Emergence of Ixodes scapularis (Acari: Ixodidae) in a Small Mammal Population in a Coastal Oak-Pine Forest, Maine, USA

In the United States, surveillance has been key to tracking spatiotemporal emergence of blacklegged ticks [Ixodes scapularis Say (Ixodida:Ixodidae)] and their pathogens such as Borrelia burgdorferi Johnson, Schmid, Hyde, Steigerwalt & Brenner (Spirochaetales: Spirochaetaceae), the agent of Lyme disease. On the Holt Research Forest in midcoastal Maine, collection of feeding ticks from live-trapped small mammal hosts allowed us to track the emergence and establishment of I. scapularis, 1989–2019. From 1989–1995, we collected only I. angustus Neumann (Ixodida: Ixodidae)(vole tick), Dermacentor variabilis Say (Ixodida: Ixodidae) (American dog tick), and I. marxi Banks (Ixodida: Ixodidae) (squirrel tick) from seven species of small mammals. The most abundant tick host was the white-footed mouse [Peromyscus leucopus Rafinesque (Rodentia:Cricetidae)] followed by the red-backed vole (Myodes gapperi Vigors (Rodentia: Cricetidae)). Emergence of I. scapularis was signaled via the appearance of subadult I. scapularis in 1996. Emergence of B. burgdorferi was signaled through its appearance in I. scapularis feeding on mice in 2005. There was a substantial increase in I. scapularis prevalence (proportion of hosts parasitized) and burdens (ticks/host) on white-footed mice and red-backed voles in 2007. The ~11-yr time-to-establishment for I. scapularis was consistent with that seen in other studies. White-footed mice comprised 65.9% of all captures and hosted 94.1% of the total I. scapularis burden. The white-footed mouse population fluctuated interannually, but did not trend up as did I. scapularis prevalence and burdens. There were concurrent declines in I. angustus and D. variabilis. We discuss these results in the broader context of regional I. scapularis range expansion.

Effects of physical impairments on fitness correlates of the white-footed mouse, Peromyscus leucopus

Physical impairments are widely assumed to reduce the viability of individual animals, but their impacts on individuals within natural populations of vertebrates are rarely quantified. By monitoring wild populations of white-footed mice over 26 years, we assessed whether missing or deformed limbs, tail or eyes influenced the survival, body mass, movement and ectoparasite burden of their bearers. Of the 27 244 individuals monitored, 543 (2%) had visible physical impairments. Persistence times (survival) were similar between mice with and without impairments. Mice with eye and tail impairments had 5% and 6% greater mass, respectively, than unimpaired mice. Mice with tail impairments had larger home ranges than did unimpaired mice. Burdens of black-legged ticks ( Ixodes scapularis ) were higher among mice with tail and limb impairments while burdens of bot fly larvae ( Cuterebra ) were higher among mice with cataracts compared to mice without impairments. Our findings do not support the presupposition that physical impairments reduce viability in their bearers and are inconsistent with the devaluation of impaired individuals that pervaded early thinking in evolutionary biology.

Long-term stress level in a small mammal species undergoing range expansion

Rapid climate change is currently altering species distribution ranges. Evaluating the long-term stress level in wild species undergoing range expansion may help better understanding how species cope with the changing environment. Here, we focused on the white-footed mouse (Peromyscus leucopus), a widespread small mammal species in North-America whose distribution range is rapidly shifting northward. We evaluated long-term stress level in several populations of P. leucopus in Quebec (Canada), from the northern edge of the species distribution to more core populations in Southern Quebec. We first tested the hypothesis that populations at the range margin are under higher stress than more established populations in the southern region of our study area. We then compared four measures of long-term stress level to evaluate the congruence between these commonly used methods. We did not detect any significant geographical trend in stress level across our study populations of P. leucopus. Most notably, we found no clear congruence between the four measures of stress level we used, and conclude that these four commonly used methods are not equivalent, thereby not comparable across studies.

Experimental Demonstration of Reservoir Competence of the White-Footed Mouse, Peromyscus leucopus (Rodentia: Cricetidae), for the Lyme Disease Spirochete, Borrelia mayonii (Spirochaetales: Spirochaetaceae)

The white-footed mouse, Peromyscus leucopus (Rafinesque), is a reservoir for the Lyme disease spirochete Borrelia burgdorferi sensu stricto in the eastern half of the United States, where the blacklegged tick, Ixodes scapularis Say (Acari: Ixodidae), is the primary vector. In the Midwest, an additional Lyme disease spirochete, Borrelia mayonii, was recorded from naturally infected I. scapularis and P. leucopus. However, an experimental demonstration of reservoir competence was lacking for a natural tick host. We therefore experimentally infected P. leucopus with B. mayonii via I. scapularis nymphal bites and then fed uninfected larvae on the mice to demonstrate spirochete acquisition and passage to resulting nymphs. Of 23 mice fed on by B. mayonii-infected nymphs, 21 (91%) developed active infections. The infection prevalence for nymphs fed as larvae on these infected mice 4 wk post-infection ranged from 56 to 98%, and the overall infection prevalence for 842 nymphs across all 21 P. leucopus was 75% (95% confidence interval, 72–77%). To assess duration of infectivity, 10 of the P. leucopus were reinfested with uninfected larval ticks 12 wk after the mice were infected. The overall infection prevalence for 480 nymphs across all 10 P. leucopus at the 12-wk time point was 26% (95% confidence interval, 23–31%), when compared with 76% (95% confidence interval, 71–79%) for 474 nymphs from the same subset of 10 mice at the 4-wk time point. We conclude that P. leucopus is susceptible to infection with B. mayonii via bite by I. scapularis nymphs and an efficient reservoir for this Lyme disease spirochete.

Aversion of the invasive Asian longhorned tick to the white-footed mouse, the dominant reservoir of tick-borne pathogens in the United States

The Asian longhorned tick (Haemaphysalis longicornis) was reported for the first time in the United States of America in 2017 and has now spread across 12 states. The potential of this invasive tick vector to transmit pathogens will be determined through its association to native hosts, such as the white-footed mouse (Peromyscus leucopus) which is the primary reservoir for the causative agent of Lyme disease (Borrelia burgdorferi) and other zoonotic pathogens. We placed larval H. longicornis on P. leucopus, 65% of the larvae (n = 40) moved off the host within a short period of time and none engorged. In contrast, larval black-legged ticks (Ixodes scapularis) did not move from where they were placed in the ear of the mouse. We then conducted a laboratory behavioural assay to assess the interaction of H. longicornis with the hair of potential mammalian host species in the United States of America. H. longicornis larvae were less likely to enter the hair zone of P. leucopus and humans compared to the hair of domestic cats, domestic dogs, and white-tailed deer. Our study identifies a tick-host hair interaction behaviour, which can be quantified in a laboratory assay to predict tick-host associations and provides insights into how ticks select a host.