{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,12]],"date-time":"2026-09-12T12:03:39Z","timestamp":1789214619576,"version":"build-2803163510"},"reference-count":69,"publisher":"American Society of Tropical Medicine and Hygiene","issue":"5","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2016,11,2]]},"abstract":"<jats:p>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 (<jats:italic>Plasmodium<\/jats:italic> and <jats:italic>Haemoproteus<\/jats:italic>) and West Nile virus (WNV) in birds and mosquitoes in suburban Chicago. We show that both pathogens vary seasonally in <jats:italic>Culex<\/jats:italic> mosquitoes and avian hosts, but that patterns of covariation are complex. Different putative <jats:italic>Plasmodium<\/jats:italic> species varied asynchronously across the season in mosquitoes and birds, suggesting that different forces may govern their transmission. Infections of <jats:italic>Culex<\/jats:italic> mosquitoes with <jats:italic>Plasmodium<\/jats:italic> 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.<\/jats:p>","DOI":"10.4269\/ajtmh.16-0236","type":"journal-article","created":{"date-parts":[[2016,9,13]],"date-time":"2016-09-13T02:38:53Z","timestamp":1473734333000},"page":"1121-1129","source":"Crossref","is-referenced-by-count":17,"title":["Overlap in the Seasonal Infection Patterns of Avian Malaria Parasites and West Nile Virus in Vectors and Hosts"],"prefix":"10.4269","volume":"95","author":[{"given":"Matthew C. I.","family":"Medeiros","sequence":"first","affiliation":[{"name":"Department of Entomology, Texas A&M University, College Station, Texas."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert E.","family":"Ricklefs","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Missouri\u2013St. Louis, St. Louis, Missouri."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeffrey D.","family":"Brawn","sequence":"additional","affiliation":[{"name":"Department of Natural Resources and Environmental Sciences, University of Illinois, Urbana, Illinois."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marilyn O.","family":"Ruiz","sequence":"additional","affiliation":[{"name":"Department of Pathobiology, University of Illinois, Urbana, Illinois."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tony L.","family":"Goldberg","sequence":"additional","affiliation":[{"name":"Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, Wisconsin."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gabriel L.","family":"Hamer","sequence":"additional","affiliation":[{"name":"Department of Entomology, Texas A&M University, College Station, Texas."}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"2795","reference":[{"key":"ref1","series-title":"Ecol Lett","first-page":"467","article-title":"Seasonality and the dynamics of infectious diseases","volume":"9","author":"Altizer","year":"2006"},{"key":"ref2","series-title":"Am J Trop Med Hyg","first-page":"489","article-title":"A simulation model of the epidemiology of urban dengue fever: literature analysis, model development, preliminary validation, and samples of simulation results","volume":"53","author":"Focks","year":"1995"},{"key":"ref3","series-title":"Parasit Vectors","first-page":"19","article-title":"Local impact of temperature and precipitation on West Nile virus infection in Culex species mosquitoes in northeast Illinois, USA","volume":"3","author":"Ruiz","year":"2010"},{"key":"ref4","series-title":"J Med Entomol","first-page":"315","article-title":"Host-feeding patterns of Culex tarsalis in the Sacramento Valley, California, with notes on other species","volume":"4","author":"Tempelis","year":"1967"},{"key":"ref5","series-title":"Am J Trop Med Hyg","first-page":"170","article-title":"A 3-year study of feeding habits of Culex tarsalis in Kern County, California","volume":"14","author":"Tempelis","year":"1965"},{"key":"ref6","series-title":"J Med Entomol","first-page":"635","article-title":"Host-feeding patterns of mosquitos, with a review of advances in analysis of blood meals by serology","volume":"11","author":"Tempelis","year":"1975"},{"key":"ref7","series-title":"Am J Trop Med Hyg","first-page":"268","article-title":"Host selection by Culex pipiens mosquitoes and West Nile virus amplification","volume":"80","author":"Hamer","year":"2009"},{"key":"ref8","series-title":"Proc Biol Sci","first-page":"2327","article-title":"Host heterogeneity dominates West Nile virus transmission","volume":"273","author":"Kilpatrick","year":"2006"},{"key":"ref9","series-title":"Am J Trop Med Hyg","first-page":"111","article-title":"Variations in feeding patterns of seven culine mosquitoes on vertebrate hosts in Weld and Larimer Counties, Colorado","volume":"16","author":"Tempelis","year":"1967"},{"key":"ref10","series-title":"Biol Lett","first-page":"567","article-title":"Winter severity predicts the timing of host shifts in the mosquito Culex erraticus","volume":"8","author":"Burkett-Cadena","year":"2012"},{"key":"ref11","series-title":"PLoS Biol","first-page":"606","article-title":"West Nile virus epidemics in North America are driven by shifts in mosquito feeding behavior","volume":"4","author":"Kilpatrick","year":"2006"},{"key":"ref12","series-title":"Mol Ecol","first-page":"5545","article-title":"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","volume":"19","author":"Kim","year":"2010"},{"key":"ref13","series-title":"J Vector Ecol","first-page":"89","article-title":"Impact of climate variation on mosquito abundance in California","volume":"33","author":"Reisen","year":"2008"},{"key":"ref14","series-title":"J Med Entomol","first-page":"800","article-title":"Mosquito species richness, composition, and abundance along habitat-climate-elevation gradients in the northern Colorado front range","volume":"45","author":"Eisen","year":"2008"},{"key":"ref15","series-title":"Funct Ecol","first-page":"358","article-title":"Reproductive investment and parasite susceptibility in the great tit","volume":"11","author":"Allander","year":"1997"},{"key":"ref16","series-title":"Proc Biol Sci","first-page":"1291","article-title":"Reproductive effort reduces specific immune response and parasite resistance","volume":"265","author":"Nordling","year":"1998"},{"key":"ref17","series-title":"Vector Borne Zoonotic Dis","first-page":"57","article-title":"Rapid amplification of West Nile virus: the role of hatch-year birds","volume":"8","author":"Hamer","year":"2008"},{"key":"ref18","series-title":"Parasit Vectors","first-page":"399","article-title":"Avian roosting behavior influences vector-host interactions for West Nile virus hosts","volume":"7","author":"Janousek","year":"2014"},{"key":"ref19","series-title":"Proc Biol Sci","first-page":"20141586","article-title":"Host group formation decreases exposure to vector-borne disease: a field experiment in a \u2018hotspot\u2019 of West Nile virus transmission","volume":"281","author":"Krebs","year":"2014"},{"key":"ref20","series-title":"Parasitology","first-page":"S23","article-title":"Concomitant infections, parasites and immune responses","volume":"122","author":"Cox","year":"2001"},{"key":"ref21","series-title":"Adv Virus Res","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/B978-0-12-800172-1.00002-1","article-title":"The role of environmental, virological and vector interactions in dictating biological transmission of arthropod-borne viruses by mosquitoes","volume":"89","author":"Kenney","year":"2014"},{"key":"ref22","series-title":"Am Nat","first-page":"613","article-title":"Hidden consequences of living in a wormy world: nematode-induced immune suppression facilitates tuberculosis invasion in African Buffalo","volume":"176","author":"Ezenwa","year":"2010"},{"key":"ref23","series-title":"Proc Natl Acad Sci USA","first-page":"9006","article-title":"Parasite diversity and coinfection determine pathogen infection success and host fitness","volume":"109","author":"Johnson","year":"2012"},{"key":"ref24","series-title":"Am J Trop Med Hyg","first-page":"105","article-title":"Dual host infections: enhanced infectivity of eastern equine encephalitis virus to Aedes mosquitoes mediated by Brugia microfilariae","volume":"54","author":"Vaughan","year":"1996"},{"key":"ref25","series-title":"Am J Trop Med Hyg","first-page":"407","article-title":"Facilitation of Rift Valley fever virus transmission by Plasmodium berghei sporozoites in Anopheles stephensi mosquitoes","volume":"55","author":"Vaughan","year":"1996"},{"key":"ref26","series-title":"Avian Malaria Parasites and Other Haemosporidia","author":"Valkiunas","year":"2005"},{"key":"ref27","series-title":"Parasitol Res","first-page":"3627","article-title":"Host immune responses to experimental infection of Plasmodium relictum (lineage SGS1) in domestic canaries (Serinus canaria)","volume":"114","author":"Ellis","year":"2015"},{"key":"ref28","series-title":"J Wildl Dis","first-page":"443","article-title":"Mechanism of spring relapse in avian malaria: effect of gonadotropin and corticosterone","volume":"6","author":"Applegate","year":"1970"},{"key":"ref29","series-title":"J Anim Ecol","first-page":"540","article-title":"Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus","volume":"77","author":"Cosgrove","year":"2008"},{"key":"ref30","series-title":"J Wildl Dis","first-page":"5","article-title":"A model for the ecology of avian malaria","volume":"7","author":"Beaudoin","year":"1971"},{"key":"ref31","series-title":"Science","first-page":"2333","article-title":"Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States","volume":"286","author":"Lanciotti","year":"1999"},{"key":"ref32","series-title":"Vet Res","first-page":"67","article-title":"West Nile virus and its emergence in the United States of America","volume":"41","author":"Murray","year":"2010"},{"key":"ref33","series-title":"Nature","first-page":"710","article-title":"West Nile virus emergence and large-scale declines of North American bird populations","volume":"447","author":"LaDeau","year":"2007"},{"key":"ref34","series-title":"Int J Environ Res Public Health","first-page":"5584","article-title":"Spatio-temporal epidemiology of human West Nile virus disease in South Dakota","volume":"10","author":"Wimberly","year":"2013"},{"key":"ref35","series-title":"Am J Trop Med Hyg","first-page":"1013","article-title":"Meteorological conditions associated with increased incidence of West Nile virus disease in the United States, 2004\u20132012","volume":"92","author":"Hahn","year":"2015"},{"key":"ref36","series-title":"Parasit Vectors","first-page":"415","article-title":"An inverse association between West Nile virus serostatus and avian malaria infection status","volume":"7","author":"Medeiros","year":"2014"},{"key":"ref37","series-title":"J Med Entomol","first-page":"461","article-title":"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","volume":"52","author":"Boothe","year":"2015"},{"key":"ref38","series-title":"J Med Entomol","first-page":"1","article-title":"Considerations for accurate identification of adult Culex restuans (Diptera: Culicidae) in field studies","volume":"45","author":"Harrington","year":"2008"},{"key":"ref39","series-title":"J Parasitol","first-page":"1044","article-title":"Detecting avian malaria: an improved polymerase chain reaction diagnostic","volume":"89","author":"Fallon","year":"2003"},{"key":"ref40","series-title":"Parasitology","first-page":"181","article-title":"Structure and organization of an avian haemosporidian assemblage in a neotropical savanna in Brazil","volume":"140","author":"Fecchio","year":"2013"},{"key":"ref41","series-title":"Parasitology","first-page":"1223","article-title":"Species limits in avian malaria parasites (Haemosporida): how to move forward in the molecular era","volume":"141","author":"Outlaw","year":"2014"},{"key":"ref42","series-title":"Ornithol Monogr","first-page":"1","article-title":"Diversity, prevalence, and host specificity of avian Plasmodium and Haemoproteus in a western Amazon assemblage","volume":"76","author":"Svensson-Coelho","year":"2013"},{"key":"ref43","series-title":"Proc Biol Sci","first-page":"20122947","article-title":"Host compatibility rather than vector-host-encounter rate determines the host range of avian Plasmodium parasites","volume":"280","author":"Medeiros","year":"2013"},{"key":"ref44","series-title":"J Evol Biol","first-page":"2520","article-title":"Specialized avian Haemosporida trade reduced host breadth for increased prevalence","volume":"27","author":"Medeiros","year":"2014"},{"key":"ref45","series-title":"J Wildl Dis","first-page":"601","article-title":"West Nile virus antibody decay rate in free-ranging birds","volume":"51","author":"Mckee","year":"2015"},{"key":"ref46","series-title":"Ecosphere","first-page":"1","article-title":"Climatic variability and landscape heterogeneity impact urban mosquito diversity and vector abundance and infection","volume":"2","author":"Chaves","year":"2011"},{"key":"ref47","series-title":"Oecologia","first-page":"415","article-title":"Avian host community structure and prevalence of West Nile virus in Chicago, Illinois","volume":"159","author":"Loss","year":"2009"},{"key":"ref48","series-title":"J Clin Microbiol","first-page":"4066","article-title":"Rapid detection of West Nile virus from human clinical specimens, field-collected mosquitoes, and avian samples by a TaqMan reverse transcriptase-PCR assay","volume":"38","author":"Lanciotti","year":"2000"},{"key":"ref49","series-title":"ggplot2: Elegant Graphics for Data Analysis","author":"Wickham","year":"2009"},{"key":"ref50","series-title":"Mol Ecol","first-page":"4545","article-title":"Avian haematozoan parasites and their associations with mosquitoes across southwest Pacific Islands","volume":"17","author":"Ishtiaq","year":"2008"},{"key":"ref51","series-title":"Mol Ecol","first-page":"1049","article-title":"Nonspecific patterns of vector, host and avian malaria parasite associations in a central African rainforest","volume":"20","author":"Njabo","year":"2011"},{"key":"ref52","series-title":"J Am Mosq Control Assoc","first-page":"275","article-title":"The abundance and seasonal distribution of Culex mosquitoes in Iowa during 1995\u201397","volume":"16","author":"Lee","year":"2000"},{"key":"ref53","series-title":"Emerg Infect Dis","first-page":"670","article-title":"Mosquito surveillance for West Nile virus in Connecticut, 2000: isolation from Culex pipiens, Cx. restuans, Cx. salinarius, Culiseta melanura","volume":"7","author":"Andreadis","year":"2001"},{"key":"ref54","series-title":"J Am Mosq Control Assoc","first-page":"360","article-title":"Oviposition preferences of Culex restuans and Culex pipiens (Diptera: Culicidae) for selected infusions in oviposition traps and gravid traps","volume":"21","author":"Jackson","year":"2005"},{"key":"ref55","series-title":"J Am Mosq Control Assoc","first-page":"206","article-title":"Seasonal abundance of Culex restuans and Culex pipiens in southwestern Virginia through ovitrapping","volume":"22","author":"Jackson","year":"2006"},{"key":"ref56","series-title":"Ekologija","first-page":"73","article-title":"Recent advances in vector studies of avian haemosporidian parasites","volume":"60","author":"\u017diegyt\u0117","year":"2015"},{"key":"ref57","series-title":"J Parasitol","first-page":"144","article-title":"Avian malaria parasites share congeneric mosquito vectors","volume":"96","author":"Kimura","year":"2010"},{"key":"ref58","series-title":"Mol Ecol","first-page":"5374","article-title":"Avian Plasmodium lineages found in spot surveys of mosquitoes from 2007 to 2010 at Sakata wetland, Japan: do dominant lineages persist for multiple years?","volume":"21","author":"Kim","year":"2012"},{"key":"ref59","series-title":"Parasit Vectors","first-page":"365","article-title":"Identifying avian malaria vectors: sampling methods influence outcomes","volume":"8","author":"Carlson","year":"2015"},{"key":"ref60","series-title":"J Parasitol","first-page":"318","article-title":"Thermal constraints to the sporogonic development and altitudinal distribution of avian malaria Plasmodium relictum in Hawaii","volume":"96","author":"LaPointe","year":"2010"},{"key":"ref61","series-title":"Proc Biol Sci","first-page":"3357","article-title":"Complex effects of temperature on mosquito immune function","volume":"279","author":"Murdock","year":"2012"},{"key":"ref62","series-title":"PLoS Pathog","first-page":"e1004308","article-title":"Evolution of plastic transmission strategies in avian malaria","volume":"10","author":"Cornet","year":"2014"},{"key":"ref63","series-title":"Vector Borne Zoonotic Dis","first-page":"1099","article-title":"Culex flavivirus and West Nile virus mosquito coinfection and positive ecological association in Chicago, United States","volume":"11","author":"Newman","year":"2011"},{"key":"ref64","series-title":"Emerg Infect Dis","first-page":"311","article-title":"Experimental infection of North American birds with the New York 1999 strain of West Nile virus","volume":"9","author":"Komar","year":"2003"},{"key":"ref65","series-title":"Malar J","first-page":"179","article-title":"Both infected and uninfected mosquitoes are attracted toward malaria infected birds","volume":"12","author":"Cornet","year":"2013"},{"key":"ref66","series-title":"Ecol Lett","first-page":"323","article-title":"Malaria infection increases bird attractiveness to uninfected mosquitoes","volume":"16","author":"Cornet","year":"2013"},{"key":"ref67","series-title":"Anim Behav","first-page":"539","article-title":"Potential evidence of parasite avoidance in an avian malarial vector","volume":"84","author":"Lalubin","year":"2012"},{"key":"ref68","series-title":"Proc Biol Sci","first-page":"763","article-title":"The malaria parasite, Plasmodium falciparum, increases the frequency of multiple feeding of its mosquito vector, Anopheles gambiae","volume":"265","author":"Koella","year":"1998"},{"key":"ref69","series-title":"PLoS Biol","first-page":"1590","article-title":"Malaria infection increases attractiveness of humans to mosquitoes","volume":"3","author":"Lacroix","year":"2005"}],"container-title":["The American Society of Tropical Medicine and 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