Jesse L. Brunner

Hosts as ecological traps for the vector of Lyme disease

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.

Pathogenicity and transmission of chytridiomycosis in tiger salamanders (Ambystoma tigrinum)

Abstract A chytrid fungus, Batrachochytrium dendrobatidis, was found in salamanders, Ambystoma tigrinum stebbinsi, collected in southern Arizona, USA. The chytrid was isolated and cultured, and Kochs postulates were satisfied by infection of metamorphosed salamanders with pure culture and subsequent reisolation from these salamanders. We used the salamander strain and a strain isolated from lowland leopard frogs in Arizona, Rana yavapaiensis, to infect metamorphosed A. tigrinum, R. yavapaiensis, and R. boylii. All three species became infected, but none of the infected salamanders died within 60 days, and mortality of infected frogs did not differ significantly from controls, although sample size was small. Chytrid infection could not be detected by light histology in most of the infected frogs and one of the infected salamanders 60 days after infection. To date, there are three records of chytridiomycosis in salamanders on websites; ours is the first complete report of occurrence and pathology of chytridiomycosis in field-collected North American salamanders. Our results also demonstrate that chytridiomycosis does not always lead to mortality. Individuals within a species vary in susceptibility to infection, animals appear to recover from the infection, and syntopic salamanders and frogs may act as reciprocal pathogen reservoirs for chytrid infections.

INTRASPECIFIC RESERVOIRS: COMPLEX LIFE HISTORY AND THE PERSISTENCE OF A LETHAL RANAVIRUS

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 >5 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.

MULTIPLE CAUSES OF VARIABLE TICK BURDENS ON SMALL‐MAMMAL HOSTS

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.

Dose and host characteristics influence virulence of ranavirus infections.

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.

Estimating Reservoir Competence of Borrelia burgdorferi Hosts: Prevalence and Infectivity, Sensitivity, and Specificity

Abstract Most vector-borne zoonotic pathogens are transmitted among several host species, but different species vary considerably in their importance to pathogen transmission, at least partially because they vary in their propensity to infect feeding vectors. This propensity is often called realized reservoir competence. Realized reservoir competence is the product of 1) the probability the individual host is infected, i.e., infection prevalence, and 2) the probability that if the host is infected, it will transmit the infection to a feeding vector, or infectivity. Prevalence varies in space and time, whereas infectivity may be a property of the host species. Both prevalence and infectivity are ecologically and epidemiologically important, but measuring them simultaneously is difficult. We present a probabilistic model that separately estimates host infection prevalence and infectivity from data on the infection status of vectors collected from individual hosts, data generally used to measure realized reservoir competence. We then consider how imperfect diagnostic tests (i.e., false negatives and positives) influence these probabilities—estimates of prevalence and infectivity are fairly robust to false negatives, but not to false positives. We thus extend the model to estimate the rate of false positives in order to improve estimates of prevalence and infectivity. We illustrate these methods by reanalyzing data from LoGiudice et al. (2003; Proc. Natl. Acad. Sci. U.S.A. 100: 567–571) on the reservoir competence of ten vertebrate hosts of Borrelia burgdorferi, the agent of Lyme disease. We find that these vertebrate hosts vary both in prevalence and infectivity and that both values are highly, positively correlated among species.

Susceptibility of the Endangered California Tiger Salamander, Ambystoma californiense, to Ranavirus Infection

Emerging infectious diseases are implicated in the declines and extinctions of amphibians worldwide. Ranaviruses in the family Iridoviridae are a global concern and have caused amphibian die-offs in wild populations in North America, Europe, South America, and in commercial populations in Asia and South America. The movement of amphibians for bait, food, pets, and research provides a route for the introduction of ranaviruses into naive and potentially endangered species. In this report, we demonstrate that the California tiger salamander, Ambystoma californiense, is susceptible to Ambystoma tigrinum virus (ATV). This virus has not been previously reported in California tiger salamander, but observed mortality in experimentally infected animals suggests that California tiger salamander populations could be adversely affected by an ATV introduction.

Ranavirus: past, present and future

Emerging infectious diseases are a significant threat to global biodiversity. While historically overlooked, a group of iridoviruses in the genus Ranavirus has been responsible for die-offs in captive and wild amphibian, reptile and fish populations around the globe over the past two decades. In order to share contemporary information on ranaviruses and identify critical research directions, the First International Symposium on Ranaviruses was held in July 2011 in Minneapolis, MN, USA. Twenty-three scientists and veterinarians from nine countries examined the ecology and evolution of ranavirus–host interactions, potential reservoirs, transmission dynamics, as well as immunological and histopathological responses to infection. In addition, speakers discussed possible mechanisms for die-offs, and conservation strategies to control outbreaks.

Co-Infection of Blacklegged Ticks with Babesia microti and Borrelia burgdorferi Is Higher than Expected and Acquired from Small Mammal Hosts

Humans in the northeastern and midwestern United States are at increasing risk of acquiring tickborne diseases – not only Lyme disease, but also two emerging diseases, human granulocytic anaplasmosis and human babesiosis. Co-infection with two or more of these pathogens can increase the severity of health impacts. The risk of co-infection is intensified by the ecology of these three diseases because all three pathogens (Borrelia burgdorferi, Anaplasma phagocytophilum, and Babesia microti) are transmitted by the same vector, blacklegged ticks (Ixodes scapularis), and are carried by many of the same reservoir hosts. The risk of exposure to multiple pathogens from a single tick bite and the sources of co-infected ticks are not well understood. In this study, we quantify the risk of co-infection by measuring infection prevalence in 4,368 questing nymphs throughout an endemic region for all three diseases (Dutchess County, NY) to determine if co-infections occur at frequencies other than predicted by independent assortment of pathogens. Further, we identify sources of co-infection by quantifying rates of co-infection on 3,275 larval ticks fed on known hosts. We find significant deviations of levels of co-infection in questing nymphs, most notably 83% more co-infection with Babesia microti and Borrelia burgdorferi than predicted by chance alone. Further, this pattern of increased co-infection was observed in larval ticks that fed on small mammal hosts, but not on meso-mammal, sciurid, or avian hosts. Co-infections involving A. phagocytophilum were less common, and fewer co-infections of A. phagocytophilum and B. microti than predicted by chance were observed in both questing nymphs and larvae fed on small mammals. Medical practitioners should be aware of the elevated risk of B. microti/B. burgdorferi co-infection.

Reservoir Competence of Vertebrate Hosts for Anaplasma phagocytophilum

Fourteen vertebrate species (10 mammals and 4 birds) were assessed for their ability to transmit Anaplasma phagocytophilum, the bacterium that causes human granulocytic anaplasmosis, to uninfected feeding ixodid ticks. Small mammals were most likely to infect ticks but all species assessed were capable of transmitting the bacterium, in contrast to previous findings.