Daniel A. Grear

Demographic patterns and harvest vulnerability of chronic wasting disease infected white-tailed deer in Wisconsin

Abstract Chronic wasting disease (CWD) is a fatal disease of white-tailed deer (Odocoileus virginianus) caused by transmissible protease-resistant prions. Since the discovery of CWD in southern Wisconsin in 2001, more than 20,000 deer have been removed from a >2,500-km2 disease eradication zone surrounding the three initial cases. Nearly all deer removed were tested for CWD infection and sex, age, and harvest location were recorded. Our analysis used data from a 310-km2 core study area where disease prevalence was higher than surrounding areas. We found no difference in harvest rates between CWD infected and noninfected deer. Our results show that the probability of infection increased with age and that adult males were more likely to be infected than adult females. Six fawns tested positive for CWD, five fawns from the core study area, including the youngest (5 months) free-ranging cervid to test positive. The increase in male prevalence with age is nearly twice the increase found in females. We concluded that CWD is not randomly distributed among deer and that differential transmission among sex and age classes is likely driving the observed patterns in disease prevalence. We discuss alternative hypotheses for CWD transmission and spread and, in addition, discuss several possible nonlinear relationships between prevalence and age. Understanding CWD transmission in free-ranging cervid populations will be essential to the development of strategies to manage this disease in areas where CWD is found, as well as for surveillance strategies in areas where CWD threatens to spread.

Does elevated testosterone result in increased exposure and transmission of parasites

Male-biased infection is a common phenomenon in vertebrate-parasite systems and male-biased transmission has been experimentally demonstrated. One mechanism that is hypothesized to create male-biased transmission is the immuno-suppressive effect of testosterone because it increases susceptibility to infection. Testosterone also influences host behaviour and, consequently, may increase exposure to parasites. To test how testosterone could increase exposure and transmission, we undertook a longitudinal mark-recapture study where we experimentally elevated testosterone levels in wild male rodents. Individuals in control populations reduced the average number of contacts over the treatment period, while populations with experimentally elevated testosterone levels maintained the number of contacts between hosts. As a result, the transmission potential was higher in testosterone treated populations compared to controls. Our results indicated that males with high-testosterone levels alter the population-level contacts, producing different social networks and increasing transmission potential compared to those where testosterone is at background levels.

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.

The impact of movements and animal density on continental scale cattle disease outbreaks in the United States.

Globalization has increased the potential for the introduction and spread of novel pathogens over large spatial scales necessitating continental-scale disease models to guide emergency preparedness. Livestock disease spread models, such as those for the 2001 foot-and-mouth disease (FMD) epidemic in the United Kingdom, represent some of the best case studies of large-scale disease spread. However, generalization of these models to explore disease outcomes in other systems, such as the United States’s cattle industry, has been hampered by differences in system size and complexity and the absence of suitable livestock movement data. Here, a unique database of US cattle shipments allows estimation of synthetic movement networks that inform a near-continental scale disease model of a potential FMD-like (i.e., rapidly spreading) epidemic in US cattle. The largest epidemics may affect over one-third of the US and 120,000 cattle premises, but cattle movement restrictions from infected counties, as opposed to national movement moratoriums, are found to effectively contain outbreaks. Slow detection or weak compliance may necessitate more severe state-level bans for similar control. Such results highlight the role of large-scale disease models in emergency preparedness, particularly for systems lacking comprehensive movement and outbreak data, and the need to rapidly implement multi-scale contingency plans during a potential US outbreak.

A Bayesian Approach for Modeling Cattle Movements in the United States: Scaling up a Partially Observed Network

Networks are rarely completely observed and prediction of unobserved edges is an important problem, especially in disease spread modeling where networks are used to represent the pattern of contacts. We focus on a partially observed cattle movement network in the U.S. and present a method for scaling up to a full network based on Bayesian inference, with the aim of informing epidemic disease spread models in the United States. The observed network is a 10% state stratified sample of Interstate Certificates of Veterinary Inspection that are required for interstate movement; describing approximately 20,000 movements from 47 of the contiguous states, with origins and destinations aggregated at the county level. We address how to scale up the 10% sample and predict unobserved intrastate movements based on observed movement distances. Edge prediction based on a distance kernel is not straightforward because the probability of movement does not always decline monotonically with distance due to underlying industry infrastructure. Hence, we propose a spatially explicit model where the probability of movement depends on distance, number of premises per county and historical imports of animals. Our model performs well in recapturing overall metrics of the observed network at the node level (U.S. counties), including degree centrality and betweenness; and performs better compared to randomized networks. Kernel generated movement networks also recapture observed global network metrics, including network size, transitivity, reciprocity, and assortativity better than randomized networks. In addition, predicted movements are similar to observed when aggregated at the state level (a broader geographic level relevant for policy) and are concentrated around states where key infrastructures, such as feedlots, are common. We conclude that the method generally performs well in predicting both coarse geographical patterns and network structure and is a promising method to generate full networks that incorporate the uncertainty of sampled and unobserved contacts.

Network transmission inference: host behavior and parasite life cycle make social networks meaningful in disease ecology.

The process of disease transmission is determined by the interaction of host susceptibility and exposure to parasite infectious stages. Host behavior is an important determinant of the likelihood of exposure to infectious stages but is difficult to measure and often assumed to be homogenous in models of disease spread. We evaluated the importance of precisely defining host contact when using networks that estimate exposure and predict infection prevalence in a replicated, empirical system. In particular, we hypothesized that infection patterns would be predicted only by a contact network that is defined according to host behavior and parasite life cycle. Two competing host contact criteria were used to construct networks defined by parasite life cycle and social contacts. First, parasite-defined contacts were based on shared space with a time delay corresponding to the environmental development time of nematode parasites with a direct fecal-oral life cycle. Second, social contacts were defined by shared space in the same time period. To quantify the competing networks of exposure and infection, we sampled natural populations of the eastern chipmunk (Tamias striatus) and infection of their gastrointestinal helminth community using replicated longitudinal capture-mark-recapture techniques. We predicted that (1) infection with parasites with direct fecal-oral life cycles would be explained by the time delay contact network, but not the social contact network; (2) infection with parasites with trophic life cycles (via a mobile intermediate host; thus, spatially decoupling transmission from host contact) would not be explained by either contact network. The prevalence of fecal-oral life cycle nematode parasites was strongly correlated to the number and strength of network connections from the parasite-defined network (including the time delay), while the prevalence of trophic life cycle parasites was not correlated with any network metrics. We concluded that incorporating the parasite life cycle, relative to the way that exposure is measured, is key to inferring transmission and can be empirically quantified using network techniques. In addition, appropriately defining and measuring contacts according the life history of the parasite and relevant behaviors of the host is a crucial step in applying network analyses to empirical systems.

Male hosts are responsible for the transmission of a trophically transmitted parasite, Pterygodermatites peromysci, to the intermediate host in the absence of sex-biased infection

Field studies have identified that male-biased infection can lead to increased rates of transmission, so we examined the relative importance of host sex on the transmission of a trophically transmitted parasite (Pterygodermatites peromysci) where there is no sex-biased infection. We experimentally reduced infection levels in either male or female white-footed mice (Peromyscus leucopus) on independent trapping grids with an anthelmintic and recorded subsequent infection levels in the intermediate host, the camel cricket (Ceuthophilus pallidipes). We found that anthelmintic treatment significantly reduced the prevalence of infection among crickets in both treatment groups compared with the control, and at a rate proportional to the number of mice de-wormed, indicating prevalence was not affected by the sex of the shedding definitive host. In contrast, parasite abundance in crickets was higher on the grids where females were treated compared with the grids where males were treated. These findings indicate that male hosts contribute disproportionately more infective stages to the environment and may therefore be responsible for the majority of parasite transmission even when there is no discernable sex-biased infection. We also investigated whether variation in nematode length between male and female hosts could account for this male-biased infectivity, but found no evidence to support that hypothesis.

Descriptive Epidemiology and Whole Genome Sequencing Analysis for an Outbreak of Bovine Tuberculosis in Beef Cattle and White-Tailed Deer in Northwestern Minnesota

Bovine tuberculosis (bTB) was discovered in a Minnesota cow through routine slaughter surveillance in 2005 and the resulting epidemiological investigation led to the discovery of infection in both cattle and white-tailed deer in the state. From 2005 through 2009, a total of 12 beef cattle herds and 27 free-ranging white-tailed deer (Odocoileus virginianus) were found infected in a small geographic region of northwestern Minnesota. Genotyping of isolates determined both cattle and deer shared the same strain of bTB, and it was similar to types found in cattle in the southwestern United States and Mexico. Whole genomic sequencing confirmed the introduction of this infection into Minnesota was recent, with little genetic divergence. Aggressive surveillance and management efforts in both cattle and deer continued from 2010–2012; no additional infections were discovered. Over 10,000 deer were tested and 705 whole herd cattle tests performed in the investigation of this outbreak.

A national-scale picture of U.S. cattle movements obtained from Interstate Certificate of Veterinary Inspection data

We present the first comprehensive description of how shipments of cattle connect the geographic extent and production diversity of the United States cattle industry. We built a network of cattle movement from a state-stratified 10% systematic sample of calendar year 2009 Interstate Certificates of Veterinary Inspection (ICVI) data. ICVIs are required to certify the apparent health of cattle moving across state borders and allow us to examine cattle movements at the county scale. The majority of the ICVI sample consisted of small shipments (<20 head) moved for feeding and beef production. Geographically, the central plains states had the most connections, correlated to feeding infrastructure. The entire nation was closely connected when interstate movements were summarized at the state level. At the county-level, the U.S. is still well connected geographically, but significant heterogeneities in the location and identity of counties central to the network emerge. Overall, the network of interstate movements is described by a hub structure, with a few counties sending or receiving extremely large numbers of shipments and many counties sending and receiving few shipments. The county-level network also has a very low proportion of reciprocal movements, indicating that high-order network properties may be better at describing a countys importance than simple summaries of the number of shipments or animals sent and received. We suggest that summarizing cattle movements at the state level homogenizes the network and a county level approach is most appropriate for examining processes influenced by cattle shipments, such as economic analyses and disease outbreaks.

The relative importance of host characteristics and co-infection in generating variation in Heligmosomoides polygyrus fecundity.

We examined the relative importance of intrinsic host factors and microparasite co-infection in generating variation in Heligmosomoides polygyrus fecundity, a parameter that serves as a proxy for infectiousness. We undertook extensive trapping of Apodemus flavicollis, the yellow-necked mouse in the woodlands of the Italian Alps and recorded eggs in utero from the dominant nematode species H. polygyrus, and tested for the presence of five microparasite infections. The results showed that sex and breeding status interact, such that males in breeding condition harboured more fecund nematodes than other hosts; in particular, worms from breeding males had, on average, 52% more eggs in utero than worms from non-breeding males. In contrast, we found a weak relationship between intensity and body mass, and no relationship between intensity and sex or intensity and breeding condition. We did not find any evidence to support the hypothesis that co-infection with microparasites contributed to variation in worm fecundity in this system. The age-intensity profiles for mice singly-infected with H. polygyrus and those co-infected with the nematode and at least one microparasite were both convex and not statistically different from each other. We concluded that intrinsic differences between hosts, specifically with regard to sex and breeding condition, contribute relatively more to the variation in worm fecundity than parasite co-infection status.