{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T00:55:45Z","timestamp":1791248145754,"version":"4.1.0"},"reference-count":102,"publisher":"Wildlife Disease Association","issue":"3","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Journal of Wildlife Diseases"],"published-print":{"date-parts":[[2024,7,8]]},"abstract":"<jats:p>Pathogens have traditionally been studied in isolation within host systems; yet in natural settings they frequently coexist. This raises questions about the dynamics of co-infections and how host life-history traits might predict co-infection versus single infection. To address these questions, we investigated the presence of two parasites, a gut parasite (Isospora coccidians) and a blood parasite (Plasmodium spp.), in House Finches (Haemorhous mexicanus), a common passerine bird in North America. We then correlated these parasitic infections with various health and condition metrics, including hematological parameters, plasma carotenoids, lipid-soluble vitamins, blood glucose concentration, body condition, and prior disease history. Our study, based on 48 birds captured in Tempe, Arizona, US, in October 2021, revealed that co-infected birds exhibited elevated circulating lutein levels and a higher heterophil: lymphocyte ratio (H\/L ratio) compared to those solely infected with coccidia Isospora spp. This suggests that co-infected birds experience heightened stress and may use lutein to bolster immunity against both pathogens, and that there are potentially toxic effects of lutein in co-infected birds compared to those infected solely with coccidia Isospora sp. Our findings underscore the synergistic impact of coparasitism, emphasizing the need for more co-infection studies to enhance our understanding of disease dynamics in nature, as well as its implications for wildlife health and conservation efforts.<\/jats:p>","DOI":"10.7589\/jwd-d-23-00175","type":"journal-article","created":{"date-parts":[[2024,7,10]],"date-time":"2024-07-10T00:32:48Z","timestamp":1720571568000},"page":"634-646","source":"Crossref","is-referenced-by-count":6,"title":["CORRELATES OF CO-INFECTION WITH COCCIDIOSIS AND AVIAN MALARIA IN HOUSE FINCHES (HAEMORHOUS MEXICANUS)"],"prefix":"10.7589","volume":"60","author":[{"given":"Victor Aguiar de Souza","family":"Penha","sequence":"first","affiliation":[{"name":"Programa de P\u00f3s-Gradua\u00e7\u00e3o em Ecologia e Conserva\u00e7\u00e3o, Universidade Federal do Paran\u00e1, Setor de Ci\u00eancias Biol\u00f3gicas, 100 Cel. Francisco H. dos Santos Avenue, Curitiba, Paran\u00e1 81531-980, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lilian Tonelli","family":"Manica","sequence":"additional","affiliation":[{"name":"Departamento de Zoologia, Setor de Ci\u00eancias Biol\u00f3gicas, Universidade Federal do Paran\u00e1, Avenida Cel. Francisco H. dos Santos Avenue, 100, Curitiba, Paran\u00e1 81531-980, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zachary A.","family":"Barrand","sequence":"additional","affiliation":[{"name":"Pathogen and Microbiome Institute, Northern Arizona University, Building 56, 1395 South Knoles Drive, Flagstaff, Arizona 86011, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Crystal M.","family":"Hepp","sequence":"additional","affiliation":[{"name":"Pathogen and Microbiome Institute, Northern Arizona University, Building 56, 1395 South Knoles Drive, Flagstaff, Arizona 86011, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kevin J.","family":"McGraw","sequence":"additional","affiliation":[{"name":"School of Life Sciences, Arizona State University, ASU Life Sciences Building E, 400 E Tyler Mal, Tempe, Arizona 85287, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"4415","reference":[{"key":"67","doi-asserted-by":"crossref","unstructured":"E P\u00e9rez-Ram\u00edrez, F Llorente, M\u00c1 Jim\u00e9nez-Clavero,  \"Viruses.\"  6, \"Experimental infections of wild birds with West Nile virus.\" 752 (2014)","DOI":"10.3390\/v6020752"},{"key":"69","unstructured":"P. Pyle,  \"Identification guide to North American birds, part 1: Columbidae to Ploceidae.\"  732 (1997)"},{"key":"5","doi-asserted-by":"crossref","unstructured":"D Bates, M M\u00e4chler, B Bolker, et al.  \"J Stat Softw.\"  67, \"Fitting linear mixed-effects models using lme4.\" 1 (2015)","DOI":"10.18637\/jss.v067.i01"},{"key":"90","doi-asserted-by":"crossref","unstructured":"R Velarde, MC Porrero, E Serrano, et al.  \"J Wildl Dis.\"  48, \"Septicemic salmonellosis caused by Salmonella Hessarek in wintering and migrating song thrushes (Turdus philomelos) in Spain.\" 113 (2012)","DOI":"10.7589\/0090-3558-48.1.113"},{"key":"35","doi-asserted-by":"crossref","unstructured":"O Hellgren, J Waldenstr\u00f6m, S Bensch,  \"J Parasitol.\"  90, \"A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood.\" 797 (2004)","DOI":"10.1645\/GE-184R1"},{"key":"95","doi-asserted-by":"crossref","unstructured":"J Waldenstr\u00f6m, S Bensch, D Hasselquist, et al.  \"J Parasitol.\"  90, \"A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood.\" 191 (2004)","DOI":"10.1645\/GE-3221RN"},{"key":"47","doi-asserted-by":"crossref","unstructured":"DH Ley, JE Berkhoff, JM McLaren,  \"Avian Dis.\"  40, \"Mycoplasma gallisepticum isolated from house finches (Carpodacus mexicanus) with conjunctivitis.\" 480 (1996)","DOI":"10.2307\/1592250"},{"key":"38","doi-asserted-by":"crossref","unstructured":"GE Hill, KL Farmer, ML Beck,  \"J Exp Biol.\"  207, \"The effect of mycoplasmosis on carotenoid plumage coloration in male house finches.\" 2095 (2004)","DOI":"10.1242\/jeb.00998"},{"key":"92","doi-asserted-by":"crossref","unstructured":"CM Vleck, N Vertalino, D Vleck, et al.  \"Condor.\"  102, \"Stress, corticosterone, and heterophil to lymphocyte ratios in free-living Ad\u00e9lie penguins.\" 392 (2000)","DOI":"10.1093\/condor\/102.2.392"},{"key":"70","unstructured":"\"R: A language and environment for statistical computing.\"  (2019)"},{"key":"33","doi-asserted-by":"crossref","unstructured":"M Giraudeau, M Mousel, S Earl, et al.  \"PLoS One.\"  9, \"Parasites in the city: Degree of urbanization predicts poxvirus and coccidian infections in house finches (Haemorhous mexicanus).\" e86747 (2014)","DOI":"10.1371\/journal.pone.0086747"},{"key":"73","doi-asserted-by":"crossref","unstructured":"MT Reinoso-P\u00e9rez, KV Dhondt, AV Sydenstricker, et al.  \"Ecol Evol.\"  10, \"Complex interactions between bacteria and haemosporidia in coinfected hosts: An experiment.\" 5801 (2020)","DOI":"10.1002\/ece3.6318"},{"key":"89","doi-asserted-by":"crossref","unstructured":"G. Valki\u016bnas,  \"Avian malaria parasites and other haemosporidia.\"  946 (2005)","DOI":"10.1201\/9780203643792"},{"key":"40","doi-asserted-by":"crossref","unstructured":"AOG Hoarau, P Mavingui, C Lebarbenchon,  \"PLoS Pathog.\"  16, \"Coinfections in wildlife: Focus on a neglected aspect of infectious disease epidemiology.\" e1008790 (2020)","DOI":"10.1371\/journal.ppat.1008790"},{"key":"15","doi-asserted-by":"crossref","unstructured":"NJ Clark, K Wells, D Dimitrov, et al.  \"J Anim Ecol.\"  85, \"Co-infections and environmental conditions drive the distributions of blood parasites in wild birds.\" 1461 (2016)","DOI":"10.1111\/1365-2656.12578"},{"key":"11","doi-asserted-by":"crossref","unstructured":"TW. Campbell,  \"Exotic Animal Hematology and Cytology.\"  \"Peripheral blood of birds.\" 37 (2015)","DOI":"10.1002\/9781118993705"},{"key":"1","unstructured":"T Ahmad, MM Hussain, A Yousaf, et al.  \"Proceedings of the 5th International Poultry Conference, Taba, Egypt, 10\u201313 March 2009.\"  \"Effects of vitamin E, selenium, and levamisole on immune response of broiler birds artificially infected with coccidiosis.\" 1389 (2013)"},{"key":"2","doi-asserted-by":"crossref","unstructured":"A Alves-Rodrigues  and A Shao  \"Toxicol Lett.\"  150, \"The science behind lutein.\" 57 (2004)","DOI":"10.1016\/j.toxlet.2003.10.031"},{"key":"3","doi-asserted-by":"crossref","unstructured":"R Baeta, B Faivre, S Motreuil, et al.  \"Proc R Soc Ser B Biol Sci.\"  275, \"Carotenoid trade-off between parasitic resistance and sexual display: An experimental study in the blackbird (Turdus merula).\" 427 (2008)","DOI":"10.1098\/rspb.2007.1383"},{"key":"4","unstructured":"K. Barton,  \"MuMIn.\"  \"MuMIn: Multi-Model inference. R package version 1.43.15.\" (2019)"},{"key":"6","doi-asserted-by":"crossref","unstructured":"M Beaulieu  and HM Schaefer  \"Anim Behav.\"  86, \"Rethinking the role of dietary antioxidants through the lens of self-medication.\" 17 (2013)","DOI":"10.1016\/j.anbehav.2013.05.022"},{"key":"7","doi-asserted-by":"crossref","unstructured":"K Becker, L Tilley, JL Vennerstrom, et al.  \"Int J Parasitol.\"  34, \"Oxidative stress in malaria parasite-infected erythrocytes: Host\u2013parasite interactions.\" 163 (2004)","DOI":"10.1016\/j.ijpara.2003.09.011"},{"key":"8","doi-asserted-by":"crossref","unstructured":"JA Bell, JD Weckstein, A Fecchio, et al.  \"Parasit Vectors.\"  8, \"A new real-time PCR protocol for detection of avian haemosporidians.\" 383 (2015)","DOI":"10.1186\/s13071-015-0993-0"},{"key":"9","doi-asserted-by":"crossref","unstructured":"WR Brawner, GE Hill, CA Sundermann,  \"Auk.\"  117, \"Effects of coccidial and mycoplasmal infections on carotenoid-based plumage pigmentation in male house finches.\" 952 (2000)","DOI":"10.1093\/auk\/117.4.952"},{"key":"10","unstructured":"KP Burnham  and DR Anderson  \"Model selection and inference: A practical information-theoretic approach.\"  515 (2002)"},{"key":"12","doi-asserted-by":"crossref","unstructured":"C Catoni, B Metzger, HM Schaefer, et al.  \"J Ornithol.\"  152, \"Garden warbler, Sylvia borin, detect carotenoids in food but differ strongly in individual food choice.\" 153 (2011)","DOI":"10.1007\/s10336-010-0560-6"},{"key":"13","doi-asserted-by":"crossref","unstructured":"WS Chang, JS Eden, J Hall, et al.  \"J Virol.\"  94, \"Metatranscriptomic analysis of virus diversity in urban wild birds with paretic disease.\" e00606 (2020)","DOI":"10.1128\/JVI.00606-20"},{"key":"14","doi-asserted-by":"crossref","unstructured":"NM Che-Ajuyo, B Liu, Z Deng, et al.  \"Parasitol Int.\"  93, \"Sex-biased, but not plumage color-based, prevalence of haemosporidian parasites in free-range chickens.\" 102722 (2023)","DOI":"10.1016\/j.parint.2022.102722"},{"key":"16","unstructured":"P Clark, W Boardman, S Raidal,  \"Atlas of clinical avian hematology.\"  184 (2009)"},{"key":"17","doi-asserted-by":"crossref","unstructured":"GL Colnago, LS Jensen, PL Long,  \"Poult Sci.\"  63, \"Effect of selenium and vitamin E on the development of immunity to coccidiosis in chickens.\" 1136 (1984)","DOI":"10.3382\/ps.0631136"},{"key":"18","doi-asserted-by":"crossref","unstructured":"AJ Cowieson, ML Livingston, B Nogal, et al.  \"Poult Sci.\"  99, \"Effect of coccidial challenge and vaccination on the performance, veterinary postmortem scores, and blood biochemistry of broiler chickens.\" 3831 (2020)","DOI":"10.1016\/j.psj.2020.05.018"},{"key":"19","doi-asserted-by":"crossref","unstructured":"RL Cromie, MJ Brown, DJ Price, et al.  \"Tubercle.\"  72, \"Susceptibility of captive wildfowl to avian tuberculosis: The importance of genetic and environmental factors.\" 105 (1991)","DOI":"10.1016\/0041-3879(91)90036-R"},{"key":"20","doi-asserted-by":"crossref","unstructured":"ICM da Silva, AML Ribeiro, CW Canal, et al.  \"Rev Bras Cienc Avi.\"  13, \"Effect of vitamin E levels on the cell-mediated immunity of broilers vaccinated against coccidiosis.\" 53 (2011)","DOI":"10.1590\/S1516-635X2011000100008"},{"key":"21","doi-asserted-by":"crossref","unstructured":"AK Davis, KC Cook, S Altizer,  \"Ecohealth.\"  1, \"Leukocyte profiles in wild house finches with and without mycoplasmal conjunctivitis, a recently emerged bacterial disease.\" 362 (2004)","DOI":"10.1007\/s10393-004-0134-2"},{"key":"22","doi-asserted-by":"crossref","unstructured":"AK Davis, WR Hood, GE Hill,  \"Ecohealth.\"  10, \"Prevalence of blood parasites in eastern versus western house finches: Are eastern birds resistant to infection?\" 290 (2013)","DOI":"10.1007\/s10393-013-0852-4"},{"key":"23","doi-asserted-by":"crossref","unstructured":"JR Dawson, WB Stone, GD Ebel, et al.  \"Emerg Infect Dis.\"  13, \"Crow deaths caused by West Nile virus during winter.\" 1912 (2007)","DOI":"10.3201\/eid1312.070413"},{"key":"24","doi-asserted-by":"crossref","unstructured":"GM De La Torre, FF Freitas, RDO Fratoni, et al.  \"Ethol Ecol Evol.\"  32, \"Hemoparasites and their relation to body condition and plumage coloration of the white-necked thrush (Turdus albicollis).\" 509 (2020)","DOI":"10.1080\/03949370.2020.1769739"},{"key":"25","doi-asserted-by":"crossref","unstructured":"J Delhaye, O Glaizot, P Christe,  \"Parasitol Res.\"  117, \"The effect of dietary antioxidant supplementation in a vertebrate host on the infection dynamics and transmission of avian malaria to the vector.\" 2043 (2018a)","DOI":"10.1007\/s00436-018-5869-8"},{"key":"26","doi-asserted-by":"crossref","unstructured":"J Delhaye, T Jenkins, O Glaizot, et al.  \"Malar J.\"  17, \"Avian malaria and bird humoral immune response.\" 77 (2018b)","DOI":"10.1186\/s12936-018-2219-3"},{"key":"27","doi-asserted-by":"crossref","unstructured":"KN DePinto  and KJ McGraw  \"J Ornithol.\"  163, \"Back to the future: Does previously grown ornamental colouration in male house finches reveal mate quality at the time of pair formation?\" 977 (2022)","DOI":"10.1007\/s10336-022-01997-y"},{"key":"28","doi-asserted-by":"crossref","unstructured":"LR Dougherty, F Rovenolt, A Luyet, et al.  \"Evol Lett.\"  7, \"Ornaments indicate parasite load only if they are dynamic or parasites are contagious.\" 176 (2023)","DOI":"10.1093\/evlett\/qrad017"},{"key":"29","doi-asserted-by":"crossref","unstructured":"FJ Duffy, EG Thompson, TJ Scriba, et al.  \"PLoS One.\"  14, \"Multinomial modelling of TB\/HIV co-infection yields a robust predictive signature and generates hypotheses about the HIV+TB+ disease state.\" e0219322 (2019)","DOI":"10.1371\/journal.pone.0219322"},{"key":"30","doi-asserted-by":"crossref","unstructured":"DW Duszynski  and SJ Upton  \"Parasitic diseases of wild mammals.\"  \"Cyclospora, imeria, Isospora, and Cryptosporidium spp.\" 416 (2001)","DOI":"10.1002\/9780470377000.ch16c"},{"key":"31","doi-asserted-by":"crossref","unstructured":"J Figuerola, G L\u00f3pez, R Soriguer,  \"Front Ecol Evol.\"  2, \"Plasma carotenoid levels in passerines are related to infection by (some) parasites.\" 47 (2014)","DOI":"10.3389\/fevo.2014.00047"},{"key":"32","doi-asserted-by":"crossref","unstructured":"PS Fitze, B Tschirren, J Gasparini, et al.  \"Am Nat.\"  169, \"Carotenoid-based plumage colors and immune function: Is there a trade-off for rare carotenoids?\" S137 (2007)","DOI":"10.1086\/510094"},{"key":"34","doi-asserted-by":"crossref","unstructured":"DM Hawley, SC Moyers, J Caceres, et al.  \"Avian Pathol.\"  47, \"Characterization of unilateral conjunctival inoculation with Mycoplasma gallisepticum in house finches.\" 526 (2018)","DOI":"10.1080\/03079457.2018.1495312"},{"key":"36","doi-asserted-by":"crossref","unstructured":"AE Henschen, LA Whittingham, PO Dunn,  \"Funct Ecol.\"  32, \"Male stress response is related to ornamentation but not resistance to oxidative stress in a warbler.\" 1810 (2018)","DOI":"10.1111\/1365-2435.13104"},{"key":"37","doi-asserted-by":"crossref","unstructured":"CM Hepp, JH Cocking, M Valentine, et al.  \"PLoS One.\"  13, \"Phylogenetic analysis of West Nile Virus in Maricopa County, Arizona: Evidence for dynamic behavior of strains in two major lineages in the American Southwest.\" e0205801 (2018)","DOI":"10.1371\/journal.pone.0205801"},{"key":"39","doi-asserted-by":"crossref","unstructured":"GE Hill, CY Inouye, R Montgomerie,  \"Proc R Soc B Biol Sci.\"  269, \"Dietary carotenoids predict plumage coloration in wild House Finches.\" 1119 (2002)","DOI":"10.1098\/rspb.2002.1980"},{"key":"41","doi-asserted-by":"crossref","unstructured":"AK Howell, SC Tongue, C Currie, et al.  \"Prev Vet Med.\"  150, \"Co-infection with Fasciola hepatica may increase the risk of Escherichia coli O157 shedding in British cattle destined for the food chain.\" 70 (2018)","DOI":"10.1016\/j.prevetmed.2017.12.007"},{"key":"42","doi-asserted-by":"crossref","unstructured":"KA Huggins, KJ Navara, MT Mendon\u00e7a, et al.  \"Naturwissenschaften.\"  97, \"Detrimental effects of carotenoid pigments: The dark side of bright coloration.\" 637 (2010)","DOI":"10.1007\/s00114-010-0679-6"},{"key":"43","doi-asserted-by":"crossref","unstructured":"E Ketema  and N Fasil  \"J Dairy Vet Sci.\"  11, \"Study on prevalence and associated risk factors of poultry coccidiosis in and around Alage at vet College, Southwestern Ethiopia.\" 555805 (2019)","DOI":"10.19080\/JDVS.2019.11.555805"},{"key":"44","doi-asserted-by":"crossref","unstructured":"N Komar, NA Panella, GR Young, et al.  \"J Am Mosq Control Assoc.\"  31, \"Methods for detection of West Nile virus antibodies in mosquito blood meals.\" 1 (2015)","DOI":"10.2987\/14-6468R.1"},{"key":"45","doi-asserted-by":"crossref","unstructured":"JR Lawal, SM Jajere, UI Ibrahim, et al.  \"Vet World.\"  9, \"Prevalence of coccidiosis among village and exotic breed of chickens in Maiduguri, Nigeria.\" 653 (2016)","DOI":"10.14202\/vetworld.2016.653-659"},{"key":"46","doi-asserted-by":"crossref","unstructured":"J Lello, SJ McClure, K Tyrrell, et al.  \"Proc R Soc B Biol Sci.\"  285, \"Predicting the effects of parasite co-infection across species boundaries.\" 20172610 (2018)","DOI":"10.1098\/rspb.2017.2610"},{"key":"48","doi-asserted-by":"crossref","unstructured":"GA. Lozano,  \"Adv Study Behav.\"  27, \"Parasitic stress and self-medication in wild animals.\" 291 (1998)","DOI":"10.1016\/S0065-3454(08)60367-8"},{"key":"49","doi-asserted-by":"crossref","unstructured":"NA. Mabbott,  \"Front Immunol.\"  9, \"The influence of parasite infections on host immunity to co-infection with other pathogens.\" 2579 (2018)","DOI":"10.3389\/fimmu.2018.02579"},{"key":"50","doi-asserted-by":"crossref","unstructured":"A Marzal, M Reviriego, F de Lope, et al.  \"Behav Ecol Sociobiol.\"  61, \"Fitness costs of an immune response in the house martin (Delichon urbica).\" 1573 (2007)","DOI":"10.1007\/s00265-007-0389-z"},{"key":"51","doi-asserted-by":"crossref","unstructured":"KJ McGraw, V Aguiar de Souza Penha, DJ Drake, et al.  \"Transboundary Emerg Dis.\"  69, \"Poxvirus infection in house finches (Haemorhous mexicanus): Genome sequence analysis and patterns of infection in wild birds.\" e2318 (2022)","DOI":"10.1111\/tbed.14575"},{"key":"52","doi-asserted-by":"crossref","unstructured":"KJ McGraw  and DR Ardia  \"Am Nat.\"  162, \"Carotenoids, immunocompetence, and the information content of sexual colors: An experimental test.\" 704 (2003)","DOI":"10.1086\/378904"},{"key":"53","doi-asserted-by":"crossref","unstructured":"KJ McGraw, MD Beebee, GE Hill, et al.  \"Comp Biochem Physiol B Biochem Mol Biol.\"  135, \"Lutein-based plumage coloration in songbirds is a consequence of selective pigment incorporation into feathers.\" 689 (2003)","DOI":"10.1016\/S1096-4959(03)00164-7"},{"key":"54","doi-asserted-by":"crossref","unstructured":"KJ McGraw, K Chou, A Bridge, et al.  \"J Exp Zool A Ecol Integr Physiol.\"  333, \"Body condition and poxvirus infection predict circulating glucose levels in a colorful songbird that inhabits urban and rural environments.\" 561 (2020)","DOI":"10.1002\/jez.2391"},{"key":"55","doi-asserted-by":"crossref","unstructured":"KJ McGraw, M Giraudeau, GE Hill, et al.  \"Arch Biochem Biophys.\"  539, \"Ketocarotenoid circulation, but not retinal carotenoid accumulation, is linked to eye disease status in a wild songbird.\" 156 (2013)","DOI":"10.1016\/j.abb.2013.09.015"},{"key":"56","doi-asserted-by":"crossref","unstructured":"KJ McGraw  and GE Hill  \"Proc R Soc B Biol Sci.\"  267, \"Differential effects of endoparasitism on the expression of carotenoid- and melanin-based ornamental coloration.\" 1525 (2000)","DOI":"10.1098\/rspb.2000.1174"},{"key":"57","doi-asserted-by":"crossref","unstructured":"KJ McGraw  and MB Toomey  \"Physiol Biochem Zool.\"  83, \"Carotenoid accumulation in the tissues of zebra finches: Predictors of integumentary pigmentation and implications for carotenoid allocation strategies.\" 97 (2010)","DOI":"10.1086\/648396"},{"key":"58","doi-asserted-by":"crossref","unstructured":"KJ McGraw, EA Tourville, MW Butler,  \"Behav Ecol Sociobiol.\"  62, \"A quantitative comparison of the commonly used methods for extracting carotenoids from avian plasma.\" 1991 (2008)","DOI":"10.1007\/s00265-008-0622-4"},{"key":"59","doi-asserted-by":"crossref","unstructured":"MCI Medeiros, TK Anderson, JM Higashiguchi, et al.  \"Parasit Vectors.\"  7, \"An inverse association between West Nile virus serostatus and avian malaria infection status.\" 415 (2014)","DOI":"10.1186\/1756-3305-7-415"},{"key":"60","doi-asserted-by":"crossref","unstructured":"S Merino, AP M\u00f8ller, F de Lope,  \"Oikos.\"  90, \"Seasonal changes in cell-mediated immunocompetence and mass gain in nestling barn swallows: A parasite-mediated effect?\" 327 (2000)","DOI":"10.1034\/j.1600-0706.2000.900213.x"},{"key":"61","doi-asserted-by":"crossref","unstructured":"C Mesa-Pineda, JL Navarro-Ru\u00edz, S L\u00f3pez-Osorio, et al.  \"Front Vet Sci.\"  8, \"Chicken coccidiosis: From the parasite lifecycle to control of the disease.\" 787653 (2021)","DOI":"10.3389\/fvets.2021.787653"},{"key":"62","doi-asserted-by":"crossref","unstructured":"S Musa, U Mackenstedt, F Woog, et al.  \"Parasitol Res.\"  121, \"Untangling the actual infection status: Detection of avian haemosporidian parasites of three Malagasy bird species using microscopy, multiplex PCR, and nested PCR methods.\" 2817 (2022)","DOI":"10.1007\/s00436-022-07606-4"},{"key":"63","doi-asserted-by":"crossref","unstructured":"KJ Navara  and GE Hill  \"Behav Ecol.\"  14, \"Dietary carotenoid pigments and immune function in a songbird with extensive carotenoid-based plumage coloration.\" 909 (2003)","DOI":"10.1093\/beheco\/arg085"},{"key":"64","doi-asserted-by":"crossref","unstructured":"SD. Ola-Fadunsin,  \"J Parasitol Res.\"  2017, \"Investigations on the occurrence and associated risk factors of avian coccidiosis in Osun State, Southwestern Nigeria.\" 9264191 (2017)","DOI":"10.1155\/2017\/9264191"},{"key":"65","doi-asserted-by":"crossref","unstructured":"S Opoku Afriyie, TK Addison, Y Gebre, et al.  \"Malar J.\"  22, \"Accuracy of diagnosis among clinical malaria patients: Comparing microscopy, RDT and a highly sensitive quantitative PCR looking at the implications for submicroscopic infections.\" 76 (2023)","DOI":"10.1186\/s12936-023-04506-5"},{"key":"66","doi-asserted-by":"crossref","unstructured":"DV. Parums,  \"Med Sci Monit.\"  29, \"Editorial: Global surveillance of highly pathogenic avian influenza viruses in poultry, wild birds, and mammals to prevent a human influenza pandemic.\" e939968 (2023)","DOI":"10.12659\/MSM.939968"},{"key":"68","doi-asserted-by":"crossref","unstructured":"SL. Perkins,  \"J Parasitol.\"  100, \"Malaria's many mates: Past, present, and future of the systematics of the order Haemosporida.\" 11 (2014)","DOI":"10.1645\/13-362.1"},{"key":"71","doi-asserted-by":"crossref","unstructured":"N Rajput, M Naeem, S Ali, et al.  \"Poult Sci.\"  92, \"The effect of dietary supplementation with the natural carotenoids curcumin and lutein on broiler pigmentation and immunity.\" 1177 (2013)","DOI":"10.3382\/ps.2012-02853"},{"key":"72","doi-asserted-by":"crossref","unstructured":"MT Reinoso-P\u00e9rez, JC Canales-Delgadillo, L Chapa-Vargas, et al.  \"Parasit Vectors.\"  9, \"Haemosporidian parasite prevalence, parasitemia, and diversity in three resident bird species at a shrubland-dominated landscape of the Mexican highland plateau.\" 307 (2016)","DOI":"10.1186\/s13071-016-1569-3"},{"key":"74","doi-asserted-by":"crossref","unstructured":"RA Rodrigues, RL Massara, LL Bailey, et al.  \"Sci Rep.\"  10, \"Using a multistate occupancy approach to determine molecular diagnostic accuracy and factors affecting avian haemosporidian infections.\" 8480 (2020)","DOI":"10.1038\/s41598-020-65523-x"},{"key":"75","doi-asserted-by":"crossref","unstructured":"MD Rodriguez, PF Doherty, AJ Piaggio, et al.  \"Parasit Vectors.\"  14, \"Sex and nest type influence avian blood parasite prevalence in a high-elevation bird community.\" 145 (2021)","DOI":"10.1186\/s13071-021-04612-w"},{"key":"76","doi-asserted-by":"crossref","unstructured":"MA Roselli, SM Cady, S Lao, et al.  \"J Med Entomol.\"  57, \"Variation in tick load among bird body parts: Implications for studying the role of birds in the ecology and epidemiology of tick-borne diseases.\" 845 (2020)","DOI":"10.1093\/jme\/tjz228"},{"key":"77","doi-asserted-by":"crossref","unstructured":"D Santiago-Alarcon, V Palinauskas, HM Schaefer,  \"Biol Rev.\"  87, \"Diptera vectors of avian Haemosporidian parasites: Untangling parasite life cycles and their taxonomy.\" 928 (2012)","DOI":"10.1111\/j.1469-185X.2012.00234.x"},{"key":"78","doi-asserted-by":"crossref","unstructured":"A Sanz-Aguilar, A Payo-Payo, A Rotger, et al.  \"Ticks Tick Borne Dis.\"  11, \"Infestation of small seabirds by Ornithodoros maritimus ticks: Effects on chick body condition, reproduction and associated infectious agents.\" 101281 (2020)","DOI":"10.1016\/j.ttbdis.2019.101281"},{"key":"79","doi-asserted-by":"crossref","unstructured":"L Schaper, P Hutton, KJ McGraw,  \"Sci Rep.\"  11, \"Bird-feeder cleaning lowers disease severity in rural but not urban birds.\" 12835 (2021)","DOI":"10.1038\/s41598-021-92117-y"},{"key":"80","doi-asserted-by":"crossref","unstructured":"F Sebaio, \u00c9M Braga, F Branquinho, et al.  \"Rev Bras Parasitol Vet.\"  21, \"Blood parasites in passerine birds from the Brazilian Atlantic Forest.\" 7 (2012)","DOI":"10.1590\/S1984-29612012000100003"},{"key":"81","doi-asserted-by":"crossref","unstructured":"JC Senar, AP M\u00f8ller, I Ruiz, et al.  \"PLoS One.\"  5, \"Specific appetite for carotenoids in a colorful bird.\" e10716 (2010)","DOI":"10.1371\/journal.pone.0010716"},{"key":"82","doi-asserted-by":"crossref","unstructured":"SM Subtain, S Manzoor, FM Khan, et al.  \"J Antivir Antiretrovir.\"  8, \"Study on coinfection of Mycoplasma gallisepticum and low pathogenic avian influenza virus H9 in broilers.\" 95 (2016)","DOI":"10.4172\/jaa.1000142"},{"key":"83","doi-asserted-by":"crossref","unstructured":"AR Sweeny, GF Albery, DJ Becker, et al.  \"J Anim Ecol.\"  90, \"Synzootics.\" 2744 (2021)","DOI":"10.1111\/1365-2656.13595"},{"key":"84","doi-asserted-by":"crossref","unstructured":"BE Sykes, P Hutton, KJ McGraw,  \"Curr Zool.\"  67, \"Sex-specific relationships between urbanization, parasitism, and plumage coloration in house finches.\" 237 (2021)","DOI":"10.1093\/cz\/zoaa060"},{"key":"86","doi-asserted-by":"crossref","unstructured":"CW Thompson, N Hillgarth, M Leu, et al.  \"Am Nat.\"  149, \"High parasite load in house finches (Carpodacus mexicanus) is correlated with reduced expression of a sexually selected trait.\" 270 (1997)","DOI":"10.1086\/285990"},{"key":"87","unstructured":"TN Tully, GM Dorrestein, AK Jones,  \"Handbook of avian medicine.\"  496 (2009)"},{"key":"88","doi-asserted-by":"crossref","unstructured":"JO Valdebenito, A Liker, N Halimubieke, et al.  \"Sci Rep.\"  10, \"Mortality cost of sex-specific parasitism in wild bird populations.\" 20983 (2020)","DOI":"10.1038\/s41598-020-77410-6"},{"key":"93","doi-asserted-by":"crossref","unstructured":"BR Vogler, K Zurfluh, P Mattmann, et al.  \"Vet Rec Open.\"  8, \"Low occurrence of Salmonella spp. in wild birds from a Swiss rehabilitation centre.\" e17 (2021)","DOI":"10.1002\/vro2.17"},{"key":"94","doi-asserted-by":"crossref","unstructured":"T von Schantz, S Bensch, M Grahn, et al.  \"Proc Biol Sci.\"  266, \"Good genes, oxidative stress and condition-dependent sexual signals.\" 1 (1999)","DOI":"10.1098\/rspb.1999.0597"},{"key":"96","doi-asserted-by":"crossref","unstructured":"F Watzinger, K Ebner, T Lion,  \"Mol Aspects Med.\"  27, \"Detection and monitoring of virus infections by real-time PCR.\" 254 (2006)","DOI":"10.1016\/j.mam.2005.12.001"},{"key":"97","doi-asserted-by":"crossref","unstructured":"CL Weitzman, C Thomason, EJA Schuler, et al.  \"Parasitol Res.\"  119, \"House finches with high coccidia burdens experience more severe experimental Mycoplasma gallisepticum infections.\" 3535 (2020)","DOI":"10.1007\/s00436-020-06814-0"},{"key":"98","doi-asserted-by":"crossref","unstructured":"GA. Wobeser,  \"Parasitic diseases of wild birds.\"  \"Parasitism: Costs and effects.\" 3 (2009)","DOI":"10.1002\/9780813804620.ch1"},{"key":"99","doi-asserted-by":"crossref","unstructured":"VP Wuerthner, J Hua, JT Hoverman,  \"J Anim Ecol.\"  86, \"The benefits of coinfection: Trematodes alter disease outcomes associated with virus infection.\" 921 (2017)","DOI":"10.1111\/1365-2656.12665"},{"key":"100","doi-asserted-by":"crossref","unstructured":"Y. Yamamoto,  \"Clin Vaccine Immunol.\"  9, \"PCR in diagnosis of infection: Detection of bacteria in cerebrospinal fluids.\" 508 (2002)","DOI":"10.1128\/CDLI.9.3.508-514.2002"},{"key":"101","doi-asserted-by":"crossref","unstructured":"CH Yun, HS Lillehoj, EP Lillehoj,  \"Dev Comp Immunol.\"  24, \"Intestinal immune responses to coccidiosis.\" 303 (2000)","DOI":"10.1016\/S0145-305X(99)00080-4"},{"key":"102","unstructured":"A Zahavi  and A Zahavi  \"The handicap principle: A missing piece of Darwin's puzzle.\"  304 (1999)"},{"key":"85","doi-asserted-by":"crossref","unstructured":"S Telfer, X Lambin, R Birtles, et al.  \"Science.\"  330, \"Species interactions in a parasite community drive infection risk in a wildlife population.\" 243 (2010)","DOI":"10.1126\/science.1190333"},{"key":"91","doi-asserted-by":"crossref","unstructured":"WN Venables  and BD Ripley  \"Modern applied statistics with S.\"  (2002)","DOI":"10.1007\/978-0-387-21706-2"}],"container-title":["Journal of Wildlife Diseases"],"original-title":[],"deposited":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T00:29:14Z","timestamp":1791246554000},"score":1,"resource":{"primary":{"URL":"https:\/\/bioone.org\/journals\/journal-of-wildlife-diseases\/volume-60\/issue-3\/JWD-D-23-00175\/CORRELATES-OF-CO-INFECTION-WITH-COCCIDIOSIS-AND-AVIAN-MALARIA-IN\/10.7589\/JWD-D-23-00175.full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,7,8]]},"references-count":102,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2024,7,1]]}},"URL":"https:\/\/doi.org\/10.7589\/jwd-d-23-00175","relation":{},"ISSN":["0090-3558","1943-3700"],"issn-type":[{"value":"0090-3558","type":"print"},{"value":"1943-3700","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,7,8]]}}}