New report of Haemaphysalis longicornis (Ixodida: Ixodidae) in Mecklenburg County, Virginia from field collections

Abstract

Introduction

Since its introduction into the United States, Haemaphysalis longicornis (Neumann) has rapidly spread across the eastern United States and become a potential economic and public health concern (Beard et al. 2018). H. longicornis can reproduce asexually via parthenogenesis, which allows it to quickly grow to high population densities in a short amount of time (Egizi et al. 2020). The adult stages of this tick prefer medium (e.g., raccoons, Procyon lotor Linnaeus) and large (i.e., white-tailed deer, Odocoileus virginianus Linnaeus) wildlife hosts, dogs, and livestock (Thompson et al. 2021, Tufts et al. 2021, Ferreira et al. 2023, USDA 2023). High densities of H. longicornis can decrease milk and meat production in cattle and, in extreme cases, cause exsanguination, resulting in an economic burden (Eleftheriou et al. 2023). Of additional concern is the ability of H. longicornis to transmit the causative agent of bovine infectious anemia in cattle, Theileria orientalis (Ikeda genotype) (Dinkel et al. 2021), which has been recovered from host-seeking H. longicornis in Virginia in 2019 (Thompson et al. 2020). Infection with Ikeda genotype T. orientalis results in severe illness in up to 5%–6% of infected cattle and may cause significant weight loss, leading to production losses in dairy and beef operations and reduced economic outputs (Eamens et al. 2013).

In addition to animal pathogens, H. longicornis serves as a vector for severe fever with thrombocytopenia syndrome in eastern Asia (Li et al. 2016, Zhuang et al. 2018), a human pathogen closely related to Heartland virus found in Amblyomma americanum (Linnaeus) ticks in the United States (Romer et al. 2022, Aziati et al. 2023). Laboratory studies have demonstrated the ability of H. longicornis to transmit Heartland and Powassan viruses and Rocky Mountain spotted fever; however, no natural transmission of these pathogens has been reported from H. longicornis bites (Stanley et al. 2020, Raney et al. 2022a, 2022b). The risk to humans is unclear, as the invasive population of this tick in the United States does not prefer humans, although there have been reported human bites (Bickerton and Toledo 2020, Wormser et al. 2020).

Haemaphysalis longicornis was first recognized in the United States in 2017 in Hunterdon County, New Jersey, but was retrospectively misidentified as Haemaphysalis leporispalustris (Packard) as early as 2010 from ticks collected on deer (Beard et al. 2018). It has since spread across much of the eastern United States, originating from 3 potential introductions from East Asian populations of this tick species (Beard et al. 2018, Egizi et al. 2020). As of October 2023, H. longicornis has been reported in 19 states: New Jersey (Rainey et al. 2018), New York (Tufts et al. 2021, Rochlin et al. 2023), Delaware (Maestas et al. 2020), Connecticut (USDA 2023), Massachusetts (USDA 2023), Maryland (USDA 2023), Rhode Island (Tufts and Diuk-Wasser 2021), Pennsylvania (Price et al. 2021), Ohio (Price et al. 2021), Indiana (USDA 2023), West Virginia (USDA 2023), Kentucky (USDA 2023), Missouri (USDA 2023), Arkansas (USDA 2023), Tennessee (Trout Fryxell et al. 2021), Georgia (USDA 2023), South Carolina (USDA 2023), North Carolina (USDA 2023), and Virginia (Thompson et al. 2020, 2021, Cumbie et al. 2022). Virginia has reported the most counties with established infestations; however, most counties reporting H. longicornis in the state are in the northern and western portions of the state at higher elevations (USDA 2023). Here we report the first documentation of H. longicornis in south-central Virginia, Mecklenburg County, through field collections. This report will provide information on the geographic expansion of H. longicornis in the southeastern United States in areas not previously described and provide context for the temporal expansion of this species.

Materials and Methods

Study Site

Our study site was located on a privately owned property located in Red Oak, Virginia, which is in a rural area in the south-central portion of the Piedmont region of Virginia. This site was located approximately 21 km from Clarksville, Virginia and approximately 32 km from the North Carolina border. The site is comprised of 67 acres of land with multiple habitat types. We selected 4 locations on the property that represent distinct habitat types to compare microhabitat differences in tick distribution. The 4 locations include forested, open long vegetation field, open short vegetation field, and an area with domiciliary buildings that is a mixture of unpaved gravel rocks, forested underbrush, and an open canopy grass patch. The study site contained a diverse vertebrate community with evidence of activity of black bears (Ursus americanus Linnaeus), white-tailed deer, groundhogs (Marmota monax Linnaeus), eastern cottontails (Sylvilagus floridanus Bachman), and wild turkeys (Meleagris gallapavo Linnaeus). In addition, there were several partially ground-dwelling birds, such as northern cardinals (Cardinalis cardinalis Linnaeus), turkey vultures (Cathartes aura Linnaeus), and black vultures (Coragyps atratus Bechstein) that may serve as hosts for ticks. To our knowledge, there were no large-scale livestock operations nearby; however, visual inspection of a nearby property revealed only one isolated domestic bull.

Field Sampling Design

All ticks were collected using standard dragging and flagging techniques consistent with previous studies. Drag cloths were made of 1 m² flannel, cotton cloths attached to a wooden dowel of 3.18 cm diameter with two 1 m sections of rope attached to a 0.3 m PVC pipe as a handle, following Centers for Disease Control and Prevention (CDC) guidelines (CDC 2020). Drag sampling was conducted by dragging the entirety of 5 m² grid square. At the end of each square, we checked the bottom and top of the drag cloth for tick presence or absence, collecting any ticks. Flagging was conducted by sweeping our flag cloth across the vegetation, checking for ticks on both sides of the flag cloth every 1 m². Flag cloths were made of 1 m² flannel, cotton cloth attached to a wooden pole (CDC 2020). Sweeping was done in each grid square regardless of vegetation length to directly compare with our drag sampling method.

We conducted all sampling across 10 days from 19 June 2023 to 17 July 2023 and avoided days with excessive rain and moisture that would hinder cloth sampling for ticks (i.e., drags and flags). All our sampling occurred between 10 AM and 2 PM when tick activity was expected to be highest (Orr et al. 2013). We established 5 m² grids that were dragged twice and flagged twice on different days, except for the forested habitat where we dragged only twice. The number of grid squares sampled for each habitat type was 22 for the forest, 960 for the short vegetation field, 180 for the long vegetation field, and 144 for the domiciliary habitat. Ticks were placed directly into 70% ethanol upon collection and stored at −20 °C for future molecular screening of pathogens, except for larval masses that could not efficiently be collected with forceps. In these cases, we utilized a lint roller to collect larvae and stored the sheets at −20 °C. All ticks were identified to species using published morphological keys, except for Ixodes spp. larvae which we only identified to genus (Clifford et al. 1961, Keirans and Litwak 1989, Durden and Keirans 1996, Dubie et al. 2017, Egizi et al. 2019, Nadolny et al. 2021).

Results

In total, we collected 1,003 ticks across 6,115 m² sampling effort, or 0.164 ticks/m² (Table 1). A breakdown of tick counts by habitat type and collection method is provided in Table 2. We collected Amblyomma americanum (159 females, 114 males, 341 nymphs, and 173 larvae) the most representing 78% of all collected ticks. Other species collected included Dermacentor variabilis Say (14 females and 11 males), Ixodes affinis (Neumann) (1 female, 3 males, and 2 nymphs), H. longicornis (1 adult female), H. leporispalustris (1 nymph), Amblyomma maculatum (Koch) (1 adult), and Ixodes spp. (182 larvae). Our H. longicornis specimen was collected from our domicile habitat type on 25th June at 1:25 PM in an ecotone adjacent to our forest habitat. We initially identified H. longicornis morphologically and confirmed this result by sending the specimen to the National Veterinary Services Laboratory in Ames, Iowa for morphological confirmation. At the time of this collection, Mecklenburg County, Virginia, had not reported this species.

Discussion

Our study presents the first known report of H. longicornis in Mecklenburg County, Virginia, based on field collections. Given that the US population of H. longicornis is parthenogenic, it is likely that this species will be reported again in this county and potentially in neighboring counties. The presence and potential establishment of this species in the region have significant implications for livestock growers, who will now need to address the challenges posed by this invasive tick and its potential pathogens.

Although we report the first observation of H. longicornis in Mecklenburg County, H. longicornis has been observed further south. There have been recent reports of H. longicornis in central North Carolina counties where it had not yet been established (e.g., Wake County) (USDA 2023), which suggests that the H. longicornis geographic distribution has potentially expanded beyond its previously documented range and will continue to expand. This expansion is due to the movement of domestic animals (e.g., cattle, companion animals) as well as wildlife with large home ranges (e.g., deer) as H. longicornis is a generalist tick that will opportunistically parasitize a variety of animal hosts (Egizi et al. 2020, Thompson et al. 2021, Tufts et al. 2021). Habitat suitability models of H. longicornis project that this species can inhabit much of the eastern United States, especially throughout the Appalachian Mountain region, as well as around the Cascade Mountain range of the western United States (Raghavan et al. 2019, Rochlin 2019). The expansion of this species has apparently supported these predictions throughout the Appalachian Mountains region (USDA 2023).

The expansion of H. longicornis potentially poses significant economic and public health consequences for the United States, particularly in south-central Virginia. This region, which regularly produces cattle and accounts for approximately 10% of the state’s cattle production, could be especially impacted. An H. longicornis-vectored cattle pathogen of concern, T. orientalis (Ikeda genotype), has been identified from host-seeking ticks in the eastern United States (Thompson et al. 2020), which has been responsible for considerable economic losses in the cattle industries of Australia and New Zealand (Eamens et al. 2013, Watts et al. 2016). This tick species is also able to transmit a suite of human pathogens, including severe fever with thrombocytopenia syndrome virus and Heartland virus, and the latter has been identified in ticks from the United States (Li et al. 2016, Zhuang et al. 2018, Raney et al. 2022a, Romer et al. 2022). These threats to human and animal health support the need to enhance surveillance of this species throughout the eastern United States to further identify when and where H. longicornis are spreading, and the economic and public health consequences of this expansion.

Despite the ongoing spread of H. longicornis, few large-scale surveillance efforts have been established to monitor its populations across its range. In addition, few control measures beyond chemical methods have been identified, limiting our ability to effectively manage H. longicornis. Current surveillance is mainly conducted through active efforts by academic and government researchers and passive reporting by livestock operations (Butler and Trout Fryxell 2023, Eleftheriou et al. 2023, USDA 2023). Recent collaborative efforts led by the US Department of Agriculture (USDA) include a widespread “tick blitz” to map the current range of H. longicornis across the eastern United States (Foley et al. 2023, Trout Fryxell et al. 2023). This initiative will greatly enhance our understanding of H. longicornis spread. Although few studies have evaluated H. longicornis control measures, integrated strategies such as maintaining closed herds, using chemical control, and applying mechanical vegetation control have been shown to reduce H. longicornis populations by up to 90% (Butler and Trout Fryxell 2023). Further research is needed to assess integrated pest management approaches to effectively mitigate the impact of H. longicornis infestations on livestock growers.

Acknowledgments

We would like to thank Allie Yackley, Carly Ward, Kaleb Ortiz, Audrey Lloyd, and Kaylin Lewandowski for their assistance with the field sampling of ticks in 2023. We would also like to thank Kaleb Ortiz and Kaylin Lewandowski for their assistance in identifying ticks collected during the field study. We would also like to thank Dr. Wes Watson for his feedback during manuscript preparation.

Funding

This work was supported by the United States Department of Agriculture Multistate Project NE-1943, “Biology, Ecology & Management of Emerging Disease Vectors.” This work was also funded by a graduate student research grant from the Triangle Center of Evolutionary Medicine (TriCEM).

Author contributions

Dayvion Adams (Conceptualization [Lead], Data curation [Lead], Formal analysis [Lead], Funding acquisition [Lead], Investigation [Lead], Methodology [Lead], Project administration [Lead], Supervision [Lead], Validation [Lead], Visualization [Lead], Writing—original draft [Lead], Writing—review & editing [Lead]), Alexis Barbarin (Funding acquisition [Equal], Resources [Lead], Writing—review & editing [Equal]), and Michael Reiskind (Funding acquisition [Equal], Project administration [Equal], Supervision [Supporting], Writing—review & editing [Equal])

References