{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,27]],"date-time":"2026-06-27T16:45:32Z","timestamp":1782578732716,"version":"3.54.5"},"reference-count":35,"publisher":"Oxford University Press (OUP)","issue":"3","funder":[{"name":"USDA-ARS National","award":["#3020\u201332000-018-00D"],"award-info":[{"award-number":["#3020\u201332000-018-00D"]}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["T35OD029981"],"award-info":[{"award-number":["T35OD029981"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,5,5]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Haemosporidian parasites of birds are maintained through complex interactions among vertebrate hosts, arthropod vectors, and the parasites themselves, yet their vector\u2013parasite relationships remain poorly resolved under natural conditions in North America. Haemoproteus species are among the most prevalent avian blood parasites and have been implicated in reduced host fitness and malaria-like disease. Here, we combined molecular and histological approaches to investigate Haemoproteus prevalence in wild birds and to identify potential Culicoides biting midge vectors in Kansas. Blood meals from field-collected Culicoides and hunter-collected turkey blood samples were screened using nested PCR targeting the Haemoproteus cytochrome b gene, followed by Sanger sequencing. We additionally dissected and microscopically examined salivary glands as well as turkey blood smears. Nearly all turkey blood samples (95.7%) were positive for Haemoproteus, revealing 2 distinct parasite clades and frequent coinfections. In contrast, Culicoides-based surveillance may have underestimated parasite prevalence in turkeys. Only Culicoides haematopotus consistently tested positive by PCR, and this species was the only one in which Haemoproteus sporozoites were detected in salivary glands. Sequencing of PCR amplicons from unfed C. haematopotus revealed amplification of a Culicoides-specific noncoding genomic region, highlighting limitations of molecular detection alone for vector incrimination. Together, these findings provide field-based evidence that C. haematopotus may serve as a vector of Haemoproteus in wild turkeys in Kansas, emphasizing the importance of integrating molecular and histological data when evaluating vector competence and potential population-level effects.<\/jats:p>","DOI":"10.1093\/jme\/tjag098","type":"journal-article","created":{"date-parts":[[2026,6,27]],"date-time":"2026-06-27T15:46:32Z","timestamp":1782575192000},"source":"Crossref","is-referenced-by-count":0,"title":["Haemosporidian parasites in Kansas birds: molecular and histological evidence implicating\n                    <i>Culicoides haematopotus<\/i>\n                    (Diptera: Ceratopogonidae) in transmission"],"prefix":"10.1093","volume":"63","author":[{"ORCID":"https:\/\/orcid.org\/0009-0000-7787-0977","authenticated-orcid":false,"given":"Ilya","family":"Verekhman","sequence":"first","affiliation":[{"name":"Diagnostic Medicine\/Pathobiology, Kansas State University College of Veterinary Medicine , Manhattan, KS,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amanda","family":"Fideldy","sequence":"additional","affiliation":[{"name":"Diagnostic Medicine\/Pathobiology, Kansas State University College of Veterinary Medicine , Manhattan, KS,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Caitlin","family":"Taylor","sequence":"additional","affiliation":[{"name":"Center for Grain and Animal Health Research, USDA Agricultural Research Service , Manhattan, KS,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alec","family":"Fehr","sequence":"additional","affiliation":[{"name":"Alec Fehr is currently unaffiliated with an institution"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bethany","family":"McGregor","sequence":"additional","affiliation":[{"name":"Center for Grain and Animal Health Research, USDA Agricultural Research Service , Manhattan, KS,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2498-9637","authenticated-orcid":false,"given":"Phillip","family":"Shults","sequence":"additional","affiliation":[{"name":"Center for Grain and Animal Health Research, USDA Agricultural Research Service , Manhattan, KS,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2026,6,27]]},"reference":[{"key":"2026062711462494900_tjag098-B1","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1093\/jmedent\/25.1.39","article-title":"Epizootiology of Haemoproteus meleagridis Protozoa: Haemosporina) in Florida: potential vectors and prevalence in naturally infected Culicoides (Diptera: Ceratopogonidae)","volume":"25","author":"Atkinson","year":"1988","journal-title":"J. Med. Entomol"},{"key":"2026062711462494900_tjag098-B2","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1002\/9780813804620.ch3","volume-title":"Parasitic diseases of wild birds","author":"Atkinson","year":"2008"},{"key":"2026062711462494900_tjag098-B3","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1002\/9780813804620","volume-title":"Parasitic diseases of wild birds","author":"Atkinson","year":"2008"},{"key":"2026062711462494900_tjag098-B4","doi-asserted-by":"crossref","first-page":"228","DOI":"10.2307\/3282448","article-title":"Pathogenicity of Haemoproteus meleagridis (Haemosporina: Haemoproteidae) in experimentally infected domestic turkeys","volume":"74","author":"Atkinson","year":"1988","journal-title":"J. Parasitol"},{"key":"2026062711462494900_tjag098-B5","doi-asserted-by":"publisher","first-page":"366","DOI":"10.7589\/0090-3558-19.4.366","article-title":"Experimental vectors of Haemoproteus meleagridis Levine from wild turkeys in Florida","volume":"19","author":"Atkinson","year":"1983","journal-title":"J. Wildl. Dis"},{"key":"2026062711462494900_tjag098-B6","volume-title":"2 Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus","author":"Atkinson","year":"1991"},{"key":"2026062711462494900_tjag098-B7","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1186\/s12936-016-1338-y","article-title":"PCR detection of malaria parasites and related haemosporidians: the sensitive methodology in determining bird-biting insects","volume":"15","author":"Bernotien\u0117","year":"2016","journal-title":"Malar. J."},{"key":"2026062711462494900_tjag098-B8","article-title":"The sand flies (Culicoides) of Florida (Diptera: Ceratopogonidae)","volume":"10","author":"Blanton","year":"1981","journal-title":"Arthropods Florida Neighbor. Land Areas"},{"key":"2026062711462494900_tjag098-B9","doi-asserted-by":"publisher","first-page":"333","DOI":"10.1017\/S0031182018001373","article-title":"High susceptibility of the laboratory-reared biting midges Culicoides nubeculosus to Haemoproteus infections, with review on Culicoides species that transmit avian haemoproteids","volume":"146","author":"Bukauskait\u0117","year":"2019","journal-title":"Parasitology"},{"key":"2026062711462494900_tjag098-B10","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1637\/0005-2086(2002)046[0249:HLIIBQ]2.0.CO;2","article-title":"Haemoproteus lophortyx infection in bobwhite quail","volume":"46","author":"Cardona","year":"2002","journal-title":"Avian Dis"},{"key":"2026062711462494900_tjag098-B12","doi-asserted-by":"publisher","first-page":"157","DOI":"10.3390\/insects15030157","article-title":"High abundance of Haemoproteus parasites in Culicoides (Diptera, Ceratopogonidae), with a confirmation of Culicoides reconditus as a new vector of these avian blood parasites","volume":"15","author":"Chagas","year":"2024","journal-title":"Insects"},{"key":"2026062711462494900_tjag098-B14","doi-asserted-by":"publisher","first-page":"304","DOI":"10.1177\/104063870802000307","article-title":"Hepatic hemorrhage, hemocoelom, and sudden death due to Haemoproteus infection in passerine birds: eleven cases","volume":"20","author":"Donovan","year":"2008","journal-title":"J. Vet. Diagn. Invest."},{"key":"2026062711462494900_tjag098-B15","doi-asserted-by":"publisher","first-page":"2824","DOI":"10.3390\/ani11102824","article-title":"First report of Haemoproteus (Haemosporida, Haemoproteidae) megalomeronts in the brain of an avian host, with description of megalomerogony of Haemoproteus pastoris, the blood parasite of the Common starling","volume":"11","author":"Duc","year":"2021","journal-title":"Animals"},{"key":"2026062711462494900_tjag098-B20","first-page":"32","author":"Durbin C. Kansas Wild Turkey Population Status Report","year":"2025"},{"key":"2026062711462494900_tjag098-B16","doi-asserted-by":"publisher","first-page":"455","DOI":"10.1139\/z60-049","article-title":"Description of Haemoproteus canachites n. sp. (Sporozoa: Haemoproteidae) and sporogony in Culicoides (Diptera: Ceratopogonidae)","volume":"38","author":"Fallis","year":"1960","journal-title":"Can. J. Zool."},{"key":"2026062711462494900_tjag098-B17","doi-asserted-by":"publisher","first-page":"562","DOI":"10.1177\/03009858241231558","article-title":"Experimental infection of domestic turkeys with lymphoproliferative disease virus of North American origin","volume":"61","author":"Goodwin","year":"2024","journal-title":"Vet. Pathol"},{"key":"2026062711462494900_tjag098-B19","doi-asserted-by":"publisher","first-page":"100840","DOI":"10.1016\/j.vprsr.2023.100840","article-title":"The first detection of avian haemosporidia from Culicoides biting midges in Japan, with notes on potential vector species and the transmission cycle","volume":"39","author":"Inumaru","year":"2023","journal-title":"Vet. Parasitol. Reg. Stud. Rep."},{"key":"2026062711462494900_tjag098-B21","doi-asserted-by":"publisher","DOI":"10.1590\/s1984-29612025048","article-title":"Molecular survey of the haemosporidians Haemoproteus and Leucocytozoon in Culicoides (Diptera: Ceratopogonidae) from the Brazilian Amazon","volume":"34","author":"Lee","year":"2025","journal-title":"Rev. Bras. Parasitol. Vet"},{"key":"2026062711462494900_tjag098-B22","doi-asserted-by":"publisher","first-page":"1092","DOI":"10.1111\/oik.02778","article-title":"A longitudinal study of age-related changes in Haemoproteus infection in a passerine bird","volume":"125","author":"Marzal","year":"2016","journal-title":"Oikos"},{"key":"2026062711462494900_tjag098-B23","doi-asserted-by":"crossref","first-page":"1192","DOI":"10.1002\/9781119371199.ch28","article-title":"Protozoal infections","author":"McDougald","year":"2020","journal-title":"Diseases Poultry"},{"key":"2026062711462494900_tjag098-B24","doi-asserted-by":"publisher","first-page":"2504","DOI":"10.3390\/ani13152504","article-title":"Host associations of Culicoides biting midges in Northeastern Kansas, USA","volume":"13","author":"McGregor","year":"2023","journal-title":"Animals"},{"key":"2026062711462494900_tjag098-B25","doi-asserted-by":"crossref","first-page":"2507","DOI":"10.1098\/rspb.2000.1312","article-title":"Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus)","volume":"267","author":"Merino","year":"2000","journal-title":"Proc. R. Soc. Lond. Ser. B Biol. Sci"},{"key":"2026062711462494900_tjag098-B26","first-page":"213","volume-title":"Biting midges (Ceratopogonidae)","author":"Mullen","year":"2019"},{"key":"2026062711462494900_tjag098-B27","doi-asserted-by":"publisher","first-page":"441","DOI":"10.1007\/s004420050608","article-title":"Health impact of blood parasites in breeding great tits","volume":"116","author":"Ots","year":"1998","journal-title":"Oecologia"},{"key":"2026062711462494900_tjag098-B28","doi-asserted-by":"publisher","first-page":"663","DOI":"10.1098\/rsbl.2010.0046","article-title":"The blood parasite Haemoproteus reduces survival in a wild bird: a medication experiment","volume":"6","author":"Puente","year":"2010","journal-title":"Biol. Lett"},{"key":"2026062711462494900_tjag098-B29","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1647\/2003-008","article-title":"Intracellular hematozoa of raptors: a review and update","volume":"18","author":"Remple","year":"2004","journal-title":"J. Avian Med. Surg"},{"key":"2026062711462494900_tjag098-B30","doi-asserted-by":"publisher","first-page":"353","DOI":"10.1002\/jmor.1051980309","article-title":"Anatomy and function of the mouthparts of the biting midge, Culicoides sanguisuga (Diptera: Ceratopogonidae)","volume":"198","author":"Sutcliffe","year":"1988","journal-title":"J. Morphol"},{"key":"2026062711462494900_tjag098-B32","doi-asserted-by":"publisher","first-page":"433","DOI":"10.1146\/annurev-ento-120811-153618","article-title":"Host preferences of blood-feeding mosquitoes","volume":"58","author":"Takken","year":"2013","journal-title":"Annu. Rev. Entomol"},{"key":"2026062711462494900_tjag098-B33","doi-asserted-by":"crossref","DOI":"10.1201\/9780203643792","volume-title":"Avian malaria parasites and other haemosporidia","author":"Valkiunas","year":"2004"},{"key":"2026062711462494900_tjag098-B34","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1186\/s12936-022-04235-1","article-title":"Keys to the avian Haemoproteus parasites (Haemosporida, Haemoproteidae)","volume":"21","author":"Valki\u016bnas","year":"2022","journal-title":"Malar. J."},{"key":"2026062711462494900_tjag098-B35","doi-asserted-by":"publisher","first-page":"524","DOI":"10.1186\/s13071-018-3098-8","article-title":"Culicoides paolae and C. circumscriptus as potential vectors of avian haemosporidians in an arid ecosystem","volume":"11","author":"Veiga","year":"2018","journal-title":"Parasit. Vectors."},{"key":"2026062711462494900_tjag098-B36","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1645\/GE-3221RN","article-title":"A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood","volume":"90","author":"Waldenstr\u00f6m","year":"2004","journal-title":"J. Parasitol"},{"key":"2026062711462494900_tjag098-B37","doi-asserted-by":"publisher","first-page":"898","DOI":"10.3390\/microorganisms10050898","article-title":"Culicoides segnis and Culicoides pictipennis biting midges (Diptera, Ceratopogonidae), new reported vectors of Haemoproteus parasites","volume":"10","author":"\u017diegyt\u0117","year":"2022","journal-title":"Microorganisms"},{"key":"2026062711462494900_tjag098-B38","doi-asserted-by":"publisher","first-page":"397","DOI":"10.1186\/s13071-017-2317-z","article-title":"The widespread biting midge Culicoides impunctatus (Ceratopogonidae) is susceptible to infection with numerous Haemoproteus (Haemoproteidae) species","volume":"10","author":"\u017diegyt\u0117","year":"2017","journal-title":"Parasit. Vectors."},{"key":"2026062711462494900_tjag098-B39","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1186\/s13071-020-04516-1","article-title":"Culicoides biting midges involved in transmission of haemoproteids","volume":"14","author":"\u017diegyt\u0117","year":"2021","journal-title":"Parasit. Vectors."}],"container-title":["Journal of Medical Entomology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/jme\/article-pdf\/63\/3\/tjag098\/68632955\/tjag098.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jme\/article-pdf\/63\/3\/tjag098\/68632955\/tjag098.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,6,27]],"date-time":"2026-06-27T15:46:40Z","timestamp":1782575200000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jme\/article\/doi\/10.1093\/jme\/tjag098\/8719556"}},"subtitle":[],"editor":[{"given":"Emily","family":"McDermott","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2026,5]]},"references-count":35,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2026,5,5]]}},"URL":"https:\/\/doi.org\/10.1093\/jme\/tjag098","relation":{},"ISSN":["0022-2585","1938-2928"],"issn-type":[{"value":"0022-2585","type":"print"},{"value":"1938-2928","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2026,5]]},"published":{"date-parts":[[2026,5]]},"article-number":"tjag098"}}