Ticks (Acari: Ixodida) on synanthropic small and medium-sized mammals in areas of the northeastern United States infested with the Asian longhorned tick, Haemaphysalis longicornis

Tick-borne diseases affecting humans in United States (US), particularly in the northeast, have been increasing since 2000 (Rosenberg et al., 2018), primarily as a result of the geographical expansion of Ixodes scapularis, the blacklegged tick (Eisen et al., 2016), and changes in the distribution of Amblyomma americanum, the lone star tick (Rochlin et al., 2022). These tick species are efficient vectors of multiple viral, bacterial, and protozoan pathogens, many of which were described in the last 20 years infecting humans, companion animals and wildlife (Goddard and Varela-Stokes, 2009, Tokarz et al., 2018, Madison-Antenucci et al., 2020, Fleshman et al., 2022).

While some tick species are considered critical pathogen vectors, their importance varies seasonally and with the relative abundance of different pathogen reservoirs they use as hosts, which in turn determines the dynamics of animal-to-animal (enzootic) and animal-to-human (zoonotic) transmission cycles (Krasnov et al., 2007, Linske et al., 2018, Ginsberg et al., 2021). Thus, it is essential to evaluate associations between tick species and their vertebrate hosts to assess pathways of tick-borne pathogen transmission. This is especially the case when trying to evaluate the potential of an invasive tick species as a vector of pathogens in its new range.

The invasive Asian longhorned tick, Haemaphysalis longicornis, is a three-host tick that was detected for the first time in the Western hemisphere in 2017 in New Jersey (US), northeastern USA (Rainey et al., 2018), and has since been detected in 19 states (USDA, 2023). So far, all populations detected in the US are parthenogenetic (Egizi et al., 2020), which explains, at least partially, the fact that this species can quickly reach high densities in new locations (Schappach et al., 2020). Importantly, H. longicornis thrives in transitional habitats on the edges of meadows and along forest pathways, which are intensely used by humans and dogs (González et al., 2023). In its native range in northeastern China, Korea, and Japan, H. longicornis is considered a critical pathogen vector of Dabie bandavirus, the causative agent of human severe fever with thrombocytopenia syndrome (Casel et al., 2021). In Asia, it is also a significant vector of agents causing canine and livestock babesiosis (Shaw et al., 2001, Bai et al., 2002, Guan et al., 2010, Sivakumar et al., 2014), and in Australasia, where it became established in the early 20th Century, it is a vector of Theileria orientalis, the agent of theileriosis, which is deadly to cattle, resulting in significant economic losses (Watts et al., 2016). The widespread distribution and adaptability of H. longicornis underscores the necessity of understanding its phenology and host associations, which could reveal potential impacts on human and animal health in new areas it colonizes.

In the Australasian, Oriental and Palearctic zoogeographical regions, H. longicornis is considered a frequent human biter (Guglielmone and Robbins, 2018) and although the impacts of this invasive tick species on human and animal health is still being investigated in the US, American populations of H. longicornis have been shown to be competent laboratory vectors of Rickettsia rickettsii, the bacterial agent of Rocky Mountain spotted fever (Stanley et al., 2020), Heartland virus and Powassan virus (Raney et al., 2022a, 2022b). Additionally, a recent examination of field collected H. longicornis found one pool of larvae, two nymphs and one adult positive for Bourbon virus (Cumbie et al., 2022). In the US state of Virginia, deaths of cattle due to infection with Theileria orientalis Ikeda, a strain new to the US, have been attributed to transmission by H. longicornis (Dinkel et al., 2021). Associations with other pathogens as populations expand across favorable areas are expected (Rochlin et al., 2023).

Within the US, NJ, the state with the highest human density and urbanization (https://www.census.gov/data/tables/time-series/dec/density-data-text.html accessed 24 October 2022), stands out for its high frequency of human-tick encounters and high incidence of tick-borne diseases in humans and their companion animals (Bowman et al., 2009, Nieto et al., 2018, Rosenberg et al., 2018, Mahachi et al., 2020). Our objective was to identify important mammalian hosts of H. longicornis. To do so we removed ticks from a variety of small and medium-sized mammals captured near paths and edges of forests where questing H. longicornis are most abundant (González et al., 2023). In the process we also collected the other epidemiologically important tick species in the northeastern US, allowing us to develop side-by-side comparisons of tick-host associations. Here we summarize our findings and discuss their implications for the epidemiology of tick-borne diseases in NJ and elsewhere.

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