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.
The regional and international trade of live animals facilitates the movement, spillover, and emergence of zoonotic and epizootic pathogens around the world. Detecting pathogens in trade is critical ...for preventing their continued movement and introduction, but screening a sufficient fraction to ensure rare infections are detected is simply infeasible for many taxa and settings because of the vast numbers of animals involved-hundreds of millions of live animals are imported into the U.S.A. alone every year. Batch processing pools of individual samples or using environmental DNA (eDNA)-the genetic material shed into an organism's environment-collected from whole consignments of animals may substantially reduce the time and cost associated with pathogen surveillance. Both approaches, however, lack a framework with which to determine sampling requirements and interpret results. Here I present formulae for pooled individual samples (e.g,. swabs) and eDNA samples collected from finite populations and discuss key assumptions and considerations for their use with a focus on detecting Batrachochytrium salamandrivorans, an emerging pathogen that threatens global salamander diversity. While empirical validation is key, these formulae illustrate the potential for eDNA-based detection in particular to reduce sample sizes and help bring clean trade into reach for a greater number of taxa, places, and contexts.
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.
Ranaviruses are pathogens of ectothermic vertebrates, including amphibians. We reviewed patterns of host range and virulence of ranaviruses in the context of virus genotype and postulate that ...patterns reflect significant variation in the historical and current host range of three groups of Ranavirus: FV3-like, CMTV-like and ATV-like ranaviruses. Our synthesis supports previous hypotheses about host range and jumps: FV3s are amphibian specialists, while ATVs are predominantly fish specialists that switched once to caudate amphibians. The most recent common ancestor of CMTV-like ranaviruses and FV3-like forms appears to have infected amphibians but CMTV-like ranaviruses may circulate in both amphibian and fish communities independently. While these hypotheses are speculative, we hope that ongoing efforts to describe ranavirus genetics, increased surveillance of host species and targeted experimental assays of susceptibility to infection and/or disease will facilitate better tests of the importance of hypothetical evolutionary drivers of ranavirus virulence and host range.
•Patterns of ranavirus host range&impact explored in the context of virus genotype.•The history of infection and disease in Europe and the Americas are compared.•Hypotheses about historic and current host use of ranavirus groups are generated.
The stress-induced susceptibility hypothesis, which predicts chronic stress weakens immune defences, was proposed to explain increasing infectious disease-related mass mortality and population ...declines. Previous work characterized wetland salinization as a chronic stressor to larval amphibian populations. Thus, we combined field observations with experimental exposures quantifying epidemiological parameters to test the role of salinity stress in the occurrence of ranavirus-associated mass mortality events. Despite ubiquitous pathogen presence (94%), populations exposed to salt runoff had slightly more frequent ranavirus related mass mortality events, more lethal infections, and 117-times greater pathogen environmental DNA. Experimental exposure to chronic elevated salinity (0.8-1.6 g l
Cl
) reduced tolerance to infection, causing greater mortality at lower doses. We found a strong negative relationship between splenocyte proliferation and corticosterone in ranavirus-infected larvae at a moderate elevation of salinity, supporting glucocorticoid-medicated immunosuppression, but not at high salinity. Salinity alone reduced proliferation further at similar corticosterone levels and infection intensities. Finally, larvae raised in elevated salinity had 10 times more intense infections and shed five times as much virus with similar viral decay rates, suggesting increased transmission. Our findings illustrate how a small change in habitat quality leads to more lethal infections and potentially greater transmission efficiency, increasing the severity of ranavirus epidemics.
A variety of challenges arise when monitoring wildlife populations for disease. Sampling tissues can be invasive to hosts, and obtaining sufficient sample sizes can be expensive and time‐consuming, ...particularly for rare species and when pathogen prevalence is low. Environmental DNA (eDNA)‐based detection of pathogens is an alternative approach to surveillance for aquatic communities that circumvents many of these issues. Ranaviruses are emerging pathogens of ectothermic vertebrates linked to die‐offs of amphibian populations. Detecting ranavirus infections is critical, but nonlethal methods have the above issues and are prone to false negatives. We report on the feasibility and effectiveness of eDNA‐based ranavirus detection in the field. We compared ranavirus titres in eDNA samples collected from pond water to titres in wood frog (Lithobates sylvaticus; n = 5) tadpoles in sites dominated by this one species (n = 20 pond visits). We examined whether ranavirus DNA can be detected in eDNA from pond water when infections are present in the pond and if viral titres detected in eDNA samples correlate with the prevalence or intensity of ranavirus infections in tadpoles. With three 250 mL water samples, we were able to detect the virus in all visits with infected larvae (0.92 diagnostic sensitivity). Also, we found a strong relationship between the viral eDNA titres and titres in larval tissues. eDNA titres increased prior to observed die‐offs and declined afterwards, and were two orders of magnitude higher in ponds with a die‐off. Our results suggest that eDNA is useful for detecting ranavirus infections in wildlife and aquaculture.
Abstract Population size is an important metric to inform the conservation and management of species. For aquatic species, environmental DNA (eDNA) concentration has been suggested for non-invasively ...estimating population size. However, many biotic and abiotic factors simultaneously influence the production and degradation of eDNA which can alter the relationship between population size and eDNA concentration. We investigated the influence of temperature, salinity, and ranavirus infection on eDNA concentrations using tadpole mesocosms. Using linear regression models, we tested the influence of each experimental treatment on eDNA concentrations at three time points before and during epidemics. Prior to infection, elevated temperatures lowered eDNA concentrations, indicating that degradation was the driving force influencing eDNA concentrations. During early epidemics, no treatments strongly influenced eDNA concentrations and in late epidemics, productive forces dominated as ranavirus intensity and dead organisms increased eDNA concentrations. Finally, population size was only an important predictor of eDNA concentration in late epidemics and we observed high levels of variation between samples of replicate mesocosms. We demonstrate the complexities of several interacting factors influencing productive and degradative forces, variation in influences on eDNA concentration over short time spans, and examine the limitations of estimating population sizes from eDNA with precision in semi-natural conditions.
Climatic conditions are widely thought to govern the distribution and abundance of ectoparasites, such as the blacklegged tick (Ixodes scapularis), vector of the agents of Lyme disease and other ...emerging human pathogens. However, translating physiological tolerances to distributional limits or mortality is challenging. Ticks may be able to avoid or tolerate unsuitable conditions, and what is lethal to one life history stage may not extend to others. Thus, even after decades of research, there are clear gaps in our knowledge about how climatic conditions determine tick distributions or patterns of abundance. We present results from a 3‐year study combining daily hazard models and data from field experiments at three sites spanning much of I. scapularis' current latitudinal distribution. We examine three predominant hypotheses regarding how temperature and vapor pressure deficits affect stage‐specific survival and transition success and consider how these results influence population growth and distribution. We found that larvae are sensitive to temperature and vapor pressure deficits, whereas mortality of nymphs and adults is consistent with depletion of energy reserves. Consistent with prior work, we found that overwinter survival was high and successful stage transitions (e.g., fed nymphs molting to adults) were sensitive to temperature. Collectively, results from this comprehensive, multiyear, multistage field study suggest that population growth of I. scapularis is less limited by restrictive climatic conditions than has been broadly assumed, although influences on larval survival may slow tick population growth and establishment in some desiccating conditions. Further studies should integrate climate effects on stage‐specific survival to better understand these effects on population dynamics and range expansion in a changing climate.
Transmission is central to our understanding and efforts to control the spread of infectious diseases. Because transmission generally requires close contact, host movements and behaviors can shape ...transmission dynamics: random and complete mixing leads to the classic density-dependent model, but if hosts primarily interact locally (e.g., aggregate) or within groups, transmission may saturate. Manipulating host behavior may thus change both the rate and functional form of transmission. We used the ranavirus–wood frog (Lithobates sylvaticus) tadpole system to test whether transmission rates reflect contacts, and whether the functional form of transmission can be influenced by the distribution of food in mesocosms (widely dispersed, promoting random movement and mixing vs. a central pile, promoting aggregations). Contact rates increased with density, as expected, but transmission rapidly saturated. Observed rates of transmission were not explained by observed contact rates or the density-dependent model, but instead transmission in both treatments followed models allowing for heterogeneities in the transmission process. We argue that contacts were not generally limiting, but instead that our results are better explained by heterogeneities in host susceptibility. Moreover, manipulating host behavior to manage the spread of infectious disease may prove difficult to implement.
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.
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