Grantee Research Project Results
Final Report: Habitat Alteration and Disease Effects on Black-Tailed Prairie Dogs
EPA Grant Number: R829091Title: Habitat Alteration and Disease Effects on Black-Tailed Prairie Dogs
Investigators: Collinger, Sharon K. , Ray, Chris , Cully, Jack , Gage, Kenneth , Kosoy, Michael
Institution: University of Colorado at Boulder , Centers for Disease Control and Prevention , Kansas State University
EPA Project Officer: Packard, Benjamin H
Project Period: December 15, 2001 through December 14, 2004 (Extended to December 14, 2005)
Project Amount: $500,000
RFA: Wildlife Risk Assessment (2001) RFA Text | Recipients Lists
Research Category: Ecological Indicators/Assessment/Restoration , Aquatic Ecosystems , Biology/Life Sciences
Objective:
Our research focused on the combined effects of habitat alteration and wildlife community structure on the risk of disease outbreaks in the black-tailed prairie dog, a species of conservation concern. This species is susceptible to bacterial blood diseases, including sylvatic plague and Bartonella, that are transmitted by fleas. Prairie dog colonies that contract plague commonly suffer 100 percent mortality, so predicting the risk of exposure to plague is critical for prairie dog conservation. Because plague may be the most critical threat to the survival of black-tailed prairie dogs, the objective of this research project was to gain a better understanding of the spatial and temporal dynamics of plague in this system.
Predicting disease outbreaks involves consideration of multiple population stressors. Most diseases spread through contact between individuals of a single species, so the prediction of outbreaks depends on prediction of population dynamics within the species. Blood diseases like the plague spread through contact between black-tailed prairie dogs and the many alternate mammalian hosts that occur in the same habitat. Therefore, our research addressed effects of landscape structure and land use on the dynamics of black-tailed prairie dogs and on the dynamics of the alternate host community.
Our field research provides data to determine the statistical relationships between outbreaks of plague and bartonellosis in black-tailed prairie dogs and in the alternate host community. First, we used historical data sets from broad geographic areas within the range of the black-tailed prairie dog to develop statistical models to evaluate characteristics of landscape structure and the relevance of climate variation in relation to plague occurrence. Second, we conducted detailed studies of landscape structure and use, population demography and disease at five study sites in Colorado, Kansas, and Wyoming.
Summary/Accomplishments (Outputs/Outcomes):
During Year 1 of our research project (2002-2003), we assembled and analyzed two long-term data sets on plague occurrence in black-tailed prairie dogs to test the hypotheses that plague occurrence is associated with colony characteristics and landscape context. We compiled data on colony locations and plague occurrence over the past 20 years, and overlaid these data in a geographical information system (GIS) with landscape features, such as roads, streams, lakes, and urban development. Our two study areas (Boulder County, Colorado, and Phillips County, Montana) differed markedly in degree of urbanization and other landscape characteristics. In both study areas, we found associations between plague occurrence and landscape and colony characteristics such as the amount of roads, streams, and lakes surrounding a prairie dog colony; the area covered by the colony and its neighbors; and the distance to the nearest plague-positive colony (Collinge, et al., 2005a). Logistic regression models were similar between the two study areas, with the best models predicting positive effects of proximity to plague-positive colonies and negative effects of road, stream, and lake cover on plague occurrence. Taken together, these results suggest that roads, streams, and lakes may serve as barriers to plague in black-tailed prairie dog colonies by affecting movement of or habitat quality for plague hosts or fleas that serve as vectors for the pathogen. The similarity in plague correlates between urban and rural study areas suggests that the correlates of plague are not altered by uniquely urban stressors.
We performed a second analysis using the data described above from Boulder County, Colorado, and Phillips County, Montana, to examine temporal variation in plague outbreaks in prairie dog colonies over the past twenty years. We examined and correlated plague occurrence with temperature and precipitation in these two regions. We found little evidence for relationships between climate variation and plague occurrence in Boulder County, which perhaps is not surprising given the unpredictability and extreme annual variation in precipitation that is characteristic of Boulder. In central Montana, however, we observed a positive association between prairie dog colony die-offs and ‘‘peak’’ (April-July) precipitation in the previous year (Collinge, et al., 2005b). The number of die-offs in this study area also was positively related to the number of “warm” (> 26.7°C) days and negatively related to the number of “hot” (> 29.4°C) days during the year.
We conclude from these two broad-scale analyses that: (1) spatial patterns of plague occurrence in prairie dog colonies are related significantly to landscape features; and (2) temporal patterns of plague occurrence are associated significantly with climate variation, at least for colonies in some parts of the prairie dog’s geographic range. Our results may allow us to be able to predict years in which plague outbreaks will likely occur based on climatic variables and to predict which prairie dog colonies are likely to be affected by plague, based on their landscape context. These results are significant because plague in prairie dogs previously has been considered highly unpredictable in space and time, a fact that challenges our ability to effectively prevent further population declines. Our models relating climate and plague occurrence in our Montana study area suggest that it would be fruitful to further investigate associations between climate and plague occurrence in prairie dogs across their geographic range. If such analyses reveal strong relationships between climate and plague occurrence, then we may be able to make predictions about the temporal patterns of plague occurrence in a given geographic area. In areas where climate is more variable, other factors may better predict plague occurrence in prairie dogs. In these situations, factors such as landscape structure may be more useful predictors of plague occurrence. Ultimately, it will be beneficial to elucidate combinations of factors that allow us to predict both spatial and temporal patterns of disease occurrence in this imperiled species.
In our intensive field studies over the past 3 years (2003-2005), our field crews trapped small mammals that potentially serve as reservoir hosts for plague at 44 sites in Boulder County and at 30 sites at three national grasslands in Wyoming, Colorado, and Kansas. We trapped prairie dogs at 20-24 sites each year in Boulder County. We collected fleas, blood, and tissue samples from each captured animal for analyses of pathogen occurrence and ectoparasite abundance and distribution, as well as for population genetic analyses of prairie dog colonies. We collected approximately 9,000 blood samples and more than 20,000 fleas during the summers of 2003, 2004, and 2005. These intensive field studies were designed to reveal relationships between prairie dogs, alternate hosts (small mammals), disease vectors (fleas), and disease-causing bacteria (Yersinia pestis and Bartonella spp.)
All of the fleas from our field collections have been counted, sorted, and identified to species. The samples were dominated numerically by two flea species: Oropsylla hirsuta, which occurs primarily on prairie dogs, and Aetheca wagneri, which occurs primarily on deer mice, but we identified about 20 different flea species on these rodents. We observed several distinct patterns that may contribute significantly to plague outbreaks in prairie dogs. First, we observed higher diversity of flea species on small mammals that occurred on prairie dog colonies compared to small mammals that occur in adjacent grasslands without prairie dogs. Second, we observed greater abundance of fleas on small mammals that occur on prairie dog colonies compared to small mammals that occur in adjacent grasslands without prairie dogs. Third, we observed significant differences between years in the abundance and diversity of fleas on small mammals at all study sites. We conclude from these results that prairie dogs have a “keystone” effect on rodent/flea assemblages by influencing the diversity and abundance of fleas on small mammals. Prairie dog colonies may provide a more suitable habitat for fleas, given that prairie dogs create burrow systems that remain “climate-controlled’ throughout the year. We still are in the process of analyzing our data on flea occurrence and on pathogen loads in fleas, and we anticipate that these analyses will increase significantly our understanding of the relationships between landscape structure and the influential effects of prairie dogs on disease vectors.
None of the fleas collected in 2003 or 2004 tested positive for the plague pathogen, Y. pestis. During these 2 years, however, we detected Y. pestis in only a few blood samples collected from rodents. In 2005, we did detect plague-positive rodent blood samples, and the fleas from 2005 still are being analyzed in the laboratory at the Centers for Disease Control and Prevention in Fort Collins, Colorado. We did detect the second bacterial pathogen, Bartonella spp., in many small mammal, prairie dog, and flea samples collected from 2003-2005. For example, Bartonella prevalence in rodent blood samples varies from 0-71 percent, depending on the species, study site, and year. Similarly, Bartonella prevalence in fleas varies from 3-26 percent, depending on the species, host, site, and year. We still are performing detailed spatial and temporal analyses of these samples and hope to develop a much clearer understanding of the ecology of this important pathogen. Our molecular analyses have revealed a new species of Bartonella that occurs in prairie dogs, and this finding will be submitted to the International Journal of Bacterial Systematics and Evolution later this year.
We have mapped the perimeters of approximately 100 prairie dog colonies in Boulder County, Colorado, and have measured colony characteristics such as area and isolation using GIS. In all 3 years of our study (2003-2005), we collected data on these colonies, including prairie dog burrow density for all 100 colonies, prairie dog density for 24 colonies, and vegetation cover for 24 colonies. These data have been input into the GIS database and georeferenced to overlay on baselayers supplied by Boulder City Open Space and Mountain Parks and Boulder County Open Space Departments. For information on prairie dog colonies in less urbanized landscapes, we mapped colonies on the Cimarron National Grassland, Kansas; Comanche National Grassland, Colorado; Kiowa National Grassland, New Mexico; Rita Blanca National Grassland, Oklahoma and Texas; and Thunder Basin National Grassland, Wyoming. We conclude from these analyses that prairie dogs occur at much higher densities in urban areas than they do in more continuous grassland habitat (Johnson and Collinge, 2004). If there are negative effects of density on survival, then urban colonies may be much more at risk of extinction than colonies in more continuous habitat. We also conclude that a comparison of population dynamics of prairie dogs in areas where prairie dogs are exposed to plague versus areas where plague is absent showed that plague significantly alters metapopulation spatial dynamics, not only by drastically decreasing colony size, but also by creating considerably longer distances between colonies, which may slow recolonization events (T. Johnson, et al., in preparation). We will continue to analyze these data to seek relationships among colony characteristics and plague occurrence in these varied landscapes.
To date we have published three research articles and two book chapters, submitted another article that currently is in review, and identified at least 12 more manuscripts that are in various stages of preparation for submission from research that benefited from the U.S. Environmental Protection Agency (EPA) Science To Achieve Results grant. This research has provided many opportunities for communication and outreach to broader audiences. The Project Director (S. Collinge) has been invited to present research results at several venues during the past 4 years. Dr. Chris Ray, Research Associate, and several graduate students conducting research funded by this grant have presented research at national or regional meetings.
Our research group will continue to collaborate to produce additional publications from our EPA-funded research. We will continue to analyze the remainder of the blood and ectoparasite samples that we have collected and to analyze field data that we collected during 2003-2005. With the field data that we have collected in the three field seasons funded by this grant (2003-2005) we will develop general mathematical models addressing the importance of habitat structure and community structure on risk resulting from diseases that infect multiple host species and specific models for predicting risk of disease outbreaks in the black-tailed prairie dog in different landscapes. These models should illustrate the potential for multiple stressors (habitat alteration, community alteration and introduced disease) to influence population risk.
Journal Articles on this Report : 12 Displayed | Download in RIS Format
Other project views: | All 47 publications | 15 publications in selected types | All 12 journal articles |
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Ahn K, Chan K, Bai Y, Kosoy M. Bayesian Inference With Incomplete Multinomial Data:A Problem in Pathogen Diversity. JOURNAL OF THE AMERICAN STATISTICAL ASSOCIATION 2010;105(490):600-611. |
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Brinkerhoff RJ, Ray C, Thiagarajan B, Collinge SK, Cully Jr. JF, Holmes B, Gage KL. Prairie dog presence affects occurrence patterns of disease vectors on small mammals. Ecography 2008;31(5):654-662. |
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Brinkerhoff R, Collinge S, Bai Y, Ray C. Are Carnivores Universally Good Sentinels of Plague?. VECTOR-BORNE AND ZOONOTIC DISEASES 2009;9(5):491-497 |
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Brinkerhoff R, Collinge S, Ray C, Gage K. Rodent and Flea Abundance Fail to Predict a Plague Epizootic in Black-Tailed Prairie Dogs. VECTOR-BORNE AND ZOONOTIC DISEASES 2010;10(1):47-52 |
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Brinkerhoff R, Martin A, Jones R, Collinge S. Population genetic structure of the prairie dog flea and plague vector, Oropsylla hirsuta. PARASITOLOGY 2011;138(1):71-79. |
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Collinge SK, Johnson WC, Ray C, Matchett R, Grensten J, Cully JF, Gage KL, Kosoy MY, Loye JE, Martin AP. Landscape structure and plague occurrence in black-tailed prairie dogs on grasslands of the western USA. Landscape Ecology 2005;20(8):941-955. |
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Collinge SK, Johnson WC, Ray C, Matchett R, Grensten J, Cully Jr. JF, Gage KL, Kosoy MY, Loye JE, Martin AP. Testing the generality of a trophic-cascade model for plague. EcoHealth 2005;2(2):102-112. |
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Cully J, Collinge S, VanNimwegen R, Ray C, Johnson W, Thiagarajan B, Conlin D, Holmes B. Spatial variation in keystone effects: small mammal diversity associated with black-tailed prairie dog colonies. ECOGRAPHY 2010;33(4):667-677 |
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Johnson WC, Collinge SK. Landscape effects on black-tailed prairie dog colonies. Biological Conservation 2004;115(3):487-497. |
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Sackett L, Cross T, Jones R, Johnson W, Ballare K, Ray C, Collinge S, Martin A. Connectivity of prairie dog colonies in an altered landscape:inferences from analysis of microsatellite DNA variation. CONSERVATION GENETICS 2012;13(2):407-418. |
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Thiagarajan B, Cully Jr. JF, Loughin TM, Montenieri JA, Gage KL. Geographic variation in rodent-flea relationships in the presence of black-tailed prairie dog colonies. Journal of Vector Ecology 2008;33(1):178-190. |
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Wilder A, Eisen R, Bearden S, Montenieri J, Tripp D, Brinkerhoff R, Gage K, Antolin M. Transmission efficiency of two flea species (Oropsylla tuberculata cynomuris and Oropsylla hirsuta) involved in plague epizootics among prairie dogs. ECOHEALTH 2008;5(2):205-212. |
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Supplemental Keywords:
risk assessment, pathogens, ecosystem, scaling, habitat, ecology, epidemiology, modeling,, RFA, Scientific Discipline, Geographic Area, Ecosystem Protection/Environmental Exposure & Risk, wildlife, Ecosystem/Assessment/Indicators, State, Environmental Monitoring, Ecological Risk Assessment, Ecology and Ecosystems, molecular epidemiology, risk assessment, ecosystem modeling, habitat, population stressors, endangered species, assessment models, ecology, ecosystem assessment, molecular diagnostics, animal responses, environmental risks, fleas, habitat loss, Wildlife Risk Assessment, conservation, genetic testing, wildlife community structure, risk models, ecological assessment, ecological impacts, ecosystem indicators, pathogen, environmental stress, ecosystem stress, ecological models, habitat alteration, prarie dogs, disease, ecological research, Colorado (CO)Relevant Websites:
http://spot.colorado.edu/~sharonc/CollingeLab.htm Exit
Progress and Final Reports:
Original AbstractThe perspectives, information and conclusions conveyed in research project abstracts, progress reports, final reports, journal abstracts and journal publications convey the viewpoints of the principal investigator and may not represent the views and policies of ORD and EPA. Conclusions drawn by the principal investigators have not been reviewed by the Agency.