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Mosquito blood-meal analysis for avian malaria study in wild bird communities: laboratory verification and application to Culex sasai (Diptera: Culicidae) collected in Tokyo, Japan

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Abstract

We conducted laboratory experiments to verify molecular techniques of avian malaria parasite detection distinguishing between an infected mosquito (oocysts on midgut wall) and infective mosquito (sporozoites in salivary glands) in parallel with blood-meal identification from individual blood-fed mosquitoes prior to application to field survey for avian malaria. Domestic fowl infected with Plasmodium gallinaceum was exposed to a vector and non-vector mosquito species, Aedes aegypti and Culex pipiens pallens, respectively, to compare the time course of polymerase chain reaction (PCR) detection for parasite between competent and refractory mosquitoes. DNA of the domestic fowl was detectable for at least 3 days after blood feeding. The PCR-based detection of P. gallinaceum from the abdomen and thorax of A. aegypti corresponded to the microscopic observation of oocysts and sporozoites. Therefore, this PCR-based method was considered useful as one of the criteria to assess developmental stages of Plasmodium spp. in mosquito species collected in the field. We applied the same PCR-based method to 21 blood-fed C. sasai mosquitoes collected in Rinshi-no-mori Park in urban Tokyo, Japan. Of 15 blood meals of C. sasai successfully identified, 86.7% were avian-derived, 13.3% were bovine-derived. Plasmodium DNA was amplified from the abdomen of three C. sasai specimens having an avian blood meal from the Great Tit (Parus major), Pale Thrush (Turdus pallidus), and Jungle Crow (Corvus macrorhynchos). This is the first field study on host-feeding habits of C. sasai in relation to the potential role as a vector for avian malaria parasites transmitted in the Japanese wild bird community.

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References

  • Apperson CS, Hassan HK, Harrison BA, Savage HM, Aspen SE, Farajollahi A, Crans W, Daniels TJ, Falco RC, Benedict M, Anderson M, McMillen L, Unnasch TR (2004) Host feeding patterns of established and potential mosquito vectors of West Nile Virus in the eastern United States. Vector Borne Zoonotic Dis 4:71–82

    Article  PubMed  Google Scholar 

  • Bak UB, Park JC, Lim YJ (1984) An outbreak of malaria in penguins at the Farm-land Zoo. Korean J Parasitol 22:267–272

    Article  Google Scholar 

  • Ejiri H, Sato Y, Sasaki E, Sumiyama D, Tsuda Y, Sawabe K, Matsuo S, Horie S, Akatani K, Takagi M, Omori S, Yukawa M, Murata K (2008) Detection of avian Plasmodium spp. DNA sequences from mosquitoes captured in Minami Daito Island of Japan. J Vet Med Sci 70:1205–1210

    Article  CAS  PubMed  Google Scholar 

  • Fabian MM, Toma H, Arakawa T, Sato Y (2004) Malaria parasite developmental analyses by the nested polymerase chain reaction method: an implication for the evaluation of mosquito infection rates in epidemiological studies. Southeast Asian J Trop Med Public Health 35:820–827

    CAS  PubMed  Google Scholar 

  • Fallon SM, Bermingham E, Ricklefts RE (2005) Host specialization and geographic localization of avian parasites: a regional analysis in the lesser Antilles. Am Nat 165:466–480

    Article  PubMed  Google Scholar 

  • Gager AB, Loaiza RJD, Dearbon DC, Bermingham E (2008) Do mosquitoes filter the access of Plasmodium cytochrome b lineages to an avian host? Mol Ecol 17:2552–2561

    Article  CAS  PubMed  Google Scholar 

  • Grim KC, Van der Merwe E, Sullivan M, Parsons N, McCutchan TF, Cranfield M (2003) Plasmodium juxtanucleare associated with mortality in Black-Footed Penguins (Spheniscus demersus) admitted to a rehabilitation center. J Zoo Wildl Med 34:250–255

    PubMed  Google Scholar 

  • Hamer GL, Kitron UD, Brawn JD, Loss SR, Ruiz MO, Goldberg TL, Walker ED (2008) Culex pipiens (Diptera: Culicidae) a bridge vector of West Nile virus to humans. J Med Entomol 45:125–128

    Article  PubMed  Google Scholar 

  • Hassan HK, Cupp EW, Hill GE, Katholi CR, Klingler KY, Unnasch TR (2003) Avian host preference by vectors of eastern equine encephalomyelitis virus. Am J Trop Med Hyg 69:641–647

    PubMed  Google Scholar 

  • Huff CG (1965) Susceptibility of mosquitoes to avian malaria. Exp Parasitol 16:107–132

    Article  CAS  PubMed  Google Scholar 

  • Huijben S, Schaftenaar W, Wijsman A, Paaijmans K, Takken W (2007) Avian malaria in Europe: an emerging infectious disease? In: Takken W, Knols BGJ (eds) Emerging pests and vector-borne diseases in Europe. Wageningen Academic Publisher, Wageningen, pp 59–74

    Google Scholar 

  • Ishtiaq F, Guillaumot L, Clegg SM, Phillimore AB, Black RA, Owens IPF, Mundy NI, Sheldon BC (2008) Avian haematozoan parasites and their associations with mosquitoes across Southwest Pacific Islands. Mol Ecol 17:4545–4555

    Article  CAS  PubMed  Google Scholar 

  • Kano R, Kimura M (1950) Studies on bird malaria (4). Natural infection of blood parasites in Japanese wild birds. Jpn J Bact 5:103–105

    Google Scholar 

  • Kent RJ, Norris DE (2005) Identification of mammalian blood meals in mosquitoes by a multiplexed polymerase chain reaction targeting cytochrome B. Am J Trop Med Hyg 73:336–342

    CAS  PubMed  Google Scholar 

  • Kim KS, Tsuda Y, Yamada A (2009) Blood-meal identification and detection of avian malaria parasite from mosquitoes (Diptera: Culicidae) inhabiting coastal areas Tokyo Bay, Japan. J Med Entomol (in press)

  • Massey B, Gleeson DM, Slaney D, Tompkins DM (2007) PCR detection of Plasmodium and blood meal identification in a native New Zealand mosquito. J Vector Ecol 32:154–156

    Article  CAS  PubMed  Google Scholar 

  • Molaei G, Andreadis TG, Armstrong PM, Anderson JF, Vossbrinck CR (2006) Host feeding patterns of Culex mosquitoes and West Nile Virus transmission, northeastern United States. Emerg Infect Dis 12:468–474

    PubMed  Google Scholar 

  • Murata K (2002) Prevalence of blood parasites in Japanese wild birds. J Vet Med Sci 64:785–790

    Article  PubMed  Google Scholar 

  • Murata K, Nii R, Sasaki E, Ishikawa S, Sato Y, Sawabe K, Tsuda Y, Matsumoto R, Suda A, Ueda M (2008) Plasmodium (Bennettinia) juxtanucleare infection in a captive white eared-pheasant (Crossoptilon crossoptilon) at a Japanese Zoo. J Vet Med Sci 70:203–205

    Article  PubMed  Google Scholar 

  • Ngo KA, Kramer LD (2003) Identification of mosquito bloodmeals using polymerase chain reaction (PCR) with order-specific primers. J Med Entomol 40:215–222

    Article  CAS  PubMed  Google Scholar 

  • Schneider D, Shahabuddin M (2000) Malaria parasite development in a Drosophila model. Science 288:2376–2379

    Article  CAS  PubMed  Google Scholar 

  • Stoffels JAW, Docters van Leeuwen WM, Post RJ (1995) Detection of Plasmodium sporozoites in mosquitoes by polymerase chain reaction and oligonucleotide rDNA probe, without dissection of the salivary glands. Med Vet Entomol 9:433–437

    Article  CAS  PubMed  Google Scholar 

  • Tanaka K, Mizusawa K, Saugstad E (1979) A revision of the adult and larval mosquitoes of Japan (including the Ryukyu Archipelago and the Ogasawara islands) and Korea (Diptera: Culicidae). Contrib Am Entomol Inst 16:1–987

    Google Scholar 

  • Tsuda Y, Kim KS (2008) Sudden autumnal appearance of adult Culex tritaeniorhynchus Giles (Diptera: Culicidae) at a park in urban Tokyo—first field evidence for pre-diapause migration. J Med Entomol 45(4):610–616

    Article  PubMed  Google Scholar 

  • Valkiūnas G (2005) Avian malaria parasites and other haemosporidia. CRC press, New York

    Google Scholar 

  • Waldenström J, Bensch S, Kiboi S, Hasselquist D, Ottosson U (2002) Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Mol Ecol 11:1545–1554

    Article  PubMed  Google Scholar 

  • Waldenström J, Bensch S, Hasselquist D, Östman Ö (2004) A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. J Parasitol 90:191–194

    Article  PubMed  Google Scholar 

  • Weathersby AB (1962) Susceptibility of certain Japanese mosquitoes to Plasmodium gallinaceum and Plasmodium berghei. J Parasitol 48:607–609

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Kyoko Sawabe, Haruhiko Isawa, Shinji Kasai, Keita Hoshino, and Osamu Komagata of the Department of Medical Entomology, National Institute of Infectious Diseases for their help with molecular laboratory work. Thanks are also due to Koichi Murata and Yukita Sato of Nihon University for their encouragement during the study. This work was partly supported by a Grant-in-Aid for Scientific Research of Emerging and Reemerging Infectious Diseases from the Ministry of Health, Labor, and Welfare of the Japanese Government (H18-Shinko-009).

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Correspondence to Kyeong Soon Kim.

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Kim, K.S., Tsuda, Y., Sasaki, T. et al. Mosquito blood-meal analysis for avian malaria study in wild bird communities: laboratory verification and application to Culex sasai (Diptera: Culicidae) collected in Tokyo, Japan. Parasitol Res 105, 1351–1357 (2009). https://doi.org/10.1007/s00436-009-1568-9

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