A Hitchhiker’s Guide to Invasion Biology: Describing the Ecological Mechanisms Underlying the Range Expansions of Two Ixodid Tick Species

Increasing incidence of many tick-borne diseases have been linked to recent expansions of tick species distributions. Many tick species are expanding their ranges because of anthropogenic changes in the landscape, shifting climatic variables, and increasing populations of suitable host species and tick habitat. Few empirical studies have been performed, however, investigating the ecological mechanisms underlying these range expansions. Ticks are parasitic organisms that disperse across landscape by hitchhiking on hosts, but must then survive in the environment for long periods of time between bloodmeals. Two species of ixodid tick, Ixodes affinis and Amblyomma maculatum, are simultaneously expanding their ranges throughout the Mid-Atlantic region of the United States, and provide a case study from which to examine the relative importance of host choice and apparent habitat preference in the resulting patterns of range expansion. The first objective of this research was to use field studies to describe the life history of each of these species in Virginia, and determine important host and habitat characteristics for the survival and expansion of these species in the Mid-Atlantic. Tick surveillance data were collected over five years in a variety of habitats throughout southeastern Virginia. These data were used to answer basic natural history questions about these ticks in novel habitats, including determining tick abundance and phenology, as well as habitat and host preferences. Although both tick species parasitized many of the same host species, differences in the habitat conditions necessary for tick population establishment resulted in different patterns of invasion. Understanding how and where these ticks establish is useful in understanding the public health risks associated with areas being invaded. The second objective of this research was to determine the ancestry of the northern populations of these ticks, using genetic connectivity among populations to determine the mostly likely pathways for dispersal from ancestral populations to the Mid-Atlantic. Despite overlapping host preferences throughout ontogeny, each species exhibited very different genetic and geographic patterns of population establishment and connectivity. Genetic evidence suggests that these species may rely on different key life stages to disperse successfully into novel environments, and that host vagility, habitat stability and habitat connectivity all play critical roles in the establishment of new tick populations. The third objective of this research was to use metrics derived from field and genetic studies to parameterize agent-based models, simulating tick range expansions under different habitat and host conditions. Incorporating parameter values specific to I. affinis and A. maculatum life history, host ranges, habitat preferences, and genetic diversity allowed for hypothesis testing on whether habitats or hosts have greater influences on the invasions of these species in the Mid-Atlantic. This research describes the first comparative case study of two tick species with unique host and habitat preferences dispersing simultaneously across a landscape, and increases our understanding of the relative importance of hosts and habitat in hitchhiker invasions

Identifying Requirements for the Invasion of a Tick Species and Tick-Borne Pathogen Through TICKSIM

Ticks and tick-borne diseases have been on the move throughout the United State over the past twenty years. We use an agent-based model, TICKSIM, to identify the key parameters that determine the success of invasion of the tick and if that is successful, the success of the tick-borne pathogen. We find that if an area has competent hosts, an initial population of ten ticks is predicted to always establish a new population. The establishment of the tick-borne pathogen depends on three parameters: the initial prevalence in the ten founding ticks, the probability that a tick infects the longer-lived hosts and the probability that a tick infects the shorter lived hosts. These results indicate that the transmission rates to hosts in the newly established area can be used to predict the potential risk of disease to humans

Modelling the Effects of Habitat and Hosts on Tick Invasions

Many tick species are invading new areas because of anthropogenic changes in the landscape, shifting climatic variables and increasing populations of suitable host species and tick habitat. However, the relative influences of habitat and hosts in tick dispersal and tick population establishment remain in question. A spatially explicit agent-based model was developed to explore the spatio-temporal dynamics of a generic tick population in the years immediately following the introduction of ticks into a novel environment. The general model was then adapted to investigate a case study of two recent tick species invasions into the Mid-Atlantic United States. The recent simultaneous range expansions of two ixodid tick species, Ixodes affinis and Amblyomma maculatum, provided an opportunity to determine if invasion patterns observed in the field could be replicated in silico on a small scale. The models presented here indicated that for generalist parasites, habitat connectivity is a better indicator than host mobility for spatial and genetic patterns of parasite range expansion. In addition, our results demonstrate the utility of including genetic variables into agent-based models: gene flow functions as a proxy for measuring dispersal, and models can be validated using results from the field

Comparative Population Genetics of Two Invading Ticks: Evidence of the Ecological Mechanisms Underlying Tick Range Expansions

Two species of ixodid tick, Ixodes affinis Neumann and Amblyomma maculatum Koch, are simultaneously expanding their ranges throughout the mid-Atlantic region of the US. Although we have some understanding of the ecology and life history of these species, the ecological mechanisms governing where and how new populations establish and persist are unclear. To assess population connectivity and ancestry, we sequenced a fragment of the 16S mitochondrial rRNA gene from a representative sample of individuals of both species from populations throughout the eastern US. We found that despite overlapping host preferences throughout ontogeny, each species exhibited very different genetic and geographic patterns of population establishment and connectivity. I. affinis was of two distinct mitochondrial clades, with a clear geographic break separating northern and southern populations. Both I. affinis populations showed evidence of recent expansion, although the southern population was more genetically diverse, indicating a longer history of establishment. A. maculatum exhibited diverse haplotypes that showed no significant relationship with geographic patterns and little apparent connectivity between sites. Heteroplasmy was also observed in the 16S mitochondrial rRNA gene in 3.5% of A. maculatum individuals. Genetic evidence suggests that these species rely on different key life stages to successfully disperse into novel environments, and that host vagility, habitat stability and habitat connectivity all play critical roles in the establishment of new tick populations

Newer Surveillance Data Extends Our Understanding of the Niche of \u3ci\u3eRickettsia montanensis\u3c/i\u3e (Rickettsiales: Rickettsiaceae) Infection of the American Dog Tick (Acari: Ixodidae) in the United States

Background: Understanding the geographic distribution of Rickettsia montanensis infections in Dermacentor variabilis is important for tick-borne disease management in the United States, as both a tick-borne agent of interest and a potential confounder in surveillance of other rickettsial diseases. Two previous studies modeled niche suitability for D. variabilis with and without R. montanensis, from 2002-2012, indicating that the D. variabilis niche overestimates the infected niche. This study updates these, adding data since 2012. Methods: Newer surveillance and testing data were used to update Species Distribution Models (SDMs) of D. variabilis, and R. montanensis infected D. variabilis, in the United States. Using random forest (RF) models, found to perform best in previous work, we updated the SDMs and compared them with prior results. Warren’s I niche overlap metric was used to compare between predicted suitability for all ticks and ‘pathogen positive niche’ models across datasets. Results: Warren’s I indicated \u3c 2% change in predicted niche, and there was no change in order of importance of environmental predictors, for D. variabilis or R. montanensis positive niche. The updated D. variabilis niche model overpredicted suitability compared to the updated R. montanensis positive niche in key peripheral parts of the range, but slightly underpredicted through the northern and midwestern parts of the range. This reinforces previous findings of a more constrained pathogen-positive niche than predicted by D. variabilis records alone. Conclusions: The consistency of predicted niche suitability for D. variabilis in the United States, with the addition of nearly a decade of new data, corroborates this is a species with generalist habitat requirements. Yet a slight shift in updated niche distribution, even of low suitability, included more southern areas, pointing to a need for continued and extended monitoring and surveillance. This further underscores the importance of revisiting vector and vector-borne disease distribution maps

Focus Stacking Images of Morphological Character States for Differentiating the Adults of \u3ci\u3eIxodes affinis\u3c/i\u3e and \u3ci\u3eIxodes scapularis\u3c/i\u3e (Acari: Ixodidae) in Areas of Sympatry

Adult females and males of Ixodes affinis and Ixodes scapularis are illustrated by focus stacking image photography, and morphological character states are described that reliably differentiate the two species. In conjunction with other environmental cues, such as the questing phenology of adults, these characteristics will enable the rapid identification of adults of either sex along the southern Coastal Plain of the United States, where these species are sympatric

Ixodes affinis (Acari: Ixodidae) in Southeastern Virginia and Implications for the Spread of Borrelia burgdorferi, the Agent of Lyme Disease

Ixodes affinis Neumann is a hard-bodied (ixodid) tick known to be a competent vector for Borrelia burgdorferi, the agent of Lyme disease, and agents of other human diseases (Keirans et al. 1999). Ixodes affinis has been reported in Florida, Georgia, and South Carolina and throughout coastal North Carolina (Clark et al. 1998, Harrison et al. 2010). Harrison et al. (2010) indicated that I. affinis was established throughout the coastal plain of North Carolina up to the Virginia border and suggested that I. affinis might occur in Virginia

LYMESIM 2.0: An Updated Simulation of Blacklegged Tick (Acari: Ixodidae) Population Dynamics and Enzootic Transmission of \u3ci\u3eBorrelia burgdorferi\u3c/i\u3e (Spirochaetales: Spirochaetaceae)

Lyme disease is the most commonly reported vector-borne disease in the United States, and the number of cases reported each year continues to rise. The complex nature of the relationships between the pathogen (Borrelia burgdorferi sensu stricto), the tick vector (Ixodes scapularis Say), multiple vertebrate hosts, and numerous environmental factors creates challenges for understanding and predicting tick population and pathogen transmission dynamics. LYMESIM is a mechanistic model developed in the late 1990s to simulate the life-history of I. scapularis and transmission dynamics of B. burgdorferi s.s. Here we present LYMESIM 2.0, a modernized version of LYMESIM, that includes several modifications to enhance the biological realism of the model and to generate outcomes that are more readily measured under field conditions. The model is tested for three geographically distinct locations in New York, Minnesota, and Virginia. Model-simulated timing and densities of questing nymphs, infected nymphs, and abundances of nymphs feeding on hosts are consistent with field observations and reports for these locations. Sensitivity analysis highlighted the importance of temperature in host finding for the density of nymphs, the importance of transmission from small mammals to ticks on the density of infected nymphs, and temperature-related tick survival for both density of nymphs and infected nymphs. A key challenge for accurate modeling of these metrics is the need for regionally representative inputs for host populations and their fluctuations. LYMESIM 2.0 is a useful public health tool that downstream can be used to evaluate tick control interventions and can be adapted for other ticks and pathogens

Ticks and Spotted Fever Group Rickettsiae of Southeastern Virginia

The incidence of tick-borne rickettsial disease in the southeastern United States has been rising steadily through the past decade, and the range expansions of tick species and tick-borne infectious agents, new and old, has resulted in an unprecedented mix of vectors and pathogens. The results of an ongoing 4-year surveillance project describe the relative abundance of questing tick populations in southeastern Virginia. Since 2009, more than 66,000 questing ticks of 7 species have been collected from vegetation in a variety of habitats, with Amblyomma americanum constituting over 95% of ticks collected. Other species represented included Ixodes scapularis, Dermacentor variabilis, Amblyomma maculatum, Ixodes affinis, Haemaphysalis leporispalustris, and Ixodes brunneus. We found that 26.9–54.9% of A. americanum ticks tested were positive for Rickettsia amblyommii, a non-pathogenic symbiont of this tick species. We also found no evidence of R. rickettsii in D. variabilis ticks, although they did show low infection rates of R. montanensis (1.5–2.0%). Rickettsia parkeri and Candidatus R. andeanae were found in 41.8–55.7% and 0– 1.5% A. maculatum ticks, respectively. The rate of R. parkeri in A. maculatum ticks is among the highest in the literature and has increased in the 2 years since R. parkeri and A. maculatum were first reported in southeastern Virginia. We conclude that tick populations in southeastern Virginia have recently undergone dramatic changes in species and abundance and that these populations support a variety of rickettsial agents with the potential for increased risk to human health

Compositional Changes in Two Small Mammal Communities During Succession in Southeastern Virginia

Changes in the composition of two small mammal communities were studied during 8 and 9 years of ecological succession in southern Chesapeake. Virginia. Using monthly live-trapping on grids of similar size and history since their abandonment as agricultural fields, we learned that house mice were early colonists on one grid but not the other. Two species of herbivorous rodent and the granivorous eastern harvest mouse were numerically dominant on both grids across the study. Some species disappeared early on one grid but persisted to the end at the other. The two arboreal small mammals, golden and white-footed mice, were most predictable between sites, showing up at year 8, after significant woody elements were present on the grids. The greatest abundances of small mammals (and probably greatest total biomass too) were seen between years 4 and 6 of ecological succession