Journal of Wildlife Diseases, 46(2), 2010, pp. 356–367 # Wildlife Disease Association 2010 FLEA ABUNDANCE, DIVERSITY, AND PLAGUE IN GUNNISON’S PRAIRIE DOGS (CYNOMYS GUNNISONI) AND THEIR BURROWS IN MONTANE GRASSLANDS IN NORTHERN NEW MEXICO Megan M. Friggens,1,4,7 Robert R. Parmenter,2 Michael Boyden,3 Paulette L. Ford,4 Kenneth Gage,5 and Paul Keim6 1 School of Forestry, 200 Pine Knoll Drive, Northern Arizona University, Flagstaff, Arizona 86011-5018, USA 2 Valles Caldera National Preserve, PO Box 359, 18161 State Highway 4, Jemez Springs, New Mexico 87025, USA 3 Department of Biology, MSC03 2020, University of New Mexico, Albuquerque, New Mexico 87131-0001, USA 4 USDA Forest Service, Rocky Mountain Research Station, 333 Broadway SE, Suite 115, Albuquerque, New Mexico 87102, USA 5 Bacterial Disease Branch, Division of Vector-Borne Infectious Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, 3150 Rampart Road, Fort Collins, Colorado 80521, USA 6 Department of Biology, PO Box 5640, Northern Arizona University, Flagstaff, Arizona 86011-5640, USA 7 Corresponding author (email: [email protected]) ABSTRACT: Plague, a flea-transmitted infectious disease caused by the bacterium Yersinia pestis, is a primary threat to the persistence of prairie dog populations (Cynomys spp.). We conducted a 3-yr survey (2004–2006) of fleas from Gunnison’s prairie dogs (Cynomys gunnisoni) and their burrows in montane grasslands in Valles Caldera National Preserve in New Mexico. Our objectives were to describe flea communities and identify flea and rodent species important to the maintenance of plague. We live-trapped prairie dogs and conducted burrow sweeps at three colonies in spring and summer of each year. One hundred thirty prairie dogs and 51 golden- mantled ground squirrels (Spermophilus lateralis) were captured over 3,640 trap nights and 320 burrows were swabbed for fleas. Five flea species were identified from prairie dogs and ground squirrels and four were identified from burrow samples. Oropsylla hirsuta was the most abundant species found on prairie dogs and in burrows. Oropsylla idahoensis was most common on ground squirrels. Two colonies experienced plague epizootics in fall 2004. Plague-positive fleas were recovered from burrows (O. hirsuta and Oropsylla tuberculata tuberculata) and a prairie dog (O. hirsuta) in spring 2005 and summer 2006. Three prairie dogs collected in summer 2005 and 2006 had plague antibody. We found a significant surge in flea abundance and prevalence, particularly within burrows, following plague exposure. We noted an increased tendency for flea exchange opportunities in the spring before O. hirsuta reached its peak population. We hypothesize that the role of burrows as a site of flea exchange, particularly between prairie dogs and ground squirrels, may be as important as summer conditions that lead to buildup in O. hirsuta populations for determining plague outbreaks. Key words: Insect vectors, Oropsylla tuberculata cynomuris, reservoir hosts, small mammals. INTRODUCTION and live in large colonies with elaborate burrow systems that favor reproduction Plague is an infectious vector-borne and survival of the flea vector (Cully and disease caused by the bacterium Yersinia Williams, 2001; Gage and Kosoy, 2005). pestis and transmitted between mammals Mortality rates in excess of 95% in by fleas (Biggins and Kosoy, 2001). Since exposed prairie dog colonies (Cully and its introduction to the United States Williams, 2001) affect not only prairie around 1899–1900, sylvatic plague has dogs, but also prairie-dog–dependent spe- become established in native rodent spe- cies including the black-footed ferret cies and contributed to the precipitous (Mustela nigripes) (Houston et al., 1986). decline of endemic prairie dog (Cynomys Prairie dog epizootics can amplify plague spp.) populations (Cully and Williams, by releasing large numbers of infected 2001; Gage and Kosoy, 2005). Prairie dogs fleas into the environment. Predators that are particularly susceptible to plague are attracted to the sick and dead prairie because they have no innate immunity dogs can become infected by consuming 356 FRIGGENS ET AL.—FLEAS, PLAGUE, AND GUNNISON’S PRAIRIE DOGS FROM NEW MEXICO 357 these animals or by being bitten by fleas. et al., 2006), and abundance and preva- Predators can spread potentially infectious lence of flea species is an important fleas to other sites, including previously determinant of Y. pestis transmission unaffected prairie dog colonies, thereby (Lorange, 2005; Eisen et al., 2006). contributing to the local spread of plague We report the results of a 3-yr survey of (Lechleitner et al., 1968). Although we flea populations from Gunnison’s prairie have yet to identify the definitive reservoir dogs and their burrows in montane host and flea vector species important to grassland in New Mexico. We also ana- the maintenance and spread of plague lyzed flea and prairie dog blood samples within the United States, it is clear that for the presence of plague. Our objectives prairie dog fleas are able to perpetuate were to describe the flea communities plague among colony members over the within the Valles Caldera National Pre- course of the epizootic (Webb et al., 2006; serve (VCNP) prairie dog towns, compare Wilder et al., 2008). However, there is animal and burrow flea loads across years little evidence to suggest that these fleas, and seasons in sites with and without or the prairie dogs, can contribute to long- plague, and identify flea species that may term plague maintenance cycles. Research be important to the maintenance or focused on the factors that precede and transmission of plague within this popula- lead to prairie dog plague epizootics are tion. needed to identify other host and flea species that maintain plague in the eco- MATERIALS AND METHODS system and transfer plague to prairie dog colonies. Site descriptions Several rodent species have been pro- The study was conducted at the VCNP, posed as enzootic or maintenance hosts, Sandoval County, New Mexico. Study areas including grasshopper mice (Onychomys were in montane grassland habitat, with elevations of 2,460–2,640 m. Annual precipita- spp.) in black-tailed prairie dog towns tion averages 638 mm, with approximately 45% (Cynomys ludovicianus) and Peromyscus falling during the summer monsoon season spp. in white-tailed (Cynomys leucurus) (July–September). Mean annual temperature is and Gunnison’s prairie dog towns (Cy- 4.5 C, with mean July temperatures of 15 C and 2 nomys gunnisoni) (Gage et al., 1995; mean January temperatures of 5.3 C. Three grassland habitats with prairie dog towns were Thiagarajan et al., 2008). Others have selected for sampling (Fig. 1): Redondo Mead- provided evidence for maintenance cycles ow (35u519330N, 106u369150W), El Cajete that involve soil or flea stages (Lechleitner (35u509180N, 106u339330W), and Valle Grande et al., 1968; Ayyadurai et al., 2008; Eisen (35u519210N, 106u299290W). The Redondo et al., 2008). The most likely long-term Meadow (elevation 2,459 m) vegetation was dominated by Bouteloua gracilis, Potentilla scenario involves several factors and relies hippiana, Erigeron flagellaris, Artemisia car- on a suite of animals, connected by flea ruthii, and Polygonum douglasii. Soils were vectors (Biggins and Kosoy, 2001). In classified as fine, smectic, superactive, frigid, general, flea species are more likely to Vertic Argialboll (Lyquilar series). The El transmit plague if they are highly suscep- Cajete (2,638 m) vegetation was dominated tible to Y. pestis and have low host by Bromus inermis, P. hippiana, Taraxacum officinale, E. flagellaris, and Achillea millefo- specificity (Gage and Kosoy, 2005). How- lium. Soils were ashy, glassy, frigid, Vitrandic ever, low-efficiency vectors may be im- Argiustoll (Jaramillo series). Valle Grande portant to the spread of plague if they are (2,590 m) vegetation was dominated by Festuca common in the environment (Kartman et arizonica, Koelaria macrantha, Poa pratensis, al., 1962; Lechleitner et al., 1968; Eisen et Muhlenbergia montana, P. hippiana, Carex spp., and Antennaria rosea. Soils were loamy al., 2006). Indeed, flea abundance is over ashy-pumiceous, mixed over glassy, super- positively related to the vector potential active, frigid Vitrandic Argisutoll (Vallande for plague for a given flea species (Krasnov series). 358 JOURNAL OF WILDLIFE DISEASES, VOL. 46, NO. 2, APRIL 2010 FIGURE 1. Location of three study sites in Valles Caldera National Preserve, northern New Mexico, USA. Outlines indicate perimeter of colony area that was the focus of trapping efforts and burrow sweeps, May 2004–September 2006. One colony, El Cajete, contained areas where prairie dog burrows were blocked at the time of study (hatched polygons). Colony surveys survey transects (Biggins et al., 1993). Active We live trapped prairie dogs and conducted count is an effective method of population burrow sweeps in spring (May–June) and estimation in both black- and white-tailed summer (August–September) each year. El prairie dogs (Fagerstone and Biggins, 1986; Cajete and Valle Grande were not sampled in Menkens et al., 1990; Severson and Plumb, 2004. Each colony lay in a valley bottom 1998). In 2004, we attempted to quantify (Fig. 1) isolated from other colonies by prairie dogs by counting the number of mountain ranges, which prevented short-term aboveground animals within a 300 3 300-m movement of prairie dogs between sites. bounded area at 15-min intervals over a 3-hr