Continental-scale dynamics of avian influenza in U.S. waterfowl are driven by demography, migration, and temperature.

Emerging diseases of wildlife origin are increasingly spilling over into humans and domestic animals. Surveillance and risk assessments for transmission between these populations are informed by a mechanistic understanding of the pathogens in wildlife reservoirs. For avian influenza viruses (AIV), much observational and experimental work in wildlife has been conducted at local scales, yet fully understanding their spread and distribution requires assessing the mechanisms acting at both local, (e.g., intrinsic epidemic dynamics), and continental scales, (e.g., long-distance migration). Here, we combined a large, continental-scale data set on low pathogenic, Type A AIV in the United States with a novel network-based application of bird banding/recovery data to investigate the migration-based drivers of AIV and their relative importance compared to well-characterized local drivers (e.g., demography, environmental persistence). We compared among regression models reflecting hypothesized ecological processes and evaluated their ability to predict AIV in space and time using within and out-of-sample validation. We found that predictors of AIV were associated with multiple mechanisms at local and continental scales. Hypotheses characterizing local epidemic dynamics were strongly supported, with age, the age-specific aggregation of migratory birds in an area and temperature being the best predictors of infection. Hypotheses defining larger, network-based features of the migration processes, such as clustering or between-cluster mixing explained less variation but were also supported. Therefore, our results support a role for local processes in driving the continental distribution of AIV.

Publisher Correction: A globally-distributed alien invasive species poses risks to United States imperiled species.

A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has been fixed in the paper.

A globally-distributed alien invasive species poses risks to United States imperiled species.

In the midst of Earth's sixth mass extinction event, non-native species are a driving factor in many imperiled species' declines. One of the most widespread and destructive alien invasive species in the world, wild pigs (Sus scrofa) threaten native species through predation, habitat destruction, competition, and disease transmission. We show that wild pigs co-occur with up to 87.2% of imperiled species in the contiguous U.S. identified as susceptible to their direct impacts, and we project increases in both the number of species at risk and the geographic extent of risks by 2025. Wild pigs may therefore present a severe threat to U.S. imperiled species, with serious implications for management of at-risk species throughout wild pigs' global distribution. We offer guidance for efficient allocation of research effort and conservation resources across species and regions using a simple approach that can be applied to wild pigs and other alien invasive species globally.

Discriminating patterns and drivers of multiscale movement in herpetofauna: The dynamic and changing environment of the Mojave desert tortoise.

Changes to animal movement in response to human-induced changes to the environment are of growing concern in conservation. Most research on this problem has focused on terrestrial endotherms, but changes to herpetofaunal movement are also of concern given their limited dispersal abilities and specialized thermophysiological requirements. Animals in the desert region of the southwestern United States are faced with environmental alterations driven by development (e.g., solar energy facilities) and climate change. Here, we study the movement ecology of a desert species of conservation concern, the Mojave desert tortoise (Gopherus agassizii). We collected weekly encounter locations of marked desert tortoises during the active (nonhibernation) seasons in 2013-2015, and used those data to discriminate movements among activity centers from those within them. We then modeled the probability of movement among activity centers using a suite of covariates describing characteristics of tortoises, natural and anthropogenic landscape features, vegetation, and weather. Multimodel inference indicated greatest support for a model that included individual tortoise characteristics, landscape features, and weather. After controlling for season, date, age, and sex, we found that desert tortoises were more likely to move among activity centers when they were further from minor roads and in the vicinity of barrier fencing; we also found that movement between activity centers was more common during periods of greater rainfall and during periods where cooler temperatures coincided with lower rainfall. Our findings indicate that landscape alterations and climate change both have the potential to impact movements by desert tortoises during the active season. This study provides an important baseline against which we can detect future changes in tortoise movement behavior.

Biotic and abiotic factors predicting the global distribution and population density of an invasive large mammal.

Biotic and abiotic factors are increasingly acknowledged to synergistically shape broad-scale species distributions. However, the relative importance of biotic and abiotic factors in predicting species distributions is unclear. In particular, biotic factors, such as predation and vegetation, including those resulting from anthropogenic land-use change, are underrepresented in species distribution modeling, but could improve model predictions. Using generalized linear models and model selection techniques, we used 129 estimates of population density of wild pigs (Sus scrofa) from 5 continents to evaluate the relative importance, magnitude, and direction of biotic and abiotic factors in predicting population density of an invasive large mammal with a global distribution. Incorporating diverse biotic factors, including agriculture, vegetation cover, and large carnivore richness, into species distribution modeling substantially improved model fit and predictions. Abiotic factors, including precipitation and potential evapotranspiration, were also important predictors. The predictive map of population density revealed wide-ranging potential for an invasive large mammal to expand its distribution globally. This information can be used to proactively create conservation/management plans to control future invasions. Our study demonstrates that the ongoing paradigm shift, which recognizes that both biotic and abiotic factors shape species distributions across broad scales, can be advanced by incorporating diverse biotic factors.

Inferring invasive species abundance using removal data from management actions.

Evaluation of the progress of management programs for invasive species is crucial for demonstrating impacts to stakeholders and strategic planning of resource allocation. Estimates of abundance before and after management activities can serve as a useful metric of population management programs. However, many methods of estimating population size are too labor intensive and costly to implement, posing restrictive levels of burden on operational programs. Removal models are a reliable method for estimating abundance before and after management using data from the removal activities exclusively, thus requiring no work in addition to management. We developed a Bayesian hierarchical model to estimate abundance from removal data accounting for varying levels of effort, and used simulations to assess the conditions under which reliable population estimates are obtained. We applied this model to estimate site-specific abundance of an invasive species, feral swine (Sus scrofa), using removal data from aerial gunning in 59 site/time-frame combinations (480-19,600 acres) throughout Oklahoma and Texas, USA. Simulations showed that abundance estimates were generally accurate when effective removal rates (removal rate accounting for total effort) were above 0.40. However, when abundances were small (<50) the effective removal rate needed to accurately estimates abundances was considerably higher (0.70). Based on our post-validation method, 78% of our site/time frame estimates were accurate. To use this modeling framework it is important to have multiple removals (more than three) within a time frame during which demographic changes are minimized (i.e., a closed population; ≤3 months for feral swine). Our results show that the probability of accurately estimating abundance from this model improves with increased sampling effort (8+ flight hours across the 3-month window is best) and increased removal rate. Based on the inverse relationship between inaccurate abundances and inaccurate removal rates, we suggest auxiliary information that could be collected and included in the model as covariates (e.g., habitat effects, differences between pilots) to improve accuracy of removal rates and hence abundance estimates.

Short-Term Space-Use Patterns of Translocated Mojave Desert Tortoise in Southern California.

Increasingly, renewable energy comprises a larger share of global energy production. Across the western United States, public lands are being developed to support renewable energy production. Where there are conflicts with threatened or endangered species, translocation can be used in an attempt to mitigate negative effects. For the threatened Mojave desert tortoise (Gopherus agassizii), we sought to compare habitat- and space-use patterns between short-distance translocated, resident, and control groups. We tested for differences in home range size based on utilization distributions and used linear mixed-effects models to compare space-use intensity, while controlling for demographic and environmental variables. In addition, we examined mean movement distances as well as home range overlap between years and for male and female tortoises in each study group. During the first active season post-translocation, home range size was greater and space-use intensity was lower for translocated tortoises than resident and control groups. These patterns were not present in the second season. In both years, there was no difference in home range size or space-use intensity between control and resident groups. Translocation typically resulted in one active season of questing followed by a second active season characterized by space-use patterns that were indistinguishable from control tortoises. Across both years, the number of times a tortoise was found in a burrow was positively related to greater space-use intensity. Minimizing the time required for translocated tortoises to exhibit patterns similar to non-translocated individuals may have strong implications for conservation by reducing exposure to adverse environmental conditions and predation. With ongoing development, our results can be used to guide future efforts aimed at understanding how translocation strategies influence patterns of animal space use.

Modeling and mapping the probability of occurrence of invasive wild pigs across the contiguous United States.

Wild pigs (Sus scrofa), also known as wild swine, feral pigs, or feral hogs, are one of the most widespread and successful invasive species around the world. Wild pigs have been linked to extensive and costly agricultural damage and present a serious threat to plant and animal communities due to their rooting behavior and omnivorous diet. We modeled the current distribution of wild pigs in the United States to better understand the physiological and ecological factors that may determine their invasive potential and to guide future study and eradication efforts. Using national-scale wild pig occurrence data reported between 1982 and 2012 by wildlife management professionals, we estimated the probability of wild pig occurrence across the United States using a logistic discrimination function and environmental covariates hypothesized to influence the distribution of the species. Our results suggest the distribution of wild pigs in the U.S. was most strongly limited by cold temperatures and availability of water, and that they were most likely to occur where potential home ranges had higher habitat heterogeneity, providing access to multiple key resources including water, forage, and cover. High probability of occurrence was also associated with frequent high temperatures, up to a high threshold. However, this pattern is driven by pigs' historic distribution in warm climates of the southern U.S. Further study of pigs' ability to persist in cold northern climates is needed to better understand whether low temperatures actually limit their distribution. Our model highlights areas at risk of invasion as those with habitat conditions similar to those found in pigs' current range that are also near current populations. This study provides a macro-scale approach to generalist species distribution modeling that is applicable to other generalist and invasive species.

Diseases at the livestock-wildlife interface: status, challenges, and opportunities in the United States.

In the last half century, significant attention has been given to animal diseases; however, our understanding of disease processes and how to manage them at the livestock-wildlife interface remains limited. In this study, we conduct a systematic review of the scientific literature to evaluate the status of diseases at the livestock-wildlife interface in the United States. Specifically, the goals of the literature review were three fold: first to evaluate domestic animal diseases currently found in the United States where wildlife may play a role; second to identify critical issues faced in managing these diseases at the livestock-wildlife interface; and third to identify potential technical and policy strategies for addressing these issues. We found that of the 86 avian, ruminant, swine, poultry, and lagomorph diseases that are reportable to the World Organization for Animal Health (OIE), 53 are present in the United States; 42 (79%) of these have a putative wildlife component associated with the transmission, maintenance, or life cycle of the pathogen; and 21 (40%) are known to be zoonotic. At least six of these reportable diseases-bovine tuberculosis, paratuberculosis, brucellosis, avian influenza, rabies, and cattle fever tick (vector control)-have a wildlife reservoir that is a recognized impediment to eradication in domestic populations. The complex nature of these systems highlights the need to understand the role of wildlife in the epidemiology, transmission, and maintenance of infectious diseases of livestock. Successful management or eradication of these diseases will require the development of cross-discipline and institutional collaborations. Despite social and policy challenges, there remain opportunities to develop new collaborations and new technologies to mitigate the risks posed at the livestock-wildlife interface.

Environmental and demographic determinants of avian influenza viruses in waterfowl across the contiguous United States.

Outbreaks of avian influenza in North American poultry have been linked to wild waterfowl. A first step towards understanding where and when avian influenza viruses might emerge from North American waterfowl is to identify environmental and demographic determinants of infection in their populations. Laboratory studies indicate water temperature as one determinant of environmental viral persistence and we explored this hypothesis at the landscape scale. We also hypothesized that the interval apparent prevalence in ducks within a local watershed during the overwintering season would influence infection probabilities during the following breeding season within the same local watershed. Using avian influenza virus surveillance data collected from 19,965 wild waterfowl across the contiguous United States between October 2006 and September 2009 We fit Logistic regression models relating the infection status of individual birds sampled on their breeding grounds to demographic characteristics, temperature, and interval apparent prevalence during the preceding overwintering season at the local watershed scale. We found strong support for sex, age, and species differences in the probability an individual duck tested positive for avian influenza virus. In addition, we found that for every seven days the local minimum temperature fell below zero, the chance an individual would test positive for avian influenza virus increased by 5.9 percent. We also found a twelve percent increase in the chance an individual would test positive during the breeding season for every ten percent increase in the interval apparent prevalence during the prior overwintering season. These results suggest that viral deposition in water and sub-freezing temperatures during the overwintering season may act as determinants of individual level infection risk during the subsequent breeding season. Our findings have implications for future surveillance activities in waterfowl and domestic poultry populations. Further study is needed to identify how these drivers might interact with other host-specific infection determinants, such as species phylogeny, immunological status, and behavioral characteristics.

Metapopulation dynamics and determinants of H5N1 highly pathogenic avian influenza outbreaks in Indonesian poultry.

In 2008, the Indonesian Government implemented a revised village-level Participatory Disease Surveillance and Response (PDSR) program to gain a better understanding of both the magnitude and spatial distribution of H5N1 highly pathogenic avian influenza (HPAI) outbreaks in backyard poultry. To date, there has been considerable collection of data, but limited publically available analysis. This study utilizes data collected by the PDSR program between April 2008 and September 2010 for Java, Bali and the Lampung Province of Sumatra. The analysis employs hierarchical Bayesian occurrence models to quantify spatial and temporal dynamics in backyard HPAI infection reports at the District level in 90 day time periods, and relates the probability of HPAI occurrence to PDSR-reported village HPAI infection status and human and poultry density. The probability of infection in a District was assumed to be dependent on the status of the District in the previous 90 day time period, and described by either a colonization probability (the probability of HPAI infection in a District given there had not been infection in the previous 90 day time period) or a persistence probability (the probability of HPAI infection being maintained in the District from the previous to current 90 day period). Results suggest that the number of surveillance activities in a district had little relationship to outbreak occurrence probabilities, but human and poultry densities were found to have non-linear relationships to outbreak occurrence probabilities. We found significant spatial dependency among neighboring districts, indicating that there are latent spatial processes that are not captured by the covariates available for this study, but which nonetheless impact outbreak dynamics. The results of this work may help improve understanding of the seasonal nature of H5N1 in poultry and the potential role of poultry density in enabling endemicity to occur, as well as to assist the Government of Indonesia target scarce resources to regions and time periods when outbreaks of HPAI in poultry are most likely to occur.

Host and viral ecology determine bat rabies seasonality and maintenance.

Rabies is an acute viral infection that is typically fatal. Most rabies modeling has focused on disease dynamics and control within terrestrial mammals (e.g., raccoons and foxes). As such, rabies in bats has been largely neglected until recently. Because bats have been implicated as natural reservoirs for several emerging zoonotic viruses, including SARS-like corona viruses, henipaviruses, and lyssaviruses, understanding how pathogens are maintained within a population becomes vital. Unfortunately, little is known about maintenance mechanisms for any pathogen in bat populations. We present a mathematical model parameterized with unique data from an extensive study of rabies in a Colorado population of big brown bats (Eptesicus fuscus) to elucidate general maintenance mechanisms. We propose that life history patterns of many species of temperate-zone bats, coupled with sufficiently long incubation periods, allows for rabies virus maintenance. Seasonal variability in bat mortality rates, specifically low mortality during hibernation, allows long-term bat population viability. Within viable bat populations, sufficiently long incubation periods allow enough infected individuals to enter hibernation and survive until the following year, and hence avoid an epizootic fadeout of rabies virus. We hypothesize that the slowing effects of hibernation on metabolic and viral activity maintains infected individuals and their pathogens until susceptibles from the annual birth pulse become infected and continue the cycle. This research provides a context to explore similar host ecology and viral dynamics that may explain seasonal patterns and maintenance of other bat-borne diseases.

Soil clay content underlies prion infection odds.

Environmental factors-especially soil properties-have been suggested as potentially important in the transmission of infectious prion diseases. Because binding to montmorillonite (an aluminosilicate clay mineral) or clay-enriched soils had been shown to enhance experimental prion transmissibility, we hypothesized that prion transmission among mule deer might also be enhanced in ranges with relatively high soil clay content. In this study, we report apparent influences of soil clay content on the odds of prion infection in free-ranging deer. Analysis of data from prion-infected deer herds in northern Colorado, USA, revealed that a 1% increase in the clay-sized particle content in soils within the approximate home range of an individual deer increased its odds of infection by up to 8.9%. Our findings suggest that soil clay content and related environmental properties deserve greater attention in assessing risks of prion disease outbreaks and prospects for their control in both natural and production settings.

Comparing national and global data collection systems for reporting, outbreaks of H5N1 HPAI.

Determining if outbreak data collected by regional or international organizations can reflect patterns observed in more detailed data collected by national veterinary services is a necessary first step if global databases are to be used for making inference about determinants of disease maintenance and spread and for emergency planning and response. We compared two data sources that capture spatial and temporal information about H5N1 highly pathogenic avian influenza outbreaks reported since 2004 in four countries: Bangladesh, Egypt, Turkey, and Vietnam. One data source consisted of reports collected as part of each country's national veterinary services surveillance program, while the other data source included reports collected using the Emergency Prevention System for Priority Animal and Plant Pests and Diseases (EMPRES-i) global animal health information system. We computed Spearman rank-order correlation statistics to compare spatial and temporal outbreak distributions, and applied a space-time permutation test to check for consistency between the two data sources. Although EMPRES-i typically captured fewer outbreaks than detailed national reporting data, the overall similarity in space and time, particularly after 2006, reflect the ability of the EMPRES-i system to portray disease patterns comparable to those observed in national data sets. Specifically, we show that the two datasets exhibit higher positive correlations in outbreak timing and reported locations after 2006 when compared to December 2003 through 2006. Strengthening the capacity of global systems to acquire data from national and regional databases will improve global analysis efforts and increase the ability of such systems to rapidly alert countries and the international community of potential disease threats.

Identifying spatio-temporal patterns of transboundary disease spread: examples using avian influenza H5N1 outbreaks.

Characterizing spatio-temporal patterns among epidemics in which the mechanism of spread is uncertain is important for generating disease spread hypotheses, which may in turn inform disease control and prevention strategies. Using a dataset representing three phases of highly pathogenic avian influenza H5N1 outbreaks in village poultry in Romania, 2005-2006, spatiotemporal patterns were characterized. We first fit a set of hierarchical Bayesian models that quantified changes in the spatio-temporal relative risk for each of the 23 affected counties. We then modeled spatial synchrony in each of the three epidemic phases using non-parametric covariance functions and Thin Plate Spline regression models. We found clear differences in the spatio-temporal patterns among the epidemic phases (local versus regional correlated processes), which may indicate differing spread mechanisms (for example wild bird versus human-mediated). Elucidating these patterns allowed us to postulate that a shift in the primary mechanism of disease spread may have taken place between the second and third phases of this epidemic. Information generated by such analyses could assist affected countries in determining the most appropriate control programs to implement, and to allocate appropriate resources to preventing contact between domestic poultry and wild birds versus enforcing bans on poultry movements and quarantine. The methods used in this study could be applied in many different situations to analyze transboundary disease data in which only location and time of occurrence data are reported.

The role of geographic information systems in wildlife landscape epidemiology: models of chronic wasting disease in Colorado mule deer.

The authors present findings from two landscape epidemiology studies of chronic wasting disease (CWD) in northern Colorado mule deer (Odocoileus hemionus). First, the effects of human land use on disease prevalence were explored by formulating a set of models estimating CWD prevalence in relation to differences in human land use, sex and geographic location. Prevalence was higher in developed areas and among male deer suggesting that anthropogenic influences (changes in land use), differences in exposure risk between sexes and landscape-scaled heterogeneity are associated with CWD prevalence. The second study focused on identifying scales of mule deer movement and mixing that had the greatest influence on the spatial pattern of CWD in north-central Colorado. The authors hypothesised that three scales of mixing - individual, winter subpopulation and summer subpopulation - might control spatial variation in disease prevalence. A fully Bayesian hierarchical model was developed to compare the strength of evidence for each mixing scale. Strong evidence was found indicating that the finest mixing scale corresponded best to the observed spatial distribution of CWD prevalence. This analysis demonstrates how information on the scales of spatial processes that generate observed patterns can be used to gain insight into the epidemiology of wildlife diseases when process data are sparse or unavailable.

Linking chronic wasting disease to mule deer movement scales: a hierarchical Bayesian approach.

Observed spatial patterns in natural systems may result from processes acting across multiple spatial and temporal scales. Although spatially explicit data on processes that generate ecological patterns, such as the distribution of disease over a landscape, are frequently unavailable, information about the scales over which processes operate can be used to understand the link between pattern and process. Our goal was to identify scales of mule deer (Odocoileus hemionus) movement and mixing that exerted the greatest influence on the spatial pattern of chronic wasting disease (CWD) in northcentral Colorado, USA. We hypothesized that three scales of mixing (individual, winter subpopulation, or summer subpopulation) might control spatial variation in disease prevalence. We developed a fully Bayesian hierarchical model to compare the strength of evidence for each mixing scale. We found strong evidence that the finest mixing scale corresponded best to the spatial distribution of CWD infection. There was also evidence that land ownership and habitat use play a role in exacerbating the disease, along with the known effects of sex and age. Our analysis demonstrates how information on the scales of spatial processes that generate observed patterns can be used to gain insight when process data are sparse or unavailable.