Ecology and Management of Plague in Diverse Communities of Rodents and Fleas

Abstract

Plague originated in Asia as a flea-borne zoonosis of mammalian hosts. Today, the disease is distributed nearly worldwide. In western United States of America, plague is maintained, transmitted, and amplified in diverse communities of rodents and fleas. We examined flea diversity on three species of prairie dogs (Cynomys spp., PDs) and six species of sympatric small rodents in Montana and Utah, United States of America. Among 2896 fleas, 19 species were identified; 13 were found on PDs and 9 were found on small rodents. In Montana, three flea species were found on PDs; the three species parasitize PDs and mice. In Utah, 12 flea species were found on PDs; the 12 species parasitize PDs, mice, voles, chipmunks, ground squirrels, rock squirrels, and marmots. Diverse flea communities and their willingness to parasitize many types of hosts, across multiple seasons and habitats, may favor plague maintenance and transmission. Flea parasitism on Peromyscus deer mice varied directly with elevation. Fleas are prone to desiccation, and might prosper at higher, mesic elevations; in addition, Peromyscus nest characteristics may vary with elevation. Effective management of plague is critical. Plague management is probably most effective when encompassing communities of rodents and fleas. Treatment of PD burrows with 0.05% deltamethrin dust, which suppressed fleas on PDs for >365 days, suppressed fleas on small rodents for at least 58 days. At one site, deltamethrin suppressed fleas on small rodents for at least 383 days. By simultaneously suppressing fleas on PDs and small rodents, deltamethrin should promote ecosystem resilience and One Health objectives.

Introduction

Fleas (Siphonaptera) are wingless, hematophagous insect parasites of vertebrates. Fleas exhibit a wide variety of life histories and host associations. Adults of some flea species specialize on a small number of hosts, whereas others feed on a wide range of hosts (generalists). Humans tend to perceive fleas as “bothersome, scabrous, tiny, and parasitical” (Lehane 1969, p. 11). Nevertheless, fleas receive considerable attention, mostly because they transmit a variety of disease-causing pathogens (Krasnov 2008).

Arguably, the best-known flea-borne agent is Yersinia pestis, a zoonotic bacterium renowned for killing millions of humans during the Black Death in Europe (Keim and Wagner 2009). In Asia, where Y. pestis originated, plague's historic effects on humans were no less profound (Achtman et al. 1999). Today, plague causes significant human mortality in Africa, Madagascar, and South America, with occasional cases in Asia and North America (D'Ortenzio et al. 2018). The disease has been classified among the zoonoses of top priority interest from a One Health perspective (https://cdc.gov/onehealth/pdfs/us-ohzdp-report-508.pdf).

The Centers for Disease Control and Prevention classifies plague as an Emerging Infectious Disease because (1) plague is spreading to new areas, (2) plague is being found in areas undergoing ecological change, and (3) plague is reemerging because of limitations with intervention measures. Scientists seek to acquire a deeper understanding of plague and to identify ways in which to manage the disease. In particular, it is important to study sylvatic plague among wild rodents and fleas; Y. pestis is maintained, transmitted, and amplified in rodent and flea communities, spilling over to humans and other mammals when conditions allow (Kalabukhov 1965, Gage and Kosoy 2006, Zeppelini et al. 2016).

Each plague focus (sensu Antolin et al. 2010) is characterized by unique communities of rodents and fleas. Within a focus, some rodent species are better than others at maintaining and amplifying Y. pestis and some flea species are better than others at transmission or maintenance (Gage and Kosoy 2006, Eisen et al. 2009, Wimsatt and Biggins 2009). Moreover, the roles of hosts and fleas, for instance in plague maintenance or amplification, change with space and time (Barnes 1982, Biggins and Kosoy 2001, Kosoy et al. 2017). Thus, generalizations are problematic.

Where humans have introduced plague, the disease is particularly destructive and disruptive, justifying appropriate countermeasures (Smith and Johnson 1985, Antolin et al. 2002, Eads and Biggins 2015). Y. pestis thus joins the lengthening list of anthropogenic invaders that require active intervention to reduce health risks for humans and other highly susceptible mammals. Given the uncertainties noted above, plague management in a selected area is probably most efficient when encompassing rodent and flea communities.

Plague transmission can be suppressed or, perhaps, entirely eliminated locally with the use of insecticides for flea control. In areas of active intervention, insecticides are presumably indiscriminate in killing specialist and generalist fleas. If distributed in an appropriate manner, insecticides might protect mammal communities, with implications for human and wildlife health. Insecticide treatments are particularly useful in habitats occupied by susceptible, imperiled host species (Biggins et al. 2010, Matchett et al. 2010) and habitats with diverse flea communities and high flea densities, as appears to be the case at high elevations in some, but not all plague foci or flea-host systems (Eisen et al. 2012, Goldberg et al. 2020).

In this study, we assess the use of deltamethrin, a pyrethroid insecticide, as a tool for suppressing fleas among rodents in western United States of America. Efficacy of deltamethrin with prairie dogs (Cynomys spp., PDs), a component of the communities examined herein, has been evaluated elsewhere (e.g., Seery et al. 2003, Biggins et al. 2010, Eads and Biggins 2019). We address the following questions:

Is deltamethrin dust an effective agent of flea control on small rodents when infused into PD burrows? In South Dakota, Maestas and Britten (2019) treated black-tailed PD (BTPD, Cynomys ludovicianus) burrows with deltamethrin dust; flea loads on small rodents were reduced by up to 49%. We studied small rodents on colonies of three PD species in Montana and Utah.

What are the diversity and host associations of fleas on PDs and associated small rodents, with an emphasis on which flea species are generalists with a cosmopolitan taste for hosts, suggesting they might bridge vector plague in mammal communities?

How much does flea parasitism vary, in absolute number and diversity, among small rodents living sympatrically on PD colonies?

Is elevation an important predictor of flea parasitism on deer mice (Peromyscus maniculatus) occupying PD colonies along an elevation gradient? Moisture tends to increase, and temperatures tend to decrease with elevation, which might benefit ectothermic, desiccation-prone fleas (Krasnov 2008). Thus, we expected to find a positive correlation.

Materials and Methods

Experimental design and sampling fleas

Procedures used in this study were approved by the Institutional Animal Care and Use Committee at the Fort Collins Science Center, U.S. Geological Survey (Biggins et al. 2010). Data were collected on 12 colonies of three PD species at five sites in Montana and Utah, 2001–2004 (Table 1). PD species included BTPDs, Utah PDs (C. parvidens, UPDs), and white-tailed PDs (C. leucurus, WTPDs). Sample sizes from six small rodents were sufficient for analysis: deer mice, grasshopper mice (Onychomys leucogaster), Ord's kangaroo rats (Dipodomys ordii), hispid pocket mice (Chaetodipus hispidus), dark kangaroo mice (Microdipodops megacephalus), and sagebrush voles (Lemmiscus curtatus). The following species were also captured, but at rates insufficient for inclusion in the study: brush mice (Peromyscus boylii), pinyon mice (Peromyscus truei), bushy-tailed woodrats (Neotoma cinerea), least chipmunks (Neotamias minimus), Richardson's ground squirrels (Spermophilus richardsoni), meadow voles (Microtus pennsylvanicus), and rabbits (Sylvilagus spp.).

Table 1.

Study Designs with Small Rodents Occupying Colonies of Black-Tailed Prairie Dogs, Utah Prairie Dogs, and White-Tailed Prairie Dogs at Five Sites, Ten Experimental Pairs, and Eleven Colonies, Montana and Utah, United States of America

PD	State	Site	Pair	Design	Small rodents in flea analyses
PD	State	Site	Pair	Design	Deer mouse	Pocket mouse	Grasshopper mouse	Kangaroo mouse	Kangaroo rat	Sagebrush vole
BTPD	Montana	Phillips County	Colony 22	Split			
			Colonies 185, 186	Separate			
UPD	Utah	Awapa Plateau	Tanks	Split						
			Big Lake	Split						
		Paunsaugunt	Johnson Bench	Split						
			Tom Best Spring	Split						
		West Desert	Horse Hollow	Split					
			Minersville #3	Split					
WTPD	Utah	Coyote Basin	Kennedy Wash	Separate					
			Rail	Split					

Experimental pairs included dusted plots in which burrows were infused with DeltaDust to suppress fleas and paired, nondusted plots (see text). We studied the effect of DeltaDust on fleas parasitizing small rodents listed in this study. Dusted plots on four pairs had been treated with DeltaDust for 3 years before our study (Minersville #3, Tanks, Kennedy Wash, and Rail), and one pair had been previously treated for 2 years (Horse Hollow).

PD, prairie dog; BTPD, black-tailed prairie dogs UPD, Utah prairie dogs; WTPD, white-tailed prairie dog.

Efficacy of deltamethrin was assessed by combing fleas from rodents on paired dusted and nondusted plots in split colonies or “separate” adjacent colonies (Table 1). Paired dusted and nondusted plots had similar physiographic and biotic attributes (e.g., slope, aspect, burrow density, quantity and type of vegetative cover, and initial PD density; Biggins et al. 2010). On the dusted plots, each PD burrow was infused with DeltaDust^® at a targeted rate of 4 g/opening (0.05% deltamethrin; Bayer Environmental Science, NC) (Biggins et al. 2010, Eads and Biggins 2019). We treated PD burrows because sympatric small rodents may commonly enter or nest in PD burrows, and PD burrow openings are often conspicuous and easy to locate.

Sampling of fleas occurred simultaneously on paired plots, thereby controlling for flea phenology when comparing flea parasitism on dusted and nondusted plots. Sampling occurred from 52 to 120 days before dusting, and from 13 to 383 days after dusting (as described below in the section on “Data analyses”).

Small rodents and PDs were live-trapped using Sherman traps (Tallahassee, FL) and Tomahawk traps (Hazelhurst, WI). Each rodent was anesthetized with isoflurane and combed for 30 s to remove fleas (Eads and Biggins 2019). Fleas from 2002 and 2003 were identified to species using dissecting microscopes and dichotomous keys.^*

Data analyses

During sampling of small rodents, >1 flea was found in only 5% of cases. No fleas were found in 88% of cases. Thus, we concentrated on indices of flea prevalence, defined as detection or nondetection of at least one flea.

Three analyses were completed to assess the effect of DeltaDust on flea prevalence. In each assessment, we analyzed data using the GLIMMIX procedure in SAS^® 9.3 (SAS Institute, Inc.) with a log-link function and maximum likelihood estimation. Parsimonious models were selected through Type III chi-squared tests and backward elimination (α = 0.050).

First, we analyzed flea data from before-after-control-impact (BACI) experiments to evaluate the efficacy of DeltaDust, with sampling taking place 120–52 days before dusting and resuming 13–47 days after dusting. Using data from deer mice and kangaroo rats (Table 1), we evaluated a model with variables for presence or absence of DeltaDust (DUST), experiment period (BEFORE–AFTER dusting), and DUST × BEFORE–AFTER interaction. The interaction helped to determine if the effect of DUST on fleas was disproportionately stronger AFTER burrow infusions. We included a random effect for experimental PAIR, thereby linking data within pairs. A variable for rodent species was unsupported and, therefore, excluded for parsimony. Notably, four pairs had been previously treated with DeltaDust for 3 years (Minersville #3, Tanks, Kennedy Wash, and Rail) and one pair had been previously treated for 2 years (Horse Hollow), allowing for potential cumulative effects of DUST in the BACI experiments.

Second, using data from designed experiments lacking pretreatment data, we assessed the efficacy of DeltaDust 10–58 days after application with deer mice and grasshopper mice (Table 1). We evaluated a model with a fixed effect for DUST and a random effect for PAIR. An unsupported variable for rodent species was excluded.

Third, we used data from deer mice, pocket mice, and sagebrush voles to assess the long-term efficacy of DeltaDust, with sampling taking place 287–383 days after dusting (Table 1). We evaluated a model with a fixed effect for DUST and a random effect for PAIR. An unsupported variable for species was excluded.

We examined differences in flea parasitism among rodent species using all possible data from nondusted plots (to remove an effect of DeltaDust and increase statistical power for this objective). We compared flea prevalence among the rodent SPECIES, while controlling for COLONY site, and MONTH and YEAR, thereby standardizing the ecological context of each comparison in space and time.

The six species of small rodents differ in mass and therefore size. Although some overlap occurs, masses range from about 11 to 16 g for dark kangaroo mice to 44–72 g for Ord's kangaroo rats (Reid 2006). We hoped to determine if any SPECIES differences in the prior analysis could be attributed to host body size; larger rodents, with more surface area, provide more habitat for fleas, and the lethal dose₅₀ of Y. pestis for susceptible rodent species might be lower for smaller species. In 76% of observations from the analysis above, spring scales were used to weigh small rodents to the nearest 0.5 g. With the reduced dataset, we evaluated SPECIES differences, while controlling for BODYSIZE, which was indexed as mass^−0.67 (Hawlena et al. 2005). Rodent age was unsupported and excluded.

To address our final study question on elevation and flea parasitism, we used data from deer mice on six UPD colonies ranging from 1585 to 2972 meter elevation, limiting the data to nondusted plots. We ran a model with fixed effects for ELEVATION and control variables for MONTH and YEAR.

Results

Among 2896 fleas collected in 2002 and 2003, 19 flea species were detected; 13 flea species were found on PDs and 9 were found on small rodents (Supplementary Data). Three species were found on both PDs and small rodents: Aetheca wagneri (common on deer mice and certain other Peromyscus spp.), Oropsylla hirsuta (a PD specialist), and Pulex spp. (generalists).

On BTPD colonies in Montana, small rodents carried six flea species, including A. wagneri, Epitidea wemmani (common on deer mice and mouse-like rodents), Stenoponia americana (generalist), Foxella ignota (common on gophers and some other rodents), and Orchopeas sexdentatus (common on wood rats and mice). On UPDs in Utah, communities of fleas were depauperate along moderate to high elevations at Paunsaugunt (O. hirsuta and Thrassis francisi) and low elevations at West Desert (O. hirsuta and T. bacchi). In contrast, seven flea species were found on UPDs at higher elevations along the Awapa Plateau (described in the next paragraph). T francisi (a ground squirrel flea) was commonly found on UPDs at Awapa and, to a lesser extent, Paunsaugunt, but was not found at West Desert, where T. bacchi was found. T. bacchi is commonly found on sagebrush voles, and on ground squirrels and some lagomorphs. WTPDs in Utah commonly carried Pulex spp., and the PD specialists O. hirsuta and O. tuberculata cynomuris. In 2002, three Cediopsylla inaequalis (a rabbit flea) were collected from WTPDs. Pulex spp. were found on kangaroo rats at WTPD colonies.

At the Awapa paired experimental sites, two PD specialist fleas were detected on UPDs, O. hirsuta and O. tuberculata cynomuris. O. tuberculata tuberculata (a flea of Otospermophilus squirrels) was more common on UPDs than PD specialist fleas. UPDs at Awapa also carried the deer mouse flea A. wagneri. Additional species included Eumolpianus eumolpi (a flea of Neotamias chipmunks), Hystrichopsylla dippei (a flea of mice and voles), O. labis (a flea of PDs, rock and ground squirrels), Rhadinopsylla fraternal (a generalist), T. acamantis (a flea of Marmota marmots), and T. francisi. Deer mice at Awapa carried A. wagneri, and harbored Catallagia decipiens (a fairly common flea of Peromyscus) and Malaraeus telchinus (a flea of mice, jumping mice, and voles).

Although not collected on the study plots considered herein, the research team collected one Hoplopsyllus anomalus (a ground squirrel flea) from a UPD at West Desert, one Meringis parkeri (a generalist of rodents most frequently found on kangaroo rats) from a WTPD, and seven Cediopsylla inaequalis from two rabbits on WTPD colonies.

During the BACI experiments, there was little evidence for cumulative effects of dusting over 2–4 consecutive years of treatment (compare flea prevalence for nondusted and dusted pairings in the BEFORE columns of Table 2). Fleas were commonly collected BEFORE treatments, and were commonly collected on the nondusted plots, but few to no fleas were collected on the dusted plots 13–47 days AFTER treatments (Table 2, DUST × BEFORE–AFTER: χ ² = 11.33, p = 0.001).

Table 2.

Results from Before–After-Control-Impact Experiments Evaluating the Effect of DeltaDust on Fleas Parasitizing Deer Mice and Kangaroo Rats at Paired Dusted and Nondusted Plots on Colonies of Utah Prairie Dogs and White-Tailed Prairie Dogs

Small rodent	Sympatric PD	Pair	Year	Nondusted before		Dusted before		Nondusted after		Dusted after
Small rodent	Sympatric PD	Pair	Year	n	Flea prevalence	n	Flea prevalence	n	Flea prevalence	n	Flea prevalence
Deer mouse	UPD	Minersville #3	2004	13	0.00	23	0.05	11	0.09	18	0.00
Deer mouse	UPD	Tanks	2004	53	0.11	42	0.21	20	0.35	52	0.00
Deer mouse	WTPD	Kennedy Wash	2004	8	0.25	9	0.00	18	0.00	14	0.00
Deer mouse	WTPD	Rail	2004	9	0.00	8	0.00	7	0.14	8	0.00
Kangaroo rat	UPD	Horse Hollow	2004	5	0.00	11	0.00	15	0.33	25	0.04

Fleas were combed from live-trapped rodents before burrows on the dusted plots were infused with DeltaDust and 13–47 days after infusions. Dusted plots on the first four pairs had been treated with DeltaDust for 3 years before our study. The dusted plot on the final pair had been previously treated for 2 years.

Regarding residual efficacy of DeltaDust for experiments lacking pretreatment data, fleas were less prevalent on dusted plots compared to their nondusted counterparts 10–58 days after dusting (Table 3, DUST: χ ² = 10.31, p = 0.001). Moreover, fleas were less prevalent on dusted plots 10–13 months after dusting (Table 4, DUST: χ ² = 13.17, p < 0.001); thus, although there was little evidence for cumulative effects over multiple years of dusting in the BACI experiments (noted above), there was evidence of effects lasting 10–13 months in this assessment (with larger sample sizes; Table 4), which suggests a single DeltaDust application can limit flea-borne spread of Y. pestis.

Table 3.

Results from Experiments Evaluating the Short-Term Effect of DeltaDust on Fleas Parasitizing Deer Mice, Grasshopper Mice, and Kangaroo Rats at Paired Dusted and Nondusted Plots on Colonies of Black-Tailed Prairie Dogs and Utah Prairie Dogs

Small rodent	Sympatric PD	Pair	Year	Days afterinfusions	Nondusted		Dusted
Small rodent	Sympatric PD	Pair	Year	Days afterinfusions	n	Flea prevalence	n	Flea prevalence
Deer mouse	BTPD	Colonies 185,186	2003	46–58	29	0.14	29	0.00
Deer mouse	BTPD	Colony 22	2003	46–58	24	0.17	40	0.08
Deer mouse	UPD	Tanks	2002	24–27	29	0.66	28	0.57
Deer mouse	UPD	Tom Best Spring	2001	10–13	19	0.21	13	0.00
Grasshopper mouse	BTPD	Colony 22	2003	56–58	13	0.46	5	0.00
Kangaroo rat	UPD	Minersville #3	2004	56–58	19	0.26	10	0.00

Fleas were combed from live-trapped rodents 10–58 days after BTPD and UPD burrows on the dusted plots were infused with DeltaDust. Dusted plots on two pairs had been treated with DeltaDust for 3 years before our study (Minersville #3 and Tanks).

Table 4.

Results from Experiments Evaluating the Long-Term Effect of DeltaDust on Fleas Parasitizing Deer Mice, Pocket Mice, and Sagebrush Voles at Paired Dusted and Nondusted Plots on Colonies of Utah Prairie Dogs

Small rodent	Sympatric PD	Pair	Year	Days after infusions	Nondusted		Dusted
Small rodent	Sympatric PD	Pair	Year	Days after infusions	n	Flea prevalence	n	Flea prevalence
Deer mouse	UPD	Tom Best Spring	2002	287–383	62	0.34	72	0.11
Deer mouse	UPD	Tom Best Spring	2004	287–383	28	0.18	43	0.07
Pocket mouse	UPD	Tom Best Spring	2002	287–383	33	0.15	14	0.07
Pocket mouse	UPD	Tom Best Spring	2004	287–383	21	0.05	20	0.00
Sagebrush vole	UPD	Tanks	2004	296–369	8	0.38	9	0.11

Fleas were combed from live-trapped rodents 287–383 days after UPD burrows on the dusted plots were infused with DeltaDust. The dusted plot at Tanks had been treated with DeltaDust for 3 years before our study.

In the comparison of flea prevalence on the six species of small rodents, three variables were supported: SPECIES (χ ² = 29.26, p < 0.001), MONTH (χ ² = 20.33, p < 0.001), and COLONY (χ ² = 28.19, p < 0.001). YEAR was retained as a temporal control (χ ² = 1.99, p = 0.159). Fleas tended to be most prevalent on sagebrush voles, followed by grasshopper mice, kangaroo rats, deer mice, pocket mice, and kangaroo mice (Table 5). The order remained the same and SPECIES was still supported (χ ² = 16.84, p = 0.005) when accounting for BODYSIZE (χ ² = 1.74, p = 0.187).

Table 5.

Flea Prevalence on Deer Mice, Grasshopper Mice, Kangaroo Mice, Kangaroo Rats, Pocket Mice, and Sagebrush Voles Occupying Colonies of Black-Tailed Prairie Dogs, Utah Prairie Dogs, and White-Tailed Prairie Dogs

Sympatric PD	Site	Colony	Year	Small rodent	n	Flea prevalence
BTPD	Phillips County	22	2003	Deer mouse	24	0.17
				Grasshopper mouse	13	0.46
		186	2003	Deer mouse	29	0.14
				Grasshopper mouse	11	0.09
UPD	Awapa Plateau	Tanks	2002	Deer mouse	29	0.66
				Pocket mouse	8	0.00
			2004	Deer mouse	73	0.18
				Pocket mouse	8	0.00
				Sagebrush vole	8	0.38
	Paunsaugunt	Johnson Bench	2002	Deer mouse	51	0.16
				Pocket mouse	4	0.00
			2004	Deer mouse	23	0.13
				Pocket mouse	24	0.04
				Sagebrush vole	22	0.32
		Tom Best Spring	2001	Deer mouse	19	0.21
				Pocket mouse	2	0.50
			2002	Deer mouse	62	0.34
				Pocket mouse	33	0.15
			2004	Deer mouse	28	0.18
				Pocket mouse	21	0.05
	West Desert	Horse Hollow	2004	Deer mouse	5	0.00
				Grasshopper mouse	3	0.67
				Kangaroo mouse	20	0.00
				Kangaroo rat	20	0.25
				Pocket mouse	6	0.00
		Minersville #3	2002	Deer mouse	5	0.00
				Pocket mouse	22	0.00
				Kangaroo rat	6	0.00
			2004	Deer mouse	24	0.04
				Pocket mouse	8	0.13
				Kangaroo rat	23	0.22
WTPD	Coyote Desert	Rail	2004	Deer mouse	16	0.06
				Kangaroo rat	6	0.33

Fleas were combed from live-trapped rodents. Data are limited to colonies and plots that were not treated with DeltaDust.

In the assessment of flea prevalence on deer mice from 1585 to 2972 meter elevation, ELEVATION was important (χ ² = 17.27, p < 0.001). MONTH and YEAR were retained as temporal controls (respectively, χ ² = 6.92, p = 0.140 and χ ² = 2.60, p = 0.273). Flea prevalence correlated positively with elevation (Table 6).

Table 6.

Flea Prevalence on Deer Mice Occupying Colonies of Utah Prairie Dogs Along an Elevation Gradient in Utah, United States of America

UPD colony	Elevation (meters)	n	Flea prevalence
Horse Hollow	1585	6	0.17
Minersville #3	1981	29	0.03
Tom Best Spring	2347	109	0.28
Johnson Bench	2408	74	0.15
Tanks	2697	102	0.31
Big Lake	2972	20	0.50

Fleas were combed from live-trapped mice. Data are limited to colonies and plots that were not treated with DeltaDust. Flea prevalence increased with elevation in a multivariate model that accounted for monthly and yearly variation in flea prevalence.

Discussion

Our results are consistent with a suppressing effect of DeltaDust on fleas parasitizing small rodents occupying PD colonies. By simultaneously suppressing fleas on PDs (Biggins et al. 2010, Eads and Biggins 2019) and small rodents (Maestas and Britten 2019, results herein), DeltaDust may dampen the spread of plague in mammal and flea communities (Matchett et al. 2010). In comparison, management tools targeting PDs only, or tools that are ineffective in rodent and flea communities, are predicted to be less useful (Bron et al. 2018).

Our results and those of Thiagarajan et al. (2008) suggest sagebrush voles, on and near PD colonies, are prone to flea parasitism. Continued study is needed to identify the mechanisms underlying this trend. Some investigators suggest sagebrush voles are colonial, which may increase their susceptibility to fleas (although other investigators suggest sagebrush voles live singly or in pairs; Mullican and Keller 1987). Perhaps nest characteristics for sagebrush voles are of high quality for fleas, or sagebrush voles explore PD burrows, which sometimes contain very large numbers of fleas (Eads 2017, Biggins and Eads 2019).

Research is also needed to evaluate the roles of sagebrush voles in plague ecology. Sagebrush voles have been considered reservoirs of plague in Washington state (James and Booth 1952, Nelson 1980). T. bacchi, most commonly found on sagebrush voles in our study areas in Montana, is capable of transmitting Y. pestis (Eisen et al. 2009). In areas where T. bacchi is found on sagebrush voles and PDs (e.g., BTPD colonies in Montana), T. bacchi might function as a bridge vector.

Plague might indirectly affect the suitability of PD colonies as habitat for sagebrush voles. PDs clip and kill sagebrush to create open viewsheds for predator detection (Whicker and Detling 1988, Biggins, personal observations). Plague suppresses PD populations, reducing their ability to kill sagebrush (Eads and Biggins 2015) and potentially providing voles with increased access to PD burrows. Such an outcome may provide sagebrush voles with improved habitat, allowing them to increase in abundance and perpetuate plague maintenance. This scenario exemplifies a feedback cycle that would diminish opportunities for PDs to maintain open viewsheds over the long term, perhaps increasing their risk of predation (resulting in additive mortality when combined with plague; Biggins and Eads 2019).

Flea prevalence was second highest on grasshopper mice. Grasshopper mice are parasitized by O. hirsuta that also feed on PDs (Franklin et al. 2010). Grasshopper mice occupy home ranges overlapping multiple PD families (Kraft and Stapp 2013), and, in theory, their space use provides them with opportunities to spread infectious O. hirsuta between PD territories (Salkeld et al. 2010). Moreover, grasshopper mice feed on live and dead rodents (providing another route of exposure) and harbor a large diversity of flea species (e.g., 57 species in Thomas 1988).

In our study, WTPDs and kangaroo rats harbored Pulex fleas, which parasitize many types of mammals (Hopla 1980) and are hypothesized to function as bridge vectors of Y. pestis (Brinkerhoff 2008, Eads et al. 2015). Kangaroo rats may play an important role in these dynamics; some of them develop high bacteremias and survive plague infections (Holdenried and Quan 1956), and susceptible individuals within a given kangaroo rat population may continue to provide infectious bloodmeals to fleas, which prolongs plague transmission (Eisen et al. 2007, Graham et al. 2014).

At Awapa Plateau, field crews found the flea O. tuberculata tuberculata, a generalist subspecies closely related to O. tuberculata cynomuris, a PD specialist. Interestingly, O. tuberculata tuberculata was more common on UPDs than O. tuberculata cynomuris. Ground and rock squirrels sometimes enter, and might nest in, UPD burrows at Awapa (Eads personal observations). Use of the same burrow systems and exchanges of fleas among UPDs, ground squirrels, and rock squirrels might allow these rodents and O. tuberculata tuberculata to maintain and, in some cases, amplify Y. pestis at Awapa Plateau.

T. acamantis, a flea of marmots, comprised 85% of fleas collected from UPDs on one of the Awapa colonies in 2002 and 2003. Marmots are heavily involved in plague cycles in central Asia, perhaps in polyhostal systems with ground squirrels, voles, and Ochotona pikas (Kalabukhov 1965). Unfortunately, the importance of plague in marmots in the western United States of America has been little studied, but the possibility exists that T. acamantis in high elevation sites may assist in cycling Y. pestis among marmots, PDs, other rodents, and additional hosts, including American pikas (O. princeps), the latter of which are known to carry T. acamantis (Foley et al. 2017) and have declined considerably in abundance, perhaps due to plague (Wilkening et al. 2011).

A. wagneri was found on deer mice and BTPDs in Montana, and on small rodents and UPDs in Utah. A. wagneri is most commonly found on deer mice which, as resource generalists, occupy much of western United States of America. The broad distribution of deer mice may bring A. wagneri into contact with many types of rodents, helping to explain why A. wagneri can be found on many rodent species. Like the fleas discussed above, A. wagneri, which has been found naturally infected with Y. pestis and proven to transmit plague bacteria under laboratory conditions (Eisen et al. 2008), might function as a bridge vector of Y. pestis.

The preceding comments on bridge vectoring might seem inconsequential when considering the inefficiency at which fleas transmit Y. pestis (Lorange et al. 2005). One might ask, for example, how could A. wagneri bridge vector Y. pestis between deer mice and PDs (or vice versa) when A. wagneri is a relatively poor vector under laboratory conditions (Eisen et al. 2008) and <1% of the fleas from PDs were A. wagneri in our study. Although Y. pestis-infected A. wagneri has been found occasionally on or near PD colonies and its primary host (P. maniculatus) has been found seropositive on PD colonies or surrounding areas (Stapp et al. 2008), Salkeld and Stapp (2008) questioned whether these mice actually play a significant role in epizootics associated with PD colonies. Despite these findings, we suggest, like others (Baltazard 1964, Easterday et al. 2012), that rare events, including bridge vector events, can play an important role in initiating epizootics and plague maintenance in a particular area. Even a single flea can transmit enough Y. pestis to induce a focal infection (Eisen et al. 2009) from which the bacteria may spread, and once plague passes to susceptible animals that are heavily parasitized by fleas, plague circulation can be relatively rapid and even explosive (Krasnov et al. 2006). Furthermore, A. wagneri can be found on hosts parasitized by more abundant, more infectious flea species, and multispecies flea pools may vector Y. pestis.

In total, 12 flea species were found on UPDs at the Awapa Plateau. Collectively, the 12 species are known to parasitize a multitude of additional plague hosts, including mice, voles, chipmunks, ground squirrels, rock squirrels, and marmots, all of which occupy portions of the plateau (providing fleas with a diversity community of hosts). Jachowski et al. (2012), Bron (2017), and Russell et al. (2018) also report a large diversity of fleas on UPD colonies at Awapa. In addition to a diverse host community, increased moisture and lower temperatures at Awapa and habitat heterogeneity may provide suitable conditions for a variety of fleas. A large diversity of fleas, many of which are willing to move among and parasitize many types of rodents in many habitats, might facilitate the maintenance and spread of plague (Eisen et al. 2012). Different flea species exhibit different phonologies, and diverse flea communities may participate in transmission cycles across multiple seasons (Ramakrishnan 2018).

Flea parasitism on deer mice in Utah increased with elevation, an observation consistent with frequent detections of plague at high elevations (Neerinckx et al. 2008, Galdan et al. 2010, Xu et al. 2014), including high elevations in Utah (Arjo et al. 2003). As flea parasitism increases, rates of plague transmission are expected to increase (Lorange et al. 2005). Mesic conditions at higher elevations might facilitate flea survival, and Y. pestis recruitment inside fleas (and subsequent transmission; Williams et al. 2013). Nest characteristics for deer mice might also vary with elevation, with implications for survival of immature and adult flea stages (Krasnov 2008).

Experiments are needed to evaluate the effects of plague on mammals at high elevations in western United States of America. Manipulation of plague risk (e.g., with deltamethrin and vaccines) coupled with mark-recapture studies provides a powerful experimental approach (Biggins et al. 2010, Matchett et al. 2010, Goldberg 2018, Ramakrishnan 2018). Recent experiments suggest an effect of plague on rodents in montane regions of western United States of America (Goldberg 2018, Goldberg et al. unpublished data). Our results with deer mice provide additional incentive for targeted study, especially with imperiled mammals occupying fragmented habitats in plague-endemic regions (e.g., American pikas and Peñasco least chipmunks, Tamias minimus atristriatus; Biggins et al. 2010).

In conclusion, treatment of PD burrows with 0.05% deltamethrin dust suppressed fleas on small rodents. By simultaneously suppressing fleas on PDs and small rodents, deltamethrin should help to promote ecosystem resilience and One Health objectives. We detected a significant, positive correlation between elevation and flea parasitism on Peromyscus mice, encouraging targeted research on plague ecology in montane ecosystems.

Footnotes

Acknowledgments

We are indebted to many crew leaders and technicians who assisted them. We are also indebted to J. Montenieri who identified fleas and contributed significantly to this work in a variety of ways. We thank J. Boulerice and an anonymous reviewer for constructive comments on a previous version of the article. Data are available from Eads (). Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the United States Government.

Author Disclosure Statement

No conflicting financial interests exist.

Funding Information

Funding and support were provided by United States Fish and Wildlife Service; United States Geological Survey; United States Forest Service; Bureau of Land Management; Denver Zoological Foundation; Utah Division of Wildlife Resources and Utah Department of Natural Resources Endangered Species Mitigation Fund; Bryce Canyon National Park; Dixie National Forest; Bureau of Land Management offices in Utah (Vernal, Cedar City, Richfield, and Torrey), Colorado (Meeker), and Montana (Malta); and Centers for Disease Control and Prevention.

Supplementary Material

Supplementary Data

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