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Award Abstract # 1518663
Can group living and the influence of Allee Effects explain infectious disease vulnerability in social species? Emergence of M. mungi in the cooperative breeding banded mongoose

NSF Org: DEB
Division Of Environmental Biology
Recipient: VIRGINIA POLYTECHNIC INSTITUTE & STATE UNIVERSITY
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 2015 = $1,427,647.00
FY 2016 = $34,600.00

FY 2017 = $379,952.00

FY 2019 = $39,106.00

FY 2020 = $95,567.00
History of Investigator:
  • Kathleen Alexander (Principal Investigator)
    kathyalx@vt.edu
  • Jeffrey Walters (Co-Principal Investigator)
  • Stephen Eubank (Former Co-Principal Investigator)
  • Bryan Lewis (Former Co-Principal Investigator)
Recipient Sponsored Research Office: Virginia Polytechnic Institute and State University
300 TURNER ST NW
BLACKSBURG
VA  US  24060-3359
(540)231-5281
Sponsor Congressional District: 09
Primary Place of Performance: Virginia Polytechnic Institute and State University
Kasane
 BC
Primary Place of Performance
Congressional District:
Unique Entity Identifier (UEI): QDE5UHE5XD16
Parent UEI: X6KEFGLHSJX7
NSF Program(s): Ecology of Infectious Diseases
Primary Program Source: 01001516DB NSF RESEARCH & RELATED ACTIVIT
01001617DB NSF RESEARCH & RELATED ACTIVIT

01001718DB NSF RESEARCH & RELATED ACTIVIT

01001920DB NSF RESEARCH & RELATED ACTIVIT

01002021DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 1228, 7218, 7242, 7744, 9169, 9178, 9179, 9251, 9261, EGCH
Program Element Code(s): 724200
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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(Showing: 1 - 10 of 35)
Alexander, KA and CE Sanderson "Losing the battle in the illegal wildlife trade ? is it time for a new approach?" Nature Ecology and Evolution , v.1 , 2017 doi.org/10.1038/s41559-017-0090
Alexander, KA, Larsen, MH, Robbe-Austermand, S, Tod, A, Stuberd, and P, Camp. "Draft genome sequence of the Mycobacterium tuberculosis complex pathogen, M. mungi, identified in a banded mongoose (Mungos mungo) in Northern Botswana." Genome Announcements , v.4 , 2016 , p.e00281-16 10.1128/genomeA.00471-16
Alexander, K.A., Sanderson, C.E., Larsen, M.H., Robbe-Austerman, S., Williams, M.C. and Palmer, M.V. "Emerging Tuberculosis Pathogen Hijacks Social Communication Behavior in the Group-Living Banded Mongoose (Mungos mungo)" MBio , v.7 , 2016 , p.e00281-16 doi: 10.1128/mBio.00281-16
Alexander, Kathleen Anne, and Carol Anne Nichols "Behavior-Landscape Interactions May Create Super-Spreader Environments: Vigilance-Olfactory Interactions Across Land Type and Disease Transmission Potential in the Banded Mongoose" Frontiers in Ecology and Evolution , v.8 , 2020 https://doi.org/10.3389/fevo.2020.00047
Alexander, Kathleen A., Peter N. Laver, Mark C. Williams, Claire E. Sanderson, Carly Kanipe, and Mitchell V. Palmer "Pathology of the emerging Mycobacterium tuberculosis complex pathogen, Mycobacterium mungi, in the banded mongoose (Mungos mungo)" Veterinary pathology , v.55 , 2018 , p.303 10.1177/030098581774173
Bonnie Fairbanks Flint,Dana M. Hawley,Kathleen A. Alexander "Do not feed the wildlife: associations between garbage use, aggression, and disease in banded mongooses (Mungos mungo)" Ecology and Evolution , 2016 10.1002/ece3.2343
Carlson, C.J., Kracalik, I.T., Ross, N., Alexander, K.A., Hugh-Jones, M.E., Fegan, M., Elkin, B.T., Epp, T., Shury, T.K., Zhang, W. and Bagirova, M. "The global distribution of Bacillus anthracis and associated anthrax risk to humans, livestock and wildlife" Nature microbiology , v.4 , 2019 , p.1337 https://doi.org/10.1038/s41564-019-0435-4
Carlson, C., Kracalik, IT, Ross, N, Alexander, KA, Hugh-Jones, ME, Fegan, ME, Elkin, B, Epp, T, Shury, TK, Bagirova, M, Getz, W., and Jason Blackburn "The global distribution of Bacillus anthracis and associated anthrax risk to humans,livestock, and wildlife" Nature Microbiology , v.1 , 2019
C.E. Sanderson and K.A. Alexander "Unchartered waters: Climate change likely to intensify infectious disease outbreaks causing mass mortality events in marine mammals" Global Change Biology , 2020 https://doi.org/10.1111/gcb.15163
Claire E. Sanderson, Ferran Jori, Nazneen Moolla, Janusz T. Paweska, Nesredin Oumer, and Kathleen A. Alexander "Rift Valley fever in humans in Botswana: the quandary of silent circulation" Emerging Infectious Diseases , 2020
Fairbanks, B.M., Hawley, D.M. and K.A. Alexander. "Do not feed the wildlife: Behavior and disease consequences of foraging in garbage for banded mongooses (Mungos mungo)." Ecology and Evolution , v.6 , 2016 10.1002/ece3.2343
(Showing: 1 - 10 of 35)

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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