Source: UNIVERSITY OF CALIFORNIA, DAVIS submitted to
DISEASE ECOLOGY OF CROWS IN URBAN AND AGRICULTURAL LANDSCAPES: ASSESSING THREATS TO WILDLIFE AND HUMAN HEALTH
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
TERMINATED
Funding Source
HATCH
Reporting Frequency
Annual
Accession No.
0231454
Grant No.
(N/A)
Project No.
CA-D-WFB-2180-H
Proposal No.
(N/A)
Multistate No.
(N/A)
Program Code
(N/A)
Project Start Date
Oct 1, 2012
Project End Date
Feb 18, 2016
Grant Year
(N/A)
Project Director
Townsend, A.
Recipient Organization
UNIVERSITY OF CALIFORNIA, DAVIS
410 MRAK HALL
DAVIS,CA 95616-8671
Performing Department
Wildlife, Fish and Conservation Biology
Non Technical Summary
Human-commensal American crows are often found in high densities in urban and agricultural landscapes throughout North America. These high densities, combined with the stress, pollution, and low-quality food often encountered by wildlife in human-dominated landscapes, could combine to elevate disease prevalence. Disease in crows could pose a threat to the health and populations of other species of wildlife, as well as to human health and to animals of economic importance. For example, previous studies have shown that West Nile virus (WNV), a zoonotic disease to which crows are particularly susceptible, has a particularly strong impact on crow populations in urban settings. Other studies have shown that feces under rook roosts in Western Europe harbor bacteria of human health concern, including antibiotic resistant E. coli and Salmonella, leading the authors to suggest that corvids could serve as reservoirs and transmitters of antibiotic resistant bacteria across the landscape. Here, we examine the ecology of disease among crows in urban and agricultural landscapes in Yolo County, California. Free-living crows in a focal site spanning the UC Davis campus and adjacent agricultural fields are caught, marked, and tested for disease presence (e.g., WNV, trichomonas, fecal parasites and bacteria, blood parasites, avian flu) and measured for overall condition. Survival and movement of these marked crows are monitored, and crows that die on the study site are submitted for diagnostics at the California Food Health and Safety Lab. Results of this work will advance public welfare, within and beyond California, by identifying environmental predictors of zoonotic wildlife diseases and by determining the role crows play in the movement of pathogens across human-dominated landscapes.
Animal Health Component
0%
Research Effort Categories
Basic
100%
Applied
(N/A)
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
3110820109010%
3110820110010%
3110820110110%
3110820111010%
3110820116010%
7120820104010%
7120820107010%
1350820104010%
1350820107020%
Knowledge Area
135 - Aquatic and Terrestrial Wildlife; 311 - Animal Diseases; 712 - Protect Food from Contamination by Pathogenic Microorganisms, Parasites, and Naturally Occurring Toxins;

Subject Of Investigation
0820 - Wild birds;

Field Of Science
1070 - Ecology; 1090 - Immunology; 1101 - Virology; 1160 - Pathology; 1100 - Bacteriology; 1110 - Parasitology; 1040 - Molecular biology;
Goals / Objectives
My research evaluates the health and disease ecology of the American Crow (Corvus brachyrhychos) in urban and agricultural settings. I assess environmental and genetic risk factors for disease, examine the fitness and population impacts of these diseases, and evaluate risks that they present to human health. This work will advance scientific knowledge by providing rare information of disease ecology in a free-living wildlife population. The information gathered will be of interest to scientists across a wide breadth of disciplines, including population ecologists interested in the factors driving population dynamics in human-commensal wildlife, evolutionary biologists interested in disease as a selection pressure, and conservation biologists interested in declining species within and on the edges of human-dominated landscapes. This work will advance public welfare by identifying environmental predictors of zoonotic wildlife diseases (e.g., West Nile virus) and by determining the role crows play in the movement of pathogens across human-dominated landscapes. Objectives: 1. To understand the ecology, feeding, and movement patterns of crows in urban and agricultural environments. 2. To characterize infectious diseases and their environmental and genetic risk factors in crows in urban and agricultural environments. 3. To assess habitat-specific fitness and population impacts of crow disease. 4. To examine the movement of pathogens of human health concern (e.g., Campylobacter, E. coli 0157; antibiotic-resistant bacteria) across the urban and agricultural landscapes through crow feces 5. To identify management practices that promote individual health and population stability of urban and agricultural wildlife, as well as human health Duration and outputs: The proposed work will require five years, including data collection and publication. Spring 2012: 100 crow nestlings marked and measured. Characterization of Campylobacter prevalence and pathogenicity underway. Campylobacter manuscript will be prepared and submitted for publication in winter 2012. 2013-2014: An additional 200 nestlings and 100 adults will be marked and measured and used to create a California crow health profile. Manuscripts reporting disease prevalence, disease risk factors, and the effects of urbanization and agricultural practices on crow health will be prepared and submitted for publication. 2015-2017: radio tags will be applied to marked birds to better assess their potential for moving pathogens across the landscape. Manuscript will be prepared and submitted for publication in winter 2017.
Project Methods
1. Crow ecology. To investigate the ecology of crows on an urban-agricultural gradient, I established a focal site spanning the UC Davis campus and the agricultural fields to the west of campus. Nestling crows from 40 nests have been marked and monitored for survival and dispersal patterns. I will begin catching, marking, and monitoring adult crows in our study site in the fall of 2012. This work will be repeated annually. In years four and five, I will put radio transmitters on the birds to better document movement patterns. 2. Infectious disease characterization. At the time of marking, crows are tested for disease presence (e.g., WNV, trichomonas, fecal parasites and bacteria, blood parasites, avian flu) and measured for overall condition (e.g., through blood chemistry, body condition, and hematology). Carcasses of crows that die on the study area are necropsied and tissues submitted for histopathology and diagnostics. Crows are genotyped at 10 microsatellite loci to determine molecularly-based inbreeding coefficients, which previous studies have shown to be predictors of disease mortality in crows (Townsend et al. 2009, Townsend et al. 2010). 3. Fitness impacts. Survival and disease outcomes will be modeled as a function of environmental and genetic characteristics to assess disease risk factors. Survival analyses are carried out in a mark-recapture modeling framework to account for imperfect detection probability. 4. Bacterial assays. Bacteria of human health concern (e.g., Campylobacter, E. coli 0157, Salmonella, antibiotic-resistant bacteria) have been cultured from crow feces. PCR-based techniques will be used to assess virulence and diversity of strains encountered. Feces will be collected from focal birds throughout the year to assess the potential for movement of these bacteria across the urban and agricultural landscape. 5. Management. Risk factors for wildlife and human disease and management strategies will be identified. This information will be disseminated on an international scale through publications in peer-reviewed journals. Information on appropriate management actions will also be disseminated to the agricultural and urban clientele though the Yolo County Cooperative Extension Advisors.

Progress 10/01/12 to 02/18/16

Outputs
Target Audience: Nothing Reported Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest? Nothing Reported What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? The faculty member has left UC Davis and the project will be closed.

Publications


    Progress 10/01/13 to 09/30/14

    Outputs
    Target Audience: Results of this work were shared through five peer-reviewed publications and through presentations by students at the Bay Area Microbial Pathogenesis Symposium (BAMPS) and Berkeley Microbiology Student Group Symposium. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? This work has supported the work of three UC Davis graduate students (Mitch Hinton, Masters student, Avian Science Graduate Group; Ryane Logsdon, Animal Behavioral Graduate Group; and Allison Weis, Microbiology Graduate Group) and two postdoctoral fellows (Dr. Sarah Wheeler, UC Davis School of Veterinary Medicine; Dr. Conor Taff, Department of Wildlife, Fish, and Conservation Biology), as well as an additional graduate student at UC San Francisco (David Freund, Biology Department). Mitch is examining horizontal transmission of West Nile virus among crows at nocturnal roosts. Sarah is sequencing and comparing strains of West Nile virus in resident and migratory birds. Conor is tracking and modeling movement of food-borne pathogens in avian hosts. Dave is examining geographic correlates of avian malaria. Allison is sequencing and comparing strains of Campylobacter in crows, humans, chickens, livestock, and non-human primates, using a full-genome sequencing approach. The project has also provided training for laboratory technician Melissa Jones, who has applied to the Avian Science Graduate Group next year because of her interest in the project. How have the results been disseminated to communities of interest? Although we have produced numerous peer-reviewed papers for the academic community this year, I am currently on Leave of Absence and haven't disseminated the results to a broader audience yet. I will increase this effort after my Leave (July 2015). What do you plan to do during the next reporting period to accomplish the goals? We collected the data that will be the basis for numerous (>4) additional papers this year, illuminating the effect of urbanization on disease prevalence of wild birds. With this critical mass of data collected, we will turn more of our attention to disseminated our results at professional meetings in the summer of 2015.

    Impacts
    What was accomplished under these goals? Our 2014 publications have illuminated the effects of urbanization on wildlife health (Townsend & Barker 2014), zoonotic diseases in urban birds (Wheeler et al. 2014; Weis et al. 2014, Hinton et al. (in revision), and Halova et al. 2014), and disease selection on MHC diversity in corvids (Eimes et al. (in revision)).

    Publications

    • Type: Journal Articles Status: Published Year Published: 2013 Citation: Oravcova VL, Ludek Z, Townsend AK, Clark AB, Ellis JC, Cizek A, & Literak I (2013) American crows as carriers of vancomycin-resistant enterococci with vanA gene. Environmental Microbiology: doi:10.1111/1462-2920.12213
    • Type: Journal Articles Status: Published Year Published: 2014 Citation: Halov� D, Papouaek I, Jamborova I, Masarikova M, Cizek A, Janecko N, Oravcova V, Zurek L, Clark A, Townsend AK, Ellis J, & Literak I (2014) Plasmid-mediated quinolone resistance genes in Enterobacteriaceae bacteria from American Crows (Corvus brachyrhynchos): high prevalence of bacteria with variable qnrB genes. Antimicrobial Agents and Chemotherapy 58(2):1257-8.
    • Type: Journal Articles Status: Published Year Published: 2014 Citation: Wheeler SS, Woods LW, Boyce WM, Eckstrand CD, Langevin SA, Reisen WK, & Townsend AK (2014) West Nile virus and non-West Nile virus mortality and coinfection of American Crows (Corvus brachyrhynchos) in California. Avian Diseases 58(2): 255-261.
    • Type: Journal Articles Status: Published Year Published: 2014 Citation: Weis AM, Miller M, Byrne B, Boyce W, & Townsend AK (2014) Prevalence and pathogenic potential of Campylobacter isolates in free-living, human commensal American Crows. Applied and Environmental Microbiology 80(5):1639.
    • Type: Journal Articles Status: Published Year Published: 2014 Citation: Townsend AK & Barker CM (2014) Plastic and the nest entanglement of urban and agricultural birds. PLoS ONE 9: e88006.
    • Type: Journal Articles Status: Under Review Year Published: 2015 Citation: Hinton MG, Reisen WK, Wheeler SS, and Townsend AK (In revision) West Nile virus activity in a winter roost of American crows (Corvus brachyrhynchos): is bird-to-bird transmission important in persistence and amplification? Journal of Medical Entomology.
    • Type: Journal Articles Status: Under Review Year Published: 2015 Citation: Eimes JA, Townsend AK., Sepil I, Nishiumi I & Satta Y (In revision) Species divergence, selection and polymorphism in the MHC of crows. PeerJ PrePrints, 2, e621v621. doi: 10.7287/peerj.preprints.621v1


    Progress 10/01/12 to 09/30/13

    Outputs
    Target Audience: Results of work completed during this time period reached two audiences: (1) the scientific community, by way of the publication of a peer-reviewed article demonstrating the presence of antibiotic-resistant bacteria in the crows of California and throughout North America (see product #1, below); (2) the public, through wide coverage by the popular press of this work (e.g., http://www.scientificamerican.com/article.cfm?id=flying-the-coop-antibiotic-resistance-spreads-to-birds-other-wildlife; http://www.onearth.org/articles/2013/11/oh-poop-wildlife-shows-signs-of-antibiotic-resistance). Several other peer-reviewed publications concerning zoonotic pathogens in urban crow roosts are currently in press and will be in print in 2014. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? Three graduate students (Mitch Hinton, Ryane Logsdon, and Alison Weis), two postdoctoral scholars (Sarah Wheeler, Conor Taff), and ten undergraduate research assistants have received training and professional development through this work. Postdoc Sarah Wheeler and graduate student Alison Weis have both submitted first-authored papers to peer-reviewed journals based on their contributions. Postdoc Taff received a prestigious NIFA/ USDA postdoctoral fellowship in 2013 to support further investigation into the movement of Campylobacter jejuni in the agricultural landscapes. How have the results been disseminated to communities of interest? Results of work completed during this time period reached two audiences: (1) the scientific community, by way of the publication of a peer-reviewed article demonstrating the presence of antibiotic-resistant bacteria in the crows of California and throughout North America (see product #1, below); (2) public media outlets, through wide coverage by the popular press of this work (e.g., http://www.scientificamerican.com/article.cfm?id=flying-the-coop-antibiotic-resistance-spreads-to-birds-other-wildlife; http://www.onearth.org/articles/2013/11/oh-poop-wildlife-shows-signs-of-antibiotic-resistance). I am also working on a public media article featuring this work in a special issue of “International Innovation” (http://www.international-innovation-northamerica.com/) with a broad focus on food, agriculture and environmental sciences, with publication expected in 2014. What do you plan to do during the next reporting period to accomplish the goals? Now that the zoonoses have been characterized, I am well-positioned to carry out the other goals of the project: (1) I will assess environmental and genetic risk factors for disease among individual crows; (2) I will assess the role of crows as a vector for zoonotic pathogens between the urban and agricultural landscapes using satellite and radio-telemetry technology; and (3) I will identify management practices that promote individual health and population stability of urban and agricultural wildlife, as well as human health. After I have identified disease risk factors and recommendations for disease management, I will disseminate information to the agricultural and urban clientele in collaboration with local and regional Cooperative Extension Advisors in the Department of Wildlife, Fish, & Conservation Biology. I will reach out directly to future stakeholders and clientele who could benefit from these management strategies, including agencies with interest in public health (e.g., California Department of Public Health), food safety (e.g., the poultry, cattle, and crop industries), and wildlife-human interactions (e.g., California Department of Fish & Game, Point Reyes Bird Observatory, The Audubon Society, and the Central Valley Joint Venture). I will also work with my partner agency at the Sacramento-Yolo Mosquito and Vector Control District to implement appropriate intervention at delineated WNV foci as part of their integrated pest management program, and share research findings with state agencies at the annual meeting of Mosquito and Vector Control Association of California and other professional societies. By informing local, state, and federal health programs, this project may improve zoonotic intervention in new, safe, economical, and effective ways.

    Impacts
    What was accomplished under these goals? We met and exceeded our own expectations for one of the major goals of this project: namely, to identify and characterize potential pathogens of human health concern in crows in the urban and agricultural landscapes of California. In 2013, we described and submitted four papers relevant to the subject. We described (1) the prevalence of two antibiotic-resistant bacterial types in urban crow roosts (vancomycin-resistant enterococci and quinolone resistance genes in Enterobacteriaceae bacteria); (2) the prevalence and pathogenic potential of Campylobacter jejuni in urban and agricultural crows; and (3) the role of co-infection and West Nile virus infection in urban crows. One paper (the vancomycin-resistant enterococci report) is in press; three additional papers have been accepted and will be published in 2014.

    Publications

    • Type: Journal Articles Status: Published Year Published: 2013 Citation: Oravcova, V., Zurek, L., Townsend, A., Clark, A.B., Ellis, J.C., Cizek, A., Literak, I., 2013. American crows as carriers of vancomycin-resistant enterococci with vanA gene. Environmental Microbiology; 6 AUG 2013
    • Type: Journal Articles Status: Published Year Published: 2013 Citation: Townsend, A.K., Sillett, T.S., Lany, N.K., Kaiser, S.A., Rodenhouse, N.L., Webster, M.S., Holmes, R.T., 2013. Warm springs, early lay dates, and double brooding in a North American migratory songbird, the Black-Throated Blue Warbler. Plos One 8, e59467.