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PREVALENCE and RISK FACTORS of TRICHOMONAS GALLINAE and TRICHOMONOSIS in GOLDEN EAGLE (AQUILA CHRYSAETOS) NESTLINGS in WESTERN NORTH AMERICA Author(S): Benjamin M

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PREVALENCE and RISK FACTORS of TRICHOMONAS GALLINAE and TRICHOMONOSIS in GOLDEN EAGLE (AQUILA CHRYSAETOS) NESTLINGS in WESTERN NORTH AMERICA Author(S): Benjamin M PREVALENCE AND RISK FACTORS OF TRICHOMONAS GALLINAE AND TRICHOMONOSIS IN GOLDEN EAGLE (AQUILA CHRYSAETOS) NESTLINGS IN WESTERN NORTH AMERICA Author(s): Benjamin M. Dudek, Michael N. Kochert, Joseph G. Barnes, Peter H. Bloom, Joseph M. Papp, Richard W. Gerhold, Kathryn E. Purple, Kenneth V. Jacobson, Charles R. Preston, Chris R. Vennum, James W. Watson, and Julie A. Heath Source: Journal of Wildlife Diseases, 54(4):755-764. Published By: Wildlife Disease Association https://doi.org/10.7589/2017-11-271 URL: http://www.bioone.org/doi/full/10.7589/2017-11-271 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. DOI: 10.7589/2017-11-271 Journal of Wildlife Diseases, 54(4), 2018, pp. 755–764 Ó Wildlife Disease Association 2018 PREVALENCE AND RISK FACTORS OF TRICHOMONAS GALLINAE AND TRICHOMONOSIS IN GOLDEN EAGLE (AQUILA CHRYSAETOS) NESTLINGS IN WESTERN NORTH AMERICA Benjamin M. Dudek,1,10 Michael N. Kochert,2 Joseph G. Barnes,3 Peter H. Bloom,4 Joseph M. Papp,4 Richard W. Gerhold,5 Kathryn E. Purple,5 Kenneth V. Jacobson,6 Charles R. Preston,7 Chris R. Vennum,8 James W. Watson,9 and Julie A. Heath1 1 Boise State University, Department of Biological Sciences and Raptor Research Center, 1910 University Dr., Boise, Idaho 83725, USA 2 US Geological Survey, Forest and Rangeland Ecosystem Science Center, 970 Lusk St., Boise, Idaho 83706, USA 3 Nevada Department of Wildlife, 4747 Vegas Dr., Las Vegas, Nevada 89108, USA 4 / Bloom Research Inc., 135812 S Cloverdale Rd., Los Angeles, California 90019, USA 5 University of Tennessee, Department of Biomedical and Diagnostic Sciences, 2407 River Dr., Knoxville, Tennessee 37996, USA 6 Arizona Department of Game and Fish, 5000 W Carefree Hwy., Phoenix, Arizona 85086, USA 7 Draper Natural History Museum, Buffalo Bill Center of the West, 720 Sheridan Ave., Cody, Wyoming 82414, USA 8 Department of Biology, University of Nevada, 1664 N Virginia St., Reno, Nevada 89557, USA 9 Washington Department of Fish and Wildlife, PO Box 43141, Olympia, Washington 98504, USA 10 Corresponding author (email: [email protected]) ABSTRACT: Avian trichomonosis, caused by the protozoan Trichomonas gallinae, affects bird-eating raptors worldwide. Raptors can develop trichomonosis by feeding on infected prey, particularly Rock Pigeons (Columba livia), which are a reservoir for T. gallinae. Raptors may be particularly vulnerable to T. gallinae infection in degraded habitats, where changes in resources may cause raptors to switch from foraging on native prey to synanthropic avian species such as Rock Pigeons. Golden Eagles (Aquila chrysaetos) typically forage on mammals; however, habitat across much of their range is experiencing degradation through changes in land use, climate, and human encroachment. In 2015, we examined the prevalence of T. gallinae infection in Golden Eagle nestlings across western North America and conducted an intensive study on factors associated with T. gallinae infection and trichomonosis in southwestern Idaho. We found T. gallinae infection in 13% (12/96) of eagle nestlings across 10 western states and in 41% (13/32) of nestlings in southwestern Idaho. At the Idaho site, the probability of T. gallinae infection increased as the proportion of Rock Pigeons in nestling diet increased. Nestlings with diets that consisted of 10% Rock Pigeons had a very high probability of T. gallinae infection. We compared historical (1971–81) and recent (2014–15) diet data and incidence of trichomonosis lesions of nestling eagles in Idaho and found that the proportion of Rock Pigeons in eagle diets was higher in recent versus historical periods, as was the proportion of eagle nestlings with trichomonosis lesions. Our results suggested that localized shifts in eagle diet that result from habitat degradation and loss of historical prey resources have the potential to affect Golden Eagle nestling survival and supported the hypothesis that land use change can alter biologic communities in a way that might have consequences for disease infection and host susceptibility. Key words: Diet shift, disease, raptor, Rock Pigeon. INTRODUCTION Trichomonas gallinae primarily affects the upper digestive tract of birds, where it can Avian trichomonosis, caused by the flagel- cause the development of caseous lesions in lated protozoan parasite Trichomonas galli- the oropharynx that can lead to starvation or nae, is an infectious disease affecting avian suffocation (Amin et al. 2014). Previously communities worldwide (Tompkins et al. unexposed avian populations can be severely 2015). Trichomonas gallinae is commonly affected by the parasite (Bunbury et al. 2008), found in birds in the Columbidae family, and significant population declines of com- and the parasite has followed the introduc- mon avian species from T. gallinae exposure tions, and range expansions, of Rock Pigeons (Robinson et al. 2010) suggest that popula- (Columba livia) worldwide (Stabler 1947). tions of rare or threatened species that are 755 756 JOURNAL OF WILDLIFE DISEASES, VOL. 54, NO. 4, OCTOBER 2018 na¨ıve to T. gallinae infection may be vulner- communities that support jackrabbits have able. been reduced through the effects of wildfire, Bird-eating raptors that feed on T. gallinae- invasive plants, and land development (Ko- infected prey are susceptible to infection and chert et al. 1999). These landscape-level the development of trichomonosis that often changes have been associated with significant results in mortality. Previous studies found shifts in Golden Eagle diets, with a decrease high rates of trichomonosis in raptors where in the proportion of jackrabbits and an loss of native habitat and prey resulted in increase in avian prey, including Rock Pigeons dietary shifts. Bonelli’s Eagles (Aquila fascia- (Heath and Kochert 2016). ta) in northeastern Spain increase their Given the changes to western North consumption of Rock Pigeons as preferred American landscapes that have altered prey prey populations decline, increasing the risk availability for Golden Eagles (Bedrosian et al. of T. gallinae infection and becoming a major 2017), and increased contact with synanthrop- cause of nestling mortality (Real et al. 2000; ic species like Rock Pigeons, our objectives Palma et al. 2006). Similar studies describe were to document the prevalence of T. high T. gallinae infection rates in local gallinae in nestling Golden Eagles, identify populations of Cooper’s Hawks (Accipiter the factors associated with infection, and cooperii) in Arizona (Boal et al. 1998) and examine whether infection risk has changed Northern Goshawks (Accipiter gentilis)in over time. We sampled Golden Eagle nest- Great Britain (Cooper and Petty 1988) and lings throughout western North America Poland (Wieliczko et al. 2003), where land- during the 2015 breeding season to assess scape-level changes and human development the geographic prevalence of T. gallinae cause shifts in diets toward higher proportions infection. In addition, we conducted an of synanthropic columbids. In addition to diet, intensive study in southwestern Idaho to oral pH may affect risk of T. gallinae infection. examine whether nestling age, oral pH, or Trichomonas gallinae persists at a pH range of proportion of Rock Pigeons in nestling diet 6.5–7.5 (Read 1957) but is less viable in more- predicted T. gallinae infection rates. Finally, acidic conditions. Oral pH of nestling Coo- we used historical (1971–81) and recent per’s Hawks creates a hospitable environment (2014–15) data to examine how nestling diet for T. gallinae, but oral pH decreases as hawks and incidence of trichomonosis have changed age, and adults are less susceptible to over time at our Idaho study site. infection (Urban and Mannan 2014). Differ- ential susceptibility in Cooper’s Hawks based on age groups suggests differences in oral pH MATERIALS AND METHODS could affect susceptibility to T. gallinae Prevalence of T. gallinae in western North America infection within individuals. From April to June 2015, we visited historical In western North America, Golden Eagles Golden Eagle nesting territories at 11 study sites (Aquila chrysaetos) occupy open habitats, in western North America to examine nestlings including shrub steppe ecosystems, and prey and collect oral swab samples (Fig. 1). At sites primarily on rabbits and hares (Leporidae) outside of Idaho, we made one or two visits to and ground squirrels (Sciuridae; Bedrosian et nests to examine all nestlings and collect swabs (n¼123) when nestlings were approximately 28 al. 2017). Over the last century, anthropogenic and 56 d old. At the intensive study site in Idaho, actions have degraded and fragmented shrub in the Morley Nelson
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