Tularemia is a bacterial zoonosis caused by Francisella tularensis. We conducted a serosurvey of black-tailed prairie dogs (Cynomys ludovicianus) in Devils Tower National Monument, Wyoming, US, following an epizootic in voles (Microtus spp.) due to F. tularensis. Only 1 of 44 (2%) sampled prairie dogs was seropositive for F. tularensis, providing evidence of survival and potentially limited spread among free-ranging prairie dogs.

Francisella tularensis causes tularemia in many mammalian hosts (Morner and Addison 2001; Feldman 2003). In North America, tularemia causes disease and mortality most often in rodents and lagomorphs (Morner and Addison 2001) and less commonly in humans (Nelson et al. 2013).

During July 2015, Devils Tower National Monument (DETO), Wyoming, park managers observed eight dead voles (Microtus spp.). One fresh vole carcass was examined and tested positive for F. tularensis via PCR through the National Park Service (NPS) Wildlife Health Diagnostic Service (Fort Collin, Colorado). Histopathology of liver, lungs, heart, and spleen showed the widespread presence of bacteria and necrosis consistent with systemic tularemia. Culture and strain typing were conducted at the Bacterial Vector-Borne Disease Branch, Centers for Disease Control and Prevention (CDC, Fort Collins, Colorado, USA), confirming F. tularensis type B.

The DETO has one 16-ha black-tailed prairie dog colony (Cynomys ludovicianus) with an estimated population of 300–500. On 19 July 2015, an adult male prairie dog carcass in good body condition was collected 400 m from the location where vole carcasses were observed. Lung and liver tissues tested positive for tularemia via PCR; confirmatory culture and strain typing at CDC found F. tularensis type B. We conducted a serosurvey and enhanced carcass surveillance to better understand the epizootiology of F. tularensis in this wild black-tailed prairie dog population.

All procedures were reviewed and approved by the NPS Institutional Animal Care and Use Committee (approved 2 October 2015). Traps were distributed near active prairie dog burrows on 6–7 October 2015 and monitored throughout the day. After a prairie dog was captured and anesthetized using isoflurane, venous blood and two oropharyngeal swabs were collected. Age, weight, tarsus length, and Likert-scale ectoparasite burden (composite count of fleas combed and fleas dropping off animal during anesthesia) were also recorded. Total immunoglobulin serology was performed at CDC (Petersen et al. 2004). A titer of ≥1:128 was considered positive.

Blood was taken from 44 of the 45 prairie dogs (12% of estimated colony count) captured, of which 23/45 (51%) were male, and 28/45 (62%) were adults. Median weight was 825 g (range: 459–1,558 g); high flea burden was observed in 38% (17/45). One of 44 sampled prairie dogs (2%) was seropositive for F. tularensis with an antibody titer of 1:256. The seropositive prairie dog was a juvenile male in poor body condition that did not have high flea burden (fewer than 10 fleas observed).

As part of enhanced F. tularensis surveillance, 11 road-killed prairie dog carcasses were collected from July through September 2015, and lung and liver tissues were tested for F. tularensis using PCR, followed by culture on PCR-positive samples. One adult male tested positive for F. tularensis type B via PCR and culture isolation. Necropsy findings included bacterial necrosis of the liver consistent with tularemia. No other carcasses tested positive for F. tularensis, and there were no observed changes to colony population size based on weekly population counts.

Few reports documenting tularemia in prairie dog populations exist (Regina et al. 1986; Petersen et al. 2004). A tularemia outbreak did occur in wild-caught prairie dogs communally housed at a commercial animal facility (Avashia et al. 2004; Petersen et al. 2004). During investigation of that outbreak, F. tularensis was cultured from all seropositive animals. Francisella tularensis was not cultured from wild prairie dogs living where the captive prairie dogs were collected; serology testing was not performed (Avashia et al. 2004). These findings suggested the possibilities that prairie dogs were chronic carriers of F. tularensis, that infection was still immunologically controlled at the time of testing, or that captive cohousing and husbandry practices might perpetuate cannibalism and therefore disease maintenance (Petersen et al. 2004). Prairie dogs are known to cannibalize carcasses in their colonies (Hoogland 1995; Petersen et al. 2004), potentially facilitating disease transmission and resulting in the high rates of positive animals in the captive facility, and accounting for the swollen submandibular lymph nodes reported in the culture-positive animals (Petersen et al. 2004). Apart from these captive outbreaks and despite extensive tularemia testing of prairie dogs during plague investigations, tularemia has rarely been reported in wild populations (Barnes 1993).

Interestingly, two prairie dog carcasses collected at DETO in 2013 were retrospectively tested during our investigation, and one was confirmed to have F. tularensis type B by PCR and culture. No significant change in the prairie dog population had been noted in 2013, and no additional carcasses were found, again suggesting that widespread transmission or mortality in the colony did not occur. Using the cohort-specific life tables of Hoogland (1995), weighted averages of 2-yr survival for age classes 0–3 produced survival estimates of 28% (males) and 42% (females), so about 35% of the prairie dogs present in 2015 would have been present in 2013. With 2 yr of tularemia detections in the DETO prairie dog colony and a tularemia seropositivity of only 2%, it is unlikely that wild prairie dogs are a significant reservoir for F. tularensis.

The route of F. tularensis exposure for the DETO prairie dogs remains unknown. Fleas were the only arthropod identified on captured prairie dogs, and fleaborne F. tularensis transmission is not thought to be a significant disease transmission route (Hopla 1974; Jellison 1974; Eisen and Gage 2012). The lack of widespread transmission in the DETO colony despite a high flea load in 38% of trapped animals suggested that fleaborne transmission of F. tularensis is unlikely. Infected prairie dog carcasses were collected near the site where vole carcasses were observed; it is possible that the dead prairie dogs might have become infected by consuming infected voles or inhaling infectious aerosols from the vole carcasses.

The lack of additional seropositive animals, coupled with the presence of F. tularensis–positive carcasses at the DETO colony, suggested that tularemia in wild prairie dogs might cause high mortality but might have lower transmission potential compared to a captive colony. However, the discovery of an apparently healthy prairie dog with F. tularensis antibodies indicated that at least some prairie dogs can survive infection. Improved understanding of the potential impacts and ecology of tularemia in prairie dog colonies could inform management decisions for high-priority prairie dog colonies.

We thank Superintendent Tim Reid, Devils Tower National Monument staff, and volunteers who assisted with prairie dog capture; NPS Wildlife Health Branch staff who assisted with study design, implementation, and review (Elizabeth Wheeler, Margaret Wild, Tracy Thompson); and CDC staff who assisted with laboratory testing and logistics (Paul Mead, Jennifer Wright, Alexia Harrist). The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the CDC or the NPS.

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