A novel method for estimating pathogen presence, prevalence, load, and dynamics at multiple scales

Abstract

The use of quantitative real-time PCR (qPCR) to monitor pathogens is common; however, quantitative frameworks that consider the observation process, dynamics in pathogen presence, and pathogen load are lacking. This can be problematic in the early stages of disease progression, where low level detections may be treated as ‘inconclusive’ and excluded from analyses. Alternatively, a framework that accounts for imperfect detection would provide more robust inferences. To better estimate pathogen dynamics, we developed a hierarchical multi-scale dynamic occupancy hurdle model (MS-DOHM). The model used data gathered during sampling for Pseudogymnoascus destructans (Pd) , the causative agent of white-nose syndrome, a fungal disease that has cause severe declines in several species of hibernating bats in North America. The model allowed us to estimate initial occupancy, colonization, persistence and prevalence of Pd at bat hibernacula. Additionally, utilizing the relationship between cycle threshold and pathogen load, we estimated pathogen detectability and modeled expected colony and bat pathogen loads. To assess the ability of MS-DOHM to estimate pathogen dynamics, we compared MS-DOHM’s results to those of a dynamic occupancy model and naïve detection/non-detection. MS-DOHM’s estimates of site-level pathogen presence were up to 11.9% higher than estimates from the dynamic occupancy model and 35.7% higher than naïve occupancy. Including prevalence and load in our modeling framework resulted in estimates of pathogen arrival that were two to three years earlier compared to the dynamic occupancy and naïve detection/non-detection, respectively. Compared to naïve values, MS-DOHM predicted greater pathogen loads on colonies; however, we found no difference between model estimates and naïve values of prevalence. While the model predicted no declines in site-level prevalence, there were instances where pathogen load decreased in colonies that had been Pd positive for longer periods of time. Our findings demonstrate that accounting for pathogen load and prevalence at multiple scales changes our understanding of Pd dynamics, potentially allowing earlier conservation intervention. Additionally, we found that accounting for pathogen load and prevalence within hibernacula and among individuals resulted in a better fitting model with greater predictive ability.