A big data-model integration approach for predicting epizootics and population recovery in a keystone species.

Infectious diseases pose a significant threat to global health and biodiversity. Yet, predicting the spatiotemporal dynamics of wildlife epizootics remains challenging. Disease outbreaks result from complex nonlinear interactions among a large collection of variables that rarely adhere to the assumptions of parametric regression modeling. We adopted a nonparametric machine learning approach to model wildlife epizootics and population recovery, using the disease system of colonial black-tailed prairie dogs (BTPD, Cynomys ludovicianus) and sylvatic plague as an example. We synthesized colony data between 2001 and 2020 from eight USDA Forest Service National Grasslands across the range of BTPDs in central North America. We then modeled extinctions due to plague and colony recovery of BTPDs in relation to complex interactions among climate, topoedaphic variables, colony characteristics, and disease history. Extinctions due to plague occurred more frequently when BTPD colonies were spatially clustered, in closer proximity to colonies decimated by plague during the previous year, following cooler than average temperatures the previous summer, and when wetter winter/springs were preceded by drier summers/falls. Rigorous cross-validations and spatial predictions indicated that our final models predicted plague outbreaks and colony recovery in BTPD with high accuracy (e.g., AUC generally >0.80). Thus, these spatially explicit models can reliably predict the spatial and temporal dynamics of wildlife epizootics and subsequent population recovery in a highly complex host-pathogen system. Our models can be used to support strategic management planning (e.g., plague mitigation) to optimize benefits of this keystone species to associated wildlife communities and ecosystem functioning. This optimization can reduce conflicts among different landowners and resource managers, as well as economic losses to the ranching industry. More broadly, our big data-model integration approach provides a general framework for spatially explicit forecasting of disease-induced population fluctuations for use in natural resource management decision-making.

Disease and weather induce rapid shifts in a rangeland ecosystem mediated by a keystone species (Cynomys ludovicianus).

Habitat loss and changing climate have direct impacts on native species but can also interact with disease pathogens to influence wildlife communities. In the North American Great Plains, black-tailed prairie dogs (Cynomys ludovicianus) are a keystone species that create important grassland habitat for numerous species and serve as prey for predators, but lethal control driven by agricultural conflict has severely reduced their abundance. Novel disease dynamics caused by epizootic plague (Yersinia pestis) within prairie dog colonies have further reduced prairie dog abundances, in turn destabilizing associated wildlife communities. We capitalized on a natural experiment, collecting data on prairie dog distributions, vegetation structure, avian abundance, and mesocarnivore and ungulate occupancy before (2015-2017) and after (2018-2019) a plague event in northeastern Wyoming, USA. Plague decimated black-tailed prairie dog populations in what was then the largest extant colony complex, reducing colony cover in the focal area from more than 10,000 ha to less than 50 ha. We documented dramatic declines in mesocarnivore occupancy and raptor abundance post-plague, with probability of occupancy or abundance approaching zero in species that rely on prairie dogs for a high proportion of their diet (e.g., ferruginous hawk [Buteo regalis], American badger [Taxidea taxus], and swift fox [Vulpes velox]). Following the plague outbreak, abnormally high precipitation in 2018 hastened vegetation recovery from prairie dog disturbance on colonies in which constant herbivory had formerly maintained shortgrass structure necessary for certain colony-associates. As a result, we observed large shifts in avian communities on former prairie dog colonies, including near-disappearance of mountain plovers (Charadrius montanus) and increases in mid-grass associated songbirds (e.g., lark bunting [Calamospiza melanocorys]). Our research highlights how precipitation can interact with disease-induced loss of a keystone species to induce drastic and rapid shifts in wildlife communities. Although grassland taxa have co-evolved with high spatiotemporal variation, fragmentation of the remaining North American rangelands paired with higher-than-historical variability in climate and disease dynamics are likely to destabilize these systems in the future.

Changes in hunting season regulations (1870s-2019) reduce harvest exposure on greater and Gunnison sage-grouse.

Hunter harvest is a potential factor contributing to population declines of sage-grouse (Centrocercus spp.). As a result, wildlife agencies throughout western North America have set increasingly more conservative harvest regulations over the past 25 years to reduce or eliminate hunter success and concomitant numbers of harvested greater (C. urophasianus) and Gunnison (C. minimus) sage-grouse. Sage-grouse hunting has varied widely over time and space, which has made a comprehensive summary of hunting management challenging. We compiled data on harvest regulations among 11 western U.S. states and 2 Canadian provinces from 1870-2019 to create a timeline representative of hunting regulations. We compared annual harvest boundaries and area-weighted average hunting regulations, 1995-2018, relative to administrative boundaries and areas of high probability of sage-grouse occupation. We also summarized estimated numbers of birds harvested and hunters afield, 1995-2018, across both species' ranges. From 1995-2018, there was a 30% reduction in administrative harvest boundaries across the greater sage-grouse range compared to a 16.6% reduction in area open to harvest within 8 km from active leks. Temporary closures occurred in response to wildfires, disease outbreaks, low population numbers, and two research projects; whereas, permanent closures primarily occurred in small populations and areas on the periphery of the species distribution. Similarly, area-weighted possession limits and season length for greater sage-grouse decreased 52.6% and 61.0%, respectively, while season start date stayed relatively stable (mean start date ~259 [mid-September]). In contrast, hunting of the now federally-threatened Gunnison sage-grouse ended after 1999. While restrictions in harvest regulations were large in area, closures near areas of high greater sage-grouse occupancy were relatively smaller with the same trend for Gunnison sage-grouse until hunting ceased. For greater sage-grouse, most states reduced bag and possession limits and appeared to adhere to recommendations for later and shorter hunting seasons, reducing potential for additive mortality.

Direct and indirect effects of a keystone engineer on a shrubland-prairie food web.

Keystone engineers are critical drivers of biodiversity throughout ecosystems worldwide. Within the North American Great Plains, the black-tailed prairie dog is an imperiled ecosystem engineer and keystone species with well-documented impacts on the flora and fauna of rangeland systems. However, because this species affects ecosystem structure and function in myriad ways (i.e., as a consumer, a prey resource, and a disturbance vector), it is unclear which effects are most impactful for any given prairie dog associate. We applied structural equation models (SEM) to disentangle direct and indirect effects of prairie dogs on multiple trophic levels (vegetation, arthropods, and birds) in the Thunder Basin National Grassland. Arthropods did not show any direct response to prairie dog occupation, but multiple bird species and vegetation parameters were directly affected. Surprisingly, the direct impact of prairie dogs on colony-associated avifauna (Horned Lark [Eremophila alpestris] and Mountain Plover [Charadrius montanus]) had greater support than a mediated effect via vegetation structure, indicating that prairie dog disturbance may be greater than the sum of its parts in terms of impacts on localized vegetation structure. Overall, our models point to a combination of direct and indirect impacts of prairie dogs on associated vegetation, arthropods, and avifauna. The variation in these impacts highlights the importance of examining the various impacts of keystone engineers, as well as highlighting the diverse ways that black-tailed prairie dogs are critical for the conservation of associated species.