The presence of Ixodes pavlovskyi and I. pavlovskyi–borne microorganisms in Rishiri Island: an ecological survey

ABSTRACT Rishiri Island, towering toward the Sea of Japan, has been volcanically dormant for approximately 8,000 years. This small inhabited island is free of middle- to large-sized wildlife and a crucial stopover for wild birds migrating along various routes of the East Asian Flyway. A 5-year survey was conducted to explore the biogeography of ticks and tick-borne microorganisms. By flagging vegetation, Ixodes pavlovskyi (Pomerantzev, 1948), distributed in limited spots in the Far East, was predominantly collected (60%–80% collection) throughout the survey period. The I. pavlovskyi consisted of two haplogroups, Asahikawa-type and Rishiri-type, with the prevalence and nucleotide diversity of Rishiri-type being over 90% and 0.068, respectively. A survey of wild animals revealed that red-backed voles and wild birds, including Oriental greenfinches and black-faced buntings, are their hosts for blood feeding. Furthermore, the red-backed voles were infected with tick-borne Candidatus Ehrlichia khabarensis (5/21, 24%). Till date, microorganisms with identical gene sequences have only been reported from Khabarovsk and Vancouver. Ca. E. khabarensis gene has also been detected in host-seeking adult I. pavlovskyi. These results indicated that Rishiri Island is a refuge for both I. pavlovskyi and I. pavlovskyi–borne microorganisms. Additionally, the Babesia microti US lineage, which is vectored by Ixodes persulcatus in the Far East, appears to be maintained between I. pavlovskyi and wild rodents. Various factors have influenced the unique ecosystem of the island. The historical and ecological biogeography of Rishiri Island helps us understand the origin, evolution, and expansion of ticks and associated microorganisms. IMPORTANCE Understanding the ecology of ticks and tick-borne microorganisms is important to assess the risk of emerging tick-borne diseases. Despite the fact that the Ixodes pavlovskyi tick bites humans, we lack information including population genetics and the reason for the inadequate distribution in Japan. A 5-year survey revealed that Rishiri Island, the main stopover in the East Asian Flyway of wild birds in the northern Sea of Japan, was a refuge of I. pavlovskyi. The I. pavlovskyi included two haplogroups, which were supposed to diverge a long time before the island separated from the continent and Hokkaido mainland. The detection of microorganisms from wildlife revealed that wild birds and rodents play a role in diffusion and settlement, respectively, of not only I. pavlovskyi but also I. pavlovskyi–borne microorganisms including Candidatus Ehrlichia khabarensis and Babesia microti US lineage. Various island-specific factors control I. pavlovskyi dominance and tick-borne pathogen maintenance. The results may enable us to explain how tick-borne infectious microorganisms are transported. Understanding the ecology of ticks and tick-borne microorganisms is important to assess the risk of emerging tick-borne diseases. Despite the fact that the Ixodes pavlovskyi tick bites humans, we lack information including population genetics and the reason for the inadequate distribution in Japan. A 5-year survey revealed that Rishiri Island, the main stopover in the East Asian Flyway of wild birds in the northern Sea of Japan, was a refuge of I. pavlovskyi. The I. pavlovskyi included two haplogroups, which were supposed to diverge a long time before the island separated from the continent and Hokkaido mainland. The detection of microorganisms from wildlife revealed that wild birds and rodents play a role in diffusion and settlement, respectively, of not only I. pavlovskyi but also I. pavlovskyi–borne microorganisms including Candidatus Ehrlichia khabarensis and Babesia microti US lineage. Various island-specific factors control I. pavlovskyi dominance and tick-borne pathogen maintenance. The results may enable us to explain how tick-borne infectious microorganisms are transported.