Vectors of infectious diseases are generally thought to be regulated by abiotic conditions such as climate or the availability of specific hosts or habitats. In this study we tested whether blacklegged ticks, the vectors of Lyme disease, granulocytic anaplasmosis and babesiosis can be regulated by the species of vertebrate hosts on which they obligately feed. By subjecting field-caught hosts to parasitism by larval blacklegged ticks, we found that some host species (e.g. opossums, squirrels) that are abundantly parasitized in nature kill 83 -96% of the ticks that attempt to attach and feed, while other species are more permissive of tick feeding. Given natural tick burdens we document on these hosts, we show that some hosts can kill thousands of ticks per hectare. These results indicate that the abundance of tick vectors can be regulated by the identity of the hosts upon which these vectors feed. By simulating the removal of hosts from intact communities using empirical models, we show that the loss of biodiversity may exacerbate disease risk by increasing both vector numbers and vector infection rates with a zoonotic pathogen.

The evidence that climate warming is changing the distribution of Ixodes ticks and the pathogens they transmit is reviewed and evaluated. The primary approaches are either phenomenological, which typically assume that climate alone limits current and future distributions, or mechanistic, asking which tick-demographic parameters are affected by specific abiotic conditions. Both approaches have promise but are severely limited when applied separately. For instance, phenomenological approaches (e.g. climate envelope models) often select abiotic variables arbitrarily and produce results that can be hard to interpret biologically. On the other hand, although laboratory studies demonstrate strict temperature and humidity thresholds for tick survival, these limits rarely apply to field situations. Similarly, no studies address the influence of abiotic conditions on more than a few life stages, transitions or demographic processes, preventing comprehensive assessments. Nevertheless, despite their divergent approaches, both mechanistic and phenomenological models suggest dramatic range expansions of Ixodes ticks and tick-borne disease as the climate warms. The predicted distributions, however, vary strongly with the models' assumptions, which are rarely tested against reasonable alternatives. These inconsistencies, limited data about key tick-demographic and climatic processes and only limited incorporation of non-climatic processes have weakened the application of this rich area of research to public health policy or actions. We urge further investigation of the influence of climate on vertebrate hosts and tick-borne pathogen dynamics. In addition, testing model assumptions and mechanisms in a range of natural contexts and comparing their relative importance as competing models in a rigorous statistical framework will significantly advance our understanding of how climate change will alter the distribution, dynamics and risk of tick-borne disease.

Blood meals by blacklegged ticks (Ixodes scapularis) on vertebrate hosts serve to transmit the agents of several zoonotic diseases, including Lyme disease, human babesiosis, and human granulocytic anaplasmosis, between host and tick. If ticks are aggregated on hosts, a small proportion of hosts may be responsible for most transmission events. Therefore, a key element in understanding and controlling the transmission of these pathogens is identifying the group(s) or individuals feeding a disproportionate number of ticks. Previous studies of tick burdens, however, have focused on differences in mean annual burdens between one or a few groups of hosts, ignoring both the strong seasonal dynamics of I. scapularis and their aggregation on hosts. We present a statistical modeling framework that predicts burdens on individual hosts throughout the year as a function of temporal-, site-, and individual-specific attributes, as well as the degree of aggregation in a negative binomial distribution. We then fit alternate versions of this model to an 11-year data set of I. scapularis burdens on white-footed mice (Peromyscus leucopus) and eastern chipmunks (Tamias striatus) to explore which factors are important to predicting tick burdens. We found that tick burdens are a complex function of many extrinsic and intrinsic factors, including seasonality. Specifically: (1) burdens on mice and chipmunks increased with densities of host-seeking ticks in a manner that suggests hosts become saturated. (2) Chipmunks draw larval ticks away from mice, which are efficient reservoirs of the Lyme disease bacterium, and mice draw nymphs away from chipmunks, which are key nymphal hosts. (3) While individual correlates were statistically important, the relationships were complex, and no group or correlate (sex, age, mass) could explain which hosts fed a disproportionate number of ticks. (4) Ticks were strongly aggregated on hosts within and across groups suggesting that some undiscovered quality of individual hosts was responsible for the aggregation. (5) Those individuals that fed more nymphs than expected, and are thus more likely to be infected with the Lyme disease agent, also tend to feed and infect more larvae than expected. Predicting which individuals those are is not yet possible.

Virulent parasites cannot persist in small host populations unless the parasite also has a reservoir host. We hypothesize that, in hosts with complex life histories, one stage may act as an intraspecific reservoir for another. In amphibians, for example, larvae often occur at high densities, but these densities are ephemeral and fixed in space, whereas metamorphs are long-lived and vagile but may be very sparse. Parasite persistence is unlikely in either stage alone, but transmission between stages could maintain virulent parasites in seasonally fluctuating amphibian populations.We examined this hypothesis with a lethal ranavirus, Ambystoma tigrinum virus (ATV), that causes recurrent epidemics in larval tiger salamander populations, but which has no reservoir host and degrades quickly in the environment. Although exposure to ATV is generally lethal, larvae and metamorphs maintained sublethal, transmissible infections for Ͼ5 mo. Field data corroborate the persistence of ATV between epidemics in sublethally infected metamorphs. Three-quarters of dispersing metamorphs during one epidemic were infected, and apparently healthy metamorphs returning to breed harbored ATV infections. Our results suggest that larval epidemics amplify virus prevalence and sublethally infected metamorphs (re)introduce the virus into uninfected larval populations. Intraspecific reservoirs may explain the persistence of parasites in and declines of small, isolated amphibian populations.

Summary1. Animal populations exhibit considerable variation in their susceptibility to infection by emerging diseases, yet it is poorly understood how environmental and intrinsic factors contribute to these patterns. Considering that intrinsic factors (e.g. life history stage, nutritional state) can impact immune function, knowledge of the physiological mechanisms that mediate susceptibility to infection may improve our understanding of the emergence of disease in natural populations. 2. Ranavirus outbreaks have been associated with die-offs of amphibians worldwide. While the ecological factors associated with epidemics have been widely studied, little is known about how physiological factors mediate amphibian responses to ranavirus infection. 3. The neuroendocrine hypothalamus-pituitary-interrenal axis (HPI) is a physiological system central to coordinating energy balance and development. It is known to both stimulate and inhibit immune function in vertebrates in different contexts. We hypothesized that the HPI axis would also mediate responses to ranavirus infection. We used wood frog (Rana sylvatica) larvae and ranavirus isolated from recent die-offs of local wood frog populations to examine the physiological responses to infection. 4. In addition to increasing odds of death with increasing doses of virus in an LD 50 study, we saw a 1AE7-fold increase in the odds of death with each increase in Gosner stage at the time of infection. 5. We then examined the HPI stress response of prometamorphic tadpoles exposed to a lethal dose of ranavirus. Infected tadpoles exhibited significantly elevated corticosterone levels, more rapid developmental changes, and a greater decrease in body weight relative to controls over 6 days after exposure. 6. Although elevated corticosterone mobilizes resources and enhances immunity, its acceleration of metamorphosis may be maladaptive in response to ranavirus infection, because it can draw energy away from expensive immune responses. These findings provide insight into how the balance of energy between development and immune function may contribute to patterns of ranavirus infection in pre-metamorphic amphibians.

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Parasites play a prominent role in the ecology, evolution, and more recently, conservation of many organisms. For example, emerging infectious diseases, including a group of lethal ranaviruses, are associated with the declines and extinctions of amphibians around the world. An increasingly important basic and applied question is: what controls parasite virulence? We used a dose-response experiment with three laboratory-bred clutches of tiger salamander larvae (Ambystoma tigrinum) to test how the size of inoculum and host genetic factors influence the dynamics and outcome of ranavirus infections. We found that infection rates increased with dose and were strongly affected by clutch identity and host life history stage. Case mortality increased with dose of inoculum, but was unaffected by host characteristics. Average survival time decreased with dose and differed among clutches, but this was largely due to differences in the time to onset of symptoms. Overall, our results suggest that dose of inoculum and host characteristics (life history stage and genetic background) influence the establishment and early virus replication, and therefore the virulence of ranavirus infections.