Spatial and temporal patterns of the emerging tick-borne pathogen Borrelia miyamotoi in blacklegged ticks (Ixodes scapularis) in New York.

Borrelia miyamotoi, a bacterium that causes relapsing fever, is found in ixodid ticks throughout the northern hemisphere. The first cases of human infection with B. miyamotoi were identified in 2011. In the eastern USA, blacklegged ticks (Ixodes scapularis) become infected by feeding on an infected vertebrate host, or through transovarial transmission. We surveyed B. miyamotoi prevalence in ticks within forested habitats in Dutchess County, New York, and identified possible reservoir hosts. To assess spatial variation in infection, we collected questing nymphal ticks at > 150 sites. To assess temporal variation in infection, we collected questing nymphs for 8 years at a single study site. We collected questing larval ticks from nine plots to estimate the amount of transovarial transmission. To evaluate potential reservoir hosts, we captured 14 species of mammal and bird hosts naturally infested with larval blacklegged ticks and held these hosts in the laboratory until ticks fed to repletion and molted to nymphs. We determined infection for all ticks using quantitative polymerase chain reaction. The overall infection prevalence of questing nymphal ticks across all sites was ~ 1%, but prevalence at individual sites was as high as 9.1%. We detected no significant increase in infection through time. Only 0.4% of questing larval ticks were infected. Ticks having fed as larvae from short-tailed shrews, red squirrels, and opossums tended to have higher infection prevalence than did ticks having fed on other hosts. Further studies of the role of hosts in transmission are warranted. The locally high prevalence of B. miyamotoi in the New York/New England landscape suggests the importance of vigilance by health practitioners and the public.

The Relationship Between Soil Arthropods and the Overwinter Survival of Ixodes scapularis (Acari: Ixodidae) Under Manipulated Snow Cover.

We explored the relationship between the diversity and abundance of the soil arthropod predator community and the overwinter survival of engorged larval Ixodes scapularis Say under variable snow cover in a hardwood forest. We reduced the snow cover over 30 soil core field microcosms, simulating predicted changes in snow pack in the northeastern United States. An additional 29 microcosms were used as references with no snow pack manipulation. Each microcosm contained 15 engorged larval I. scapularis. We expected lower soil temperature without insulating snow cover to reduce tick survival. However, we observed that reduced snow cover had no effect, with 44.2 and 44.7% overwintering successfully in the reference and snow-removal plots, respectively. Increasing taxonomic family richness of arthropod predators and the total number of large (>1 mm) arthropod predators significantly reduced the overwinter survivorship of I. scapularis within the microcosms. Small (<1 mm) arthropod predator abundance had no effect. Our results suggest that forests with complex natural arthropod predator communities show reduced tick survival.

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.

Biodiversity loss and the rise of zoonotic pathogens.

The unprecedented loss of biological diversity from anthropogenic causes has profound impacts on human health. One way that biodiversity loss threatens human health is by exacerbating risk and incidence of infectious diseases. This paper briefly reviews two zoonotic diseases--West Nile virus (WNV) illness and Lyme disease (LD)--in which high diversity in the community of vertebrate hosts for arthropod vectors strongly reduces human risk. In both cases, the primary reservoirs for the pathogen are species that dominate in human-impacted, low-diversity communities. As a result, the generalist vectors responsible for transmitting the pathogens to humans have relatively high feeding rates on these reservoirs, leading to high infection prevalence in mosquito (for WNV) and tick (for LD) vectors. In contrast, where native vertebrate diversity is high, mosquito and tick vectors evidently feed from a wider variety of hosts, most of which are poor reservoirs for the pathogens, resulting in lower infection prevalence. Protection of humans against exposure to zoonotic pathogens should be added to the list of utilitarian functions provided by high biodiversity.

Impacts of large herbivorous mammals on bird diversity and abundance in an African savanna.

Large native mammals are declining dramatically in abundance across Africa, with strong impacts on both plant and animal community dynamics. However, the net effects of this large-scale loss in megafauna are poorly understood because responses by several ecologically important groups have not been assessed. We used a large-scale, replicated exclusion experiment in Kenya to investigate the impacts of different guilds of native and domestic large herbivores on the diversity and abundance of birds over a 2-year period. The exclusion of large herbivorous native mammals, including zebras (Equus burchelli), giraffes (Giraffa camelopardalis), elephants (Loxodonta africana), and buffalos (Syncerus caffer), increased the diversity of birds by 30%. Most of this effect was attributable to the absence of elephants and giraffes; these megaherbivores reduced both the canopy area of subdominant woody vegetation and the biomass of ground-dwelling arthropods, and both of these factors were good predictors of the diversity of birds. The canopy area of subdominant trees was positively correlated with the diversity of granivorous birds. The biomass of ground-dwelling arthropods was positively correlated with the diversity of insectivorous birds. Our results suggest that most native large herbivores are compatible with an abundant and diverse bird fauna, as are cattle if they are at a relatively low stocking rate. Future research should focus on determining the spatial arrangements and densities of megaherbivores that will optimize both megaherbivore abundance and bird diversity.

Effects of species diversity on disease risk.

The transmission of infectious diseases is an inherently ecological process involving interactions among at least two, and often many, species. Not surprisingly, then, the species diversity of ecological communities can potentially affect the prevalence of infectious diseases. Although a number of studies have now identified effects of diversity on disease prevalence, the mechanisms underlying these effects remain unclear in many cases. Starting with simple epidemiological models, we describe a suite of mechanisms through which diversity could increase or decrease disease risk, and illustrate the potential applicability of these mechanisms for both vector-borne and non-vector-borne diseases, and for both specialist and generalist pathogens. We review examples of how these mechanisms may operate in specific disease systems. Because the effects of diversity on multi-host disease systems have been the subject of much recent research and controversy, we describe several recent efforts to delineate under what general conditions host diversity should increase or decrease disease prevalence, and illustrate these with examples. Both models and literature reviews suggest that high host diversity is more likely to decrease than increase disease risk. Reduced disease risk with increasing host diversity is especially likely when pathogen transmission is frequency-dependent, and when pathogen transmission is greater within species than between species, particularly when the most competent hosts are also relatively abundant and widespread. We conclude by identifying focal areas for future research, including (1) describing patterns of change in disease risk with changing diversity; (2) identifying the mechanisms responsible for observed changes in risk; (3) clarifying additional mechanisms in a wider range of epidemiological models; and (4) experimentally manipulating disease systems to assess the impact of proposed mechanisms.

Effects of acorn production and mouse abundance on abundance and Borrelia burgdorferi infection prevalence of nymphal Ixodes scapularis ticks.

Risk of exposure to Lyme disease is a function of the local abundance of nymphal Ixodes ticks that are infected with the etiological agent, the spirochete Borrelia burgdorferi. We monitored abundance of white-footed mice (the principal B. burgdorferi reservoir in the eastern and central United States) and acorns (a critical food resource for mice), and Ixodes scapularis ticks, as well as ambient temperature (cumulative growing degree days) and growing season precipitation, in a forested landscape of southeastern New York State from 1994 to 2000. We found that acorn production in autumn strongly influenced abundance of white-footed mice the following summer and that abundance of mice in summer, when larval ticks are active, influenced the abundance of infected nymphs the following year. Consequently, the abundance of infected nymphal ticks can be predicted from acorn production 1.75 years earlier. Monitoring of natural fluctuations in acorn production thus supports results of prior acorn addition experiments that were conducted at small spatial scales. Growing degree days and precipitation either had no significant effect on density of nymphs or marginally increased the explanatory power of models that included acorns or mouse density as independent variables. We conclude that, at our study site in New York, the risk of human exposure to Lyme disease is affected by mouse density in the prior year and by acorn production 2 years previously.

Spatiotemporal variation in a Lyme disease host and vector: black-legged ticks on white-footed mice.

We monitored population density of white-footed mice (Peromyscus leucopus), burdens of immature black-legged ticks (Ixodes scapularis) on mice, and infection prevalence of host-seeking ticks on six forest plots in southeastern New York State from 1995 through 1999. Despite densities of mice that fluctuated two orders of magnitude, average larval and nymphal tick burdens per mouse remained remarkably constant. Spatial variability in mouse density and tick burdens was modest. The total number of larval and nymphal ticks that fed on the mouse population each year depended strongly on population density of mice; a steady increase was observed in both mouse density and total tick meals on mice from 1996 through 1999. The result was a steady increase in the infection prevalence of nymphal and adult ticks with the etiological agent of Lyme disease, Borrelia burgdorferi, over this time. We suggest that fluctuations in population density of mice, combined with possible regulation of tick burdens on mice, may influence risk of human exposure to Lyme disease.

Infestation of Peromyscus leucopus and Tamias striatus by Ixodes scapularis (Acari: Ixodidae) in relation to the abundance of hosts and parasites.

The risk of humans acquiring Lyme disease is a function of the local density of nymphal and adult ticks that are infected with Lyme disease spirochetes. This in turn, will be related to host-use patterns of ticks and to the densities of both juvenile ticks and their hosts. At a forested site in Dutchess County, NY, we quantified host-use patterns of larval and nymphal Ixodes scapularis Say infesting the 2 dominant vertebrate hosts, white-footed mice and eastern chipmunks, during a 3-yr period. Larval tick burdens were 2-3 times higher on mice than they were on chipmunks, whereas nymphal tick burdens were > 3 times higher on chipmunks than they were on mice. We used multiple regression analysis to examine juvenile tick and host densities as independent variables influencing tick burdens. The density of questing larval ticks was positively correlated with larval tick burdens on mice, whereas the density of questing nymphs was weakly related to nymphal burdens on either host. Effects of the densities of mice and chipmunks on tick burdens were strong in some years, but weak in others. Moreover, the sign of the regression coefficients changed from one year to the next. We argue that these results are inconsistent with a passive encounter model of host selection, and suggest instead that either tick behavior or host responses cause strong biases in the distribution of juvenile ticks on their hosts.

Experimental studies of interactions between wild turkeys and black-legged ticks.

Wild turkeys are increasing in abundance and distribution in eastern North America, but their potential role as hosts for ticks, or as predators on ticks, is unknown. We performed two experiments, one to determine whether juvenile black-legged ticks (Ixodes scapularis) feed successfully on turkeys, and the other to determine if turkeys depredate adult black-legged ticks in forest habitats. Of 550 larval ticks placed directly on 5 captive wild turkeys, none engorged and only 7 (1.3%) were recovered; the remainder apparently were consumed during preening. Of 165 nymphal ticks placed on the turkeys, 5 engorged and 8 unengorged ticks were collected; 152 (93.3%) were apparently consumed. Of 250 adult ticks introduced into forest enclosures exposed to turkey foraging, 89.5% were recaptured, which was not significantly different from the 92.2% recaptured in control enclosures from which turkeys were excluded. We conclude that wild turkeys are unlikely to host juvenile black-legged ticks in nature, and that turkey foraging is unlikely to reduce local density of adult ticks.

Coinfection of blacklegged ticks (Acari: Ixodidae) in Dutchess County, New York, with the agents of Lyme disease and human granulocytic ehrlichiosis.

Adult blacklegged ticks, Ixodes scapularis Say, collected from forested sites in Dutchess County, NY, were tested for infection with the etiologic agents of Lyme disease, Borrelia burgdorferi Johnson, Schmid, Hyde, Steigerwalt & Brenner, and human granulocytic ehrlichiosis (HGE). Rates of infection with the 2 pathogens were high and independent of one another, confirming prior findings and suggesting that a variety of hosts may be competent reservoirs of the HGE agent.

Chain reactions linking acorns to gypsy moth outbreaks and Lyme disease risk.

In eastern U.S. oak forests, defoliation by gypsy moths and the risk of Lyme disease are determined by interactions among acorns, white-footed mice, moths, deer, and ticks. Experimental removal of mice, which eat moth pupae, demonstrated that moth outbreaks are caused by reductions in mouse density that occur when there are no acorns. Experimental acorn addition increased mouse density. Acorn addition also increased densities of black-legged ticks, evidently by attracting deer, which are key tick hosts. Mice are primarily responsible for infecting ticks with the Lyme disease agent. The results have important implications for predicting and managing forest health and human health.

Temporal and spatial dynamics of Ixodes scapularis (Acari: Ixodidae) in a rural landscape.

We studied seasonal, interannual, and both small- and large-scale spatial variation in the abundance of blacklegged ticks, Ixodes scapularis Say, in a semirural landscape in southeastern New York. Using transect drag sampling, we found that ticks were approximately twice as abundant in 1994 as in the preceding 2 yr. In 1994, larval ticks showed a strong peak in activity in late spring, coincident with the nymphal peak that year. All post-egg life stages were more abundant in forested than in shrubby or herbaceous habitat types, but peak abundance of larvae shifted from oak-dominated forest in 1992 to maple-dominated forest in 1993 and 1994. All life stages were highly clumped at small spatial scales, but larvae were the most aggregated. Within the forested habitat types, we observed an initial increase followed by a decrease in small-scale clumping during seasonal activity for each life stage. We discuss potential effects of the observed temporal and spatial variation on risk of Lyme disease. Because of pronounced variation in abundance and activity patterns among years and habitat types, we caution against generalizing from short-term or spatially limited studies.

Larval density and feeding success of Ixodes scapularis on two species of Peromyscus.

One potential mechanism for the regulation of tick populations is density-dependent feeding success on vertebrate hosts. In a series of laboratory experiments, we tested whether the density of larval Ixodes scapularis on the mice Peromyscus maniculatus and Peromyscus leucopus influenced tick feeding success. For both host species, the proportion of ticks feeding to repletion was constant (approximately 40-50%) over a range of infestation from 5 to 100 ticks per mouse. For P. leucopus, neither mass nor molting success of fed ticks was significantly related to tick density on the host. However, for P. maniculatus, we observed a statistically significant increase in molting success with increasing tick density on hosts, thus demonstrating facilitation rather than density-dependent regulation. Although results were not statistically significant, we observed a tendency for previously exposed P. leucopus to support lower tick feeding success than naive mice; however, even for previously exposed mice, tick feeding success was not density dependent. Our results do not support the notion that density-dependent feeding on hosts regulates density of I. scapularis populations at the numbers tested.

Intrinsic density-dependent regulation of vole populations.

Considerable controversy exists over the role of density-dependent processes in controlling animal population size. In populations that fluctuate cyclically or erratically, for example many voles and insects, theory predicts that either density-dependence is weak, or that density-dependent responses lag behind density. One key mechanism for lagged density-dependence is a delay in regeneration of food resources following heavy exploitation. Here we show that meadow vole (Microtus pennsylvanicus) populations respond immediately to high density by reducing breeding effort and hence population growth, disproving the hypothesis that density-dependence is weak. In addition, vole populations do not show a delay in growth following marked reduction in plant biomass (their source of food and cover). We conclude that intrinsic density-dependence processes tend to stabilize vole populations, and that cyclic dynamics are not caused by lagged effects of resource exploitation.

The ecology of territoriality in small mammals.

Recent research on space use and social behavior of small mammals has revealed pronounced differences in the degree of territoriality between species and between sexes within species. Hypotheses to explain these differences have been based on optimality approaches. Leading hypotheses are that the spatial distribution, abundance and renewal rates of food resources determine whether females defend territories, and that the spatial and temporal pattern of availability of females determines whether males are territorial. Other hypotheses invoke resources other than food, or maintain that territoriality in females deters infanticide. This review briefly summarizes these hypotheses and evaluates recently collected evidence from comparative and experimental studies.