David A. Eads

Using occupancy models to investigate the prevalence of ectoparasitic vectors on hosts: An example with fleas on prairie dogs.

Graphical abstract

Plague bacterium as a transformer species in prairie dogs and the grasslands of western North America.

Invasive transformer species change the character, condition, form, or nature of ecosystems and deserve considerable attention from conservation scientists. We applied the transformer species concept to the plague bacterium Yersinia pestis in western North America, where the pathogen was introduced around 1900. Y. pestis transforms grassland ecosystems by severely depleting the abundance of prairie dogs (Cynomys spp.) and thereby causing declines in native species abundance and diversity, including threatened and endangered species; altering food web connections; altering the import and export of nutrients; causing a loss of ecosystem resilience to encroaching invasive plants; and modifying prairie dog burrows. Y. pestis poses an important challenge to conservation biologists because it causes trophic-level perturbations that affect the stability of ecosystems. Unfortunately, understanding of the effects of Y. pestis on ecosystems is rudimentary, highlighting an acute need for continued research.

Seasonal and among-site variation in the occurrence and abundance of fleas on California ground squirrels (Otospermophilus beecheyi)

ABSTRACT: An improved understanding of the ecology of fleas on California ground squirrels, Otospermophilus beecheyi, is warranted given the role of fleas in the transmission, and perhaps persistence, of the plague-causing bacterium Yersinia pestis. We sampled O. beecheyi on a seasonal basis from three study sites, each representing a different land use type (preserve, pasture, and agriculture) in the San Joaquin Valley, CA. Overall, the abundance of fleas on squirrels was greatest in spring at the preserve site, in summer at the agriculture and pasture sites, and in winter at the pasture site. Hoplopsyllus anomalus, the species most frequently found on squirrels, was most abundant in spring at the preserve site and in summer at the agriculture and pasture sites. Oropsylla montana was most abundant in winter at the pasture site and on adult squirrels. Echidnophaga gallinacea was most abundant in fall on juvenile squirrels at the preserve site. All three flea species we encountered are known to be potential vectors of Y. pestis. Future efforts to predict flea species occurrence and abundance (and plague risk) at sites of concern should consider seasonal microclimatic conditions and the potential influence of human land use practices.

Deltamethrin flea-control preserves genetic variability of black-tailed prairie dogs during a plague outbreak

Genetic variability and structure of nine black-tailed prairie dog (BTPD, Cynomys ludovicianus) colonies were estimated with 15 unlinked microsatellite markers. A plague epizootic occurred between the first and second years of sampling and our study colonies were nearly extirpated with the exception of three colonies in which prairie dog burrows were previously dusted with an insecticide, deltamethrin, used to control fleas (vectors of the causative agent of plague, Yersinia pestis). This situation provided context to compare genetic variability and structure among dusted and non-dusted colonies pre-epizootic, and among the three dusted colonies pre- and post-epizootic. We found no statistical difference in population genetic structures between dusted and non-dusted colonies pre-epizootic. On dusted colonies, gene flow and recent migration rates increased from the first (pre-epizootic) year to the second (post-epizootic) year which suggested dusted colonies were acting as refugia for prairie dogs from surrounding colonies impacted by plague. Indeed, in the dusted colonies, estimated densities of adult prairie dogs (including dispersers), but not juveniles (non-dispersers), increased from the first year to the second year. In addition to preserving BTPDs and many species that depend on them, protecting colonies with deltamethrin or a plague vaccine could be an effective method to preserve genetic variability of prairie dogs.

ABOVEGROUND PREDATION BY AN AMERICAN BADGER (TAXIDEA TAXUS) ON BLACK-TAILED PRAIRIE DOGS (CYNOMYS LUDOVICIANUS)

Abstract During research on black-tailed prairie dogs (Cynomys ludovicianus), we repeatedly observed a female American badger (Taxidea taxus) hunting prairie dogs on a colony in southern Phillips County, Montana. During 1–14 June 2006, we observed 7 aboveground attacks (2 successful) and 3 successful excavations of prairie dogs. The locations and circumstances of aboveground attacks suggested that the badger improved her probability of capturing prairie dogs by planning the aboveground attacks based on perceptions of speeds, angles, distances, and predicted escape responses of prey. Our observations add to previous reports on the complex and varied predatory methods and cognitive capacities of badgers. These observations also underscore the individuality of predators and support the concept that predators are active participants in predator-prey interactions.

Importance of lunar and temporal conditions for spotlight surveys of adult black-footed ferrets

ABSTRACT. Black-footed ferrets (Mustela nigripes) spend most daylight hours underground in prairie dog (Cynomys) burrows and exhibit aboveground movements primarily at night. Moonlight can influence the activity patterns of ferrets and, consequently, might influence the efficiency of spotlight surveys used by biologists to monitor ferret populations. We related detection of adult ferrets during postbreeding spotlight surveys to lunar and temporal conditions. We most frequently located ferrets during surveys in which the moon breached the horizon. The data suggested intersexual differences in response to moonlight. We located male ferrets most frequently during nights with greater moon illumination, but we did not detect a correlation between moon illumination and spotlight detection of female ferrets. In general, moonlight could facilitate aboveground navigation by ferrets. However, it seems activity under bright moonlight could be costly for female ferrets while they raise young. Detection of ferrets also varied among months. We detected female ferrets most frequently in August–September, when mothers increase hunting efforts to acquire prey for growing offspring (kits). Detection of adult female ferrets declined in October, when kits were likely independent of their mother. We located male ferrets most frequently in September–October, when males might increase activity to monitor female ferrets and male competitors. Consideration of lunar and temporal influences and standardization of postbreeding surveys could enhance site-specific assessment of reintroduction success and across-site assessment of species recoveiy progress. We suggest that postbreeding surveys for ferrets should be enhanced by concentrating efforts in August–September during moonlit nights when the moon is above the horizon.

Precipitation, Climate Change, and Parasitism of Prairie Dogs by Fleas that Transmit Plague

Abstract Fleas (Insecta: Siphonaptera) are hematophagous ectoparasites that can reduce the fitness of vertebrate hosts. Laboratory populations of fleas decline under dry conditions, implying that populations of fleas will also decline when precipitation is scarce under natural conditions. If precipitation and hence vegetative production are reduced, however, then herbivorous hosts might suffer declines in body condition and have weakened defenses against fleas, so that fleas will increase in abundance. We tested these competing hypotheses using information from 23 yr of research on 3 species of colonial prairie dogs in the western United States: Gunnisons prairie dog (Cynomys gunnisoni, 1989–1994), Utah prairie dog (Cynomys parvidens, 1996–2005), and white-tailed prairie dog (Cynomys leucurus, 2006–2012). For all 3 species, flea-counts per individual varied inversely with the number of days in the prior growing season with >10 mm of precipitation, an index of the number of precipitation events that might have caused a substantial, prolonged increase in soil moisture and vegetative production. Flea-counts per Utah prairie dog also varied inversely with cumulative precipitation of the prior growing season. Furthermore, flea-counts per Gunnisons and white-tailed prairie dog varied inversely with cumulative precipitation of the just-completed January and February. These results complement research on black-tailed prairie dog (Cynomys ludovicianus) and might have important ramifications for plague, a bacterial disease transmitted by fleas that devastates populations of prairie dogs. In particular, our results might help to explain why, at some colonies, epizootics of plague, which can kill >95% of prairie dogs, are more likely to occur during or shortly after periods of reduced precipitation. Climate change is projected to increase the frequency of droughts in the grasslands of western North America. If so, then climate change might affect the occurrence of plague epizootics among prairie dogs and other mammalian species that associate with them.

Prevalence of the Generalist Flea Pulex simulans on Black-tailed Prairie Dogs (Cynomys ludovicianus) in New Mexico, USA: The Importance of Considering Imperfect Detection

Abstract If a parasite is not detected during a survey, one of two explanations is possible: the parasite was truly absent or it was present but not detected. We fit occupancy models to account for imperfect detection when combing fleas (Siphonaptera) from black-tailed prairie dogs (Cynomys ludovicianus) during June–August 2012 in the Vermejo Park Ranch, New Mexico, USA. With the use of detection histories from combing events during monthly trapping sessions, we fit occupancy models for two flea species: Oropsylla hirusta (a prairie dog specialist) and Pulex simulans (a generalist). Detection probability was <100% for both species and about 21% lower for P. simulans. Pulex simulans may be especially difficult to detect because it is about half the size of O. hirusta. Monthly occupancy (prevalence) for P. simulans was estimated at 24% (June, 95% confidence interval = 19–30), 39% (July, 32–47), and 56% (August, 49–64) in new prairie dog colonies, and 43% (32–54), 61% (49–71), and 79% (70–87) in old colonies. These results suggest P. simulans can attain high prevalence on prairie dogs, especially in old colonies. If P. simulans is highly prevalent on prairie dogs, it may serve as a “bridge vector” between Cynomys and other mammalian hosts of the plague bacterium Yersinia pestis, and even function as a reservoir of Y. pestis between outbreaks.

Patterns of Surface Burrow Plugging in a Colony of Black-Tailed Prairie Dogs Occupied by Black-Footed Ferrets

ABSTRACT. Black-tailed prairie dogs (Cynomys ludovicianus) can surface-plug openings to a burrow occupied by a black-footed ferret (Mustela nigripes). At a coarse scale, surface plugs are more common in colonies of prairie dogs occupied by ferrets than in colonies without ferrets. However, little is known about spatial and temporal patterns of surface plugging in a colony occupied by ferrets. In a 452-ha colony of black-tailed prairie dogs in South Dakota, we sampled burrow openings for surface plugs and related those data to locations of ferrets observed during spotlight surveys. Of 67,574 burrow openings in the colony between June and September 2007, 3.7% were plugged. In a colony-wide grid of 80 m × 80 m cells, the occurrence of surface plugging (≥1 opening plugged) was greater in cells used by ferrets (93.3% of cells) than in cells not observably used by ferrets (70.6%). Rates of surface plugging (percentages of openings plugged) were significantly higher in cells used by ferrets (median = 3.7%) than in cells without known ferret use (median = 3.2%). Also, numbers of ferret locations in cells correlated positively with numbers of mapped surface plugs in the cells. To investigate surface plugging at finer temporal and spatial scales, we compared rates of surface plugging in 20-m-radius circle-plots centered on ferret locations and in random plots 1–4 days after observing a ferret (Jun–Oct 2007 and 2008). Rates of surface plugging were greater in ferret-plots (median = 12.0%) than in random plots (median = 0%). For prairie dogs and their associates, the implications of surface plugging could be numerous. For instance, ferrets must dig to exit or enter plugged burrows (suggesting energetic costs), and surface plugs might influence microclimates in burrows and consequently influence species that cannot excavate soil (e.g., fleas that transmit the plague bacterium Yersinia pestis).

American badgers selectively excavate burrows in areas used by black-footed ferrets: implications for predator avoidance

Abstract We evaluated how American badgers (Taxidea taxus) might exert selective pressure on black-footed ferrets (Mustela nigripes) to develop antipredator defenses. In a colony of black-tailed prairie dogs (Cynomys ludovicianus) in South Dakota, badgers concentrated their activities where burrow openings and prairie dogs were abundant, a selective behavior that was exhibited by ferrets in the same colony. Badgers excavated burrows more often when in areas recently used by a ferret, suggesting that badgers hunt ferrets or steal prey from ferrets, or both. We also conducted an analysis of survival studies for ferrets and Siberian polecats (M. eversmanii) released onto prairie dog colonies. This polecat is the ferrets ecological equivalent but evolved without a digging predator. Badgers accounted for 30.0% of predation on polecats and 5.5% of predation on ferrets. In contrast, both polecats and ferrets have evolutionary experience with canids, providing a plausible explanation for the similar relative impact of coyotes (Canis latrans) on them (65.0% and 67.1% of predation, respectively). We hypothesize that ferrets and badgers coexist because ferrets are superior at exploitation competition and are efficient at avoiding badgers, and badgers are superior at interference competition.