Potential Effects of Climate Change on Tick-borne Diseases in Rhode Island.

Human cases of tick-borne diseases have been increasing in the United States. In particular, the incidence of Lyme disease, the major vector-borne disease in Rhode Island, has risen, along with cases of babesiosis and anaplasmosis, all vectored by the blacklegged tick. These increases might relate, in part, to climate change, although other environmental changes in the northeastern U.S. (land use as it relates to habitat; vertebrate host populations for tick reproduction and enzootic cycling) also contribute. Lone star ticks, formerly southern in distribution, have been spreading northward, including expanded distributions in Rhode Island. Illnesses associated with this species include ehrlichiosis and alpha-gal syndrome, which are expected to increase. Ranges of other tick species have also been expanding in southern New England, including the Gulf Coast tick and the introduced Asian longhorned tick. These ticks can carry human pathogens, but the implications for human disease in Rhode Island are unclear.

Correction: Why Lyme disease is common in the northern US, but rare in the south: The roles of host choice, host-seeking behavior, and tick density.

[This corrects the article DOI: 10.1371/journal.pbio.3001066.].

Why Lyme disease is common in the northern US, but rare in the south: The roles of host choice, host-seeking behavior, and tick density.

Lyme disease is common in the northeastern United States, but rare in the southeast, even though the tick vector is found in both regions. Infection prevalence of Lyme spirochetes in host-seeking ticks, an important component to the risk of Lyme disease, is also high in the northeast and northern midwest, but declines sharply in the south. As ticks must acquire Lyme spirochetes from infected vertebrate hosts, the role of wildlife species composition on Lyme disease risk has been a topic of lively academic discussion. We compared tick-vertebrate host interactions using standardized sampling methods among 8 sites scattered throughout the eastern US. Geographical trends in diversity of tick hosts are gradual and do not match the sharp decline in prevalence at southern sites, but tick-host associations show a clear shift from mammals in the north to reptiles in the south. Tick infection prevalence declines north to south largely because of high tick infestation of efficient spirochete reservoir hosts (rodents and shrews) in the north but not in the south. Minimal infestation of small mammals in the south results from strong selective attachment to lizards such as skinks (which are inefficient reservoirs for Lyme spirochetes) in the southern states. Selective host choice, along with latitudinal differences in tick host-seeking behavior and variations in tick densities, explains the geographic pattern of Lyme disease in the eastern US.

Local abundance of Ixodes scapularis in forests: Effects of environmental moisture, vegetation characteristics, and host abundance.

Ixodes scapularis is the primary vector of Lyme disease spirochetes in eastern and central North America, and local densities of this tick can affect human disease risk. We sampled larvae and nymphs from sites in Massachusetts and Wisconsin, USA, using flag/drag devices and by collecting ticks from hosts, and measured environmental variables to evaluate the environmental factors that affect local distribution and abundance of I. scapularis. Our sites were all forested areas with known I. scapularis populations. Environmental variables included those associated with weather (e.g., temperature and relative humidity), vegetation characteristics (at canopy, shrub, and ground levels), and host abundance (small and medium-sized mammals and reptiles). The numbers of larvae on animals at a given site and season showed a logarithmic relationship to the numbers in flag/drag samples, suggesting limitation in the numbers on host animals. The numbers of nymphs on animals showed no relationship to the numbers in flag/drag samples. These results suggest that only a small proportion of larvae and nymphs found hosts because in neither stage did the numbers of host-seeking ticks decline with increased numbers on hosts. Canopy cover was predictive of larval and nymphal numbers in flag/drag samples, but not of numbers on hosts. Numbers of small and medium-sized mammal hosts the previous year were generally not predictive of the current year's tick numbers, except that mouse abundance predicted log numbers of nymphs on all hosts the following year. Some measures of larval abundance were predictive of nymphal numbers the following year. The mean number of larvae per mouse was well predicted by measures of overall larval abundance (based on flag/drag samples and samples from all hosts), and some environmental factors contributed significantly to the model. In contrast, the mean numbers of nymphs per mouse were not well predicted by environmental variables, only by overall nymphal abundance on hosts. Therefore, larvae respond differently than nymphs to environmental factors. Furthermore, flag/drag samples provide different information about nymphal numbers than do samples from hosts. Flag/drag samples can provide information about human risk of acquiring nymph-borne pathogens because they provide information on the densities of ticks that might encounter humans, but to understand the epizootiology of tick-borne agents both flag/drag and host infestation data are needed.

Environmental Factors Affecting Survival of Immature Ixodes scapularis and Implications for Geographical Distribution of Lyme Disease: The Climate/Behavior Hypothesis.

Recent reports suggest that host-seeking nymphs in southern populations of Ixodes scapularis remain below the leaf litter surface, while northern nymphs seek hosts on leaves and twigs above the litter surface. This behavioral difference potentially results in decreased tick contact with humans in the south, and fewer cases of Lyme disease. We studied whether north-south differences in tick survival patterns might contribute to this phenomenon. Four month old larvae resulting from a cross between Wisconsin males and South Carolina females died faster under southern than under northern conditions in the lab, as has previously been reported for ticks from both northern and southern populations. However, newly-emerged larvae from Rhode Island parents did not differ consistently in mortality under northern and southern conditions, possibly because of their younger age. Survival is lower, and so the north-south survival difference might be greater in older ticks. Larval survival was positively related to larval size (as measured by scutal area), while survival was positively related to larval fat content in some, but not all, trials. The difference in larval survival under northern vs. southern conditions might simply result from faster metabolism under warmer southern conditions leading to shorter life spans. However, ticks consistently died faster under southern than under northern conditions in the laboratory when relative humidity was low (75%), but not under moderate (85%) or high (95%) RH. Therefore, mortality due to desiccation stress is greater under southern than under northern conditions. We hypothesize that mortality resulting from the greater desiccation stress under southern conditions acts as a selective pressure resulting in the evolution of host-seeking behavior in which immatures remain below the leaf litter surface in southern I. scapularis populations, so as to avoid the desiccating conditions at the surface. If this hypothesis is correct, it has implications for the effect of climate change on the future distribution of Lyme disease.

Relationships Between Maternal Engorgement Weight and the Number, Size, and Fat Content of Larval Ixodes scapularis (Acari: Ixodidae).

The relationship between engorgement weight of female Ixodes scapularis Say and characteristics of offspring was studied using field-collected females fed on rabbits in the laboratory. The number of eggs laid was positively related to maternal engorgement weight in one trial, and larval size (estimated by scutal area) was positively related to maternal engorgement weight in the other. These results suggest a trade-off in number of eggs produced versus average size of offspring, possibly determined during late engorgement. The adults for the two trials were collected from different sites in southern Rhode Island and in different seasons (the fall adults were newly emerged, while the spring adults had presumably lived through the winter), so it is not clear whether these results reflect genetic differences or subtle environmental differences between trials. Percent egg hatch and average fat content of larvae were not related to female engorgement weight. We present a modified method to measure lipid content of pooled larval ticks.

Comparison of survival patterns of northern and southern genotypes of the North American tick Ixodes scapularis (Acari: Ixodidae) under northern and southern conditions.

BACKGROUND: Several investigators have reported genetic differences between northern and southern populations of Ixodes scapularis in North America, as well as differences in patterns of disease transmission. Ecological and behavioral correlates of these genetic differences, which might have implications for disease transmission, have not been reported. We compared survival of northern with that of southern genotypes under both northern and southern environmental conditions in laboratory trials. METHODS: Subadult I. scapularis from laboratory colonies that originated from adults collected from deer from several sites in the northeastern, north central, and southern U.S. were exposed to controlled conditions in environmental chambers. Northern and southern genotypes were exposed to light:dark and temperature conditions of northern and southern sites with controlled relative humidities, and mortality through time was recorded. RESULTS: Ticks from different geographical locations differed in survival patterns, with larvae from Wisconsin surviving longer than larvae from Massachusetts, South Carolina or Georgia, when held under the same conditions. In another experiment, larvae from Florida survived longer than larvae from Michigan. Therefore, survival patterns of regional genotypes did not follow a simple north-south gradient. The most consistent result was that larvae from all locations generally survived longer under northern conditions than under southern conditions. CONCLUSIONS: Our results suggest that conditions in southern North America are less hospitable than in the north to populations of I. scapularis. Southern conditions might have resulted in ecological or behavioral adaptations that contribute to the relative rarity of I. scapularis borne diseases, such as Lyme borreliosis, in the southern compared to the northern United States.

Effect of Temperature on Feeding Period of Larval Blacklegged Ticks (Acari: Ixodidae) on Eastern Fence Lizards.

Ambient temperature can influence tick development time, and can potentially affect tick interactions with pathogens and with vertebrate hosts. We studied the effect of ambient temperature on duration of attachment of larval blacklegged ticks, Ixodes scapularis Say, to eastern fence lizards, Sceloporus undulatus (Bosc & Daudin). Feeding periods of larvae that attached to lizards under preferred temperature conditions for the lizards (WARM treatment: temperatures averaged 36.6°C at the top of the cage and 25.8°C at the bottom, allowing behavioral thermoregulation) were shorter than for larvae on lizards held under cool conditions (COOL treatment temperatures averaged 28.4°C at top of cage and 24.9°C at the bottom). The lizards were infested with larvae four times at roughly monthly intervals. Larval numbers successfully engorging and dropping declined and feeding period was longer after the first infestation.

Environmental management of mosquito-borne viruses in Rhode Island.

West Nile Virus (WNV) and Eastern Equine Encephalitis Virus (EEEV) are both primarily bird viruses, which can be transmitted by several mosquito species. Differences in larval habitats, flight, and biting patterns of the primary vector species result in substantial differences in epidemiology, with WNV more common, primarily occurring in urban areas, and EEEV relatively rare, typically occurring near swamp habitats. The complex transmission ecology of these viruses complicates prediction of disease outbreaks. The Rhode Island Department of Environmental Management (DEM) and Department of Health (DoH) provide prevention assistance to towns and maintain a mosquito surveillance program to identify potential disease risk. Responses to potential outbreaks follow a protocol based on surveillance results, assessment of human risk, and technical consultation.

Evaluation of nontarget effects of methoprene applied to catch basins for mosquito control.

The mosquito larvicide methoprene is a juvenile growth hormone mimic that is widely used to control mosquito larvae in stormwater catch basins. This study addresses two concerns pertaining to methoprene's use for mosquito control. First, measurements of methoprene concentrations were made from water in catch basins that had been treated with methoprene and from an adjoining salt pond near where the treated catch basins emptied. The concentrations of methoprene in catch basins and at drainage outlets after application at the rates currently used for mosquito control in southern Rhode Island were 0.5 ppb and lower, orders of magnitude below what has been determined as detrimental to organisms other than mosquitoes. Second, the effects of methoprene on the communities that live in catch basins were evaluated both in simulated catch basins in the laboratory and in actual catch basins in the field. We found no evidence of declines in abundances of any taxa attributable to the application. Furthermore, we found no consistent changes in community-level parameters (e.g., taxonomic richness, and dominance-diversity relationships) related to methoprene application in either field or laboratory trials.

Host-seeking activity and avian host preferences of mosquitoes associated with West Nile virus transmission in the northeastern U.S.A.

Mosquito host-seeking activity was studied using a custom-designed trap to explore: (1) at which time interval of the night adult mosquito abatement would be most effective, and (2) if there exists an avian-specific host-seeking preference. Overnight trials using traps baited with dry ice showed that Aedes taeniorhynchus (Wiedemann) was most active at dusk and was then captured throughout the night. In contrast, Culex spp. (Cx. pipiens (Linnaeus) and Cx. restuans (Theobald) delayed most activity until about two h after dusk and were then captured through the night. This pattern suggests that management activities directed at adult Culex spp. would be most effective if initiated well after sunset. Mosquito capture rates in traps baited with birds in net bags were significantly greater than those with empty net bags, indicating that mosquitoes were attracted to the birds and not incidentally being sucked in by the custom trap's strong fan motor (Wilcoxon matched-pairs signed-ranks test, n=24, t=30, p<0.05). Regression analysis showed that bird weight influenced mosquito attraction (r2=0.21, p=0.02). Trials with paired traps that contained different native bird species showed that Gray Catbirds, Dumatella carolinensis, attracted more mosquitoes than the heavier Northern Cardinals, Cardinalis cardinalis (paired samples t-test, t=2.58, df=7, p=0.04). However, attractiveness did not differ substantially among bird species, and Gray Catbirds did not attract more mosquitoes than all other birds combined as a group. American Robins, Turdus migratorius (n=4) were comparable in attractiveness to other bird species, but not enough American Robins were captured for a comprehensive study of mosquito avian preference.

Efficacy of methoprene for mosquito control in storm water catch basins.

This study evaluated the efficacy of methoprene, a widely used juvenile hormone mimic, formulated as 30-day slow release Altosid pellets, at controlling mosquitoes in underground storm water drainage catch basins. Data from applications to 1/4-sized cement catch basins in the laboratory, field observations from treated and untreated basins, and an experiment that confined mosquito larvae in floating emergence jars in catch basins showed that methoprene effectively controlled mosquitoes for a month under field conditions and substantially longer under laboratory conditions when applied at a dose of 3.5-g pellets per average-sized catch basin.

Effects of methoprene on oviposition by Aedes japonicus and Culex spp.

The mosquito larvicide methoprene is a juvenile growth hormone mimic that is widely used to control mosquitoes. This chemical disrupts normal mosquito development, drastically inhibiting emergence from the pupal to the adult stage. If the presence of methoprene attracts or deters mosquitoes from ovipositing it could have implications for mosquito control. This study evaluates whether methoprene attracts or deters mosquitoes likely to oviposit in catch basins. In a field experiment, methoprene formulated as liquid larvicide did not affect oviposition of either Culex spp. or Aedes japonicus in 19-1 plastic buckets.