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Mechanisms of mortality in Culicoides biting midges due to Haemoproteus infection

Published online by Cambridge University Press:  09 September 2016

DOVILĖ BUKAUSKAITĖ ,
RASA BERNOTIENĖ ,
TATJANA A. IEZHOVA  and
GEDIMINAS VALKIŪNAS
DOVILĖ BUKAUSKAITĖ*
Affiliation:
Institute of Ecology, Nature Research Centre, Akademijos 2, LT-08412 Vilnius, Lithuania
RASA BERNOTIENĖ
Affiliation:
Institute of Ecology, Nature Research Centre, Akademijos 2, LT-08412 Vilnius, Lithuania
TATJANA A. IEZHOVA
Affiliation:
Institute of Ecology, Nature Research Centre, Akademijos 2, LT-08412 Vilnius, Lithuania
GEDIMINAS VALKIŪNAS
Affiliation:
Institute of Ecology, Nature Research Centre, Akademijos 2, LT-08412 Vilnius, Lithuania
*
*Corresponding author: Institute of Ecology, Nature Research Centre, Akademijos 2, LT-08412 Vilnius, Lithuania. E-mail: dovilebu7@gmail.com
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Summary

We examined the effects of Haemoproteus infection on the survival and pathology caused in the biting midges. Forty-six females of Culicoides impunctatus were exposed experimentally by allowing them to feed on a naturally infected red-backed shrike infected with Haemoproteus lanii (lineage hRB1, gametocytaemia 5·2%). Seventeen females were fed on an uninfected bird (controls). Dead insects were collected, counted and used for dissection, histological examination and polymerase chain reaction-based testing. Parasites were present in all experimentally infected biting midges, but absent from control insects. Survivorship differed significantly between the control and infected groups. Twelve hours post-exposure (PE), 45 (98%) experimentally infected midges were dead, but all control midges remained alive, and many of them survived until 7 day PE. The migrating ookinetes of H. lanii overfilled midgut, markedly damaged the midgut wall, entered the haemocoel and overfilled the abdomen and thorax of exposed biting midges. Massive infection by migrating ookinetes led to damage of abdomen and thorax of biting midges. The parasites often present in large clumps in the haemocoel in abdomen and thorax, leading to the interruption of the haemolymph circulation. These are the main reasons for rapid death of biting midges after feeding on high-intensity infections of Haemoproteus parasites.

Keywords

Haemosporidian parasitesHaemoproteusCulicoidesbiting midgesmortalityhistologyookinetes
Type
Research Article
Information
Parasitology , Volume 143 , Issue 13 , November 2016 , pp. 1748 - 1754
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Allison, F. R., Desser, S. S. and Whitten, L. K. (1978). Further observations on the life cycle and vectors of the haemosporidian Leucocytozoon tawaki and its transmission to the Fiordland crested penguin. New Zealand Journal of Zoology 5, 371–374.Google Scholar
Arai, M., Billker, O., Morris, H. R., Panico, M., Delcroix, M., Dixon, D., Ley, S. V. and Sinden, R. E. (2001). Both mosquito-derived xanthurenic acid and a host blood-derived factor regulate gametogenesis of Plasmodium in the midgut of the mosquito. Molecular and Biochemical Parasitology 116, 17–24.Google Scholar
Asghar, M., Hasselquist, D. and Bensch, S. (2011). Are chronic avian haemosporidian infections costly in wild birds? Journal of Avian Biology 42, 530–537.Google Scholar
Atkinson, C. T. (1991). Vectors, epizootiology, and pathogenicity of avian species of Haemoproteus (Haemosporina: Haemoproteidae). Bulletin of the Society for Vector Ecology 16, 109–126.Google Scholar
Atkinson, C. T. (2008). Haemoproteus . In Parasitic Diseases of Wild Birds (ed. Atkinson, C. T., Thomas, N. J. and Hunter, B. C.), pp. 13–34. Wiley-Blackwell, Ames, Iowa.Google Scholar
Bensch, S., Stjernman, M., Hasselquist, D., Ostman, O., Hansson, B., Westerdahl, H. and Pinheiro, R. T. (2000). Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proceedings of the Royal Society London B 267, 1583–1589.CrossRefGoogle ScholarPubMed
Blackwell, A. (1997). Diel flight periodicity of the biting midge Culicoides impunctatus and the effects of meteorological conditions. Medical and Veterinary Entomology 11, 361–367.Google Scholar
Bukauskaitė, D., Žiegytė, R., Palinauskas, V., Iezhova, A. T., Dimitrov, D., Ilgūnas, M., Bernotienė, R., Markovets, M.Yu. and Valkiūnas, G. (2015). Biting midges (Culicoides, Diptera) transmit Haemoproteus parasites of owls: evidence from sporogony and molecular phylogeny. Parasites and Vectors 8, 303.CrossRefGoogle ScholarPubMed
Desser, S. S. and Yang, Y. J. (1973). Sporogony of Leucocytozoon spp. in mammalophilic simuliids. Canadian Journal of Zoology 51, 793.CrossRefGoogle ScholarPubMed
Ferguson, H. M. and Read, A. F. (2002). Why is the effect of malaria parasites on mosquito survival still unresolved? Trends in Parasitology 18, 256–2561.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Garnham, P. C. C. (1966). Malaria Parasites and other Haemosporidia. Blackwell Scientific Publications, Oxford, UK.Google Scholar
Garvin, M. C., Homer, B. L. and Greiner, E. C. (2003). Pathogenicity of Haemoproteus danilevskyi, Kruse, 1890, in blue jays (Cyanocitta cristata). Journal of Wildlife Diseases 39, 161–169.Google Scholar
Glukhova, V. M. (1989). Blood-sucking midges of the genera Culicoides and Forcipomyia (Ceratopogonidae). In Dipteran Insects (ed. Fauna of the USSR), pp. 1–408. Nauka Publishers, Leningrad, (in Russian).Google Scholar
Glukhova, V. M. and Valkiūnas, G. (1993). On the fauna and ecology of biting midges (Ceratopogonidae: Culicoides) in the Kuršių Nerija, the methods of their collection from the birds and experimental infection with Haemoproteids (Haemosporidia: Haemoproteidae). Ekologija 2, 68–73.Google Scholar
Gutsevich, A. V. (1973). The bloodsucking midges (Ceratopogonidae). In Dipteran Insects, vol. 3, part 5 (ed. Fauna of the USSR), pp. 1–270. Nauka Press, Leningrad, USSR, (in Russian).Google Scholar
Hall, T. A. (1999). A user-friendly biological sequence alignment editor and analysis program for Windows 98/98/NT. Nucleic Acid Symposium Series 41, 95–98.Google 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.Google Scholar
La Puente, J. M., Merino, S., Toma, G., Moreno, J., Morales, J., Lobato, E., Garcia-Fraile, S. and Belda, E. J. (2010). The blood parasite Haemoproteus reduces survival in a wild bird: a medication experiment. Biology Letters 6, 663–665.CrossRefGoogle Scholar
Levin, I. I., Valkiūnas, G., Santiago-Alarcon, D., Cruz, L. L., Iezhova, T. A., O'Brien, S. L., Hailer, F., Dearborn, D., Schreiber, E. A., Fleischer, R. C., Ricklefs, R. E. and Parker, P. G. (2011). Hippoboscid-transmitted Haemoproteus parasites (Haemosporida) infect Galapagos pelecaniform birds: evidence from molecular and morphological studies, with a description of Haemoproteus iwa . International Journal of Parasitology 15, 1019–1027.CrossRefGoogle Scholar
Liutkevičius, G. (2000). The study of the effects of Haemoproteus dolniki, H. balmorali, H. tartakovskyi (Haemosporida: Haemoproteidae) on the mortality of Culicoides impunctatus (Diptera: Ceratopogonidae). Acta Zoologica Lituanica 2, 3–8.CrossRefGoogle Scholar
Marzal, A., de Lopes, F., Navarro, C. and MØller, A. P. (2005). Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia 142, 541–545.Google Scholar
Mehlhorn, H. (2015). Encyclopedia of Parasitology, 4th Edn. Springer, Berlin.Google Scholar
Merino, S., Moreno, J., Jose-Sanz, J. and Arriero, E. (2000). Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proceedings of the Royal Society London B 267, 2507–2510.Google Scholar
Palinauskas, V., Žiegytė, R., Ilgūnas, M., Iezhova, T. A., Bernotienė, R., Bolshakov, C. and Valkiūnas, G. (2015). Description of the first cryptic avian malaria parasite, Plasmodium homocircumflexum n. sp. with experimental data on its virulence and development in avian hosts and mosquitoes. International Journal of Parasitology 45, 51–62.Google Scholar
Pérez-Tris, J., Helgren, O., Križanauskienė, A., Waldenström, J., Secondi, J., Bonneaud, C., Fjeldså, J., Hasselquist, D. and Bensch, S. (2007). Within-host speciation of malaria parasites. PLoS ONE 2, e235. doi: http://dx.doi.org/10.1371/journal.pone.0000235.Google Scholar
Richardson, D. S., Jury, F. L., 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.CrossRefGoogle Scholar
Schneider, D. and Shahabuddin, M. (2000). Malaria parasite development in a Drosophila model. Science 288, 2376–2379.Google Scholar
Sinden, R. E. (2009). Malaria, sexual development and transmission: retrospect and prospect. Parasitology 136, 1427–1434.Google Scholar
Valkiūnas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton, FL, USA.Google Scholar
Valkiūnas, G. and Iezhova, T. A. (2004). Detrimental effects of Haemoproteus infections on the survival of biting midge Culicoides impunctatus (Diptera: Ceratopogonidae). Journal of Parasitology 90, 194–196. doi: http://dx.doi.org/10.1645/GE-3206RN.Google Scholar
Valkiūnas, G., Iezhova, T. A. and Shapoval, A. P. (2003). High prevalence of blood parasites in hawfinch Coccothraustes coccothraustes . Journal of Natural History 37, 2647–2652.Google Scholar
Valkiūnas, G., Žičkus, T., Shapoval, A. P. and Iezhova, T. A. (2006). Effect of Haemoproteus belopolskyi (Haemosporida: Haemoproteidae) on body mass of the blackcap Sylvia atricapilla . Journal of Parasitology 92, 1123–1125. doi: http://dx.doi.org/10.1645/GE-3564-RN.1.CrossRefGoogle ScholarPubMed
Valkiūnas, G., Palinauskas, V., Križanauskienė, A., Bernotienė, R., Kazlauskienė, R. and Iezhova, T. A. (2013). Further observations on in vitro hybridization of hemosporidian parasites: patterns of ookinete development in Haemoproteus spp. Journal of Parasitology 99, 124–136.Google Scholar
Valkiūnas, G., Kazlauskienė, R., Bernotienė, R., Bukauskaitė, D., Palinauskas, V. and Iezhova, T. A. (2014). Haemoproteus infections (Haemosporida, Haemoproteidae) kill bird biting mosquitoes. Parasitology Research 113, 1011–1018.Google Scholar
Žiegytė, R., Palinauskas, V., Bernotienė, R., Iezhova, T. A. 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.CrossRefGoogle ScholarPubMed
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