Molecular screening for bacteria and protozoa in great cormorants (Phalacrocorax carbo sinensis) nesting in Slovakia, central Europe
-
Bronislava Víchová
, Katarína Reiterová
, Silvia Špilovská , Lucia Blaňarová , Zuzana Hurníková and Ĺudmila Turčeková
Abstract
This study brings the data about the occurrence of bacterial and protozoan pathogens in 32 great cormorants (Phalacrocorax carbo sinensis), representing approximately 20% of the population nesting in the surroundings of water basin Liptovská Mara (northern part of Central Slovakia). A survey revealed the presence of tick-borne bacteria Anaplasma phagocytophilum (6.25%) and parasitic protozoa Toxoplasma gondii (3.1%). These data indicate an infectious status of the great cormorant population nesting in Slovakia; they might suggest a degree of environmental contamination by infectious agents and demonstrate the role of migratory seabirds in the circulation and dispersal of pathogens with zoonotic potential.
Acknowledgements
Study was realized within the frame of project "Centrum of Excellence for Parasitology" No. 26220120022 supported by operating program "Research and Development" funded by European Fund for Regional Development (0.4), project of the Scientific Grant Agency of the Ministry of Education of the Slovak Republic and Slovak Academy of Sciences; VEGA 2/0126/16, VEGA 2/0068/15 and and Project of Slovak Research and Development Agency APVV-14-0274.
Conflict of interest
The authors have no conflict of interest.
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© W. Stefański Institute of Parasitology, PAS
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