Neospora Caninum Exposure in Overlapping Populations of Coyotes (Canis Latrans) and Feral Swine (Sus Scrofa)
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DOI: 10.7589/2013-02-034 Journal of Wildlife Diseases, 49(4), 2013, pp. 1028–1032 # Wildlife Disease Association 2013 Neospora caninum Exposure in Overlapping Populations of Coyotes (Canis latrans) and Feral Swine (Sus scrofa) Sarah Bevins,1,4 Emily Blizzard,1 Luis Bazan,2 and Pat Whitley31Department of Biomedical Sciences, Colorado State University and USDA/APHIS National Wildlife Research Center, 4101 Laporte Ave., Fort Collins, Colorado 80521, USA; 2USDA/APHIS/Wildlife Services Texas, San Antonio, Texas 78269, USA; 3USDA/APHIS/ Wildlife Services Oklahoma, Durant, Oklahoma 74701, USA; 4Corresponding author (email: Sarah.Bevins@ colostate.edu) ABSTRACT: Limited information exists on are exposed to N. caninum (Dubey and Neospora caninum transmission dynamics in Schares, 2011), but the parasite has been Downloaded from http://meridian.allenpress.com/jwd/article-pdf/49/4/1028/2243275/2013-02-034.pdf by guest on 03 October 2021 wildlife. This coccidian parasite, whose pres- successfully isolated from only a few ence can lead to substantial economic losses in cattle operations, requires a canid definitive species. The primary interest in this host for reproduction. We examined exposure organism stems from it being a primary in a definitive host, coyotes (Canis latrans), and cause of abortion in dairy and beef cattle in overlapping populations of feral swine (Sus (Anderson et al., 1991). Transmission in scrofa) to determine if spatial proximity be- cattle is primarily vertical, with infected tween a definitive and incidental host influenc- es the likelihood of parasite exposure. Eighteen females passing the infection to calves. percent of coyotes (95% confidence interval Epidemic outbreaks have been document- [CI]514.2–21.8) and 15.8% of feral swine ed where .50% of dairy cows in a herd (95% CI512.5–19.2) had been exposed to N. abort within several weeks of each other, caninum, and this is the first report of exposure but recrudescence is unpredictable in in US feral swine populations. Analyses suggest infected adult cows, which generally that the parasite is present throughout the environment and that exposure is not tempo- exhibit no clinical signs. Economic im- rally or spatially linked to antibody-positive pacts associated with N. caninum are coyotes. Antibody-positive feral swine were substantial, with annual losses in individ- found in an area where the only definitive host ual US states approaching tens of millions is domestic dogs (Canis familiaris), indicating of dollars (Trees et al., 1999; Larson et al., that wild canids are not required to maintain the parasite in the environment. 2004). In addition to cattle, N. caninum Key words: Canine, coccidian, feral swine, can cause clinical disease in dogs, sheep, Neospora, surveillance. and goats (Dubey and Schares, 2011). To understand N. caninum presence in the Neospora caninum is a coccidian para- environment better, blood samples from site that produces environmentally resis- coyotes, a definitive host, and feral swine, tant, infective oocysts that are passed an invasive species that is expanding its through the digestive system of definitive range and abundance, were screened for hosts as part of a complex reproductive N. caninum antibodies. cycle. The only definitive hosts for N. A majority of samples were opportunis- caninum identified to date are canids, tically collected in conjunction with work including coyotes (Canis latrans; Gondim conducted by United State Department of et al., 2004), domestic dogs (Canis famil- Agriculture (USDA)/Animal Plant Health iaris; Dubey et al., 1988b), and wolves Inspection Agency (APHIS)/Wildlife Ser- (Canis lupus; Dubey et al., 2011). Neo- vices (WS). Samples were collected from spora caninum was only first recognized as 2009 through 2011, in cooperation with a separate parasite from Toxoplasma state and other federal agencies, from the gondii in 1988 (Dubey et al., 1988a) and southwestern and south central United the list of canid definitive hosts will likely States (Fig. 1). This region was preferen- increase. tially targeted because of overlapping Serologic surveys suggest that a large populations of both species. Sample number of domestic and wild mammals selection was refined by focusing on 1028 SHORT COMMUNICATIONS 1029 Downloaded from http://meridian.allenpress.com/jwd/article-pdf/49/4/1028/2243275/2013-02-034.pdf by guest on 03 October 2021 FIGURE 1. Sample locations for 71 Neospora caninum–positive coyotes and 74 N. caninum–positive feral swine in Oklahoma, New Mexico, and Texas, 2009–2011. counties where coyotes and feral swine with the use of a commercially available had been concurrently sampled. For competitive ELISA for N. caninum (VMRD, coyotes, blood was collected on Nobuto Inc., Pullman, Washington, USA) that has (Advantec MFS, Dublin, California, USA) been extensively used in multiple species, filter paper and stored at 220 C in the including S. scrofa, because of high spec- National Wildlife Disease Program No- ificity and sensitivity, as well as the low buto Sample Archive, at the USDA/ cross-reactivity to closely related parasites APHIS/WS/National Wildlife Research (Haddad et al., 2005; Almerı´a et al., 2007). Center in Fort Collins, Colorado, USA. All samples, positive controls, and negative For feral swine, blood was collected in controls were run in duplicate according to ethylenediaminetetraacetic acid or serum manufacturer’s instructions. For both as- separating tubes, processed according to says, the optical density sample-to-control protocol (Pedersen, 2012), and stored at ratio positive cutoff was $0.30. 280 C in the Feral Swine Serum Archive Data were mapped using ArcMap, v.10 at the NWDP. (ESRI, Redlands, California, USA). Mean Blood samples collected from coyotes antibody prevalence and 95% confidence on filter paper were eluted with phos- limits were determined with the use of a phate-buffered saline with the use of binomial distribution for prevalence in previously reported protocols, resulting both species. Separate logistic regression in a 1:10 sample dilution (Dusek et al., analyses were also run (SAS, v.9.2, Cary, 2011). Samples were screened with the use North Carolina, USA) for each species in of a commercially available N. caninum order to determine pathogen associated enzyme-linked immunosorbent assay risk in relation to animal sex, age (adult, (ELISA, BiovetH, Saint-Hyacinthe, Quebec, subadult), and their interaction. Both Canada), validated for use in multiple canine variables are known to impact parasite species, including coyotes (Wapenaar et al., exposure risk (Wouda et al., 1999). In 2007), at the manufacturer’s suggested 1:10 addition, we ran a bivariate K-function sample dilution. Feral swine sera were tested analysis in program R with the use of 1030 JOURNAL OF WILDLIFE DISEASES, VOL. 49, NO. 4, OCTOBER 2013 TABLE 1. Mean Neospora caninum antibody prevalence and 95% confidence intervals (CI) in coyotes and feral swine from the southwest and south central United States, 2009–2011. Species Variable Category Prevalence (%)95% CI Coyote (Canis latrans) Age Adult 17.4 13.30–21.43 Subadult 22 11.13–33.31 Sex Female 18.7 13.23–24.27 Male 17.4 11.98–22.76 Feral swine (Sus scrofa) Age Adult 19.3 14.81–23.72 Subadult 9.6 5.15–14.13 Sex Female 19.3 14.4–24.14 Male 11.7 7.40–16.06 Downloaded from http://meridian.allenpress.com/jwd/article-pdf/49/4/1028/2243275/2013-02-034.pdf by guest on 03 October 2021 spatstat (Baddeley and Turner, 2005) to CI51.001–2.865) and adults were more determine the degree of clustering be- likely to be infected than younger animals tween positive definitive hosts and positive (x256.25, P50.01; OR52.1, 95% CI5 swine. 1.17–3.85). Results from the bivariate-K Samples from 394 coyotes and 467 feral spatial analyses revealed that positive feral swinewerescreenedforN. caninum swine did not tend to cluster with positive antibodies (Table 1). In total, 334 of the coyotes. coyotes sampled were adults and 54 were We examined N. caninum exposure in a subadults. Feral swine samples consisted definitive host, coyotes, and in overlapping of 301 adults and 166 subadults. Sampling populations of feral swine. The absence of of males and females was roughly equal, differences in N. caninum antibody preva- with 192 female and 190 male coyotes lence between coyote age classes or sexes sampled, and 254 female and 213 male suggests that exposure to the parasite is feral swine sampled. Both species showed ubiquitous. As a definitive host (Gondim exposure to N. caninum across Oklahoma, et al., 2004), coyotes are likely exposed New Mexico, and Texas (Fig. 1). Overall, through multiple routes of infection, in- 18% of coyotes (95% CI514.2–21.8) and cluding environmental contamination and 15.8% of feral swine (95% CI 5 12.5– ingestion of infected prey. This is supported 19.2) had been exposed to the parasite by our finding of exposure in both adult (Table 1). The mean inhibition for positive animals and younger animals, with the latter feral swine was 41.8% (SD514.0); the possibly being exposed in denning sites. mean optical density sample ratio for Conversely, feral swine showed signifi- positive coyotes 44.6 (SD516.9). Positive cant differences in antibody prevalence in control means were 56.4 (SD57.6) and relation to both age and sex. The higher 1.0 (SD50.0), respectively, for feral swine prevalence in adult animals may be and coyotes. indicative of an increased chance for Logistic regression revealed different exposure over time through rooting be- parasite exposure patterns for the two haviors. It is also possible that adult species. For coyotes, neither sex, age, nor animals are more likely to eat an interme- their interaction were significant predic- diate host (Barrett, 1978). A higher N. tors of N. caninum exposure; however, age caninum antibody prevalence in female (F56.26, P50.01) and sex (F53.8, feral swine may reflect different behaviors P50.04) were significant in feral swine.