Skip to main content

Advertisement

Log in

Seasonal pattern of avian Plasmodium-infected mosquitoes and implications for parasite transmission in central Panama

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

Abstract

Aedeomyia squamipennis and Culex (Melanoconion) ocossa, two ubiquitous Neotropical mosquito species, are likely involved in the transmission of several bird pathogens in Gamboa, central Panama. However, knowledge on their eco-epidemiological profiles is still incomplete. Our goal in this study was to investigate temporal trends of vector density and their relationship with avian plasmodia prevalence. This information is central to identifying the risk posed by each vector species to the avian community locally. We found that A. squamipennis maintains stable population size across climatic seasons and thus maybe a more efficient vector of avian malaria than C. ocossa. In contrast, C. ocossa, which undergoes considerable population expansion in the rainy season and contraction in the dry season, is likely only an important avian malaria vector during part of the year. This is consistent with the larger number of parasite isolations and Plasmodium cyt b lineages recovered from A. squamipennis than from C. ocossa and might be explained by marked differences in their seasonality and host-feeding preferences. More Plasmodium PCR testing in mosquito communities from other areas of Panama might reveal additional vectors of avian plasmodia.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aguila Y (1987) Efecto inmediato de dos herbicidas sobre las larvas de Mansonia y Coquillettidia (Diptera: Culicidae) al ser aplicados a cinco malezas acuáticas. Tesis de maestría. Universidad de Panamá. 64 páginas

  • Bonneaud C, Sepil I, Milá B, Buermann W, Pollinger J, Sehgal RNM, Valkiūnas G, Iezhova TA, Saatchi S, Smith TB (2009) The prevalence of avian Plasmodium is higher in undisturbed tropical forests of Cameroon. J Trop Ecol 25:439–447

    Article  Google Scholar 

  • Braga EM, Silveira P, Belo NO, Valkiūnas G (2011) Recent advances in the study of avian malaria: an overview with an emphasis on the distribution of Plasmodium spp. in Brazil. Mem Inst Oswaldo Cruz 106:3–1

    PubMed  Google Scholar 

  • Bustamante DM, Lord CC (2010) Sources of error in the estimation of mosquito infection rates used to assess risk of Arbovirus transmission. Am J Trop Med Hyg 82:1172–1184

    Article  PubMed  Google Scholar 

  • Calisher CH, John SL, Gustavo J, Thomas PM, Ernesto GV, Marta SS, Werner LJ (1981) Viruses isolated from Aedeomyia squamipennis mosquitoes collected in Panama, Ecuador and Argentina establishment of the Gamboa serogroup. Am J Trop Med Hyg 30:219–223

    PubMed  CAS  Google Scholar 

  • Carlson J, Martinez J, Cornel AJ, Loiseau C, Sehgal RNM (2011) Implications of Plasmodium parasite infected mosquitoes on an insular avifauna: the case of Socorro Island, Mexico. J Vector Ecol 36:213–220

    Article  PubMed  Google Scholar 

  • Christensen HA, De Vasquez AM, Boreham MM (1996) Host-feeding patterns of mosquitoes (Diptera: Culicidae) from Central Panama. Am J Trop Med Hyg 55:202–208

    PubMed  CAS  Google Scholar 

  • Dutary BE, Petersen JL, Peralta PH, Tesh RB (1989) Transovarial transmission mosquito, Aedeomyia squamipennis. Am J Trop Med Hyg 40:108–113

    PubMed  CAS  Google Scholar 

  • Ejiri H, Sato Y, Sawai R, Sasaki E, Matsumoto R, Ueda M, Higa Y, Tsuda Y, Omori S, Murata K, Yukawa M (2009) Prevalence of avian malaria parasite in mosquitoes collected at a zoological garden in Japan. Parasitol Res 105:629–633

    Article  PubMed  Google Scholar 

  • Franklin DC, Whelan PI (2009) Tropical mosquito assemblages demonstrate ‘textbook’ annual cycles. PLoS ONE 12:e8296

    Article  Google Scholar 

  • Gabaldon A, Ulloa G (1980) Holoendemicity of malaria: an avian model. Trans R Soc Trop Med Hyg 74:501–507

    Article  PubMed  CAS  Google Scholar 

  • Gabaldon A, Ulloa G, Godoy N, Marquez E, Pulido J (1977a) Aedeomyia squamipennis (Diptera: Culicidae) vector natural de malaria aviaria en Venezuela. Bol Dir Malariol San Amb 17:9–13

    Google Scholar 

  • Gabaldon A, Ulloa G, Pulido J, Sutil E (1977b) Especies de la Familia Culicidae que presentan ornitofilia en Venezuela. Bol Dir Malariol San Amb 17:3–8

    Google Scholar 

  • Gabaldon A, Ulloa G, Pulido J (1981) Distribución geográfica, ecología y etología de Aedeomyia squamipennis, importante vector natural de malaria aviaria en Venezuela. Bol Dir Malariol San Amb 21:103–113

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Galardo AK, Arruda M, D’Almeida CAA, Wirtz R, Lounibos LP, Zimmerman RH (2007) Malaria vector incrimination in three rural riverine villages in the Brazilian Amazon. Am J Trop Med Hyg 76:461–469

    PubMed  Google Scholar 

  • Galindo P (1972) Endemic vectors of Venezuelan encephalitis. PAHO Sc Public 243:249–253

    Google Scholar 

  • Galindo P, Adames AJ (1972) Colonization of Culex Melanoconion aikenii (Aiken & Rowland, 1906) in Panama. Mosq News 32:196–200

    Google Scholar 

  • Galindo P, Adames AJ (1973) Ecological profile of Culex (Melanoconion) aikenii (Diptera: Culicidae), vector of endemic Venezuelan encephalitis in Panama. Environ Entomol 2:81–86

    Google Scholar 

  • Galindo P, Grayson MA (1971) Culex (Melanoconion) aikenii: natural vector in Panama of endemic Venezuelan encephalitis. Science 172:594–595

    Article  PubMed  CAS  Google Scholar 

  • Galindo P, Adames AJ, Peralta PH, Johnson CM, Read R (1983) Impacto de la hidroeléctrica de Bayano en la transmisión de arbovirus. Rev Med Panama 8:89–134

    PubMed  CAS  Google Scholar 

  • Glaizot O, Fumagalli L, Iritano K, Lalubin F, Van Rooyen J, Christe P (2012) High prevalence and lineage diversity of avian malaria in wild populations of Great Tits (Parus major) and mosquitoes (Culex pipiens). PLoS ONE 7(4):e34964

    Article  PubMed  CAS  Google Scholar 

  • Heinemann SJ, Belkin JN (1978) Collection records of the project “Mosquitoes of Middle America”. Panama, including the Canal Zone. Mosq Syst 10:119–196

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ishtiaq F, Clegg SM, Philimore AB, Black RA, Owens IPF, Sheldon BC (2010) Biogeographical patterns of blood parasite lineage diversity in avian hosts from southern Melanesian islands. J Biogeogr 37:120–132

    Article  Google Scholar 

  • Jones JW, Turell MJ, Sardelis MR, Watts DM, Coleman RE, Fernandez R, Carbajal F, Pecor JE, Calampa C, Klein TA (2004) Seasonal distribution, biology, and human attraction patterns of culicine mosquitoes (Diptera: Culicidae) in a forest near Puerto Almendras, Iquitos, Peru. J Med Entomol 41:349–360

    Article  PubMed  Google Scholar 

  • Kim KS, Tsuda Y (2010) Seasonal changes in the feeding pattern of Culex pipiens pallens govern the transmission dynamics of multiple lineages of avian malaria parasites in Japanese wild bird community. Mol Ecol 19:5545–5554

    Article  PubMed  CAS  Google Scholar 

  • Kim KS, Tsuda Y, Sasaki T, Kobayashi M, Hirota Y (2009) 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

    Article  PubMed  Google Scholar 

  • Kimura M, Darbro JM, Harrington LC (2010) Avian malaria parasites share congeneric mosquito vectors. J Parasitol 96:144–151

    Article  PubMed  CAS  Google Scholar 

  • Levine ND (1988) The protozoan phylum Apicomplexa. CRC, Boca Raton

    Google Scholar 

  • Lourenço-de-Oliveira R, De Castro FA (1991) Culex saltanensis Dyar, 1928: natural vector of Plasmodium juxtanucleare in Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 86:87–94

    Article  PubMed  Google Scholar 

  • Loiseau C, Iezhova TA, Valkiūnas G, Chasar A, Hutchinson A, Buermann W, Smith T, Sehgal RN (2010) Spatial variation of haemosporidian parasite infection in African rainforest bird species. J Parasitol 96:21–29

    Article  PubMed  Google Scholar 

  • Lopez J, Lozovei AL (1995) Ecologia do mosquito (Díptera: Culicidae) em criadouros naturais e artificiais de áreas rural do Norte do Estado do Paraná, Brasil, I – coleta ao longo do leito de Ribeirão. Rev Saúde Publica 29:183–197

    Google Scholar 

  • Njabo KY, Cornel AJ, Sehgal RNM, Loiseau C, Buermann W, Harrigan RJ, Pollinger J, Valkiūnas G, Smith TB (2010) Coquillettidia (Culicidae: Diptera) mosquitoes are natural vectors of avian malaria in Africa. Mal J 8:193

    Article  Google Scholar 

  • Njabo KY, Cornel AJ, Bonneaud C, Toffelmier E, Sehgal RNM, Valkiūnas G, Russell AF, Smith TB (2011) Nonspecific patterns of vector, host and avian malaria parasite associations in a central African rainforest. Mol Ecol 20:1049–1061

    Article  PubMed  CAS  Google Scholar 

  • Pecor JE, Mallampalli VL, Harbach RE, Peyton EL (1992) Catalog and illustrated review of the subgenus Melanoconion of Culex. Contr Entomol Inst 27:1–228

    Google Scholar 

  • Read RG, Adames AJ (1980) Atmospheric stimulation of man-biting activity in tropical insects. Environ Entomol 9:677–680

    Google Scholar 

  • Santiago-Alarcon D, Havelka P, Schaefer HM, Segelbacher G (2012) Bloodmeal analysis reveals avian Plasmodium infections and broad host preferences of Culicoides (Diptera: Ceratopogonidae) vectors. PLoS ONE 7(2):e31098

    Article  PubMed  CAS  Google Scholar 

  • Sehgal RNM (2010) Deforestation and avian infectious diseases. J Exp Biol 213:955–960

    Article  PubMed  CAS  Google Scholar 

  • Service M (2008) Medical entomology for students. Cambridge University Press, Cambridge, p 289

    Google Scholar 

  • Synek P, Munclinger P, Albrecht T, Votypka J (2012) Avian haemosporidians in haematophagous insects in the Czech Republic. Paraitol Res. doi:10.1007/s00436-012-3204-3

    Google Scholar 

  • Tempelis CH, Galindo P (1975) Host-feeding patterns of Culex (Melanoconion) and Culex (Aedinus) mosquitoes collected in Panama. J Med Entomol 12:205–209

    PubMed  CAS  Google Scholar 

  • Turell MJ, Barth J, Coleman RE (1999) Potential for Central American mosquitoes to transmit epizootic and enzootic of Venezuelan equine encephalitis virus. J Am Mosq Control Assoc 15:295–298

    PubMed  CAS  Google Scholar 

  • Valkiūnas G (2005) Avian malaria parasites and other haemosporidia. CRC Press, Boca Raton

    Google Scholar 

  • Wolda H, Galindo P (1981) Population fluctuations of mosquitoes in the non-seasonal tropics. Ecol E 6:99–106

    Article  Google Scholar 

Download references

Acknowledgments

We thank Andrea Gager, formerly from Princeton University, for the opportunity to collaborate on her Ph.D. thesis project; Eldredge Bermingham; and Oris I. Sanjur from the Smithsonian Tropical Research Institute (STRI) for logistical support and academic guidance. We acknowledge the help of Sara Veronica Pinzon, Jose R. Rovira, and Jorge Morales in collecting mosquito larvae in Gamboa. Additionally, we thank James Pecor from the Walter Reed Biosystematics Units (WRBU), U.S.A., and Luis Guillermo Chaverry from the National Institute of Biodiversity of Costa Rica (INBio) for assisting with species identification in the subgenus Melanoconion of Culex. Milton Solano produced the map on Fig. 1, Eyda Gomez offered logistic support throughout the study, and Marilyn Scott, from McGill University, critically commented on an earlier version of this work. Funding was provided by INDICASAT AIP, STRI, and the National Secretariat for Science, Technology, and Innovation of Panama (SENACYT)–Research Investigator Award (SNI) granted to JRL.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jose R. Loaiza.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Loaiza, J.R., Miller, M.J. Seasonal pattern of avian Plasmodium-infected mosquitoes and implications for parasite transmission in central Panama. Parasitol Res 112, 3743–3751 (2013). https://doi.org/10.1007/s00436-013-3562-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-013-3562-5

Keywords

Navigation