Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-19T22:48:38.325Z Has data issue: false hasContentIssue false
  • English
  • Français

High susceptibility of the laboratory-reared biting midges Culicoides nubeculosus to Haemoproteus infections, with review on Culicoides species that transmit avian haemoproteids

Published online by Cambridge University Press:  04 September 2018

Dovilė Bukauskaitė Open the ORCID record for Dovilė Bukauskaitė [Opens in a new window] ,
Tatjana A. Iezhova ,
Mikas Ilgūnas  and
Gediminas Valkiūnas
Dovilė Bukauskaitė*
Affiliation:
Institute of Ecology, Nature Research Centre, Akademijos 2, Vilnius 21, LT-09412, Lithuania
Tatjana A. Iezhova
Affiliation:
Institute of Ecology, Nature Research Centre, Akademijos 2, Vilnius 21, LT-09412, Lithuania
Mikas Ilgūnas
Affiliation:
Institute of Ecology, Nature Research Centre, Akademijos 2, Vilnius 21, LT-09412, Lithuania
Gediminas Valkiūnas
Affiliation:
Institute of Ecology, Nature Research Centre, Akademijos 2, Vilnius 21, LT-09412, Lithuania
*
Author for correspondence: Dovilė Bukauskaitė, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Haemosporidian parasites belonging to Haemoproteus cause avian diseases, however, vectors remain unidentified for the majority of described species. We used the laboratory-reared biting midges Culicoides nubeculosus to determine if the sporogonic development of three widespread Haemoproteus parasites completes in this insect. The midges were reared and fed on one common blackbird, white wagtail and thrush nightingale naturally infected with Haemoproteus minutus, Haemoproteus motacillae and Haemoproteus attenuatus, respectively. The engorged females were dissected in order to follow their sporogonic development. Microscopic examination was used to identify sporogonic stages. Bayesian phylogeny based on partial cytochrome b gene was constructed in order to determine phylogenetic relationships among Culicoides species-transmitted haemoproteids. All three parasites completed sporogony. Phylogenetic analysis placed Culicoides species transmitted haemoproteids in one well-supported clade, proving that such analysis readily indicates groups of dipteran insects transmitting avian haemoproteids. Available data show that 11 species of Culicoides have been proved to support complete sporogony of 18 species of avian haemoproteids. The majority of Culicoides species can act as vectors for many Haemoproteus parasites, indicating the low specificity of these parasites to biting midges, whose are globally distributed. This calls for control of haemoproteid infections during geographical translocation of infected birds.

Keywords

BirdsCulicoides nubeculosusCulicoides species colonyHaemoproteussporogonyvectors
Type
Research Article
Information
Parasitology , Volume 146 , Issue 3 , March 2019 , pp. 333 - 341
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Atkinson, CT (2008) Haemoproteus. In Atkinson, CT, Thomas, NJ and Hunter, BC (eds), Parasitic Diseases of Wild Birds. Ames, Iowa: Wiley-Blackwell, pp. 13–35.10.1002/9780813804620Google Scholar
Atkinson, CT, Greiner, EC and Forrester, DJ (1983) Experimental vectors of Haemoproteus meleagridis Levine from wild turkeys in Florida. Journal of Wildlife Diseases 19, 366–368.10.7589/0090-3558-19.4.366Google Scholar
Atkinson, CT, Forrester, DJ and Greiner, EC (1988) Pathogenicity of Haemoproteus meleagridis (Haemosporina: Haemoproteidae) in experimentally infected domestic turkeys. Journal of Parasitology 74, 228–239.10.2307/3282448Google Scholar
Belo, NO, Pinheiro, RT, Reis, ES, Ricklefs, RE and Braga, EM (2011) Prevalence and lineage diversity of avian haemosporidians from three distinct cerrado habitats in Brazil. PLos ONE 6, e17654.10.1371/journal.pone.0017654Google Scholar
Bennett, GF and Fallis, AM (1960) Blood parasites of birds in Algonquin Park, Canada, and a discussion of their transmission. Canadian Journal of Zoology 38, 261–273.10.1139/z60-033Google Scholar
Bensch, S, Stjernman, M, Hasselquist, D, Ostman, O, Hansson, B, Westerdahl, H and Pinheiro, RT (2000) Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proceedings of the Royal Society of London B: Biological Sciences 267, 1583–1589.10.1098/rspb.2000.1181Google Scholar
Bensch, S, Hellgren, O and Pérez-Tris, J (2009) A public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources 9, 1353–1358.10.1111/j.1755-0998.2009.02692.xGoogle Scholar
Bensch, S, Canbäck, B, DeBarry, JD, Johansson, T, Hellgren, O, Kissinger, JC, Palinauskas, V, Videvall, E and Valkiūnas, G (2016) The genome of Haemoproteus tartakovskyi and its relationship to human malaria parasites. Genome Biology and Evolution 8, 1361–1373.10.1093/gbe/evw081Google Scholar
Blackwell, A, Lock, KA, Marshall, B, Boag, B and Gordon, SC (1999) The spatial distribution of larvae of Culicoides impunctatus biting midges. Medical and Veterinary Entomology 13, 362–371.10.1046/j.1365-2915.1999.00180.xGoogle Scholar
Boorman, J (1974) The maintenance of laboratory colonies of Culicoides variipenis (Coq.), C. nubeculosus (mg.) and C. riethi kieff. (Diptera, Ceratopogonidae). Bulletin of Entomological Research 64, 371–377.10.1017/S0007485300031254Google Scholar
Bukauskaitė, D, Žiegytė, R, Palinauskas, V, Iezhova, TA, Dimitrov, D, Ilgūnas, M, Bernotienė, R, Markovets, MY and Valkiūnas, G (2015) Biting midges (Culicoides, Diptera) transmit Haemoproteus parasites of owls: evidence from sporogony and molecular phylogeny. Parasites & Vectors 8, 303.10.1186/s13071-015-0910-6Google Scholar
Bukauskaitė, D, Bernotienė, R, Iezhova, TA and Valkiūnas, G (2016) Mechanisms of mortality in Culicoides biting midges due to Haemoproteus infection. Parasitology 143, 1748–1754.10.1017/S0031182016001426Google Scholar
Cannell, BL, Krasnec, KV, Campbell, K, Jones, HI, Miller, RD and Stephens, N (2013) The pathology and pathogenicity of a novel Haemoproteus spp. Infection in wild Little Penguins (Eudyptula minor). Veterinary Parasitology 197, 74–84.10.1016/j.vetpar.2013.04.025Google Scholar
Cardona, CJ, Ihejirika, A and McClellan, L (2002) Haemoproteus lophortyx infection in bobwhite quail. Avian Diseases 46, 249–255.10.1637/0005-2086(2002)046[0249:HLIIBQ]2.0.CO;2Google Scholar
Carlson, JS, Martínez-Gómez, JE, Valkiūnas, G, Loiseau, C, Bell, DG and Seghal, RNM (2013) Diversity and phylogenetic relationships of haemosporidian parasites in birds of Socorro island, Mexico, and their role in the re-introduction of the Socorro dove (Zenaida graysoni). Journal of Parasitology 99, 270–276.10.1645/GE-3206.1Google Scholar
Dimitrov, D, Zehtindjiev, P and Bensch, S (2010) Genetic diversity of avian blood parasites in SE Europe: cytochrome b lineages of the genera Plasmodium and Haemoproteus (haemosporida) from Bulgaria. Acta Parasitologica 55, 201–209.10.2478/s11686-010-0029-zGoogle Scholar
Donovan, TA, Schrenzel, M, Tucker, TA, Pessier, AP and Stalis, IH (2008) Hepatic haemorrhage, hemocoelom, and sudden death due to Haemoproteus infection in passerine birds: eleven cases. Journal of Veterinary Diagnostics Investigation 20, 304–313.10.1177/104063870802000307Google Scholar
Fallis, AM and Bennett, GF (1960) Description of Haemoproteus canachites n. sp. (Sporozoa: Haemoproteidae) and sporogony in Culicoides (diptera: Ceratopogonidae). Canadian Journal of Zoology 38, 455–464.10.1139/z60-049Google Scholar
Fallis, AM and Bennett, GF (1961) Sporogony of Leucocytozoon and Haemoproteus in simuliids and ceratopogonids and revised classification of the Haemosporidiida. Canadian Journal of Zoology 39, 215–228.10.1139/z61-026Google Scholar
Fallis, AM and Wood, DM (1957) Biting midges (Diptera: Ceratopogonidae) as intermediate hosts for Haemoproteus of ducks. Canadian Journal of Zoology 35, 425–435.10.1139/z57-033Google Scholar
Ferraguti, M, Puente, JM, Ruiz, S, Soriguer, R and Figuerola, J (2013) On the study of the transmission networks of blood parasites from SW Spain: diversity of avian haemosporidians in the biting midge Culicoides circumscriptus and wild birds. Parasites & Vectors 6, 208.10.1186/1756-3305-6-208Google Scholar
Garnham, PCC (1966) Malaria Parasites and Other Haemosporidia. Oxford, UK: Blackwell Scientific Publications.Google Scholar
Garvin, MC and Greiner, EC (2003) Ecology of Culicoides (diptera: Ceratopogonidae) in southcentral Florida and experimental Culicoides vectors of the avian Hematozoan Haemoproteus danilewskyi Kruse. Journal of Wildlife Diseases 39, 170–178.10.7589/0090-3558-39.1.170Google Scholar
Garvin, MC, Homer, BL and Greiner, EC (2003) Pathogenicity of Haemoproteus danilewskyi, Kruse, 1890, in blue jays (Cyanocitta cristata). Journal of Wildlife Diseases 39, 161–169.10.7589/0090-3558-39.1.161Google Scholar
Glukhova, VM and Valkiūnas, G (1993) On the fauna and ecology of biting midges (Ceratopogonidae: Culicoides) in the Curonian spit, the methods of their collection from the birds and experimental infection with haemoproteids (Haemosporidia: Haemoproteidae). Ekologija 2, 68–73.Google Scholar
Hall, TA (1999) A user-friendly biological sequence alignment editor and analysis program for Windows 98/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hall, N, Karras, M, Raine, JD, Carlton, JM, Kooij, TW, Berriman, M, Florens, L, Janssen, CS, Pain, A, Christophides, GK, James, K, Rutherford, K, Harris, B, Harris, D, Churcher, C, Quail, MA, Ormond, D, Doggett, J, Trueman, HE, Mendoza, J, Bidwell, SL, Rajandream, MA, Carucci, DJ, Yates, JR 3rd, Kafatos, FC, Janse, CJ, Barrell, B, Turner, CM, Waters, AP and Sinden, RE (2005) A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307, 82–86.10.1126/science.1103717Google Scholar
Hellgren, O, Waldenström, J and Bensch, S (2004) A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium and Haemoproteus from avian blood. Journal of Parasitology 90, 797–802.10.1645/GE-184R1Google Scholar
Hino, A, Hirai, M, Tanaka, TQ, Watanabe, Y, Matsuoka, H and Kita, K (2012) Critical roles of the mitochondrial complex II in oocyst formation of rodent malaria parasite Plasmodium berghei. The Journal of Biochemistry 152, 259–268.10.1093/jb/mvs058Google Scholar
Ishtiaq, F, Gering, E, Rappole, JH, Rahmani, AR, Jhala, YV, Dove, CJ, Milensky, C, Olson, SL, Peirce, MA and Fleischer, RC (2007) Prevalence and diversity of avian hematozoan parasites in Asia: a regional survey. Journal of Wildlife Diseases 43, 382–398.10.7589/0090-3558-43.3.382Google Scholar
Ishtiaq, F, Guillaumot, L, Clegg, SM, Phillimore, AB, Black, RA, Owens, IPF, Mundy, NI and Sheldon, BC (2008) Avian haematozoan parasites and their associations with mosquitoes across Southwest Pacific Islands. Molecular Ecology 17, 4545–4555.10.1111/j.1365-294X.2008.03935.xGoogle Scholar
Ivanova, K, Zehtindjiev, P, Mariaux, J and Georgiev, BB (2015) Genetic diversity of avian haemosporidians in Malaysia: cytochrome b lineages of the genera Plasmodium and Haemoproteus (haemosporida) from Selangor. Infection, Genetics and Evolution 31, 33–39.10.1016/j.meegid.2015.01.004Google Scholar
Jacot, D, Waller, RF, Soldati-Favre, D, MacPherson, DA and MacRae, JI (2016) Apicomplexan energy metabolism: carbon source promiscuity and the quiescence hyperbole. Trends in Parasitology 32, 56–70.10.1016/j.pt.2015.09.001Google Scholar
Jennings, DM and Mellor, PS (1988) The vector potential of British Culicoides species for bluetongue virus. Veterinary Microbiology 17, 1e10.10.1016/0378-1135(88)90074-0Google Scholar
Khan, RA and Fallis, AM (1971) A note on the sporogony of Parahaemoproteus velans (=Haemoproteus velans Coatney and Roudabush) (Haemosporidia: Haemoproteidae) in species of Culicoides. Canadian Journal of Zoology 49, 420.10.1139/z71-062Google Scholar
Latta, SC and Ricklefs, RE (2010) Prevalence patterns of avian haemosporida on Hispaniola. Journal of Avian Biology 41, 25–33.10.1111/j.1600-048X.2009.04685.xGoogle Scholar
Levin, II, Valkiūnas, G, Iezhova, TA, O'brien, SL and Parker, PG (2012) Novel Haemoproteus species (Haemosporida: Haemoproteidae) from the swallow-tailed gull (Lariidae), with remarks on the host range of hippoboscid-transmitted avian hemoproteids. Journal of Parasitology 98, 847–854.10.1645/GE-3007.1Google Scholar
Liutkevičius, G (2000) The new data on the epidemiology of bird haemoproteids (Haemosporida: Haemoproteidae) on the Curonian spit. Acta Zoologica Lithuania 2, 72–77.10.1080/13921657.2000.10512328Google Scholar
Loiseau, C, Iezhova, TA, Valkiūnas, G, Chasar, A, Hutchinson, A, Buermann, W, Smith, TB and Sehgal, RN (2010) Spatial variation of haemosporidian parasite infection in African rainforest bird species. Journal of Parasitology 96, 21–29.10.1645/GE-2123.1Google Scholar
Martínez-de la Puente, J, Martinez, J, Rivero-de Aguilar, J, Herrero, J and Merino, S (2011) On the specificity of avian blood parasites: revealing specific and generalist relationships between haemosporidians and biting midges. Molecular Ecology 20, 3275–3287.Google Scholar
Martinsen, ES, Perkins, SL and Schall, JJ (2008) A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches. Molecular Phylogenetics and Evolution 47, 261–273.Google Scholar
Mathieu, B, Cêtre-Sossah, C, Garros, C, Chavernac, D, Balenghien, T, Carpenter, S, Setier-Rio, ML, Vignes-Lebbe, R, Ung, V, Candolfi, E and Delécolle, JC (2012) Development and validation of IIKC: an interactive identification key for Culicoides (diptera: Ceratopogonidae) females from the Western Palaearctic region. Parasites & Vectors 5, 137.10.1186/1756-3305-5-137Google Scholar
Miltgen, F, Landau, I, Ratanaworabhan, N and Yenbutra, S (1981) Parahaemoproteus dessert n. sp.; Gamétogonie et Schizogonie chez l'hôte naturel: Psittacula roseata de Thaïlande, et Sporogonie expérimentale chez Culicoides nubeculosus. Annales de Parasitologie Humaine et Compareer 56, 123–130.Google Scholar
Neto, JM, Pérez-Rodríguez, A, Haase, M, Flade, M and Bensch, S (2015) Prevalence and diversity of Plasmodium and Haemoproteus parasites in the globally-threatened Aquatic Warbler Acrocephalus paludicola. Parasitology 142, 1183–1189.Google Scholar
Njabo, KY, Cornel, AJ, Bonneaud, C, Toffelmier, E, Sehgal, RN, Valkiūnas, G, Russell, AF and Smith, TB (2011) Nonspecific patterns of vector, host and avian malaria parasite associations in a central African rainforest. Molecular Ecology 20, 1049–1061.Google Scholar
Olias, P, Wegelin, M, Freter, S, Gruber, AD and Klopfleisch, R (2011) Avian malaria deaths in parrots, Europe. Emerging Infectious Diseases 17, 950–952.Google Scholar
Olsson-Pons, S, Clark, NJ, Ishtiaq, F and Clegg, SM (2015) Differences in host species relationships and biogeographic influences produce contrasting patterns of prevalence, community composition and genetic structure in two genera of avian malaria parasites in southern Melanesia. Journal of Animal Ecology 84, 985–998.Google Scholar
Opitz, HM, Jakob, HJ, Wiensenhuetter, E and Vasandradevi, V (1982) A myopathy associated with protozoan schizonts in chickens in commercial farms in peninsular Malaysia. Avian Pathology 11, 527–534.Google Scholar
Pacheco, MA, Escalante, AA, Garner, MM, Bradley, GA and Aguilar, RF (2011) Haemosporidian infection in captive masked bobwhite quail (Colinus virginianus ridgwayi), an endangered subspecies of the northern bobwhite quail. Veterinary Parasitology 182, 113–120.Google Scholar
Pacheco, MA, Matta, NE, Valkiūnas, G, Parker, PG, Mello, B, Stanley, CE Jr, Lentino, M, Garcia-Amado, MA, Cranfield, M, Kosakovsky Pond, SL and Escalante, AA (2018) Mode and rate of evolution of Haemosporidian mitochondrial genomes: timing the radiation of avian parasites. Molecular Biology and Evolution 35, 383–403.Google Scholar
Pages, N, Bréard, E, Urien, C, Talavera, S, Viarouge, C, Lorca-Oro, C, Jouneau, L, Charley, B, Zientara, S, Bensaid, A, Solanes, D, Pujols, J and Schwartz-Cornil, I (2014) Culicoides midge bites modulate the host response and impact on bluetongue virus infection in sheep. PloS ONE 9, e83683.Google Scholar
Patakakis, MJ, Papazahariadou, M, Wilson, A, Mellor, PS, Frydas, S and Papadopoulos, O (2009) Distribution of Culicoides in Greece. Journal of Vector Ecology 34, 243–251.Google Scholar
Pèrez-Tris, J and Bensch, S (2005) Diagnosing genetically diverse avian malarial infections using mixed-sequence analysis and TA-cloning. Parasitology 131, 15–23.Google Scholar
Posada, D and Crandall, KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics (Oxford, England) 14, 817–818.Google Scholar
Reeves, AB, Smith, MM, Meixell, BW, Fleskes, JP and Ramey, AM (2015) Genetic diversity and host specificity varies across three genera of blood parasites in ducks of the Pacific Americas flyway. PLos ONe 10, e0116661.Google Scholar
Richardson, DS, Jury, FL, Blaakmeer, K, Komdeur, J and Burke, T (2001) Parentage assignment and extra-group paternity in a cooperative breeder: the Seychelles warbler (Acrocephalus sechellensis). Molecular Ecology 10, 2263–2273.Google Scholar
Ronquist, F and Heulsenbeck, JP (2003) Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics (Oxford, England) 19, 1572–1574.Google Scholar
Santiago-Alarcon, D, Outlaw, DC, Ricklefs, RE and Parker, PG (2010) Phylogenetic relationships of haemosporidian parasites in New World Columbiformes, with emphasis on the endemic Galapagos dove. International Journal for Parasitology 40, 463–470.Google Scholar
Santiago-Alarcon, D, Palinauskas, V and Schaefer, HM (2012) Diptera vectors of avian Haemosporidian parasites: untangling parasite life cycles and their taxonomy. Biological Reviews of the Cambridge Philosophical Society 87, 928–964.Google Scholar
Scheuerlein, A and Ricklefs, RE (2004) Prevalence of blood parasites in European passeriform birds. Proceedings of the Royal Society B: Biological Sciences 271, 1363–1370.Google Scholar
Silva-Iturriza, A, Ketmaier, V and Tiedemann, R (2012) Prevalence of avian haemosporidian parasites and their host fidelity in the central Philippine islands. Parasitology International 61, 650–657.Google Scholar
Smith, MM and Ramey, AM (2015) Prevalence and genetic diversity of haematozoa in South American waterfowl and evidence for intercontinental redistribution of parasites by migratory birds. International Journal for Parasitology: Parasites and Wildlife 4, 22–28.Google Scholar
Smith, MM, Van Hemert, C and Merizon, R (2016) Haemosporidian parasite infections in gouse and ptarmigan: prevalence and genetic diversity of blood parasites in resident Alaskan birds. International Journal for Parasitology: Parasites and Wildlife 5, 229–239.Google Scholar
Svobodova, M, Dolnik, OV, Čepička, I and Radrova, J (2017) Biting midges (Ceratopogonidae) as vector of avian trypanosomes. Parasites & Vectors 10, 224.Google Scholar
Szymanski, MM and Lovette, IJ (2005) High lineage diversity and host sharing of malarial parasites in a local avian assemblage. Journal of Parasitology 91, 768–774.Google Scholar
Valkiūnas, G (1997) Bird Haemosporida. Vilnius: Institute of Ecology.Google Scholar
Valkiūnas, G (2005) Avian Malaria Parasites and Other Haemosporidia. Boca Raton, FL, USA: CRC Press.Google Scholar
Valkiūnas, G (2015) Haemoproteus species. In Mehlhorn, H (ed), Encyclopedia of Parasitology. Berlin: Springer, pp. 1–9.Google Scholar
Valkiūnas, G and Iezhova, TA (2004 a) The transmission of Haemoproteus belopolskyi (Haemosporida: Haemoproteidae) of Blackcap by Culicoides impunctatus (Diptera, Ceratopogonidae). Journal of Parasitology 90, 196–198.Google Scholar
Valkiūnas, G and Iezhova, TA (2004 b) Detrimental effects of Haemoproteus infections on the survival of biting midge Culicoides impunctatus (Diptera: Ceratopogonidae). Journal of Parasitology 90, 194–196.Google Scholar
Valkiūnas, G and Iezhova, TA (2017) Exo-erythrocytic development of avian malaria and related haemosporidian parasites. Malaria Journal 16, 101.Google Scholar
Valkiūnas, G, Liutkevičius, G and Iezhova, TA (2002) Complete development of three species of Haemoproteus (haemosporida, Haemoproteidae) in the biting midge Culicoides impunctatus (Diptera, Ceratopogonidae). Journal of Parasitology 88, 864–868.Google Scholar
Valkiūnas, G, Križanauskienė, A, Iezhova, TA, Hellgren, O and Bensch, S (2007) Molecular phylogenetic analysis of circumnuclear hemoproteids (Haemosporida: Haemoproteidae) of sylviid birds, with a description of Haemoproteus parabelopolskyi sp. nov. Journal of Parasitology 93, 680–687.Google Scholar
Valkiūnas, G, Kazlauskienė, R, Bernotienė, R, Palinauskas, V and Iezhova, TA (2013 a) Abortive long-lasting sporogony of two Haemoproteus species (Haemosporida, Haemoproteidae) in the mosquito Ochlerotatus cantans, with perspectives on haemosporidian vector research. Parasitology Research 112, 2159–2169.Google Scholar
Valkiūnas, G, Palinauskas, V, Križanauskienė, A, Bernotienė, R, Kazlauskienė, R and Iezhova, TA (2013 b) Further observations on in vitro hybridization of hemosporidian parasites: patterns of ookinete development in Haemoproteus spp. Journal of Parasitology 1, 124–136.Google Scholar
Yoshimura, A, Koketsu, M, Bando, H, Saiki, E, Suzuki, M, Watanabe, Y, Kanuka, H and Fukumoto, S (2014) Phylogenetic comparison of avian haemosporidian parasites from resident and migratory birds in northern Japan. Journal of Wildlife Diseases 50, 235–242.Google Scholar
Žiegytė, R, Palinauskas, V, Bernotienė, R, Iezhova, TA and Valkiūnas, G (2014) Haemoproteus minutus and Haemoproteus belopolskyi (Haemoproteidae): complete sporogony in the biting midge Culicoides impunctatus (Ceratopogonidae), with implications on epidemiology of haemoproteosis. Experimental Parasitology 145, 74–79.Google Scholar
Žiegytė, R, Bernotienė, R, Palinauskas, V and Valkiūnas, G (2016) Haemoproteus tartakovskyi (haemoproteidae): complete sporogony in Culicoides nubeculosus (Ceratopogonidae), with implications for avian haemoproteid experimental research. Experimental Parasitology 160, 17–22.Google Scholar
Žiegytė, R, Markovets, MYU, Bernotienė, R, Mukhin, A, Iezhova, TA, Valkiūnas, G and Palinauskas, V (2017) The widespread biting midge Culicoides impunctatus (Ceratopogonidae) is susceptible to infection with numerous Haemoproteus (haemoproteidae) species. Parasites & Vectors 10, 397.Google Scholar