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Prevalence and Potential Impact Of PREVALENCE AND POTENTIAL IMPACT OF TOXOPLASMA GONDII ON THE ENDANGERED AMARGOSA VOLE (MICROTUS CALIFORNICUS SCIRPENSIS), CALIFORNIA, USA Authors: Amanda Poulsen, Heather Fritz, Deana L. Clifford, Patricia Conrad, Austin Roy, et. al. Source: Journal of Wildlife Diseases, 53(1) : 62-72 Published By: Wildlife Disease Association URL: https://doi.org/10.7589/2015-12-349 BioOne Complete (complete.BioOne.org) is a full-text database of 200 subscribed and open-access titles in the biological, ecological, and environmental sciences published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Complete website, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/terms-of-use. Usage of BioOne Complete 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. Downloaded From: https://bioone.org/journals/Journal-of-Wildlife-Diseases on 16 Sep 2019 Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP) DOI: 10.7589/2015-12-349 Journal of Wildlife Diseases, 53(1), 2017, pp. 62–72 Ó Wildlife Disease Association 2017 PREVALENCE AND POTENTIAL IMPACT OF TOXOPLASMA GONDII ON THE ENDANGERED AMARGOSA VOLE (MICROTUS CALIFORNICUS SCIRPENSIS), CALIFORNIA, USA Amanda Poulsen,1,5 Heather Fritz,2,4 Deana L. Clifford,1,3 Patricia Conrad,4 Austin Roy,1,2 Elle Glueckert,1 and Janet Foley1 1 Department of Veterinary Medicine and Epidemiology, University of California, One Shields Avenue, Davis, California 95616, USA 2 Department of Veterinary Microbiology and Pathology, Washington State University, PO Box 647040, Pullman, Washington 99164, USA 3 Wildlife Investigations Lab, California Department of Fish and Wildlife, 1701 Nimbus Road Suite D, Rancho Cordova, California 95670, USA 4 Department of Pathology, Microbiology, and Immunology, University of California, One Shields Avenue, Davis, California 95616, USA 5 Corresponding author (email: [email protected]) ABSTRACT: We investigated the prevalence of Toxoplasma gondii in 2011–15 to assess its potential threat on the endangered Amargosa vole (Microtus californicus scirpensis) in California, US. Surveillance was simultaneously performed on populations of syntopic rodent species. We detected antibodies to T. gondii in sera from 10.5% of 135 wild-caught Amargosa voles; 8% of 95 blood samples were PCR-positive for the T. gondii B1 gene, and 5.0% of 140 sympatric rodent brain samples were PCR-positive. Exposure to T. gondii did not change the probability that an animal would be recaptured in the field study. Behavioral response to domestic cat (Felis catus) and bobcat (Lynx rufus) urine was evaluated in five nonendangered Owens Valley voles (Microtus californicus vallicola) as surrogates for Amargosa voles and seven uninfected controls. Voles showed mild attraction to mouse urine and had neutral reactions to domestic cat urine whether or not infected. Time spent near bobcat urine was approximately twice as high in infected than in uninfected voles (although not statistically significant). The presence of T. gondii in wild Amargosa vole and sympatric rodent populations may hinder the endangered Amargosa vole population’s ability to recover in the wild. Key words: Amargosa vole, behavior, Microtus californicus, Toxoplasma gondii. INTRODUCTION voles may maintain T. gondii in nature (e.g., Hejlicek and Literak 1998). The Amargosa vole (Microtus californicus Toxoplasma gondii is a zoonotic protozoan, scirpensis) is a federally and state-endangered infecting 30–40% of humans worldwide (Ten- California vole subspecies under the US ter et al. 2000). Most human infections are Endangered Species Act. It inhabits Mojave asymptomatic but can be fatal to immuno- Desert marshes only near Tecopa, Inyo compromised individuals (Nissapatorn 2009), County, California (Cudworth and Koprowski and T. gondii causes birth defects and 2010). Little research has been done on this miscarriages (Jones et al. 2003). Toxoplasma animal (US Fish and Wildlife Service gondii only sexually reproduces in felines, [USFWS] 1997), but its populations have a including cats (Felis catus) and bobcats (Lynx rufus) (Kikuchi et al. 2004). Oocysts passed in narrow niche breadth, long isolation from felid feces may remain viable in feces, water, other California voles, and low numbers or soil for months to years (Yilmaz and (Klinger et al. 2013). Habitat degradation, Hopkins 1972; Baldursson and Karanis 2011; predation, low genetic diversity, and disease Lelu et al. 2012), serving as a source of are important threats (USFWS 1997). In infection to intermediate hosts, which include 2013, Toxoplasma gondii DNA was found in most warm-blooded animals (Tenter et al. 13% of Amargosa voles and antibodies in 8% 2000). Infection leads to formation of latent (Ott-Conn et al. 2014), suggesting Amargosa tissue cysts in muscle and brain (Dubey 2010) 62 Downloaded From: https://bioone.org/journals/Journal-of-Wildlife-Diseases on 16 Sep 2019 Terms of Use: https://bioone.org/terms-of-use Access provided by Universidade de Sao Paulo (USP) POULSEN ET AL.—TOXOPLASMA GONDII IN THE ENDANGERED AMARGOSA VOLE 63 that are transmitted through tissue consump- Trapping and sample collection tion. Transplacental transmission is also a Small mammals were live-trapped intermittent- major route in small mammals (e.g., Marshall ly over approximately 5-d intervals in December et al. 2004). 2013, every month in 2014 except February and Low-dose tachyzoite infection can be sub- December, and January 2015 using large Sher- clinical in rats, mice, and voles, whereas man traps (HB Sherman Traps, Tallahassee, Florida, USA) in marsh groups Shoshone, One, infection with oocysts can cause muscle NC Trailer, Grimshaw, and Trans (Fig. 1). Traps lesions and locomotory or breathing difficul- were baited with peanut butter, oats, and alfalfa, ties (Dubey and Frenkel 1973; Sedlak et al. with an apple slice during summer. Traps were set 2001). Toxoplasma gondii causes reduced in covered areas and checked every 4–6 h. Voles aversion to felids in some rodents (Berdoy et were ear-tagged with numbered bands (1005-1 Monel, National Band and Tag Co., Newport, al. 2000; Vyas et al. 2007), a form of parasite- Kentucky, USA). A maximum of 0.05 mL of blood increased trophic transmission (PITT) was taken using retro-orbital abrasion (Mills et al. (Seppal¨ a¨ et al. 2008) that can increase 1995), and animals were released at the trap site. transmission to the definitive feline host. If Western harvest mice (Reithrodontomys mega- PITT occurs in voles, then T. gondii may lotis), house mice (Mus musculus), and cactus mice (Peromyscus eremicus) were euthanatized contribute to Amargosa vole population de- with a ketamine/xylazine overdose (.100 mg cline. ketamine and .10 mg xylazine) and cervical We assessed the effect of T. gondii on dislocation and kept frozen before postmortem Amargosa voles, specifically to 1) determine examination at the laboratory for collection of the prevalence of T. gondii in voles and blood from the chest cavity and brain tissue. sympatric rodents, 2) evaluate whether infect- Bobcats were assessed with remote cameras and scat surveys. We set 3–5 motion-activated ed voles from a related subspecies exhibit HyperFire PC700 cameras (Reconyx, Holmen, attraction to felids, and 3) determine whether Wisconsin, USA) around perimeters facing pred- naturally infected Amargosa voles have re- ator trails in each marsh (depending on marsh duced survival. size) for 13 mo and checked them monthly. Scat surveys were done along 200–700-m transects at the periphery of marshes monthly for 12 mo. MATERIALS AND METHODS Photographs from cameras were examined for bobcats by a trained researcher. Feces was Study area attributed to bobcats if it was 1–2.537.5–23 cm, We captured rodents in marshes near Tecopa smooth and tubular, and segmented with a twisted Hot Springs (3585202000 N, 11681305700 W) and pattern and had a blunt or slightly pointed end Shoshone (3585802300 N, 11681601600 W), Califor- (Elbroch 2003). If bobcats were observed on nia (Fig. 1). The climate is arid with average camera, bobcat scat was confirmed, or a bobcat summer temperatures of 31.2 C, winter of 10.7 sighting was reported by a resident, that marsh C, and 12.3 cm precipitation annually (NOAA was classed ‘‘bobcat present.’’ 2010). Vegetation is primarily bulrush (Schoeno- Blood was tested for T. gondii antibodies by plectus americanus), salt grass (Distichlis spica- indirect immunofluorescent assays (IFA) (Fritz et ta), rush (Juncus spp.), alkali heath (Frankenia al. 2012). Serum was diluted 1:25 in phosphate- salina), and arrow grass (Triglochin concinna). buffered saline (PBS), placed on slides, and The surrounding desert is harsh alkali playa, with incubated at 37 C for 24 h. After slides were the marshes minimally disturbed except for a hot washed in PBS, fluorescein isothiocyanate–la- spring used by people and dogs for recreation. beled anti-rat immunoglobulin G (Kirkegaard & The marshes are near town and residents’ cats Perry, Gaithersburg, Maryland, USA) diluted 1:25 may occasionally enter. Work with voles was in PBS was applied, and slides were incubated at done under University of California, Davis 37 C for 45 min. Slides were again washed with Institutional Animal Care and Use Committee PBS, stained with eriochrome black, and scanned authorization, with a State of California Scientific by two independent readers for fluorescence of Collection permit, Bureau of Land Management crescent-shaped T. gondii. DNA from brain and letter of authorization, and USFWS 10a.1.a blood was extracted using a Qiagen Blood and permit for take of endangered species. Author- Tissue kit (Qiagen, Valencia, California, USA) and ities also approved work with Owens Valley voles, used for PCR targeting the T.
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