The more, the healthier: Tree diversity reduces forest pests and pathogens.

How frequently, and under what conditions, biodiversity reduces disease through "dilution effects" has been a subject of ongoing research. A new study of forest pests in PLOS Biology provides strong evidence for their generality.

Effects of residential acaricide treatments on patterns of pathogen coinfection in blacklegged ticks.

Medically important ixodid ticks often carry multiple pathogens, with individual ticks frequently coinfected and capable of transmitting multiple infections to hosts, including humans. Acquisition of multiple zoonotic pathogens by immature blacklegged ticks (Ixodes scapularis) is facilitated when they feed on small mammals, which are the most competent reservoir hosts for Anaplasma phagocytophilum (which causes anaplasmosis in humans), Babesia microti (babesiosis) and Borrelia burgdorferi (Lyme disease). Here, we used data from a large-scale, long-term experiment to ask whether patterns of single and multiple infections in questing nymphal I. scapularis ticks from residential neighbourhoods differed from those predicted by independent assortment of pathogens, and whether patterns of coinfection were affected by residential application of commercial acaricidal products. Quantitative polymerase chain reaction was used for pathogen detection in multiplex reactions. In control neighbourhoods and those treated with a fungus-based biopesticide deployed against host-seeking ticks (Met52), ticks having only single infections of either B. microti or B. burgdorferi were significantly less common than expected, whereas coinfections with these 2 pathogens were significantly more common. However, use of tick control system bait boxes, which kill ticks attempting to feed on small mammals, eliminated the bias towards coinfection. Although aimed at reducing the abundance of host-seeking ticks, control methods directed at ticks attached to small mammals may influence human exposure to coinfected ticks and the probability of exposure to multiple tick-borne infections.

Impacts of biodiversity and biodiversity loss on zoonotic diseases.

Zoonotic diseases are infectious diseases of humans caused by pathogens that are shared between humans and other vertebrate animals. Previously, pristine natural areas with high biodiversity were seen as likely sources of new zoonotic pathogens, suggesting that biodiversity could have negative impacts on human health. At the same time, biodiversity has been recognized as potentially benefiting human health by reducing the transmission of some pathogens that have already established themselves in human populations. These apparently opposing effects of biodiversity in human health may now be reconcilable. Recent research demonstrates that some taxa are much more likely to be zoonotic hosts than others are, and that these animals often proliferate in human-dominated landscapes, increasing the likelihood of spillover. In less-disturbed areas, however, these zoonotic reservoir hosts are less abundant and nonreservoirs predominate. Thus, biodiversity loss appears to increase the risk of human exposure to both new and established zoonotic pathogens. This new synthesis of the effects of biodiversity on zoonotic diseases presents an opportunity to articulate the next generation of research questions that can inform management and policy. Future studies should focus on collecting and analyzing data on the diversity, abundance, and capacity to transmit of the taxa that actually share zoonotic pathogens with us. To predict and prevent future epidemics, researchers should also focus on how these metrics change in response to human impacts on the environment, and how human behaviors can mitigate these effects. Restoration of biodiversity is an important frontier in the management of zoonotic disease risk.

Deployment of a Reservoir-Targeted Vaccine Against Borrelia burgdorferi Reduces the Prevalence of Babesia microti Coinfection in Ixodes scapularis Ticks.

In the Northeast and upper Midwest of the United States, Babesia microti and Borrelia burgdorferi use Ixodes scapularis ticks as vector and Peromyscus leucopus mice as major reservoir host. We previously established, in a 5-year field trial, that a reservoir-targeted outer surface protein A vaccine reduces the prevalence of B. burgdorferi-infected ticks. We accessed ticks and mouse blood samples collected during the trial, extracted total DNA, and amplified the B. microti 18S rRNA gene. Vaccine deployment reduced the prevalence of ticks coinfected with B. microti and that of mice infected with B. microti. Breaking the enzootic cycle of B. burgdorferi may reduce the incidence of babesiosis.

Effects of Tick-Control Interventions on Tick Abundance, Human Encounters with Ticks, and Incidence of Tickborne Diseases in Residential Neighborhoods, New York, USA.

Tickborne diseases (TBDs) such as Lyme disease result in ≈500,000 diagnoses annually in the United States. Various methods can reduce the abundance of ticks at small spatial scales, but whether these methods lower incidence of TBDs is poorly understood. We conducted a randomized, replicated, fully crossed, placebo-controlled, masked experiment to test whether 2 environmentally safe interventions, the Tick Control System (TCS) and Met52 fungal spray, used separately or together, affected risk for and incidence of TBDs in humans and pets in 24 residential neighborhoods. All participating properties in a neighborhood received the same treatment. TCS was associated with fewer questing ticks and fewer ticks feeding on rodents. The interventions did not result in a significant difference in incidence of human TBDs but did significantly reduce incidence in pets. Our study is consistent with previous evidence suggesting that reducing tick abundance in residential areas might not reduce incidence of TBDs in humans.

Dilution effects in disease ecology.

For decades, people have reduced the transmission of pathogens by adding low-quality hosts to managed environments like agricultural fields. More recently, there has been interest in whether similar 'dilution effects' occur in natural disease systems, and whether these effects are eroded as diversity declines. For some pathogens of plants, humans and other animals, the highest-quality hosts persist when diversity is lost, so that high-quality hosts dominate low-diversity communities, resulting in greater pathogen transmission. Meta-analyses reveal that these natural dilution effects are common. However, studying them remains challenging due to limitations on the ability of researchers to manipulate many disease systems experimentally, difficulties of acquiring data on host quality and confusion about what should and should not be considered a dilution effect. Because dilution effects are widely used in managed disease systems and have been documented in a variety of natural disease systems, their existence should not be considered controversial. Important questions remain about how frequently they occur and under what conditions to expect them. There is also ongoing confusion about their relationships to both pathogen spillover and general biogeographical correlations between diversity and disease, which has resulted in an inconsistent and confusing literature. Progress will require rigorous and creative research.

Effects of physical impairments on fitness correlates of the white-footed mouse, Peromyscus leucopus.

Physical impairments are widely assumed to reduce the viability of individual animals, but their impacts on individuals within natural populations of vertebrates are rarely quantified. By monitoring wild populations of white-footed mice over 26 years, we assessed whether missing or deformed limbs, tail or eyes influenced the survival, body mass, movement and ectoparasite burden of their bearers. Of the 27 244 individuals monitored, 543 (2%) had visible physical impairments. Persistence times (survival) were similar between mice with and without impairments. Mice with eye and tail impairments had 5% and 6% greater mass, respectively, than unimpaired mice. Mice with tail impairments had larger home ranges than did unimpaired mice. Burdens of black-legged ticks (Ixodes scapularis) were higher among mice with tail and limb impairments while burdens of bot fly larvae (Cuterebra) were higher among mice with cataracts compared to mice without impairments. Our findings do not support the presupposition that physical impairments reduce viability in their bearers and are inconsistent with the devaluation of impaired individuals that pervaded early thinking in evolutionary biology.

Risk Factors for Bites and Diseases Associated With Black-Legged Ticks: A Meta-Analysis.

The emergence and spread of Lyme disease and other infections associated with black-legged ticks is causing a public health crisis. No human vaccines are currently available, and both diagnosis and treatment are sometimes ineffectual, leading to advocacy for self-directed preventative measures. These recommendations are widely communicated to the public, but there is limited evidence for their efficacy. We undertook a systematic review and mixed-effects meta-regression analysis of factors purported to increase or decrease risk of black-legged tick bites and tick-borne disease. Published articles used in the study spanned the years 1984-2018. Variables associated with increased probability of tick-borne disease, with odds ratios significantly greater than 1, included deer abundance, high density of nymph-stage black-legged ticks, landscapes with interspersed herbaceous and forested habitat, low human population density, gardens, cat ownership, and race. Contrary to recommendations, use of landscape-related tick control measures, such as clearing brush, trimming branches, and having a dry barrier between lawn and woods, tended to increase risk. Pet ownership increased bite risk. Bite risk was highest for children aged 5 years or less, with a secondary peak in persons aged 50-70 years. Although some widely disseminated recommendations are supported by the research analyzed, others require further evaluation. Additional research is also needed to understand the mechanisms underlying significant relationships.

Correction to: Systematic review and meta-analysis of tick-borne disease risk factors in residential yards, neighborhoods, and beyond.

Following publication of the original article [1], one of the authors, Dr. Sarah E. Bowden reported that at the time of the study she wasn't working for the Division of Global Migration and Quarantine, Centers for Disease Control, 1600 Clifton Road, Atlanta, GA 30329-4027, USA.

Systematic review and meta-analysis of tick-borne disease risk factors in residential yards, neighborhoods, and beyond.

BACKGROUND: Exposure to blacklegged ticks Ixodes scapularis that transmit pathogens is thought to occur peri-domestically. However, the locations where people most frequently encounter infected ticks are not well characterized, leading to mixed messages from public health officials about where risk is highest. METHODS: We conducted a systematic review and meta-analysis on spatial risk factors for tick-borne disease and tick bites in eastern North America. We examined three scales: the residential yard, the neighborhood surrounding (but not including) the yard, and outside the neighborhood. Nineteen eligible studies represented 2741 cases of tick-borne illness and 1447 tick bites. Using random effects models, we derived pooled odds ratio (OR) estimates. RESULTS: The meta-analysis revealed significant disease risk factors at the scale of the yard (OR 2.60 95% CI 1.96 - 3.46), the neighborhood (OR 4.08 95% CI 2.49 - 6.68), and outside the neighborhood (OR 2.03 95% CI 1.59 - 2.59). Although significant risk exists at each scale, neighborhood scale risk factors best explained disease exposure. Analysis of variance revealed risk at the neighborhood scale was 57% greater than risk at the yard scale and 101% greater than risk outside the neighborhood. CONCLUSIONS: This analysis emphasizes the importance of understanding and reducing tick-borne disease risk at the neighborhood scale. Risk-reducing interventions applied at each scale could be effective, but interventions applied at the neighborhood scale are most likely to protect human health. TRIAL REGISTRATION: The study was registered with PROSPERO: CRD42017079169 .

Tick-borne disease risk in a forest food web.

Changes to the community ecology of hosts for zoonotic pathogens, particularly rodents, are likely to influence the emergence and prevalence of zoonotic diseases worldwide. However, the complex interactions between abiotic factors, pathogens, vectors, hosts, and both food resources and predators of hosts are difficult to disentangle. Here we (1) use 19 yr of data from six large field plots in southeastern New York to compare the effects of hypothesized drivers of interannual variation in Lyme disease risk, including the abundance of acorns, rodents, and deer, as well as a series of climate variables; and (2) employ landscape epidemiology to explore how variation in predator community structure and forest cover influences spatial variation in the infection prevalence of ticks for the Lyme disease bacterium, Borrelia burgdorferi, and two other important tick-borne pathogens, Anaplasma phagocytophilum and Babesia microti. Acorn-driven increases in the abundance of mice were correlated with a lagged increase in the abundance of questing nymph-stage Ixodes scapularis ticks infected with Lyme disease bacteria. Abundance of white-tailed deer 2 yr prior also correlated with increased density of infected nymphal ticks, although the effect was weak. Density of rodents in the current year was a strong negative predictor of nymph density, apparently because high current abundance of these hosts can remove nymphs from the host-seeking population. Warm, dry spring or winter weather was associated with reduced density of infected nymphs. At the landscape scale, the presence of functionally diverse predator communities or of bobcats, the only obligate carnivore, was associated with reduced infection prevalence of I. scapularis nymphs with all three zoonotic pathogens. In the case of Lyme disease, infection prevalence increased where coyotes were present but smaller predators were displaced or otherwise absent. For all pathogens, infection prevalence was lowest when forest cover within a 1 km radius was high. Taken together, our results suggest that a food web perspective including bottom-up and top-down forcing is needed to understand drivers of tick-borne disease risk, a result that may also apply to other rodent-borne zoonoses. Prevention of exposure based on ecological indicators of heightened risk should help protect public health.

Cattle and rainfall affect tick abundance in central Kenya.

East Africa is a global hot spot for the diversity of ixodid ticks. As ectoparasites and as vectors of pathogens, ticks negatively affect the well-being of humans, livestock and wildlife. To prevent tick infestations, livestock owners and managers typically treat livestock with acaricides that kill ticks when they attempt to feed on livestock hosts. Because of the costs of preventing and mitigating tick parasitism, predicting where and when ticks will be abundant is an important challenge in this region. We used a 7-year monthly record of tick abundance on large experimental plots to assess the effects of rainfall, wildlife and cattle on larvae, nymphs and adults of two common tick species, Rhipicephalus pulchellus and Rhipicephalus praetextatus. Nymphal and adult ticks were more abundant when there had been high cumulative rainfall in the prior months. They were less abundant when cattle were present than when only large wild mammals were. Larval abundance was not affected by the presence of cattle, and larvae did not appear to be sensitive to rainfall in prior months, though they were less abundant in our surveys when rainfall was high in the sampling month. The challenges of managing ticks in this region are being exacerbated rapidly by changes in rainfall patterns wrought by climate change, and by overall increases in livestock, making efforts to predict the impacts of these drivers all the more pressing.

Quantifying dilution and amplification in a community of hosts for tick-borne pathogens.

Recent controversy over whether biodiversity reduces disease risk (dilution effect) has focused on the ecology of Lyme disease, a tick-borne zoonosis. A criticism of the dilution effect is that increasing host species richness might amplify disease risk, assuming that total host abundance, and therefore feeding opportunities for ticks, increase with species richness. In contrast, a dilution effect is expected when poor quality hosts for ticks and pathogens (dilution hosts) divert tick blood meals away from competent hosts. Even if host densities are additive, the relationship between host density and tick encounters can be nonlinear if the number of ticks that encounter a host is a saturating function of host density, which occurs if ticks aggregate on the remaining hosts rather than failing to find a host before death. Both dilution and amplification are theoretical possibilities, and assessing which is more prevalent required detailed analyses of empirical systems. We used field data to explore the degree of tick redistribution onto fewer individuals with variation in intraspecific host density and novel data-driven models for tick dynamics to determine how changes in vertebrate community composition influence the density of nymphs infected with the Lyme bacterium. To be conservative, we allowed total host density to increase additively with species richness. Our long-term field studies found that larval and nymphal ticks redistribute onto fewer individuals as host densities decline, that a large proportion of nymphs and adults find hosts, and that mice and chipmunks feed a large proportion of nymphs. White-footed mice, eastern chipmunks, short-tailed shrews, and masked shrews were important amplification hosts that greatly increased the density of infected nymphs. Gray squirrels and Virginia opossums were important dilution hosts. Removing these two species increased the maximum number of larvae attached to amplification hosts by 57%. Raccoons and birds were minor dilution hosts under some conditions. Even under the assumption of additive community assembly, some species are likely to reduce the density of infected nymphs as diversity increases. If the assumption of additivity is relaxed, then species that reduce the density of small mammals through predation or competition might substantially reduce disease risk.

Impacts of biodiversity on the emergence and transmission of infectious diseases.

Current unprecedented declines in biodiversity reduce the ability of ecological communities to provide many fundamental ecosystem services. Here we evaluate evidence that reduced biodiversity affects the transmission of infectious diseases of humans, other animals and plants. In principle, loss of biodiversity could either increase or decrease disease transmission. However, mounting evidence indicates that biodiversity loss frequently increases disease transmission. In contrast, areas of naturally high biodiversity may serve as a source pool for new pathogens. Overall, despite many remaining questions, current evidence indicates that preserving intact ecosystems and their endemic biodiversity should generally reduce the prevalence of infectious diseases.

Human health impacts of ecosystem alteration.

Human activity is rapidly transforming most of Earth's natural systems. How this transformation is impacting human health, whose health is at greatest risk, and the magnitude of the associated disease burden are relatively new subjects within the field of environmental health. We discuss what is known about the human health implications of changes in the structure and function of natural systems and propose that these changes are affecting human health in a variety of important ways. We identify several gaps and limitations in the research that has been done to date and propose a more systematic and comprehensive approach to applied research in this field. Such efforts could lead to a more robust understanding of the human health impacts of accelerating environmental change and inform decision making in the land-use planning, environmental conservation, and public health policy realms.

Frontiers in research on biodiversity and disease.

Global losses of biodiversity have galvanised efforts to understand how changes to communities affect ecological processes, including transmission of infectious pathogens. Here, we review recent research on diversity-disease relationships and identify future priorities. Growing evidence from experimental, observational and modelling studies indicates that biodiversity changes alter infection for a range of pathogens and through diverse mechanisms. Drawing upon lessons from the community ecology of free-living organisms, we illustrate how recent advances from biodiversity research generally can provide necessary theoretical foundations, inform experimental designs, and guide future research at the interface between infectious disease risk and changing ecological communities. Dilution effects are expected when ecological communities are nested and interactions between the pathogen and the most competent host group(s) persist or increase as biodiversity declines. To move beyond polarising debates about the generality of diversity effects and develop a predictive framework, we emphasise the need to identify how the effects of diversity vary with temporal and spatial scale, to explore how realistic patterns of community assembly affect transmission, and to use experimental studies to consider mechanisms beyond simple changes in host richness, including shifts in trophic structure, functional diversity and symbiont composition.

Bottlenecks in domestic animal populations can facilitate the emergence of Trypanosoma cruzi, the aetiological agent of Chagas disease.

Faeces-mediated transmission of Trypanosoma cruzi (the aetiological agent of Chagas disease) by triatomine insects is extremely inefficient. Still, the parasite emerges frequently, and has infected millions of people and domestic animals. We synthesize here the results of field and laboratory studies of T. cruzi transmission conducted in and around Arequipa, Peru. We document the repeated occurrence of large colonies of triatomine bugs (more than 1000) with very high infection prevalence (more than 85%). By inoculating guinea pigs, an important reservoir of T. cruzi in Peru, and feeding triatomine bugs on them weekly, we demonstrate that, while most animals quickly control parasitaemia, a subset of animals remains highly infectious to vectors for many months. However, we argue that the presence of these persistently infectious hosts is insufficient to explain the observed prevalence of T. cruzi in vector colonies. We posit that seasonal rains, leading to a fluctuation in the price of guinea pig food (alfalfa), leading to annual guinea pig roasts, leading to a concentration of vectors on a small subpopulation of animals maintained for reproduction, can propel T. cruzi through vector colonies and create a considerable force of infection for a pathogen whose transmission might otherwise fizzle out.

Reservoir targeted vaccine against Borrelia burgdorferi: a new strategy to prevent Lyme disease transmission.

A high prevalence of infection with Borrelia burgdorferi in ixodid ticks is correlated with a high incidence of Lyme disease. The transmission of B. burgdorferi to humans can be disrupted by targeting 2 key elements in its enzootic cycle: the reservoir host and the tick vector. In a prospective 5-year field trial, we show that oral vaccination of wild white-footed mice resulted in outer surface protein A-specific seropositivity that led to reductions of 23% and 76% in the nymphal infection prevalence in a cumulative, time-dependent manner (2 and 5 years, respectively), whereas the proportion of infected ticks recovered from control plots varied randomly over time. Significant decreases in tick infection prevalence were observed within 3 years of vaccine deployment. Implementation of such a long-term public health measure could substantially reduce the risk of human exposure to Lyme disease.

When is a parasite not a parasite? Effects of larval tick burdens on white-footed mouse survival.

Many animal species can carry considerable burdens of ectoparasites: parasites living on the outside of a host's body. Ectoparasite infestation can decrease host survival, but the magnitude and even direction of survival effects can vary depending on the type of ectoparasite and the nature and duration of the association. When ectoparasites also serve as vectors of pathogens, the effects of ectoparasite infestation on host survival have the potential to alter disease dynamics by regulating host populations and stabilizing transmission. We quantified the impact of larval Ixodes scapularis tick burdens on both within-season and overwinter survival of white-footed mice (Peromyscus leucopus) using a hierarchical Bayesian capture-mark-recapture model. I. scapularis and P. leucopus are, respectively, vectors and competent reservoirs for the causative agents of Lyme disease, anaplasmosis, and babesiosis. Using a data set of 5587 individual mouse capture histories over sixteen years, we found little evidence for any effect of tick burdens on either within-season or overwinter mouse survival probabilities. In male mice, tick burdens were positively correlated with within-season survival probabilities. Mean maximum tick burdens were also positively correlated with population rates of change during the concurrent breeding season. The apparent indifference of mice to high tick burdens may contribute to their effectiveness as reservoir hosts for several human zoonotic pathogens.