Co-invasion of the ladybird Harmonia axyridis and its parasites Hesperomyces virescens fungus and Parasitylenchus bifurcatus nematode to the Caucasus

Study of parasites in recently established populations of invasive species can shed lite on sources of invasion and possible indirect interactions of the alien species with native ones. We studied parasites of the global invader Harmonia axyridis (Coleoptera: Coccinellidae) in the Caucasus. In 2012 the first established population of H. axyridis was recorded in the Caucasus in Sochi (south of European Russia, Black sea coast). By 2018 the ladybird has spread to the vast territory: Armenia, Georgia and south Russia: Adygea, Krasnodar territory, Stavropol territory, Dagestan, Kabardino-Balkaria and North Ossetia. Examination of 213 adults collected in Sochi in 2018 have shown that 53% of them are infested with Hesperomyces virescens fungi (Ascomycota: Laboulbeniales) and 8% with Parasitylenchus bifurcatus nematodes (Nematoda: Tylenchida, Allantonematidae). Examined H. axyridis specimens were free of parasitic mite Coccipolipus hippodamiae. An analysis of the phylogenetic relationships of Parasitylenchus bifurcatus based on 18S rDNA confirmed the morphological identification of this species. Hesperomyces virescens and Parasitylenchus bifurcatus are firstly recorded from the Caucasus and Russia, though widespread in Europe. It probably indicates that they appeared as a result of co-invasion with their host. Harmonia axyridis was released in the region for pest control, but laboratory cultures are always free of H. virescens and P. bifurcatus. Therefore, detection of H. virescens and P. bifurcatus indicates that population of H. axyridis in the Caucasus cannot derive exclusively from released specimens. We did not find H. virescens on 400 specimens of 31 other ladybird species collected in the same localities with H. axyridis in the Caucasus. No reliable correlation between infestation by H. virescens and P. bifurcatus has been found. Besides these two parasites an unidentified species of the order Mermithida is recorded. It is the first documented case of H. axyridis infestation by a parasitic nematode of this order in nature.