
NSF Org: |
DEB Division Of Environmental Biology |
Recipient: |
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Initial Amendment Date: | August 13, 2015 |
Latest Amendment Date: | July 1, 2022 |
Award Number: | 1518663 |
Award Instrument: | Continuing Grant |
Program Manager: |
Samuel Scheiner
DEB Division Of Environmental Biology BIO Directorate for Biological Sciences |
Start Date: | August 15, 2015 |
End Date: | July 31, 2023 (Estimated) |
Total Intended Award Amount: | $1,807,599.00 |
Total Awarded Amount to Date: | $1,976,872.00 |
Funds Obligated to Date: |
FY 2016 = $34,600.00 FY 2017 = $379,952.00 FY 2019 = $39,106.00 FY 2020 = $95,567.00 |
History of Investigator: |
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Recipient Sponsored Research Office: |
300 TURNER ST NW BLACKSBURG VA US 24060-3359 (540)231-5281 |
Sponsor Congressional District: |
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Primary Place of Performance: |
Kasane BC |
Primary Place of
Performance Congressional District: |
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Unique Entity Identifier (UEI): |
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Parent UEI: |
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NSF Program(s): | Ecology of Infectious Diseases |
Primary Program Source: |
01001617DB NSF RESEARCH & RELATED ACTIVIT 01001718DB NSF RESEARCH & RELATED ACTIVIT 01001920DB NSF RESEARCH & RELATED ACTIVIT 01002021DB NSF RESEARCH & RELATED ACTIVIT |
Program Reference Code(s): |
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Program Element Code(s): |
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Award Agency Code: | 4900 |
Fund Agency Code: | 4900 |
Assistance Listing Number(s): | 47.074 |
ABSTRACT
Many wildlife species are social and live in groups, which provides benefits critical to survival. Group living and cooperation between individuals improve group performance by enhancing reproduction, improving foraging success, and increasing the ability to defend against predators. However, it is also known that the relative size of the group matters. If the number of individuals in a group decreases, the benefits also may decrease, potentially threatening group persistence. This phenomenon is referred to as the Allee effect: a population or group is at an increased risk of extinction when the number or density of individuals falls below a certain threshold due to either ecological or genetic factors (or a combination of the two). On the other hand, increased populations and increased population densities also can be problematic because they enhance group vulnerability to infectious disease. Allee effects have been widely studied and are known to have important implications for wildlife ecology but the connection between Allee effects and disease emergence is much less well understood. Understanding how group size and Allee effects drive infectious disease interactions is critical, however, to the conservation and management of endangered social species as well as to the control of emerging diseases that infect group-living species and threaten both human and animal health. In the research funded by this award, Dr. Kathleen Alexander (Virginia Polytechnic Institute State University) and her team will take an innovative approach to address this critical knowledge gap. They will integrate empirical field studies with mathematical modeling to investigate and identify principles and processes that influence disease transmission in group-living species. They also will establish international scientific networks linked to a comprehensive postdoctoral and graduate student-training program to produce multidisciplinary scientists with skills in international emerging infectious disease research, an area of increasing need. Other education components of the project include a structured K-7 educational program to foster interest and increase understanding of infectious disease ecology in children in the study region. The research project will also establish a foundation to foster collaborative learning between Botswana youth and undergraduate minority students in the United through interactive lectures and contemporary learning media including podcasts and social media. This program will link students from Botswana, where infectious disease deaths from HIV/AIDS and tuberculosis are common, and the United States where pandemic infectious disease is rarely experienced. Students will explore disease causation and control on a broad level with a focus on the common global need. This approach is directed at strengthening cross-cultural understanding and international leadership capacity in minority-driven scientific discovery in the ecology of emerging infectious disease.
To study the connection between Allee effects and infectious disease emergence, Alexander and her team will build on their long-term study of banded mongoose (Mungos mungo) in northern Botswana. The highly social banded mongoose is threatened with a novel, emerging tuberculosis (TB) pathogen, Mycobacterium mungi. This pathogen is closely related to the human TB pathogen, M. africanum, and causes high levels of mortality among banded mongoose, threatening the persistence of smaller social groups. The research team will take an integrated methodological approach that links molecular genetic studies of the host and pathogen with population biology and behavioral ecology studies of mongoose social groups that occur across both protected and unprotected areas of the landscape. They will use this empirical study system to investigate and identify dominant factors, processes, and thresholds that determine the outcome of the interaction between infectious disease and Allee effects. Research results will be used to develop a conceptual framework and advance knowledge and theory that can be used to determine if and when Allee effects should be included in models of infectious disease in group-living species and how these interaction should be computationally characterized. Results will be important to the management of social wildlife species involved in transmission of infectious diseases of importance to both animal and public health as well as to the conservation of endangered group-living species.
PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH
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PROJECT OUTCOMES REPORT
Disclaimer
This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.
Intellectual Merit
We characterized Allee effects (AEs) on pathogen persistence and transmission in a socially structured, group-living species, the banded mongoose in Northern Botswana. While AEs were important in predicting group demographic dynamics, they did not moderate pathogen persistence potential. Rather, troops with more persistent disease had more variable troop sizes than those without disease (n=76 troop-years), suggesting pathogen transmission and persistence is driven by more complex environment-host-pathogen interactions. Group extinction thresholds are identified (n=6 mongoose, n=21 study years), with constraints on minimum groups size influenced likely by resource availability.
We constructed dynamic models of pathogen transmission including a network transmission model from indirect and direct social networks. We also evaluated methods to predict the epidemic threshold for temporal contact network models and identify areas that remain unexplored. We characterized our model system allowing for enhanced understanding of pathogen-host-landscape interactions including the influence of humans on these dynamics and improved model development. Banded mongooses in our study site had significantly higher within-troop aggression levels when foraging in garbage compared to other foraging habitats. Our data suggest that mongoose troops that forage in garbage may be at greater risk of acquiring TB by incurring injuries that may allow for pathogen invasion. Our study suggests the need to consider the indirect effects of garbage on behavior and wildlife health when developing waste management approaches in human-modified areas. Although banded mongoose are territorial, den use by troops other than the resident troop was observed, but only for anthropogenic dens sites. These space-sharing behaviors can significantly impact pathogen transmission dynamics and disease spread in these human-modified landscapes. Mongooses living in association with humans was more concentrated in the dry season than the wet season, when historically accepted ecological theory predicted more dispersed space use. Resource richness factors such as building density were associated with space use only during the dry season underscoring the important influence urban environments can have on modifying wildlife behavior. There is growing need to explicitly incorporate human–animal interactions into ecological theory and research. We also identify nocturnal space use in this diurnal species independent of lunar phase. Enhanced understanding of wildlife activity patterns might provide new insights into the interaction between ecological phenomenon and species biology that spans the diurnal–nocturnal spectrum.
Banded mongooses also exhibited seasonal chronic glucocorticoid elevation, associated primarily with food limitation and secondarily with reproduction. Magnitude and duration of this elevation suggests that this may be maladaptive for some animals, with possible fitness consequences. In late dry season, this population may face a convergence of stressors (food limitation, agonistic encounters at concentrated food resources, evictions, estrus, mate competition, parturition, and predation pressure on pups), which may induce homeostatic overload. These dynamics may underpin the more seasonal presentation of this TB disease.
In this study, we also fully characterized the pathological and clinical presentation of M. mungi in the banded mongoose host. We identify primary environmental transmission that occurs in association with social communication behavior. We have detected differences in lipid production in anal gland secretions collected from healthy and infected mongoose. We also note significant differences in the mongoose gut microbiome structure when Mycobacterium spp. are detected as part of the gut microbial community, particularly a positive correlation between Mycobacterium and members of the family Rhizobiaceae, and a negative correlation with the family Bacteroides.
We also identified bidirectional interactions between land use, vigilance, group size, and olfactory behaviors that influence pathogen transmission dynamics, creating the potential for spatial hot spots of transmission. We identified dispersal estimates through microsatellite markers across land type; sequenced the genome of both host (banded mongoose) and the nonculturable tuberculosis (TB) pathogen, M. mungi. We created a novel transcriptomic marker assay for disease state detection, and cementum aging approaches to improve the tractability of this host-pathogen systems, applications that have broad impacts to studying wildlife across systems.
Broader impacts
This work has contributed to 16 publications, one book chapter, and six conference presentations. The project has trained USA and Botswana scholars including 27 undergraduate students, 17 REU participants, 7 veterinary students, 11 graduate students (1 Botswana citizen, 1 Botswana government biologist), 8 postdoctoral associates, 25 Botswana field and lab technicians and numerous Botswana Government officers (>15). A field-based course was developed (6 units) and delivered in 2019 and 2022 in Botswana to a total of 17 USA undergraduates (some under minority REU funding) and one Botswana undergraduate. Eight minority USA high school students/teachers traveled to the study site for experiential learning in 2019 and 1 teacher and two students in 2022. The project educational program was delivered across 12 schools to more than 420 children per week across years reaching thousands of children. Outputs of this project have informed wildlife management approaches in Botswana, communicated across the Botswana Government ministries and departments.
Last Modified: 05/27/2024
Modified by: Kathleen A Alexander
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