMed  CAS  Google Scholar 

  • Kutz SJ, Hoberg EP, Polley L (2001) Umingmakstrongylus pallikuukensis (Nematoda: Protostrongylidae) in gastropods: larval morphology, morphometrics, and development rates. J Parasitol 87:527–535

    PubMed  CAS  Google Scholar 

  • Lin JX, Li YS, Zhu K, Chen BJ, Cheng YZ, Lin JC, Cao Y, Chen RZ (2003) Epidemiological study on group infection of Angiostrongylus cantonensis in Changle City. Chin J Parasitol Parasitic Dis 21:110–112 (in Chinese)

    Google Scholar 

  • Lin JX, Zhou XN, Li LS, Zhang Y, Cheng YZ, Zhang RY, Li YY, Li CX, Chen BJ, Li YS, Dai MY (2005) Bellamya aeruginosa acts as the intermediate host for Angiostrongylus cantonensis. Chin J Zoonoses 21:24–26 (in Chinese)

    Google Scholar 

  • Mackerras MJ, Sandars DF (1955) The life history of the rat lung-worm, Angiostrongylus cantonensis (Chen) (Nematoda: Metastrongylidae). Aust J Zool 3:1–21

    Article  Google Scholar 

  • McCarthy JJ, Canziani OF, Leary NA, Dokken DJ, White KS (2001) Climate change 2001: impacts, adaptation & vulnerability. Contribution of Working Group II to the Third Assessment Report of the Intergovernmental Panel on Climate Change (IPCC). Cambridge University Press, UK

    Google Scholar 

  • Nishimura K, Mogi M, Okazawa T, Sato Y, Toma H, Wakibe H (1986) Angiostrongylus cantonensis infection in Ampullarius canaliculatus (Lamarck) in Kyushu, Japan. Southeast Asian J Trop Med Public Health 17:595–600

    PubMed  CAS  Google Scholar 

  • Nomura S, Lin PH (1945) First case report of human infection with Haemostrongylus ratti Yokogawa. Taiwan No Ikai 3:589–592

    Google Scholar 

  • Prociv P, Spratt DM, Carlisle MS (2000) Neuro-angiostrongyliasis: unresolved issues. Int J Parasitol 30:1295–1303

    Article  PubMed  CAS  Google Scholar 

  • Raccurt CP, Blaise J, Durette-Desset MC (2003) Presence of Angiostrongylus cantonensis in Haiti. Trop Med Int Health 8:423–426

    Article  PubMed  Google Scholar 

  • Slom TJ, Cortese MM, Gerber SI, Jones RC, Holtz TH, Lopez AS, Zambrano CH, Sufit RL, Sakolvaree Y, Chaicumpa W, Herwaldt BL, Johnson S (2002) An outbreak of eosinophilic meningitis caused by Angiostrongylus cantonensis in travelers returning from the Caribbean. N Engl J Med 346:668–675

    Article  PubMed  Google Scholar 

  • State Environmental Protection Administration of China and Chinese Academy of Sciences (2003) Circular on publishing the list of the first batch of alien invasive species in China. (Issue 23)

  • Tsai TH, Liu YC, Wann SR, Lin WR, Lee SJ, Lin HH, Chen YS, Yen MY, Yen CM (2001) An outbreak of meningitis caused by Angiostrongylus cantonensis in Kaohsiung. J Microbiol Immunol Infect 34:50–56

    PubMed  CAS  Google Scholar 

  • Tsai HC, Liu YC, Kunin CM, Lai PH, Lee SS, Chen YS, Wann SR, Lin WR, Huang CK, Ger LP, Lin HH, Yen MY (2003) Eosinophilic meningitis caused by Angiostrongylus cantonensis associated with eating raw snails. Am J Trop Med Hyg 68:281–285

    PubMed  Google Scholar 

  • Tsai HC, Lee SS, Huang CK, Yen CM, Chen ER, Liu YC (2004) Outbreak of eosinophilic meningitis associated with drinking raw vegetable juice in southern Taiwan. Am J Trop Med Hyg 71:222–226

    PubMed  Google Scholar 

  • Tsoularis A, Wallace J (2002) Analysis of logistic growth models. Math Biosci 179:21–55

    Article  PubMed  CAS  Google Scholar 

  • Xing WL, Pan CW, Liang SH, Lin HB, Huang HC, Yi WP, Lin BC, Wang KH, Lin DX, Zhou ZL (1998) Distribution of Angiostrongylus cantonensis larvae in Pomacea canaliculata in Wenzhou City. J Wenzhou Med Coll 28:297–298 (in Chinese)

    Google Scholar 

  • Xue DY, Ruan YZ, Lin BC, Zheng RY, Fang JQ, Zhao QX, Li MF, Pan CW (2000) Epidemiological investigation on an outbreak of angiostrongyliasis cantonensis in Wenzhou. Chin J Parasitol Parasitic Dis 18:176–178

    CAS  Google Scholar 

  • Yang S, Logan J, Coffey DL (1995) Mathematical formulae for calculating the base temperature for growing degree days. Agric Meteorol 74:61–74

    Article  Google Scholar 

  • Yousif F, Lammler G (1975) The suitability of several aquatic snails as intermediate hosts for Angiostrongylus cantonensis. Z Parasitenkd 47:203–210

    Article  PubMed  CAS  Google Scholar 

  • Zhou WC, Wu YF, Yang JQ (2003) Viability of the Ampullaria snail in China. Fujian J Agric Sci 18:25–28

    Google Scholar 

Download references

Acknowledgements

This work received financial support from the Ministry of Science and Technology, China (Grant No. 2003BA712A09-01). We thank Dr. Jin-Xiang Lin, Li-Sha Li, and their coworkers from Fujiang Center for Disease Control and Prevention for the snails and the A. cantonensis larvae.

The execution of the experiments described in this article complied with all applicable laws of the People’s Republic of China.

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Correspondence to Xiao-Nong Zhou.

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Lv, S., Zhou, XN., Zhang, Y. et al. The effect of temperature on the development of Angiostrongylus cantonensis (Chen 1935) in Pomacea canaliculata (Lamarck 1822). Parasitol Res 99, 583–587 (2006). https://doi.org/10.1007/s00436-006-0198-8

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  • DOI: https://doi.org/10.1007/s00436-006-0198-8

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