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Overlap in the Seasonal Infection Patterns of Avian Malaria Parasites and West Nile Virus in Vectors and Hosts
Matthew C. I. Medeiros
Matthew C. I. Medeiros
Department of Entomology, Texas A&M University, College Station, Texas.
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Robert E. Ricklefs
Robert E. Ricklefs
Department of Biology, University of Missouri–St. Louis, St. Louis, Missouri.
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Jeffrey D. Brawn
Jeffrey D. Brawn
Department of Natural Resources and Environmental Sciences, University of Illinois, Urbana, Illinois.
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Marilyn O. Ruiz
Marilyn O. Ruiz
Department of Pathobiology, University of Illinois, Urbana, Illinois.
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Tony L. Goldberg
Tony L. Goldberg
Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, Wisconsin.
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Gabriel L. Hamer
Gabriel L. Hamer
Department of Entomology, Texas A&M University, College Station, Texas.
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Multiple vector-borne pathogens often circulate in the same vector and host communities, and seasonal infection dynamics influence the potential for pathogen interactions. Here, we explore the seasonal infection patterns of avian malaria (Haemosporida) parasites (Plasmodium and Haemoproteus) and West Nile virus (WNV) in birds and mosquitoes in suburban Chicago. We show that both pathogens vary seasonally in Culex mosquitoes and avian hosts, but that patterns of covariation are complex. Different putative Plasmodium species varied asynchronously across the season in mosquitoes and birds, suggesting that different forces may govern their transmission. Infections of Culex mosquitoes with Plasmodium parasites were positively associated with WNV infections in pools of individuals aggregated from the same time and site, suggesting that these pathogens respond to common environmental drivers and co-circulate among the same host and vector populations. Future research should focus on these common drivers, and whether these pathogens interact in vectors and hosts.
Author Notes
Financial support: This study was supported by the National Science Foundation grants EF-0429124 and EF-0840403 (awarded to Uriel Kitron, Tony Goldberg, Jeffrey Brawn, Marilyn Ruiz, and Edward Walker), the Whitney Harris World Ecology Center, and the St. Louis Audubon Society.
Authors' addresses: Matthew C. I. Medeiros and Gabriel L. Hamer, Department of Entomology, Texas A&M University, College Station, TX, E-mails: matthewcimedeiros@tamu.edu and ghamer@tamu.edu. Robert E. Ricklefs, Department of Biology, University of Missouri–St. Louis, St. Louis, MO, E-mail: ricklefs@umsl.edu. Jeffrey D. Brawn, Department of Natural Resources and Environmental Sciences, University of Illinois, Urbana, IL, E-mail: jbrawn@illinois.edu. Marilyn O. Ruiz, Department of Pathobiology, University of Illinois, Urbana, IL, E-mail: moruiz@illinois.edu. Tony L. Goldberg, Department of Pathobiological Sciences, University of Wisconsin, Madison, WI, E-mail: tgoldberg@vetmed.wisc.edu.
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-
1.
Altizer S, Dobson A, Hosseini P, Hudson P, Pascual M, Rohani P, 2006. Seasonality and the dynamics of infectious diseases. Ecol Lett 9: 467–484.
-
2.
Focks DA, Daniels E, Haile DG, Keesling JE, 1995. A simulation model of the epidemiology of urban dengue fever: literature analysis, model development, preliminary validation, and samples of simulation results. Am J Trop Med Hyg 53: 489–506.
-
3.
Ruiz MO, Chaves LF, Hamer GL, Sun T, Brown WM, Walker ED, Haramis L, Goldberg TL, Kitron UD, 2010. Local impact of temperature and precipitation on West Nile virus infection in Culex species mosquitoes in northeast Illinois, USA. Parasit Vectors 3: 19.
-
4.
Tempelis CH, Washino RK, 1967. Host-feeding patterns of Culex tarsalis in the Sacramento Valley, California, with notes on other species. J Med Entomol 4: 315–318.
-
5.
Tempelis CH, Reeves WC, Bellamy RE, Lofy MF, 1965. A 3-year study of feeding habits of Culex tarsalis in Kern County, California. Am J Trop Med Hyg 14: 170.
-
6.
Tempelis CH, 1975. Host-feeding patterns of mosquitos, with a review of advances in analysis of blood meals by serology. J Med Entomol 11: 635–653.
-
7.
Hamer GL, Kitron UD, Goldberg TL, Brawn JD, Loss SR, Ruiz MO, Hayes DB, Walker ED, 2009. Host selection by Culex pipiens mosquitoes and West Nile virus amplification. Am J Trop Med Hyg 80: 268–278.
-
8.
Kilpatrick AM, Daszak P, Jones MJ, Marra PP, Kramer LD, 2006. Host heterogeneity dominates West Nile virus transmission. Proc Biol Sci 273: 2327–2333.
-
9.
Tempelis CH, Francy DB, Hayes RO, Lofy MF, 1967. Variations in feeding patterns of seven culine mosquitoes on vertebrate hosts in Weld and Larimer Counties, Colorado. Am J Trop Med Hyg 16: 111.
-
10.
Burkett-Cadena ND, Hassan HK, Eubanks MD, Cupp EW, Unnasch TR, 2012. Winter severity predicts the timing of host shifts in the mosquito Culex erraticus. Biol Lett 8: 567–569.
-
11.
Kilpatrick AM, Kramer LD, Jones MJ, Marra PP, Daszak P, 2006. West Nile virus epidemics in North America are driven by shifts in mosquito feeding behavior. PLoS Biol 4: 606–610.
-
12.
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.
-
13.
Reisen WK, Cayan D, Tyree M, Barker CA, Eldridge B, Dettinger M, 2008. Impact of climate variation on mosquito abundance in California. J Vector Ecol 33: 89–98.
-
14.
Eisen L, Bolling BG, Blair CD, Beaty BJ, Moore CG, 2008. Mosquito species richness, composition, and abundance along habitat-climate-elevation gradients in the northern Colorado front range. J Med Entomol 45: 800–811.
-
15.
Allander K, 1997. Reproductive investment and parasite susceptibility in the great tit. Funct Ecol 11: 358–364.
-
16.
Nordling D, Andersson M, Zohari S, Gustafsson L, 1998. Reproductive effort reduces specific immune response and parasite resistance. Proc Biol Sci 265: 1291–1298.
-
17.
Hamer GL, Walker ED, Brawn JD, Loss SR, Ruiz MO, Goldberg TL, Schotthoefer AM, Brown WM, Wheeler E, Kitron UD, 2008. Rapid amplification of West Nile virus: the role of hatch-year birds. Vector Borne Zoonotic Dis 8: 57–67.
-
18.
Janousek WM, Marra PP, Kilpatrick AM, 2014. Avian roosting behavior influences vector-host interactions for West Nile virus hosts. Parasit Vectors 7: 399.
-
19.
Krebs BL, Anderson TK, Goldberg TL, Hamer GL, Kitron UD, Newman CM, Ruiz MO, Walker ED, Brawn JD, 2014. Host group formation decreases exposure to vector-borne disease: a field experiment in a ‘hotspot’ of West Nile virus transmission. Proc Biol Sci 281: 20141586.
-
20.
Cox FEG, 2001. Concomitant infections, parasites and immune responses. Parasitology 122: S23–S38.
-
21.
Kenney JL, Brault AC, 2014. The role of environmental, virological and vector interactions in dictating biological transmission of arthropod-borne viruses by mosquitoes. Adv Virus Res 89: 39–83.
-
22.
Ezenwa VO, Etienne RS, Luikart G, Beja-Pereira A, Jolles AE, 2010. Hidden consequences of living in a wormy world: nematode-induced immune suppression facilitates tuberculosis invasion in African Buffalo. Am Nat 176: 613–624.
-
23.
Johnson PTJ, Hoverman JT, 2012. Parasite diversity and coinfection determine pathogen infection success and host fitness. Proc Natl Acad Sci USA 109: 9006–9011.
-
24.
Vaughan JA, Turell MJ, 1996. Dual host infections: enhanced infectivity of eastern equine encephalitis virus to Aedes mosquitoes mediated by Brugia microfilariae. Am J Trop Med Hyg 54: 105–109.
-
25.
Vaughan JA, Turell MJ, 1996. Facilitation of Rift Valley fever virus transmission by Plasmodium berghei sporozoites in Anopheles stephensi mosquitoes. Am J Trop Med Hyg 55: 407–409.
-
26.
Valkiunas G, 2005. Avian Malaria Parasites and Other Haemosporidia. Boca Raton, FL: CDC Press.
-
27.
Ellis VA, Cornet S, Merrill L, Kunkel MR, Tsunekage T, Ricklefs RE, 2015. Host immune responses to experimental infection of Plasmodium relictum (lineage SGS1) in domestic canaries (Serinus canaria). Parasitol Res 114: 3627–3636.
-
28.
Applegate JE, Beaudoin RL, 1970. Mechanism of spring relapse in avian malaria: effect of gonadotropin and corticosterone. J Wildl Dis 6: 443–447.
-
29.
Cosgrove CL, Wood MJ, Day KP, Sheldon BC, 2008. Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. J Anim Ecol 77: 540–548.
-
30.
Beaudoin RL, Applegate JE, Davis DE, McLean RG, 1971. A model for the ecology of avian malaria. J Wildl Dis 7: 5–13.
-
31.
Lanciotti RS, Roehrig JT, Deubel V, Smith J, Parker M, Steele K, Crise B, Volpe KE, Crabtree MB, Scherret JH, Hall RA, MacKenzie JS, Cropp CB, Panigrahy B, Ostlund E, Schmitt B, Malkinson M, Banet C, Weissman J, Komar N, Savage HM, Stone W, McNamara T, Gubler DJ, 1999. Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States. Science 286: 2333–2337.
-
32.
Murray KO, Mertens E, Despres P, 2010. West Nile virus and its emergence in the United States of America. Vet Res 41: 67.
-
33.
LaDeau SL, Kilpatrick AM, Marra PP, 2007. West Nile virus emergence and large-scale declines of North American bird populations. Nature 447: 710–713.
-
34.
Wimberly MC, Giacomo P, Kightlinger L, Hildreth MB, 2013. Spatio-temporal epidemiology of human West Nile virus disease in South Dakota. Int J Environ Res Public Health 10: 5584–5602.
-
35.
Hahn MB, Monaghan AJ, Hayden MH, Eisen RJ, Delorey MJ, Lindsey NP, Nasci RS, Fischer M, 2015. Meteorological conditions associated with increased incidence of West Nile virus disease in the United States, 2004–2012. Am J Trop Med Hyg 92: 1013–1022.
-
36.
Medeiros MCI, Anderson TK, Higashiguchi JM, Kitron UD, Walker ED, Brawn JD, Krebs BL, Ruiz MO, Goldberg TL, Ricklefs RE, Hamer GL, 2014. An inverse association between West Nile virus serostatus and avian malaria infection status. Parasit Vectors 7: 415.
-
37.
Boothe E, Medeiros MCI, Kitron UD, Brawn JD, Ruiz MO, Goldberg TL, Walker ED, Hamer GL, 2015. Identification of avian and hemoparasite DNA in blood-engorged abdomens of Culex pipiens (Diptera; Culicidae) from a West Nile virus epidemic region in suburban Chicago, Illinois. J Med Entomol 52: 461–468.
-
38.
Harrington LC, Poulson RL, 2008. Considerations for accurate identification of adult Culex restuans (Diptera: Culicidae) in field studies. J Med Entomol 45: 1–8.
-
39.
Fallon SM, Ricklefs RE, Swanson BL, Bermingham E, 2003. Detecting avian malaria: an improved polymerase chain reaction diagnostic. J Parasitol 89: 1044–1047.
-
40.
Fecchio A, Lima MR, Svensson-Coelho M, Marini MA, Ricklefs RE, 2013. Structure and organization of an avian haemosporidian assemblage in a neotropical savanna in Brazil. Parasitology 140: 181–192.
-
41.
Outlaw DC, Ricklefs RE, 2014. Species limits in avian malaria parasites (Haemosporida): how to move forward in the molecular era. Parasitology 141: 1223–1232.
-
42.
Svensson-Coelho M, Blake JG, Loiselle BA, Penrose AS, Parker PG, Ricklefs RE, 2013. Diversity, prevalence, and host specificity of avian Plasmodium and Haemoproteus in a western Amazon assemblage. Ornithol Monogr 76: 1–47.
-
43.
Medeiros MCI, Hamer GL, Ricklefs RE, 2013. Host compatibility rather than vector-host-encounter rate determines the host range of avian Plasmodium parasites. Proc Biol Sci 280: 20122947.
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