Ticks (Acari: Ixodidae) parasitizing migrating and local breeding birds in Finland

Ticks are globally renowned vectors for numerous zoonoses, and birds have been identified as important hosts for several species of hard ticks (Acari: Ixodidae) and tick-borne pathogens. Many European bird species overwinter in Africa and Western Asia, consequently migrating back to breeding grounds in Europe in the spring. During these spring migrations, birds may transport exotic tick species (and associated pathogens) to areas outside their typical distribution ranges. In Finland, very few studies have been conducted regarding ticks parasitizing migrating or local birds, and existing data are outdated, likely not reflecting the current situation. Consequently, in 2018, we asked volunteer bird ringers to collect ticks from migrating and local birds, to update current knowledge on ticks found parasitizing birds in Finland. In total 430 ticks were collected from 193 birds belonging to 32 species, caught for ringing between 2018 and 2020. Furthermore, four Ixodes uriae were collected from two roosting islets of sea birds in 2016 and 2020. Ticks collected on birds consisted of: Ixodes ricinus (n = 421), Ixodes arboricola (4), Ixodes lividus (2) and Hyalomma marginatum (3). Ixodes ricinus loads (nymphs and larvae) were highest on thrushes (Passeriformes: Turdidae) and European robins (Erithacus rubecula). The only clearly imported exotic tick species was H. marginatum. This study forms the second report of both I. uriae and I. arboricola from Finland, and possibly the northernmost observation of I. arboricola from Europe. The importation of exotic tick species by migrating birds seems a rare occurrence, as over 97% of all ticks collected from birds arriving in Finland during their spring migrations were I. ricinus, a species native to and abundant in Finland.

Circumpolar diversification of the Ixodes uriae tick virome

Ticks (order: Ixodida) are a highly diverse and ecologically important group of ectoparasitic blood-feeding organisms. One such species, the seabird tick (Ixodes uriae), is widely distributed around the circumpolar regions of the northern and southern hemispheres. It has been suggested that Ix. uriae spread from the southern to the northern circumpolar region millions of years ago and has remained isolated in these regions ever since. Such a profound biographic subdivision provides a unique opportunity to determine whether viruses associated with ticks exhibit the same evolutionary patterns as their hosts. To test this, we collected Ix. uriae specimens near a Gentoo penguin (Pygoscelis papua) colony at Neko harbour, Antarctica, and from migratory birds - the Razorbill (Alca torda) and the Common murre (Uria aalge) - on Bonden island, northern Sweden. Through meta-transcriptomic next- generation sequencing we identified 16 RNA viruses, seven of which were novel. Notably, we detected the same species, Ronne virus, and two closely related species, Bonden virus and Piguzov virus, in both hemispheres indicating that there have been at least two cross- circumpolar dispersal events. Similarly, we identified viruses discovered previously in other locations several decades ago, including Gadgets Gully virus, Taggert virus and Okhotskiy virus. By identifying the same or closely related viruses in geographically disjunct sampling locations we therefore provide evidence for virus dispersal within and between the circumpolar regions. In marked contrast, our phylogenetic analysis revealed no movement of the Ix. uriae hosts between the same locations. Combined, these data suggest that migratory birds are responsible for the movement of viruses at both the local and global scales.Author summary/ImportanceAs host populations diverge, so may those microorganisms, including viruses, that are dependent on those hosts. To examine this key issue in host-microbial evolution we compared the co-phylogenies of the seabird tick, Ixodes uriae, and their RNA viruses sampled from the far northern and southern hemispheres. Despite the huge geographic distance between them, phylogeographic analysis reveals that the same viruses were found both within and between the northern and southern circumpolar regions, most likely reflecting transfer by virus-infected migratory birds. In contrast, genomic data suggested that the Ix. uriae populations were phylogenetically distinct between the northern and southern hemispheres. This work emphasises the importance of migratory birds and ticks as vectors and sources of virus dispersal and introduction at both the local and global scales.

Ticks collected from soil/nest litter and live and dead nestlings of migratory seabirds during their breeding season at six uninhabited Islands, Republic of Korea during 2009 and 2014–2017

The 65th Medical Brigade (MED BDE)/Medical Department Activity-Korea (MEDDAC-K), in collaboration with the Migratory Birds Research Center, National Park Research Institute, conducted migratory bird tick-borne disease surveillance at six small, remote, uninhabited islands near the western (Nan Island), southwestern (Chilbal, Gugul, Gaerin, Hong, and Sogugul islands) and southeastern (Hong Island) coastal areas of the Republic of Korea (ROK) during 2009 and from 2014–2017. Ticks were collected from nest soil/litter of the Ancient Murrelet (Synthliboramphus antiquus), Japanese Murrelet (Synthliboramphus wumizusume), Swinhoe’s Storm Petrel (Hydrobates monorhis), Black-tailed Gull (Larus crassirostris), Pacific Swift (Apus pacificus), and Streaked Shearwater (Calonectris leucomelas) using Tullgren funnels. Ticks also were collected from recently dead nestlings of Swinhoe’s Storm Petrel and Black-tailed Gull at Gugul, Sogugul, Gaerin, Nan, and Hong islands, and single ticks were collected from vegetation (tick drag) and a human bitten on Chilbal Island. A total of 1,578 ticks (61 females, 122 males, 290 nymphs, and 1,105 larvae), belonging to four genera and six species, were collected. Ornithodoros capensis (73.00%; 1,152) was the most commonly collected tick on migratory seabirds, followed by Ornithodoros sawaii (26.55%; 420), Ixodes uriae (0.19%; 3), and Ixodes signatus (0.13%, 2). One (0.06%) Haemaphysalis flava was collected by tick drag and one (0.06%) Amblyomma testudinarium was collected while biting one of the survey members. Ornithodoros species were identified morphologically and confirmed using polymerase chain reaction (PCR) techniques. This is the first record of O. sawaii collected from nest soil/litter during the 2017 nesting season of the Pacific Swift and Streaked Shearwater in the ROK.

Population structure ofBorrelia gariniifromIxodes uriaecollected in seabird colonies of the northwestern Atlantic Ocean

The occurrence ofBorrelia gariniiin seabird ticks,Ixodes uriae, associated with different species of colonial seabirds has been studied since the early 1990s. Research on the population structure of this bacterium in ticks from seabird colonies in the northeastern Atlantic Ocean has revealed admixture between marine and terrestrial tick populations. We studiedB. gariniipopulation structure inI. uriaecollected from seabird colonies in the northwestern Atlantic Ocean, in Newfoundland and Labrador, Canada. We applied a multi-locus sequence typing (MLST) scheme toB. gariniifound in ticks from four species of seabirds. TheB. gariniistrains found in this seabird colony ecosystem were diverse. Some were very similar to strains from Asia and Europe, including some obtained from human clinical samples, while others formed a divergent group specific to this region of the Atlantic Ocean.ImportanceThis study provides the firstB. gariniisequences from North American seabird ticks that were characterized using an MLST approach. This revealed new MLST sequence types and alleles, enhancing our knowledge ofB. gariniidiversity. Our findings highlight the genetic complexity ofB. gariniicirculating among seabird ticks and their avian hosts but also demonstrate surprisingly close connections betweenB. gariniiin this ecosystem and terrestrial sources in Eurasia. Genetic similarities amongB. gariniifrom seabird ticks and humans indicate the possibility thatB. gariniicirculating within seabird tick-avian host transmission cycles could directly, or indirectly via connectivity with terrestrial transmission cycles, have consequences for human health.

Genera, subgenera, species and subspecies of hard ticks (Acari: Ixodidae) described, named, renamed or given new rank by Paul Schulze (1887–1949) and their current status

The names for 19 genera, 17 subgenera, 150 species and 150 subspecies of Ixodidae described by Paul Schulze, names changed by him after the revision of certain taxa, new ranks for names originally described by other authors, a few lapsus calamorum and some incorrect names ascribed to Schulze by other workers are discussed. Two genera (Cosmiomma and Nosomma) are valid, but most of Schulze’s subgenera are difficult to assess because of the current disarray that prevails at this classificatory level in the Ixodidae. Thirty-six of 150 species names discussed by Schulze are considered valid herein (3 species of Amblyomma, 1 Bothriocroton, 1 Cosmiomma, 6 Dermacentor, 4 Haemaphysalis, 5 Hyalomma, 13 Ixodes, 1 Nosomma and 2 Rhipicephalus), while 28 are valid species epithets that are currently assigned to different genera (e.g., Acarus undatus was formerly classified in the genus Aponomma but is currently known as Bothriocroton undatum). Twenty-nine of these valid species names were authored by Schulze or Schulze & Schlottke. The remaining species names are mostly synonyms or names that are incertae sedis, nomen nudum or lapsus calamorum. The 150 subspecific names are treated as synonyms of valid species or as nomina nuda, nomina dubia, incertae sedis or lapsus calamorum. Many names used by Schulze have been synonymized based on sound systematic research, but the justification for synonymizing other names is occasionally weak. It will be important to take these names into account if, as has already happened, future molecular and morphological studies result in the reinstatement of Schulze names currently considered synonyms. This situation has particular relevance for Amblyomma geoemydae, the Amblyomma marmoreum species complex, Amblyomma testudinarium, Oriental species of Dermacentor, Hyalomma in general, Ixodes arboricola, Ixodes canisuga, Ixodes lividus, Ixodes trianguliceps and Ixodes uriae. In conclusion, the prolific contributions of Paul Schulze have their weak points —the many species and subspecies of Hyalomma described by him are unjustified as is the alleged worldwide distribution of the former genus Aponomma—but his perception of the complexity of the genus Dermacentor (under Indocentor) in the Oriental and Australasian Zoogeographic Regions, as well as his understanding of tick biodiversity in these regions constitute seminal scientific achievements.

Evidence for Borrelia bavariensis Infections of Ixodes uriae within Seabird Colonies of the North Atlantic Ocean

ABSTRACT The first report of members of the spirochete genus Borrelia in the seabird tick, Ixodes uriae, and seabird colonies occurred during the early 1990s. Since then, Borrelia spp. have been detected in these ticks and seabird colonies around the world. To date, the primary species detected has been Borrelia garinii, with rare occurrences of Borrelia burgdorferi sensu stricto and Borrelia lusitaniae. During our research on Borrelia and I. uriae in seabird colonies of Newfoundland and Labrador, Canada, we have identified Borrelia bavariensis in I. uriae. To our knowledge, B. bavariensis has previously been found only in the Eurasian tick species Ixodes persulcatus and Ixodes ricinus, and it was believed to be a rodent-specific Borrelia ecotype. We found B. bavariensis within I. uriae from three seabird colonies over three calendar years. We also reanalyzed B. garinii sequences collected from I. uriae from Eurasian seabird colonies and determined that sequences from two Russian seabird colonies likely also represent B. bavariensis. The Canadian B. bavariensis sequences from I. uriae analyzed in this study cluster with previously described sequences from Asia. Overall, this is an important discovery that illustrates and expands the range of hosts and vectors for B. bavariensis, and it raises questions regarding the possible mechanisms of pathogen dispersal from Asia to North America. IMPORTANCE To our knowledge, this is the first documentation of B. bavariensis outside Eurasia. Additionally, the bacterium was found in a marine ecosystem involving the seabird tick I. uriae and its associated seabird hosts. This indicates that the epizootiology of B. bavariensis transmission is much different from what had been described, with this species previously believed to be a rodent-specific ecotype, and it indicates that this pathogen is established, or establishing, much more widely.