Josef Harl1, Tanja Himmel2, Gediminas Valkiūnas3, Mikas Ilgūnas3, Nora Nedorost2, Julia Matt2, Anna Kübber-Heiss4, Amer Alic5, Cornelia Konicek6, Herbert Weissenböck2. 1. Institute of Pathology, Department of Pathobiology, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210, Vienna, Austria. josef.harl@vetmeduni.ac.at. 2. Institute of Pathology, Department of Pathobiology, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210, Vienna, Austria. 3. Nature Research Centre, Akademijos 2, 08412, Vilnius, Lithuania. 4. Research Institute of Wildlife Ecology, Department of Integrative Biology and Evolution, University of Veterinary Medicine Vienna, Savoyenstraße 1, 1160, Vienna, Austria. 5. Department of Pathology, Faculty of Veterinary Medicine, University of Sarajevo, Zmaja od Bosne 90, 71000, Sarajevo, Bosnia and Herzegovina. 6. Service for Birds and Reptiles, Clinic for Small Animal Internal Medicine, Department for Companion Animals and Horses, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210, Vienna, Austria.
Abstract
BACKGROUND: The order Accipitriformes comprises the largest group of birds of prey with 260 species in four families. So far, 21 haemosporidian parasite species have been described from or reported to occur in accipitriform birds. Only five of these parasite species have been characterized molecular genetically. The first part of this study involved molecular genetic screening of accipitriform raptors from Austria and Bosnia-Herzegovina and the first chromogenic in situ hybridization approach targeting parasites in this host group. The aim of the second part of this study was to summarize the CytB sequence data of haemosporidian parasites from accipitriform raptors and to visualize the geographic and host distribution of the lineages. METHODS: Blood and tissue samples of 183 accipitriform raptors from Austria and Bosnia-Herzegovina were screened for Plasmodium, Haemoproteus and Leucocytozoon parasites by nested PCR, and tissue samples of 23 PCR-positive birds were subjected to chromogenic in situ hybridization using genus-specific probes targeting the parasites' 18S rRNAs. All published CytB sequence data from accipitriform raptors were analysed, phylogenetic trees were calculated, and DNA haplotype network analyses were performed with sequences from clades featuring multiple lineages detected in this host group. RESULTS: Of the 183 raptors from Austria and Bosnia-Herzegovina screened by PCR and sequencing, 80 individuals (44%) were infected with haemosporidian parasites. Among the 39 CytB lineages detected, 18 were found for the first time in the present study. The chromogenic in situ hybridization revealed exo-erythrocytic tissue stages of Leucocytozoon parasites belonging to the Leucocytozoon toddi species group in the kidneys of 14 infected birds. The total number of CytB lineages recorded in accipitriform birds worldwide was 57 for Leucocytozoon, 25 for Plasmodium, and 21 for Haemoproteus. CONCLUSION: The analysis of the DNA haplotype networks allowed identifying numerous distinct groups of lineages, which have not yet been linked to morphospecies, and many of them likely belong to yet undescribed parasite species. Tissue stages of Leucocytozoon parasites developing in accipitriform raptors were discovered and described. The majority of Leucocytozoon and Haemoproteus lineages are specific to this host group, but most Plasmodium lineages were found in birds of other orders. This might indicate local transmission from birds kept at the same facilities (raptor rescue centres and zoos), likely resulting in abortive infections. To clarify the taxonomic and systematic problems, combined morphological and molecular genetic analyses on a wider range of accipitriform host species are needed.
BACKGROUND: The order Accipitriformes comprises the largest group of birds of prey with 260 species in four families. So far, 21 haemosporidian parasite species have been described from or reported to occur in accipitriform birds. Only five of these parasite species have been characterized molecular genetically. The first part of this study involved molecular genetic screening of accipitriform raptors from Austria and Bosnia-Herzegovina and the first chromogenic in situ hybridization approach targeting parasites in this host group. The aim of the second part of this study was to summarize the CytB sequence data of haemosporidian parasites from accipitriform raptors and to visualize the geographic and host distribution of the lineages. METHODS: Blood and tissue samples of 183 accipitriform raptors from Austria and Bosnia-Herzegovina were screened for Plasmodium, Haemoproteus and Leucocytozoon parasites by nested PCR, and tissue samples of 23 PCR-positive birds were subjected to chromogenic in situ hybridization using genus-specific probes targeting the parasites' 18S rRNAs. All published CytB sequence data from accipitriform raptors were analysed, phylogenetic trees were calculated, and DNA haplotype network analyses were performed with sequences from clades featuring multiple lineages detected in this host group. RESULTS: Of the 183 raptors from Austria and Bosnia-Herzegovina screened by PCR and sequencing, 80 individuals (44%) were infected with haemosporidian parasites. Among the 39 CytB lineages detected, 18 were found for the first time in the present study. The chromogenic in situ hybridization revealed exo-erythrocytic tissue stages of Leucocytozoon parasites belonging to the Leucocytozoon toddi species group in the kidneys of 14 infected birds. The total number of CytB lineages recorded in accipitriform birds worldwide was 57 for Leucocytozoon, 25 for Plasmodium, and 21 for Haemoproteus. CONCLUSION: The analysis of the DNA haplotype networks allowed identifying numerous distinct groups of lineages, which have not yet been linked to morphospecies, and many of them likely belong to yet undescribed parasite species. Tissue stages of Leucocytozoon parasites developing in accipitriform raptors were discovered and described. The majority of Leucocytozoon and Haemoproteus lineages are specific to this host group, but most Plasmodium lineages were found in birds of other orders. This might indicate local transmission from birds kept at the same facilities (raptor rescue centres and zoos), likely resulting in abortive infections. To clarify the taxonomic and systematic problems, combined morphological and molecular genetic analyses on a wider range of accipitriform host species are needed.
Authors: Julio Rozas; Albert Ferrer-Mata; Juan Carlos Sánchez-DelBarrio; Sara Guirao-Rico; Pablo Librado; Sebastián E Ramos-Onsins; Alejandro Sánchez-Gracia Journal: Mol Biol Evol Date: 2017-12-01 Impact factor: 16.240
Authors: Elvin J Lauron; Claire Loiseau; Rauri C K Bowie; Greg S Spicer; Thomas B Smith; Martim Melo; Ravinder N M Sehgal Journal: Parasitology Date: 2014-10-29 Impact factor: 3.234
Authors: E Nilsson; H Taubert; O Hellgren; X Huang; V Palinauskas; M Y Markovets; G Valkiūnas; S Bensch Journal: J Evol Biol Date: 2016-06-27 Impact factor: 2.411
Authors: Yvonne R Schumm; Dimitris Bakaloudis; Christos Barboutis; Jacopo G Cecere; Cyril Eraud; Dominik Fischer; Jens Hering; Klaus Hillerich; Hervé Lormée; Viktoria Mader; Juan F Masello; Benjamin Metzger; Gregorio Rocha; Fernando Spina; Petra Quillfeldt Journal: Parasitol Res Date: 2021-02-01 Impact factor: 2.289