Silent travelers: the potential of migratory birds and their ticks to introduce emerging viruses into Switzerland

Abstract

Switzerland hosts over 400 bird species, many of which are migratory. Through diverse movement patterns, ranging from short distances to almost global migrations, these birds can introduce zoonotic viruses, such as West Nile virus (WNV) or avian influenza virus (AIV), as well as unknown and potentially emerging viruses. Furthermore, they facilitate the global dispersal of infected ectoparasites, particularly ticks, risking the introduction of novel tick-borne diseases. To assess this risk, we sampled 42 bird species (39 migratory, 3 resident) over seven months in 2023 at the Bolle di Magadino nature reserve and the Piano di Magadino area in the canton Ticino (Switzerland). This region, because of its transitional climate, serves as an important resting and breeding ground for migratory birds. In total, 496 oropharyngeal-cloacal swabs, 164 sera, and 22 associated ticks were collected. While RT-qPCR of the swabs detected no active WNV or AIV infections, ELISA testing identified Orthoflavivirus antibodies in 15 of 164 sera, indicating prior exposure. Metagenomic next-generation sequencing revealed a viral landscape spanning 33 families (29 of which were identified in birds). Within this virome, DNA viruses, predominantly Circoviridae, Genomoviridae, and Parvoviridae, dominated in abundance but exhibited low diversity. In contrast, the highly diverse RNA virome primarily reflected the birds dietary habits and the local habitat at the nature reserve. Notably, we report the first detection of Bole tick virus 4 (BoTV4) in Switzerland, identified in several ticks (Rhipicephalus turanicus) associated with long-distance migrants. This member of the newly established Pestiviridae family is already established in parts of Asia, Africa, and Europe. This study provides the first active surveillance of the wild bird virome in Switzerland. Our findings establish a framework for the early detection of emerging viruses and underscore the role of migratory birds as dispersal vectors for ticks and novel tick-borne viruses.