Messaging Should Reflect the Nuanced Relationship between Land Change and Zoonotic Disease Risk.

A hallmark of the media publicity surrounding COVID-19 has been the message that land change causes zoonotic diseases to spill over from wild animals to humans. The secondary peer-reviewed literature sends a similar message. However, as indicated in the primary peer-reviewed literature, the complexity of interacting variables involved in zoonotic disease spillover makes it unlikely for such a claim to be universally applicable. The secondary peer-reviewed literature and the mainstream media also differ markedly from the primary peer-reviewed literature in their lack of nuance in messaging about the relationship between land change and spillover risk. We advocate accurate, nuanced messaging for the sake of the local communities at greatest risk from zoonotic disease, for the sake of scientific credibility, and so that proportionate attention may be given to other possible drivers of spillover risk.

Examining Prevalence and Diversity of Tick-Borne Pathogens in Questing Ixodes pacificus Ticks in California.

Tick-borne diseases in California include Lyme disease (caused by Borrelia burgdorferi), infections with Borrelia miyamotoi, and human granulocytic anaplasmosis (caused by Anaplasma phagocytophilum). We surveyed multiple sites and habitats (woodland, grassland, and coastal chaparral) in California to describe spatial patterns of tick-borne pathogen prevalence in western black-legged ticks (Ixodes pacificus). We found that several species of Borrelia-B. burgdorferi, Borrelia americana, and Borrelia bissettiae-were observed in habitats, such as coastal chaparral, that do not harbor obvious reservoir host candidates. Describing tick-borne pathogen prevalence is strongly influenced by the scale of surveillance: aggregating data from individual sites to match jurisdictional boundaries (e.g., county or state) can lower the reported infection prevalence. Considering multiple pathogen species in the same habitat allows a more cohesive interpretation of local pathogen occurrence. IMPORTANCE Understanding the local host ecology and prevalence of zoonotic diseases is vital for public health. Using tick-borne diseases in California, we show that there is often a bias to our understanding and that studies tend to focus on particular habitats, e.g., Lyme disease in oak woodlands. Other habitats may harbor a surprising diversity of tick-borne pathogens but have been neglected, e.g., coastal chaparral. Explaining pathogen prevalence requires descriptions of data on a local scale; otherwise, aggregating the data can misrepresent the local dynamics of tick-borne diseases.

Borrelia miyamotoi Infections in Small Mammals, California, USA.

Surveillance to investigate the wildlife-vector transmission cycle of the human pathogen Borrelia miyamotoi in California, USA, revealed infections in dusky-footed woodrats, brush mice, and California mice. Phylogenetic analyses suggest a single, well-supported clade of B. miyamotoi is circulating in California.

Declines in large wildlife increase landscape-level prevalence of rodent-borne disease in Africa.

Populations of large wildlife are declining on local and global scales. The impacts of this pulse of size-selective defaunation include cascading changes to smaller animals, particularly rodents, and alteration of many ecosystem processes and services, potentially involving changes to prevalence and transmission of zoonotic disease. Understanding linkages between biodiversity loss and zoonotic disease is important for both public health and nature conservation programs, and has been a source of much recent scientific debate. In the case of rodent-borne zoonoses, there is strong conceptual support, but limited empirical evidence, for the hypothesis that defaunation, the loss of large wildlife, increases zoonotic disease risk by directly or indirectly releasing controls on rodent density. We tested this hypothesis by experimentally excluding large wildlife from a savanna ecosystem in East Africa, and examining changes in prevalence and abundance of Bartonella spp. infection in rodents and their flea vectors. We found no effect of wildlife removal on per capita prevalence of Bartonella infection in either rodents or fleas. However, because rodent and, consequently, flea abundance doubled following experimental defaunation, the density of infected hosts and infected fleas was roughly twofold higher in sites where large wildlife was absent. Thus, defaunation represents an elevated risk in Bartonella transmission to humans (bartonellosis). Our results (i) provide experimental evidence of large wildlife defaunation increasing landscape-level disease prevalence, (ii) highlight the importance of susceptible host regulation pathways and host/vector density responses in biodiversity-disease relationships, and (iii) suggest that rodent-borne disease responses to large wildlife loss may represent an important context where this relationship is largely negative.

Ecological Traits Driving the Outbreaks and Emergence of Zoonotic Pathogens.

Infectious diseases that are transmitted from wildlife hosts to humans, such as the Ebola virus and MERS virus, can be difficult to understand because the pathogens emerge from complex multifaceted ecological interactions. We use a wildlife-pathogen system-prairie dogs (Cynomys ludovicianus) and the plague bacterium (Yersinia pestis)-to describe aspects of disease ecology that apply to many cases of emerging infectious disease. We show that the monitoring and surveillance of hosts and vectors during the buildup to disease outbreaks are crucial for understanding pathogen-transmission dynamics and that a community-ecology framework is important to identify reservoir hosts. Incorporating multidisciplinary approaches and frameworks may improve wildlife-pathogen surveillance and our understanding of seemingly sporadic and rare pathogen outbreaks.

Metatranscriptomic investigation of single Ixodes pacificus ticks reveals diverse microbes, viruses, and novel mRNA-like endogenous viral elements.

Ticks are increasingly important vectors of human and agricultural diseases. While many studies have focused on tick-borne bacteria, far less is known about tick-associated viruses and their roles in public health or tick physiology. To address this, we investigated patterns of bacterial and viral communities across two field populations of western black-legged ticks (Ixodes pacificus). Through metatranscriptomic analysis of 100 individual ticks, we quantified taxon prevalence, abundance, and co-occurrence with other members of the tick microbiome. In addition to commonly found tick-associated microbes, we assembled 11 novel RNA virus genomes from Rhabdoviridae, Chuviridae, Picornaviridae, Phenuiviridae, Reoviridae, Solemovidiae, Narnaviridae and two highly divergent RNA virus genomes lacking sequence similarity to any known viral families. We experimentally verified the presence of these in I. pacificus ticks across several life stages. We also unexpectedly identified numerous virus-like transcripts that are likely encoded by tick genomic DNA, and which are distinct from known endogenous viral element-mediated immunity pathways in invertebrates. Taken together, our work reveals that I. pacificus ticks carry a greater diversity of viruses than previously appreciated, in some cases resulting in evolutionarily acquired virus-like transcripts. Our findings highlight how pervasive and intimate tick-virus interactions are, with major implications for both the fundamental biology and vectorial capacity of I. pacificus ticks. IMPORTANCE: Ticks are increasingly important vectors of disease, particularly in the United States where expanding tick ranges and intrusion into previously wild areas has resulted in increasing human exposure to ticks. Emerging human pathogens have been identified in ticks at an increasing rate, and yet little is known about the full community of microbes circulating in various tick species, a crucial first step to understanding how they interact with each and their tick host, as well as their ability to cause disease in humans. We investigated the bacterial and viral communities of the Western blacklegged tick in California and found 11 previously uncharacterized viruses circulating in this population.

A meta-analysis suggesting that the relationship between biodiversity and risk of zoonotic pathogen transmission is idiosyncratic.

Zoonotic pathogens are significant burdens on global public health. Because they are transmitted to humans from non-human animals, the transmission dynamics of zoonoses are necessarily influenced by the ecology of their animal hosts and vectors. The 'dilution effect' proposes that increased species diversity reduces disease risk, suggesting that conservation and public health initiatives can work synergistically to improve human health and wildlife biodiversity. However, the meta-analysis that we present here indicates a weak and highly heterogeneous relationship between host biodiversity and disease. Our results suggest that disease risk is more likely a local phenomenon that relies on the specific composition of reservoir hosts and vectors, and their ecology, rather than patterns of species biodiversity.

Plague outbreaks in prairie dog populations explained by percolation thresholds of alternate host abundance.

Highly lethal pathogens (e.g., hantaviruses, hendra virus, anthrax, or plague) pose unique public-health problems, because they seem to periodically flare into outbreaks before disappearing into long quiescent phases. A key element to their possible control and eradication is being able to understand where they persist in the latent phase and how to identify the conditions that result in sporadic epidemics or epizootics. In American grasslands, plague, caused by Yersinia pestis, exemplifies this quiescent-outbreak pattern, because it sporadically erupts in epizootics that decimate prairie dog (Cynomys ludovicianus) colonies, yet the causes of outbreaks and mechanisms for interepizootic persistence of this disease are poorly understood. Using field data on prairie community ecology, flea behavior, and plague-transmission biology, we find that plague can persist in prairie-dog colonies for prolonged periods, because host movement is highly spatially constrained. The abundance of an alternate host for disease vectors, the grasshopper mouse (Onychomys leucogaster), drives plague outbreaks by increasing the connectivity of the prairie dog hosts and therefore, permitting percolation of the disease throughout the primary host population. These results offer an alternative perspective on plague's ecology (i.e., disease transmission exacerbated by alternative hosts) and may have ramifications for plague dynamics in Asia and Africa, where a single main host has traditionally been considered to drive Yersinia ecology. Furthermore, abundance thresholds of alternate hosts may be a key phenomenon determining outbreaks of disease in many multihost-disease systems.

Surveillance of Rocky Mountain wood ticks (Dermacentor andersoni) and American dog ticks (Dermacentor variabilis) in Colorado.

Ticks pose an emerging threat of infectious pathogen transmission in the United States in part due to expanding suitable habitat ranges in the wake of climate change. Active and passive tick surveillance can inform maps of tick distributions to warn the public of their risk of exposure to ticks. In Colorado, widespread active surveillance programs have difficulty due to the state's diverse terrain. However, combining multiple citizen science techniques can create a more accurate representation of tick distribution than any passive surveillance dataset alone. Our study uses county-level tick distribution data from Northern Arizona University, the Colorado Department of Public Health and the Environment, and veterinary surveillance in addition to literature data to assess the distribution of the Rocky Mountain wood tick, Dermacentor andersoni, and the American dog tick, Dermacentor variabilis. We found that D. andersoni for the most part inhabits counties at higher elevations than D. variabilis in Colorado.

Citizen Science Provides an Efficient Method for Broad-Scale Tick-Borne Pathogen Surveillance of Ixodes pacificus and Ixodes scapularis across the United States.

Tick-borne diseases have expanded over the last 2 decades as a result of shifts in tick and pathogen distributions. These shifts have significantly increased the need for accurate portrayal of real-time pathogen distributions and prevalence in hopes of stemming increases in human morbidity. Traditionally, pathogen distribution and prevalence have been monitored through case reports or scientific collections of ticks or reservoir hosts, both of which have challenges that impact the extent, availability, and accuracy of these data. Citizen science tick collections and testing campaigns supplement these data and provide timely estimates of pathogen prevalence and distributions to help characterize and understand tick-borne disease threats to communities. We utilized our national citizen science tick collection and testing program to describe the distribution and prevalence of four Ixodes-borne pathogens, Borrelia burgdorferi sensu lato, Borrelia miyamotoi, Anaplasma phagocytophilum, and Babesia microti, across the continental United States. IMPORTANCE In the 21st century, zoonotic pathogens continue to emerge, while previously discovered pathogens continue to have changes within their distribution and prevalence. Monitoring these pathogens is resource intensive, requiring both field and laboratory support; thus, data sets are often limited within their spatial and temporal extents. Citizen science collections provide a method to harness the general public to collect samples, enabling real-time monitoring of pathogen distribution and prevalence.

Predicting the current and future distribution of the western black-legged tick, Ixodes pacificus, across the Western US using citizen science collections.

In the twenty-first century, ticks and tick-borne diseases have expanded their ranges and impact across the US. With this spread, it has become vital to monitor vector and disease distributions, as these shifts have public health implications. Typically, tick-borne disease surveillance (e.g., Lyme disease) is passive and relies on case reports, while disease risk is calculated using active surveillance, where researchers collect ticks from the environment. Case reports provide the basis for estimating the number of cases; however, they provide minimal information on vector population or pathogen dynamics. Active surveillance monitors ticks and sylvatic pathogens at local scales, but it is resource-intensive. As a result, data are often sparse and aggregated across time and space to increase statistical power to model or identify range changes. Engaging public participation in surveillance efforts allows spatially and temporally diverse samples to be collected with minimal effort. These citizen-driven tick collections have the potential to provide a powerful tool for tracking vector and pathogen changes. We used MaxEnt species distribution models to predict the current and future distribution of Ixodes pacificus across the Western US through the use of a nationwide citizen science tick collection program. Here, we present niche models produced through citizen science tick collections over two years. Despite obvious limitations with citizen science collections, the models are consistent with previously-predicted species ranges in California that utilized more than thirty years of traditional surveillance data. Additionally, citizen science allows for an expanded understanding of I. pacificus distribution in Oregon and Washington. With the potential for rapid environmental changes instigated by a burgeoning human population and rapid climate change, the development of tools, concepts, and methodologies that provide rapid, current, and accurate assessment of important ecological qualities will be invaluable for monitoring and predicting disease across time and space.

Estimating disease vector population size from citizen science data.

Citizen science projects have the potential to address hypotheses requiring extremely large datasets that cannot be collected with the financial and labour constraints of most scientific projects. Data collection by the general public could expand the scope of scientific enquiry if these data accurately capture the system under study. However, data collection inconsistencies by the untrained public may result in biased datasets that do not accurately represent the natural world. In this paper, we harness the availability of scientific and public datasets of the Lyme disease tick vector to identify and account for biases in citizen science tick collections. Estimates of tick abundance from the citizen science dataset correspond moderately with estimates from direct surveillance but exhibit consistent biases. These biases can be mitigated by including factors that may impact collector participation or effort in statistical models, which, in turn, result in more accurate estimates of tick population sizes. Accounting for collection biases within large-scale, public participation datasets could update species abundance maps and facilitate using the wealth of citizen science data to answer scientific questions at scales that are not feasible with traditional datasets.

Community ecology and disease risk: lizards, squirrels, and the Lyme disease spirochete in California, USA.

Vector-borne zoonotic diseases are often maintained in complex transmission cycles involving multiple vertebrate hosts and their arthropod vectors. In the state of California, U.S.A., the spirochete Borrelia burgdorferi, which causes Lyme disease, is transmitted between vertebrate hosts by the western black-legged tick, Ixodes pacificus. Several mammalian species serve as reservoir hosts of the spirochete, but levels of tick infestation, reservoir competence, and Borrelia-infection prevalence vary widely among such hosts. Here, we model the host (lizards, Peromyscus mice, Californian meadow voles, dusky-footed wood rats, and western gray squirrels), vector, and pathogen community of oak woodlands in northwestern California to determine the relative importance of different tick hosts. Observed infection prevalence of B. burgdorferi in host-seeking I. pacificus nymphs was 1.8-5.3%, and our host-community model estimated an infection prevalence of 1.6-2.2%. The western gray squirrel (Sciurus griseus) was the only source of infected nymphs. Lizards, which are refractory to Borrelia infection, are important in feeding subadult ticks but reduce disease risk (nymphal infection prevalence). Species identity is therefore critical in understanding and determining the local disease ecology.

Ecological Fallacy and Aggregated Data: A Case Study of Fried Chicken Restaurants, Obesity and Lyme Disease.

Interdisciplinary approaches are merited when attempting to understand the complex and idiosyncratic processes driving the spillover of pathogens from wildlife and vector species to human populations. Public health data are often available for zoonotic pathogens but can lead to erroneous conclusions if the data have been spatially or temporally aggregated. As an illustration, we use human Lyme disease incidence data as a case study to examine correlations between mammalian biodiversity, fried chicken restaurants and obesity rates on human disease incidence. We demonstrate that Lyme disease incidence is negatively correlated with mammalian biodiversity, the abundance of fried chicken restaurants and obesity rates. We argue, however, that these correlations are spurious, representing both an 'ecologic fallacy' and Simpson's paradox, and are generated by the use of aggregated data. We argue that correlations based on aggregated data across large spatial scales must be rigorously examined before being invoked as proof of disease ecology theory or as a rationale for public health policy.

Inferring host-parasite relationships using stable isotopes: implications for disease transmission and host specificity.

Identifying the roles of different hosts and vectors is a major challenge in the study of the ecology of diseases caused by multi-host pathogens. Intensive field studies suggested that grasshopper mice (Onychomys leucogaster) help spread the bacterium that causes plague (Yersinia pestis) in prairie dog colonies by sharing fleas with prairie dogs (Cynomys ludovicianus); yet conclusive evidence that prairie dog fleas (Oropsylla hirsuta) feed on grasshopper mice is lacking. Using stable nitrogen isotope analysis, we determined that many blood-engorged O. hirsuta collected from wild grasshopper mice apparently contained blood meals of prairie dogs. These results suggest that grasshopper mice may be infected with Y. pestis via mechanisms other than flea feeding, e.g., early phase or mechanical transmission or scavenging carcasses, and raise questions about the ability of grasshopper mice to maintain Y. pestis in prairie dog colonies during years between plague outbreaks. They also indicate that caution may be warranted when inferring feeding relationships based purely on the occurrence of fleas or other haematophagous ectoparasites on hosts. Stable-isotope analysis may complement or provide a useful alternative to immunological or molecular techniques for identifying hosts of cryptically feeding ectoparasites, and for clarifying feeding relationships in studies of host-parasite interactions.

Evidence for the involvement of an alternate rodent host in the dynamics of introduced plague in prairie dogs.

1. The introduction of plague to North America is a significant threat to colonies of prairie dogs (Cynomys ludovicianus), a species of conservation concern in the Great Plains. Other small rodents are exposed to the causative agent, Yersinia pestis, during or after epizootics; yet, its effect on these rodents is not known, and their role in transmitting and maintaining plague in the absence of prairie dogs remains unclear. 2. We live-trapped small rodents and collected their fleas on 11 colonies before, during and after plague epizootics in Colorado, USA, from 2004 to 2006. Molecular genetic (polymerase chain reaction) assays were used to identify Y. pestis in fleas. 3. Abundance of northern grasshopper mice (Onychomys leucogaster) was low on sites following epizootics in 2004, and declined markedly following plague onset on other colonies in 2005. These changes coincided with exposure of grasshopper mice to plague, and with periods when mice became infested with large numbers of prairie dog fleas (Oropsylla hirsuta), including some that were infected with Y. pestis. Additionally, several Pleochaetis exilis, fleas restricted to grasshopper mice and never found on prairie dogs on our site, were polymerase chain reaction-positive for Y. pestis, indicating that grasshopper mice can infect their own fleas. No changes in abundance of other rodent species could be attributed to plague, and no other rodents hosted O. hirsuta during epizootics, or harboured Y. pestis-infected fleas. 4. In spring 2004, grasshopper mice were most numerous in colonies that suffered plague the following year, and the pattern of colony extinctions over a 12-year period mirrored patterns of grasshopper mouse abundance in our study area, suggesting that colonies with high densities of grasshopper mice may be more susceptible to outbreaks. We speculate that grasshopper mice help spread Y. pestis during epizootics through their ability to survive infection, harbour prairie dog fleas and, during their wide-ranging movements, transport infected fleas among burrows, which functionally connects prairie dog coteries that would otherwise be socially distinct.

Effects of weather and plague-induced die-offs of prairie dogs on the fleas of northern grasshopper mice.

Plague, the disease caused by the bacterium Yersinia pestis, can have devastating impacts on black-tailed prairie dogs (Cynomys ludovicianus Ord). Other mammal hosts living on prairie dog colonies may be important in the transmission and maintenance of plague. We examined the flea populations of northern grasshopper mice (Onychomys leucogaster Wied) before, during, and after plague epizootics in northern Colorado and studied the influence of host and environmental factors on flea abundance patterns. Grasshopper mice were frequently infested with high numbers of fleas, most commonly Pleochaetis exilis Jordan and Thrassis fotus Jordan. Flea loads changed in response to both environmental temperature and rainfall. After plague-induced prairie dog die-offs, flea loads and likelihood of infestation were unchanged for P. exilis, but T. fotus loads declined.

Spatial analysis of plague in California: niche modeling predictions of the current distribution and potential response to climate change.

BACKGROUND: Plague, caused by the bacterium Yersinia pestis, is a public and wildlife health concern in California and the western United States. This study explores the spatial characteristics of positive plague samples in California and tests Maxent, a machine-learning method that can be used to develop niche-based models from presence-only data, for mapping the potential distribution of plague foci. Maxent models were constructed using geocoded seroprevalence data from surveillance of California ground squirrels (Spermophilus beecheyi) as case points and Worldclim bioclimatic data as predictor variables, and compared and validated using area under the receiver operating curve (AUC) statistics. Additionally, model results were compared to locations of positive and negative coyote (Canis latrans) samples, in order to determine the correlation between Maxent model predictions and areas of plague risk as determined via wild carnivore surveillance. RESULTS: Models of plague activity in California ground squirrels, based on recent climate conditions, accurately identified case locations (AUC of 0.913 to 0.948) and were significantly correlated with coyote samples. The final models were used to identify potential plague risk areas based on an ensemble of six future climate scenarios. These models suggest that by 2050, climate conditions may reduce plague risk in the southern parts of California and increase risk along the northern coast and Sierras. CONCLUSION: Because different modeling approaches can yield substantially different results, care should be taken when interpreting future model predictions. Nonetheless, niche modeling can be a useful tool for exploring and mapping the potential response of plague activity to climate change. The final models in this study were used to identify potential plague risk areas based on an ensemble of six future climate scenarios, which can help public managers decide where to allocate surveillance resources. In addition, Maxent model results were significantly correlated with coyote samples, indicating that carnivore surveillance programs will continue to be important for tracking the response of plague to future climate conditions.