Potential Effects of Environmental Conditions on Prairie Dog Flea Development and Implications for Sylvatic Plague Epizootics

Abstract

Fleas are common ectoparasites of vertebrates worldwide and vectors of many pathogens causing disease, such as sylvatic plague in prairie dog colonies. Development of fleas is regulated by environmental conditions, especially temperature and relative humidity. Development rates are typically slower at low temperatures and faster at high temperatures, which are bounded by lower and upper thresholds where development is reduced. Prairie dogs and their associated fleas (mostly Oropsylla spp) live in burrows that moderate outside environmental conditions, remaining cooler in summer and warmer in winter. We found burrow microclimates were characterized by stable daily temperatures and high relative humidity, with temperatures increasing from spring through summer. We previously showed temperature increases corresponded with increasing off-host flea abundance. To evaluate how changes in temperature could affect future prairie dog flea development and abundance, we used development rates of O. montana (a species related to prairie dog fleas), determined how prairie dog burrow microclimates are affected by ambient weather, and combined these results to develop a predictive model. Our model predicts burrow temperatures and flea development rates will increase during the twenty-first century, potentially leading to higher flea abundance and an increased probability of plague epizootics if Y. pestis is present.

Full text

Potential Effects of Environmental Conditions on Prairie Dog
Flea Development and Implications for Sylvatic Plague Epi-
zootics
Michael D. Samuel,
1
Julia E. Poje,
1
Tonie E. Rocke,
2
and Marco E. Metzger
3,4
1
Department of Forest and Wildlife Ecology, University of Wisconsin-Madison, Madison, WI 53706
2
U.S. Geological Survey, National Wildlife Health Center, Madison, WI 53711
3
Department of Entomology, University of California, Riverside, CA 92521
4
Vector-Borne Disease Section, Division of Communicable Disease Control, Center for Infectious Diseases, California Department of Public Health,
Ontario, CA 91764
Abstract: Fleas are common ectoparasites of vertebrates worldwide and vectors of many pathogens causing
disease, such as sylvatic plague in prairie dog colonies. Development of fleas is regulated by environmental
conditions, especially temperature and relative humidity. Development rates are typically slower at low tem-
peratures and faster at high temperatures, which are bounded by lower and upper thresholds where devel-
opment is reduced. Prairie dogs and their associated fleas (mostly Oropsylla spp) live in burrows that moderate
outside environmental conditions, remaining cooler in summer and warmer in winter. We found burrow
microclimates were characterized by stable daily temperatures and high relative humidity, with temperatures
increasing from spring through summer. We previously showed temperature increases corresponded with
increasing off-host flea abundance. To evaluate how changes in temperature could affect future prairie dog flea
development and abundance, we used development rates of O. montana (a species related to prairie dog fleas),
determined how prairie dog burrow microclimates are affected by ambient weather, and combined these results
to develop a predictive model. Our model predicts burrow temperatures and flea development rates will
increase during the twenty-first century, potentially leading to higher flea abundance and an increased
probability of plague epizootics if Y. pestis is present.
Keywords: Fleas, Prairie dogs, Sylvatic plague, Development rate, Climate change
INTRODUCTION
Fleas (order Siphonaptera) are common ectoparasites of
vertebrates worldwide (Krasnov, 2008) and are vectors of
many pathogens that cause disease, including murine ty-
phus (Rickettsia typhi) (Azad, 2002), myxomatosis virus
(Myxoma virus) (Rothschild, 1965), cat scratch disease
(Bartonella henselae) (Chomel et al. 1996), and sylvatic
plague (Yersinia pestis) (Eisen and Gage, 2012). The plague
bacterium was introduced to the western USA at the start
of the twentieth century and quickly spread among native
rodents. Plague now regularly occurs in rodents and other
Correspondence to: Michael D. Samuel, e-mail: mdsamuel@wisc.edu
EcoHealth
https://doi.org/10.1007/s10393-022-01615-6
Original Contribution
2022 This is a U.S. Government work and not under copyright protection in the US;
foreign copyright protection may apply

species from the Pacific coast to the eastern edge of the
Great Plains (Fig. 1A). Plague epizootics can be particularly
devastating to highly susceptible prairie dogs, often causing
local population extirpation (Pauli et al. 2006). These
outbreaks can also directly affect other rodents and carni-
vores associated with prairie dog colonies, domestic ani-
mals, and even humans, although rarely. Many other
species directly or indirectly depend on prairie dogs, and
although their status as keystone species has been debated,
colony extirpation can have cascading effects throughout
the grassland ecosystem they inhabit (Miller et al. 1994;
Stapp, 1998; Kotliar et al. 2006; Eads and Biggins, 2015).
Endangered black-footed ferrets (Mustela nigripes) cannot
survive without large prairie dog colonies and are also
highly susceptible to Y. pestis infection (Williams et al.
1994). Reduced black-tailed prairie dog (Cynomys ludovi-
cianus) populations have hindered efforts to reintroduce
black-footed ferrets to their historical range (USFWS,
2013). Hence, minimizing plague outbreaks is an important
goal in black-footed ferret recovery efforts (USFWS, 2013).
In the USA, flea vectors of Y. pestis among ground
dwelling sciurids commonly belong to the genus Oropsylla
(Burroughs, 1947), although fleas of other genera, in par-
ticular the generalist Pulex simulans, may also play an
important role. Oropsylla montana is a common parasite of
rock squirrels (Otospermophilus variegatus) and California
ground squirrels (Ot. beecheyi) west of the Rocky Moun-
tains (Hubbard, 1968). In the intermountain west and the
Great Plains, Or. hirsuta,Or. tuberculata cynomuris, and Or.
labis are common ectoparasites of prairie dogs (Lewis,
2002). These nidicolous fleas develop from egg to adult in
protected microhabitats within host burrows. Like other
insects, flea development is generally regulated by species-
specific environmental conditions, especially temperature
and relative humidity. Development only occurs within a
specific range of temperature and relative humidity,
bounded by lower temperature thresholds, where immature
fleas cannot develop, and upper thresholds, where devel-
opment rates decline and/or the fleas die (Gilbert and
Raworth, 1996). To complete development, fleas and other
insects typically need to accumulate heat energy, which can
be measured in degree-days (Wilson and Barnett, 1983). As
a result, development rates are typically slower at low
temperatures and faster at high temperatures (Damos and
Savopoulou-Soultani, 2012), although this is not always the
case (Krasnov 2008). Immature fleas are also highly sensi-
Figure 1. A Plague seropositive and seronegative samples collected from wild canids, 2005–2018 (From Bevins et al. 2021). BThe range of
black-tailed prairie dogs in the U.S. and study sites located on their colonies at selected sites including the Charles M. Russell (CMR) National
Wildlife Refuge (Phillips County, Montana), Theodore Roosevelt (TR) National Park (Billings County, North Dakota), Buffalo Gap (BG)
National Grassland (Pennington County, South Dakota), Lower Brule (LB) Sioux Reservation (Lyman County, South Dakota), Pueblo
Chemical Depot (PCD; Pueblo County, Colorado), and Bureau of Land Management (BLM) land surrounding Roswell, New Mexico (Chaves
County, New Mexico; 2017 only).
M. D. Samuel et al.

tive to desiccation and, if relative humidity is too low, fleas
will not complete development even when the temperature
is favorable (Krasnov et al. 2001ab; Kreppel et al. 2016).
These temperature thresholds and heat energy require-
ments play key roles in determining species ranges and
abundance of insects (Andrewartha and Birch, 1986), and
the expansion and contraction of insect ranges as local
climates cool or warm is well documented (Parmesan et al.
1999). The Oropsylla species that occur on prairie dogs
have not been colonized in laboratory settings, so the exact
relationship between temperature and their development
has not been determined. However, these species are
known to have different seasonal and geographic patterns
of abundance (Salkeld and Stapp, 2008; Tripp et al. 2009),
indicating that environmental conditions likely play an
important role in these observed patterns.
Ground dwelling mammals typically dig burrows that
serve as their primary refugia from predators and adverse
weather (Fitch, 1948; Longanecker and Burroughs, 1952;
Hoogland, 1995). These burrows moderate the effect of the
outside environment, remaining cooler in summer and
warmer in winter (Pike and Mitchell, 2013). Ground-
dwelling rodent burrows also provide the required habitat
for all life stages of Oropsylla fleas (Eskey and Haas, 1940;
Sheets et al. 1971). Understanding the relationship between
prairie dog burrow microclimate and flea abundance is
important, because high flea numbers can adversely affect
hosts from parasitism, such as dermatitis and anemia
(Scheidt, 1988; Yeruham et al. 1989; Arau
´jo et al. 1998;
Bond et al. 2007). In addition, peak seasonal abundance of
prairie dog fleas has been correlated with the risk of Y.
pestis transmission (Tripp et al. 2009; Biggins et al. 2010;
Biggins and Eads, 2019). On-host flea abundance has been
repeatedly shown to increase during plague outbreaks as
fleas leave dying hosts to concentrate on fewer animals
(Tripp et al. 2009; Biggins and Eads, 2019). In contrast,
throughout this paper, we are specifically referring to off-
host flea abundance in burrows prior to plague epizootics.
Previously, we reported that off-host flea abundance
and prevalence in prairie dog burrows increased with
monthly mean ambient high temperature and declined
with higher winter precipitation (Poje et al. 2020). Deter-
mining how burrow temperature and relative humidity
effect flea development could help us predict how off-host
flea populations may change in the future and the potential
implications for plague epizootics. In this paper, we
examined how burrow microclimate temperature was af-
fected by ambient weather patterns. We then evaluated the
effect of temperature and relative humidity on develop-
ment rates of Or. montana fleas, which infest ground
squirrels, as a proxy for related species of prairie dog fleas.
We found that burrow relative humidity was consistently
above the threshold required for optimal flea development
and chose not to include it in our analysis. We linked
ambient environmental temperatures to prairie dog burrow
microclimate and flea development and used these results
to predict how climate change could affect future flea
abundance, while accounting for the ability of prairie dog
burrows to buffer environmental conditions.
METHODS
Burrow Microclimates
We conducted field studies in 2016 and 2017 at six sites
that were broadly distributed across the range of black-
tailed prairie dogs within the USA (Fig. 1B). We conducted
studies at Charles M. Russell National Wildlife Refuge
(Phillips County, Montana), Theodore Roosevelt National
Park (Billings County, North Dakota), Buffalo Gap Na-
tional Grassland (Pennington County, South Dakota),
Lower Brule Sioux Reservation (Lyman County, South
Dakota), Pueblo Chemical Depot (Pueblo County, Color-
ado), and Bureau of Land Management land surrounding
Roswell, NM (Chaves County, New Mexico; 2017 only).
We selected three prairie dog colonies at each site that had
landowner or lessee permission to access the land, an active
prairie dog population, and no history of pesticide treat-
ment. Each colony was sampled during two sessions, once
during May or June (spring), and once in August (sum-
mer) (Table 1). The North Dakota site was added to the
study during the summer of 2016 and so was only sampled
during August that year. For a related part of the study, we
swabbed 100 burrows per colony to collect off-host fleas to
assess the effects of environmental conditions on flea
abundance and flea prevalence in burrows (Poje et al.
2020).
Burrow and ambient temperatures and relative
humidity were measured by iButton Hygrochron data
loggers (DS1923, Maxim Integrated). Loggers were at-
tached to the end of flexible plumbing snakes and inserted
as far as possible (mean 2.35 m, range 1–4.5 m), hereafter
considered logger depth, into prairie dog burrows. Data
were recorded every 30 min over a three- to four-day
period, during spring (May–June) and summer (August),
Potential Effects of Environmental Conditions on Prairie Dog Flea Development

except for at the Charles M. Russell National Wildlife Re-
fuge in spring 2016, where loggers were set to record every
20 min for roughly 23–26 h. The loggers were synchro-
nized to take simultaneous readings. In 2016, we placed
loggers in up to nine burrows at each site and three on the
surface at burrow entrances. The loggers on the surface
were not shaded, which may have resulted in artificially
high ambient temperature measurements due to solar
radiation (Hubbart, 2011). Several loggers malfunctioned,
resulting in data from 62 burrows and 18 surface loggers
(Table 1). In 2017, we placed loggers in up to nine burrows
at each site at the start of the spring session and left them in
burrows through August (n= 72 burrows monitored)
(Table 1). We calculated the mean burrow and surface
temperature and relative humidity for spring and summer
each year by taking the mean of the burrow data loggers at
each 20 or 30-min timestep during a three- to four-day
interval at each site. Loggers placed at the surface were used
to compare daily fluctuations with burrow temperatures
(Fig. 2). Monthly mean ambient high temperatures for
each site (Table 1) were obtained from NOAA’s National
Centers for Environmental Information for the nearest
weather station with complete data for each sample period
(Poje et al. 2020).
We assessed the relationship between mean burrow
temperature and the monthly mean ambient high tem-
perature from weather stations, season (spring or summer),
year, and logger depth using a linear mixed model. Mean
burrow temperature was modeled as a response to the fixed
effects of monthly mean high temperature, season (spring
Table 1. Summary of Burrow Sampling Data during 2016–2017 at Six Study Sites.
Site Year Session n Burrow temp mean and
range
Relative humidity Logger depth Monthly high temp Weather station distance
MT 2016 Spr 4 13.5 13.1–13.8 98.8 ** 26.4 75
Aug 4 16.9 16.3–19.6 98.6 ** 28.5
MT 2017 Spr 4 14.1 11.9–17.8 97.9 2.8 27.1
Aug 4 18.8 15.6–22.2 94.9 2.8 29.1
ND 2016 Spr Not done 11
Aug 9 19.6 14.5–22.3 98.8 1.9 28.2
ND 2017 Spr 3 13.7 10.2–16.1 100 3.5 26.2
Aug 2 17.1 16.6–17.6 100 3.0 25.8
LB 2016 Spr 9 17.8 13.3–22.0 100 1.4 30.1 35
Aug 6 20.1 16.9–24.0 98.2 2.7 30.2
LB 2017 Spr 9 14.2 10.1–16.7 97.9 2.1* 28.9
Aug 3 17.1 13.1–19.6 100 2.7 27.7
BG 2016 Spr 9 17.5 13.9–20.2 99.2 1.8 30.6 50
Aug 9 20.2 18.0–22.2 99.2 1.8 28.8
BG 2017 Spr 4 12.7 10.1–14.4 99 3.4 28.6
Aug 3 17.5 13.7–20.1 95 3.7 28.7
CO 2016 Spr 8 19.4 14.1–22.6 98.9 1.4 33.8 15
Aug 3 24.1 22.2–25.3 89.1 1.7 32.4
CO 2017 Spr 9 14.6 13.6–16.1 98.7 2.6 31.8
Aug 8 21.0 18.6–23.1 97 2.7 30.1
NM 2017 Spr 6 19.6 17.2–21.8 97.5 3.2 36.9 15
Aug 6 23.1 19.1–26.0 100 3.2 33.0
Number of burrows sampled (n), mean burrow temperature (°C) and range, mean relative humidity (%), monthly mean ambient high temperature (°C) for
each year and sampling session (spring = Spr or August = Aug), mean logger depth (m), and distance to National Oceanic and Atmospheric
Administration weather station (km) at the Charles M. Russell National Wildlife Refuge, Montana (MT), Theodore Roosevelt National Park, North Dakota
(ND), Lower Brule Sioux Reservation, South Dakota (LB), Buffalo Gap National Grassland, South Dakota (BG), Pueblo Chemical Depot, Colorado (CO),
and near Roswell, New Mexico, (NM).
*Logger depth only recorded for 8 burrows.
**No logger depths were recorded.
M. D. Samuel et al.

or summer), logger depth, and year, with study site in-
cluded as a random effect, using Proc Mixed in SAS/STAT
Software (SAS Institute Inc., 2013).
Flea Development Rates
Of the Oropsylla fleas, only Or. montana, the primary
vector of Y. pestis in California ground squirrels, has been
successfully colonized in the laboratory on their native
host. Specifically, Metzger (2000) documented egg-to-adult
development of Or. montana under different combinations
of constant temperature (15.5, 21.1, and 26.7°C) and rel-
ative humidity (55%, 65%, 75%, and 85%). We used these
data from Or. montana as a proxy for Or. hirsuta and Or.
tuberculata cynomuris, because the microclimates governing
their development and the life history of their hosts are
presumed to be similar. Like prairie dogs, California
ground squirrels dig extensive burrow systems that they use
for sleeping, shelter, and rearing young (Fitch, 1948;
Hoogland, 1995). The microclimate of ground squirrel
burrows is similar to conditions we measured in prairie dog
burrows (high relative humidity, temperatures ranging
Figure 2. Illustrations of daily burrow and ambient surface temperatures measured by iButton data loggers during spring 2016 in burrows at
the Buffalo Gap National Grassland, South Dakota (BG), Pueblo Chemical Depot, Colorado (CO), Lower Brule Sioux Reservation, South
Dakota (LB), Charles M. Russell National Wildlife Refuge, Montana (MT), Theodore Roosevelt National Park, North Dakota (ND), and near
Roswell, New Mexico, (NM).
Potential Effects of Environmental Conditions on Prairie Dog Flea Development

from 15°C in May to 20°C in August) (Longanecker and
Burroughs, 1952), and both adult Or. hirsuta and Or.
montana are commonly found in burrows of their respec-
tive hosts (Eskey and Haas, 1940). Although ground
squirrel nests are shallower than prairie dog nests, tem-
peratures within burrows are still highly stable (Longa-
necker and Burroughs, 1952). We used the mean number
of days needed for Or. montana fleas to complete devel-
opment (Table 2) to estimate the development rate (1/
number of days to adult emergence). We modeled flea
development rate (which must be >0 and is likely non-
linear) as a natural log response to the fixed effects of
temperature at 85% relative humidity which was consid-
erably below the high humidity levels found in prairie dog
burrows (Table 1), allowing us to ignore potential impact
of humidity on flea development. We then used the inverse
of the predicted development rate to determine the number
of days required for a flea to complete development at a
given burrow temperature.
Climate Change and Flea Development
We used a Bayesian model to combine our models for
predicting prairie dog burrow microclimate from ambient
temperature and O. montana flea development from pre-
dicted burrow temperature. From this Bayesian model, we
estimated how future climate could affect flea development
rates within prairie dog burrows. The Bayesian approach
allowed us to incorporate parameter uncertainty from both
models to predict development rates and times for future
temperature projections. The Bayesian model was devel-
oped for monthly mean high temperature (MMHT), bur-
row temperature (BT), and daily development rate (DDR)
as follows:
BT ¼b1MMHT
DDR ¼exp a2þb2BTðÞ
DDR ¼exp a2þb2b1MMHTðÞ
ð1Þ
where b
1
= 0.70 is the estimated slope from the regression
of summer burrow temperature on monthly mean high
temperature [see results and Eq. (3)]. We used the esti-
mated mean and variance from b
1
(Var = 0.0072) as priors
to simultaneously estimate a
2
and b
2
and predict median
development rates from monthly mean high temperature.
We used the inverse of the predicted median development
rate and 95% Bayesian creditable interval (BCI) from the
final Bayesian model to predict the number of days re-
quired for flea development under future climate changes.
We simplified the model by making predictions based on
summer burrow temperatures and mean logger depth,
which allowed us to remove these two conditions from
Eq. (1) [see results and Eq. (3)]. Because the field sites in
Table 2. Adult Emergence (days) and Development Rate for Oropsylla montana Fleas.
Temperature Relative humidity Sex n Adult emergence (days) (SE) Development rate
15.5 65% Female 56 56.4 (0.33) 0.018
Male 44 59.8 (0.58) 0.017
75% Female 117 56.1 (0.88) 0.018
Male 85 62.3 (0.96) 0.016
85% Female 113 41.2 (0.24) 0.024
Male 109 46.5 (0.28) 0.022
21.1 65% Female 99 37.1 (0.43) 0.027
Male 97 38.9 (0.86) 0.026
75% Female 109 26.5 (0.19) 0.038
Male 128 28.1 (0.15) 0.036
85% Female 121 24.4 (0.12) 0.041
Male 128 27 9 (0.13) 0.037
26.7 75% Female 21 20.8 (0.13) 0.048
Male 11 22.5 (0.14) 0.044
85% Female 112 18.8 (0.11) 0.053
Male 104 20.6 (0.15) 0.049
Mean number of days and standard error (SE) required for adult emergence of Oropsylla montana from eggs at different temperatures (°C) and relative
humidity (%). Development rate = 1/adult emergence. Data summarized from Metzger (2000).
M. D. Samuel et al.

the northern plains (Montana, North Dakota, and South
Dakota) have a cooler, wetter climate than those in the
southern plains (Colorado and New Mexico), we estimated
mean changes in future development rates for each region
separately.
We also used a simple linear regression of Or. montana
development time based on temperature (Table 2) to esti-
mate the lower temperature threshold for flea development
(T
b
) (Damos and Savopoulou-Soultani, 2012):
1=DDR ¼a3þb3BT and
Tb¼a3=b3
ð2Þ
RESULTS
Burrow Microclimate
Prairie dog burrow temperatures remained stable at all
study sites despite wide fluctuations in outside tempera-
tures (Fig. 2). Burrow temperatures varied across study
locations, with the highest temperature recorded in New
Mexico in August (26.0°C) and the coolest temperature at
Lower Brule and Buffalo Gap in spring 2016 (10.1°C);
however, most burrow temperatures were below 21°C
(Table 1). Mean relative humidity was uniformly high
(>89%) across sites, sampling sessions, and years (Ta-
ble 1). Humidity was always above the threshold level
(75%) where flea development was affected and was
therefore deleted from further analysis.
The linear mixed model analysis showed that the
model intercept (t= 1.28, df = 5, P= 0.26) and year
(t= 0.88, df = 105, P= 0.38) were not significant in pre-
dicting burrow temperature and were dropped from our
global model. The resulting linear equation was:
BT ¼a1MMT þa2LD þa3SS ð3Þ
where SS is the sampling session (spring or summer) where
a
1
= 0.70 (standard error (SE) = 0.085, t= 8.25, df = 106,
P<0.0001), a
2
=-1.46 (SE = 0.22, t= 6.68, df = 106,
P<0.0001) when logger depth (LD) was centered around
the mean of 2.35 m, a
3
=-4.95 for spring (SE = 0.41,
t= 12.1, df = 106, P<0.0001) and a3 = 0 for summer.
Mean burrow temperature increased 0.70°C (95% confi-
dence interval (CI) = 0.53–0.87) for every 1°C increase in
monthly mean high temperature. Mean burrow tempera-
ture (least square means) during summer was 20.9°C (95%
CI = 20.3–21.5) compared to spring (15.9, 95% CI = 15.3–
16.5).
Oropsylla Montana Development
Optimal development of Or. montana occurred at 85%
relative humidity with reduced development between 65
and 75% relative humidity, with little development at 65%
at <26.7°C (Metzger, 2000). Low relative humidity
inhibited Or. montana development, as no fleas completed
development at 55% relative humidity. We estimated the
lower temperature threshold [Eq. (2)] for Or. montana
development at 6°C. According to our model, the flea
development rates increased with burrow temperature. Our
Bayesian model [Eq. (1)] predicted the daily development
rate (DDR) based on monthly mean high temperature
(MMHT):
DDR ¼exp a1þa2b1MMHTðÞ
with a
1
=-4.83 (95% BCI -5.1 to -4.5), b
1
= 0.70
(95% BCI 0.53–0.86), a2 = 0.070 (95% BCI 0.058–0.082),
at mean logger depth (2.35 m) during summer. For every
1°C increase in daily summer temperature (i.e., degree-
day), the development rate increased by 0.001–0.002,
depending on ambient environmental temperature (Fig. 3).
At our study sites in the northern plains (Montana,
South Dakota, North Dakota), the August monthly mean
high temperature was 28°C (25.8°C min, 30.2°C max), with
a predicted prairie dog burrow temperature of 20°C.
Assuming Oropsylla sp. fleas are similar in their develop-
ment requirements, our model predicted a flea develop-
ment rate of 0.032 (95% BCI = 0.022–0.045), indicating it
takes 32 days (95% BCI = 22–46) for a newly laid Or.
hirsuta or Or. tuberculata cynomuris egg to complete
development (Fig. 3). At our study sites in the southern
plains (Colorado, New Mexico), the August monthly mean
high temperature was 31.5°C (min 30.1°C, max 33.0°C),
with a predicted burrow temperature of 22°C and an
estimated flea development rate of approximately 0.038
(95% BCI 0.025–0.057), with adults emerging 26 days
(95% BCI = 17–39) after eggs are laid.
DISCUSSION
Model predictions from our study indicate that prairie dog
flea development rates are strongly linked to burrow tem-
perature and that increasing ambient temperature, which
raises burrow temperatures, could shorten flea develop-
ment time. Understanding how temperature and relative
humidity affects flea development is important for pre-
dicting how flea populations in prairie dog colonies may
Potential Effects of Environmental Conditions on Prairie Dog Flea Development

change in the future and the potential implications for
plague epizootics.
Prairie dog fleas have proven challenging to rear in
experimental settings where development rates could be
determined under varying conditions of temperature and
relative humidity. A related flea species, Or. montana,
which infests ground squirrels, has been colonized, and the
effects of temperature and humidity on their development
were determined by Metzger (2000). We hypothesize that
Or. montana development rates provide a reasonable sur-
rogate for the effects of temperature and humidity on the
development of prairie dog fleas, especially Or. hirsuta and
Or. tuberculata cynomuris, but this would need to be con-
firmed when these species can be colonized in a laboratory
setting. To evaluate the potential influence of future climate
warming on flea development in prairie dog colonies, we
determined how prairie dog burrow microclimates are af-
fected by ambient weather patterns, linked burrow tem-
peratures to O. montana development, and used these
results to predict how climate change could affect future
off-host prairie dog flea abundance.
Burrow microclimates remained quite stable compared
to daily ambient conditions. This pattern was consistent at
all our study sites, where daily temperatures measured at
the surface of burrows spanned 20–40°C but temperatures
measured in burrows fluctuated by less than 1°C (Fig. 2).
Our results are consistent with data collected from burrow
systems of many different terrestrial species that show
stable burrow temperatures and humidity compared to
ambient cycles (Kay and Whitford, 1978; Hall and Myers,
1978; Reichman and Smith, 1990; Shenbrot et al. 2002; Pike
and Mitchell, 2013). The stability of burrow temperatures is
generally attributed to the buffering capacity of the soil.
Because soil has a higher thermal capacity than the atmo-
sphere, it takes longer to heat up than the outside air,
creating a refuge within the burrow to allow respite from
fluctuating ambient conditions. We also found that relative
humidity in burrows was above the 75% threshold where
flea development was adversely affected, seasonally
Figure 3. Bayesian model [Eq. (1)] predicted median flea development time (days) with 95% Bayesian Credible Intervals based on monthly
mean ambient high temperature (°C) and relative humidity >85% during August at mean burrow depth of 2.35 m. Based on corresponding
predicted burrow temperature and associated flea development rates for Oropsylla montana from Metzger (2000). Predicted flea development
time would be lower in spring and at greater burrow depths due to lower temperatures. Ambient temperatures between 16 and 38°C
correspond to burrow temperatures between 11 and 27°C, which are within the range used by Metzger (2000) and above the estimated lower
temperature threshold of 6°C.
M. D. Samuel et al.

stable and consistent across latitudes (Table 1). High rates
of water loss are a substantial problem for many desert
animals (Schmidt-Nielsen, 1964), and many of these spe-
cies use burrows that provide a microclimate that reduces
water loss (Bulova, 2002). The high relative humidity found
in prairie dog burrows provides ideal conditions for flea
development (Salkeld and Stapp, 2008; Eads et al. 2020).
Although burrow temperatures were stable short-term,
they also changed seasonally, increasing an average of 5°C
from spring to late summer (Table 1). As expected, burrow
temperatures and ambient temperatures both declined with
higher latitude. These longer-term patterns follow seasonal
and latitudinal climatic conditions driven by solar radiation
(Bennett et al. 1988). We found that mean burrow tem-
perature was driven by monthly mean high temperature of
the ambient environment. Burrow temperatures were buf-
fered from ambient temperatures, however, as a 1°C in-
crease in monthly mean high temperature produced a
0.7°C (95% CI = 0.53–0.87) increase in mean burrow
temperature. Higher burrow temperatures are typically
favorable for flea development and correspond with higher
abundance of both off- and on-host fleas in prairie dog
colonies (Salkeld and Stapp, 2008; Russell et al. 2018; Poje
et al. 2020). For example, on our study sites, off-host flea
populations increased about 80–110% for each 1°C in-
crease in ambient temperature (Poje et al. 2020). The
positive relationship observed between temperature and
Or. montana development in a laboratory setting parallels
those observed for cat (Metzger and Rust 1997), rat
(Kreppel et al. 2016), and jirid (Krasnov et al. 2001b) fleas.
The commonality of these relationships across several flea
species increases the likelihood that Or. hirsuta and Or.
tuberculata cynomuris also develop more rapidly at higher
temperatures, leading to the observed increases in flea
abundance, as we reported previously (Poje et al. 2020).
High temperatures and low precipitation can also alter
prairie dog behavior in ways that leave them more sus-
ceptible to flea infestation (Eads et al. 2020), possibly
adding to the effect of high temperatures on flea develop-
ment.
Earth’s climate has been warming since the middle of
the twentieth century and is likely to continue (IPCC,
2014). Under conservative estimates, temperatures in the
US Great Plains states are likely to increase by 1.9–3.6°Cby
2085 (Kunkel et al. 2013ab). As the climate warms and
future ambient temperatures increase by 4°C, our model
indicates that summer prairie dog burrow temperatures, in
both the southern and northern plains, will increase by
2.8°C (95% CI = 2.1–3.5). Assuming Oropsylla sp. fleas
have similar development patterns, the number of days
required to complete flea development in summer is pre-
dicted to decrease in the northern plains from 32 days to
approximately 27 days and in the southern plains from
26 days to approximately 23 days (Fig. 3). For example, the
number of Or. hirsuta generations produced over a 150-day
period may increase from 4.7 to 5.6 in the northern plains,
and from 5.8 to 6.5 in the southern plains by late in the
twenty-first century. These correspond to a potential flea
population increase of approximately 110–120% in the
northern and southern plains. However, flea populations
may also respond to other factors in addition to tempera-
ture changes. Host factors, such as hormone and pher-
omones, can affect fleas (Krasnov, 2008), and some species
experience cyclical booms and busts in their populations
while living in stable environmental conditions (Metzger,
2000). Prairie dog flea dynamics are still poorly under-
stood, but it is likely that host factors play a role in their
population dynamics and temporal abundance in ways that
could amplify or dampen the effects of temperature on
development rates. This may be particularly true for Or.
tuberculata cynomuris populations, which peak in abun-
dance during the spring and decline by summer (Tripp
et al. 2009).
Another consequence of warming climates is a decrease
in the number of cold days, leading to shorter winters. In
temperate regions, warming throughout the twentieth
century has been correlated with earlier spring emergence
for many insect species. If the date of first emergence be-
comes early enough, insects can increase the number of
generations that are produced during the warm season
(Altermatt, 2010), leading to a population that is present
on the landscape for a longer period. Consequently, climate
warming also means a longer period when ambient tem-
peratures are likely to exceed the minimum threshold for
prairie dog flea development. In the northern plains, a 4°C
increase in ambient temperature is likely to extend the
favorable period for flea development, as temperatures
would remain above the 6°C lower temperature threshold
for flea development approximately one month later in the
fall. In addition, warmer winters mean that temperatures
would reach the 6°C threshold approximately one month
earlier in the spring. These shorter winters can lead to
earlier spring emergence of the first generation of adult
fleas (Robinet and Roques, 2010). Additionally, the
fecundity of several flea species increases with temperature
(Krasnov, 2008), leading to higher rates of recruitment.
Potential Effects of Environmental Conditions on Prairie Dog Flea Development

Together, faster development rates over longer growing
seasons coupled with higher recruitment rates would in-
crease flea abundance during spring and summer and
provide a longer period for potential Y. pestis transmission
by fleas. On the other hand, excessively high temperatures
(above the upper temperature threshold) in some regions
could also decrease flea survival (Silverman et al. 1981;
Kraznov et al. 2001a) and have negative effects on plant
production and prairie dog condition, which can in turn
influence flea abundance (Eads and Biggins, 2015). Thus,
further research would be beneficial to specifically deter-
mine how Or. hirsuta and Or. tuberculata cynomuris re-
spond to warmer and longer periods of favorable
temperatures, including development rates and lower and
upper temperature thresholds.
Recent modeling indicates that fleas initiate >70% of
plague outbreaks in prairie dogs (Richgels et al. 2016;
Russell et al. 2021) compared to direct forms of transmis-
sion (e.g., direct contact between prairie dogs or scavenging
plague-killed carcasses). If fleas are present in prairie dog
colonies for longer periods of time and at higher abun-
dance, then it is reasonable to hypothesize that plague
events could occur more frequently with higher risk of
depopulation, and epizootics could last longer and be more
widespread with increased risk of Y. pestis transmission to
other species. In the Great Plains, El Nin
˜o events lead to
flea-friendly warmer, and somewhat wetter winters, indi-
cating that future warming could produce similar results
(Parmenter et al. 1999). Models of prairie dog colonies in
Colorado found a heightened risk of extirpation due to
plague outbreaks following these El Nin
˜o events (Stapp
et al. 2004). Similar effects of climate change have been
reported for avian malaria in the Hawaiian Islands, where
cool winter temperatures in high altitude forests provide an
avian refuge from mosquito vector and parasite develop-
ment (LaPointe et al. 2012). As the climate warms, this
refuge is expected to shrink, as increasing temperatures
facilitate year-round mosquito populations supporting
higher and longer transmission of malaria (Liao et al.
2017). Shorter, milder winters have also been implicated in
outbreaks of winter ticks (Dermacentor albipictus) causing
mortality in moose (Dunfey-Ball, 2009; Holmes et al.
2018). Warmer temperatures during fall questing decrease
tick mortality and increase the likelihood of finding a host.
Similarly, Ixodes ricinus, a vector of pathogens causing
Lyme disease and tick-borne encephalitis, became active
year-round in Scotland as winter temperatures rose (Fur-
ness and Furness, 2018), increasing the chances of an in-
fected tick transmitting pathogen(s) to a host.
Although our study indicates higher temperature could
lead to higher flea abundance, it is important to note that
plague epizootics are complex, potentially involving several
hosts and flea species that peak at different times of the year
(Tripp et al. 2009) with different transmission efficiencies
for Y. pestis (Wilder et al. 2008). Only a few studies have
systematically measured flea abundance in prairie dog co-
lonies prior to outbreaks or investigated correlations be-
tween flea abundance and plague outbreaks. Tripp et al.
(2009) found that outbreaks correlated with peak abun-
dance of fleas, but noticeable increases did not occur until
after outbreaks occurred, when prairie dogs died, and fleas
were concentrated on fewer hosts. Salkeld and Stapp (2008)
reported that flea abundance did not differ between sites
with and without outbreaks, although increases were noted
during outbreaks. In addition, favorable temperatures for
the flea vector may not be favorable for the pathogen. For
example, transmission of Y. pestis by Or. montana was
lower at 23°C than 15°C, 10°C, or 6°C (Williams et al.
2013). Lastly, plague outbreaks have been documented at
sites where pesticides have been applied to control fleas and
flea abundance was negligible (Tripp et al. 2017), implying
other modes of Y. pestis transmission may initiate plague
outbreaks. While Y. pestis transmission by direct contact
between animals or consumption of infected carcasses may
be infrequent, modeling studies indicate these plague ini-
tiation events are more likely to result in prairie dog
extirpations (Russell et al. 2021). Much is still unknown
about how the interaction of host, pathogen, and flea
populations affect plague epizootics on prairie dog co-
lonies, adding to the challenges of predicting the outcome
of climate change on epizootic dynamics.
CONCLUSIONS
Large-scale climatic changes can have profound effects on
ecosystems, biodiversity, and conservation (Mawdsley et al.
2009). Warmer temperatures or altered precipitation will
shift ecosystems by changing species distribution and
composition, enhancing the spread of infectious diseases
(Mawdsley et al. 2009). These changes can lead to wildlife
population declines (Harvell et al. 2002) and disease spil-
lover to humans (Daszak et al. 2000). Increasingly favorable
conditions for vector-borne disease transmission have
substantial implications for conservation and public health.
M. D. Samuel et al.

As the climate warms, insect vectors can expand their
geographic distribution into previously inhospitable terri-
tory, leading to increased incidence of diseases beyond
historical ranges. Shorter development times of both pa-
thogens and vectors because of warmer temperatures can
increase vector abundance and pathogen transmission. In
parts of the USA, warming temperatures could favor faster
prairie dog flea development over a longer season, poten-
tially leading to more frequent and severe plague epizootics,
with potential spillover to other grassland species like
endangered black-footed ferrets. However, unlike many
other vectors whose development is driven directly by
ambient temperatures, flea development is moderated by
reduced burrow temperatures. Because summer prairie dog
burrows are cooler than ambient temperatures, flea popu-
lations may be affected to a lesser degree than what external
conditions might predict.
ACKNOWLEDGEMENTS
This work was funded by the United States Department of
Defense Strategic Environment Research and Development
Program Number 16 RC01-012. S. Eyob, C. Malave, N.
Vlotho, and G. Corriveau assisted with flea collections in
the field, and N. Vlotho and G. Corrievau helped identify
fleas in the laboratory. We would like to thank R. Matchett,
C. Jones, P. Dobesh, T. Willman, S. Grassel, B. McCann, H.
Hicks, D. Baggao, and R. Howard for their help with site
selection and access. Three anonymous reviewers provided
valuable comments that improved the paper. Any use of
trade, firm, or product names is for descriptive purposes
only and does not imply endorsement by the U.S.
Government. Data are available online at https://doi.org/
10.5066/P93TCY21 (Poje et al. 2022).
REFERENCES
Altermatt F (2010) Climatic warming increases voltinism in
European butterflies and moths. Proceedings of the Royal Society
B277:1281–1287
Andrewartha HG, Birch L (1986) The ecological web: More on the
distribution and abundance of animals, Chicago: University of
Chicago Press
Arau
´jo FR, Silva MP, Lopes AA, Ribeiro OC, Pires PP, Carvalho
CME, Balbuena CB, Villas AA, Ramos JKM (1998) Severe cat
flea infestation of dairy calves in Brazil. Veterinary Parasitology
80:83–86
Azad A (2002) Epidemiology of murine typhus. Annual Review of
Entomology 35:553–569
Bennett NC, Jarvis JUM, Davies KC (1988) Daily and seasonal
temperatures in the burrows of African rodent moles. South
African Journal of Zoology 3:189–195
Bevins SN, Chandler JC, Barrett N, Schmit BS, Wiscomb GW,
Shriner SA (2021) Plague exposure in mammalian wildlife
across the western United States. Vector Borne Zoonotic Disease
9:667–674
Biggins DE, Godbey JL, Gage KL, Carter LG, Montenieri JA
(2010) Vector control improves survival of three species of
prairie dogs (Cynomys) in areas considered enzootic for plague.
Vector-Borne Zoonotic Diseases 10:17–26
Biggins DE, Eads DA (2019) Prairie dogs, persistent plague,
flocking fleas, and pernicious positive feedback. Frontiers in
Veterinary Science 6:1–12
Bond R, Riddle A, Mottram L, Beugnet F, Stevenson R (2007)
Survey of flea infestation in dogs and cats in the United King-
dom during 2005. Veterinary Record 160:503–506
Bulova SJ (2002) How temperature, humidity, and burrow
selection affect evaporative water loss in desert tortoises. Journal
of Thermal Biology 27:175–189
Burroughs AL (1947) Sylvatic plague studies. The vector efficiency
of nine species of fleas compared with Xenopsylla cheopis.Epi-
demiology and Infection 45:371–396
Chomel BB, Kasten RW, Floyd-Hawkins K, Chi B, Yamamoto K,
Roberts-Wilson J, Gurfield AN, Abbott RC, Pedersen NC,
Koehler JE (1996) Experimental transmission of Bartonella
henselae by the cat flea. Journal of Clinical Microbiology 34:1952–
1956
Damos P, Savopoulou-Soultani M (2012) Temperature-driven
models for insect development and vital thermal requirements.
Psyche 2012:1–13
Daszak P, Cunningham CC, Hyatt AD (2000) Emerging infectious
disease of wildlife – threats to biodiversity and human health.
Science 287:443–449
Dunfey-Ball KR (2009) Moose density, habitat, and winter tick
epizootics in a changing climate, Thesis: University of New
Hampshire, Durham, New Hampshire
Eads DA, Biggins DE (2015) Plague bacterium as a transformer
species in prairie dogs and the grasslands of western North
America. Conservation Biology 29:1086–1093
Eads DA, Abbott RC, Biggins DE, Rocke TE (2020) Flea para-
sitism and host survival in a plague-relevant system: theoretical
and conservation implications. Journal of Wildlife Diseases
56:378–387
Eisen RJ, Gage KL (2012) Transmission of flea-borne zoonotic
agents. Annual Review of Entomology 57:61–82
Eskey CR, Haas VH (1940) Plague in the western part of the
United States. Public Health Bulletin 254:1–83
Fitch HS (1948) Ecology of the California ground squirrel on
grazing lands. The American Midland Naturalist 39:513–596
Furness RW, Furness EN (2018) Ixodes ricinus parasitism of birds
increases at higher winter temperatures. Journal of Vector Ecol-
ogy 43:59–62
Gilbert N, Raworth DA (1996) Insects and temperature - a general
theory. The Canadian Entomologist 128:1–13
Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld
RS, Samuel MD (2002) Climate warming and disease risks for
terrestrial and marine biota. Science 297:2158–2162
Hall LS, Myers K (1978) Variations in the microclimate in rabbit
warrens in semi-arid New South Wales. Australian Journal of
Ecology 3:187–194
Potential Effects of Environmental Conditions on Prairie Dog Flea Development

Holmes CJ, Dobrotka CJ, Farrow DW, Rosendale AJ, Benoit JB,
Pekins PJ, Yoder JA (2018) Low and high thermal tolerance
characteristics for unfed larvae of the winter tick Dermacentor
albipictus (Acari: Ixodidae) with special reference to moose.
Ticks and Tick-Borne Diseases 9:25–30
Hoogland JL (1995) The black-tailed prairie dog: social life of a
burrowing mammal, Chicago: University of Chicago Press
Hubbard C (1968) Fleas of Western North America, New York:
Hafner Publishing Company
Hubbart JA (2011) An inexpensive alternative solar radiation
shield for ambient air temperature micro-sensors. Journal of
Natural & Environmental Sciences 2:9–14
IPCC (2014) Climate change 2014: Synthesis report. Contribution
of working groups I, II and III to the fifth assessment report of
the intergovernmental panel on climate change. R.K. Pachauri
and L.A. Meyer editors. Intergovernmental Panel on Climate
Change, Geneva, Switzerland.
Kay FR, Whitford WG (1978) The burrow environment of the
banner-tailed kangaroo rat, Dipodomys spectabilis, in south-
central New Mexico. American Midland Naturalist 99:270
Kotliar N, Miller B, Reading R, Clark T (2006) The prairie dog as a
keystone species. In: Conservation of the Black-Tailed Prairie
Dog: Saving North America’s Western Grasslands, Hoogland J
(editor), Washington, D.C.: Island Press, pp 53–64
Krasnov B (2008) Functional and evolutionary ecology of fleas: A
model for ecological parasitology, Cambridge: Cambridge
University Press
Krasnov BR, Khokhlova IS, Fielden LJ, Burdelova NV (2001) Ef-
fect of air temperature and humidity on the survival of pre-
imaginal stages of two flea species (Siphonaptera: Pulicidae).
Journal of Medical Entomology 38:629–637
Krasnov BR, Khokhlova IS, Fielden LJ, Burdelova NV (2001)
Development rates of two Xenopsylla flea species in relation to
air temperature and humidity. Medical and Veterinary Ento-
mology 15:249–258
Kreppel KS, Telfer S, Rajerison SM, Morse A, Baylis M (2016)
Effect of temperature and relative humidity on the development
times and survival of Synopsyllus fonquerniei and Xenopsylla
cheopis, the flea vectors of plague in Madagascar. Parasites &
Vectors 9:1–10
Kunkel KE, Stevens LE, Stevens SE, Sun L, Janssen E, Wuebbles D,
Kruk MC, Thomas DP, Shulski MD, Umphlett NA, Hubbard
KG, Robbins K, Romolo L, Akyuz A, Pathak TB, Bergantino TR,
Dobson JG (2013a) Regional climate trends and scenarios for
the U.S. national climate assessment. Part 4. Climate of the U.S.
Great Plains. NOAA Technical Report NESDIS 142–4. NOAA
National Environmental Satellite, Data, and Information Ser-
vice, Washington, D.C., USA.
Kunkel KE, Stevens LE, Stevens SE, Sun L, Janssen E, Wuebbles D,
Redmond KT, Dobson JG (2013b) Regional climate trends and
scenarios for the U.S. national climate assessment. Part 5. Cli-
mate of the southwest U.S. NOAA Technical Report NESDIS
142–4. NOAA National Environmental Satellite, Data, and
Information Service, Washington, D.C., USA.
LaPointe DA, Atkinson CT, Samuel MD (2012) Ecology and
conservation biology of avian malaria. Annals of the New York
Academy of Sciences 1249:211–226
Liao W, Atkinson CT, LaPointe DA, Samuel MD (2017) Miti-
gating future avian malaria threats to Hawaiian forest birds
from climate change. PLOS ONE 12:e0168880
Lewis RE (2002) A review of the North American species of
Oropsylla Wagner and Ioff, 1926 (Siphonaptera: Ceratophyllidae:
Ceratophyllinae).Journal of Vector Ecology 27:184–206
Longanecker DS, Burroughs A (1952) Sylvatic plague studies, IX.
Studies of the microclimate of the California ground squirrel
burrow and its relation to seasonal changes in the flea popu-
lation. Ecology 33:488–499
Mawdsley JR, O’Malley R, Ojima DS (2009) A review of climate-
change adaption strategies for wildlife management and biodi-
versity conservation. Conservation Biology 23:1080–1089
Metzger ME (2000) Studies on the bionomics of California
ground squirrel fleas and evaluation of insecticides applied
topically to their hosts for control. PhD. dissertation. University
of California Riverside, Riverside, CA, USA.
Metzger ME, Rust MK (1997) Effect of temperature on cat flea
(Siphonaptera:Pulicidae) development and overwintering.
Journal of Medical Entomology 34:173–178
Miller B, Ceballos G, Reading R (1994) The prairie dog and biotic
diversity. Conservation Biology 8:677–681
Parmenter RR, Yadav EP, Parmenter CA, Ettestad P, Gage KL
(1999) ncidence of plague associated with increased winter-
spring precipitation in New Mexico. American Journal of
Tropical Medicine and Hygiene 61:814–821
Parmesan C, Ryrholm N, Stefanescu NC, Hill JK, Thomas CD,
Descimon H, Huntley B, Kaila L, Kullberg J, Tammaru T,
Tennent WJ, Thomas JA, Warren M (1999) Poleward shifts in
geographical ranges of butterfly species associated with regional
warming. Nature 399:579–583
Pauli JN, Buskirk SW, Williams ES, Edwards WH (2006) A plague
epizootic in the black-tailed prairie dog (Cynomys ludovicianus).
Journal of Wildlife Diseases 42:74–80
Pike DA, Mitchell CJ (2013) Burrow-dwelling ecosystem engineers
provide thermal refugia throughout the landscape. Animal
Conservation 16:694–703
Poje JE, Rocke TE, Samuel MD (2020) Impacts of environmental
conditions on fleas in black-tailed prairie dog burrows. Journal
of Vector Ecology 45:356–365
Poje JE, Rocke TE, Samuel MD (2022) Temperatures of black-
tailed prairie dog burrows through the U.S. Great Plains. U.S.
Geological Survey data release, https://doi.org/10.5066/P93TC
Y21.
Reichman O, Smith S (1990) Burrows and burrowing behavior by
mammals. Current Mammology 2:197–244
Richgels KLD, Russell RE, Bron GM, Rocke TE (2016) Evaluation
of Yersinia pestis transmission pathways for sylvatic plague in
prairie dog populations in the western U.S. EcoHealth 13:415–
427
Robinet C, Roques A (2010) Direct impacts of recent climate
warming on insect populations. Integrative Zoology 5:132–142
Rothschild M (1965) Myxomatosis and the rabbit flea. Nature
207:1162–1163
Russell RE, Abbott RC, Tripp DW, Rocke TE (2018) Local factors
associated with on-host flea distributions on prairie dog co-
lonies. Ecology and Evolution 8:8951–8972
Russell RE, Walsh DP, Samuel MD, Grunnill MD, Rocke TE
(2021) Space matters: host spatial structure and the dynamics of
plague transmission. Ecological Modelling .https://doi.org/
10.1016/j.ecolmodel.2021.109450
Salkeld DJ, Stapp P (2008) Prevalence and abundance of fleas in
black-tailed prairie dog burrows: implications for the trans-
M. D. Samuel et al.

mission of plague (Yersinia pestis). Journal of Parasitology
94:616–621
SAS Institute Inc. (2013) SAS/ACCESSÒ9.4 Interface to ADA-
BAS: Reference. Cary, NC: SAS Institute Inc.
Scheidt VJ (1988) Flea allergy dermatitis. Veterinary Clinics of
North America: Small Animal Practice 18:1023–1042
Schmidt-Nielsen K (1964) Desert Animals: Physiological Problems
of Heat and Water, New York: Oxford University Press
Sheets RG, Linder RL, Dahlgren RB (1971) Burrow systems of
prairie dogs in South Dakota. Journal of Mammalogy 52:451–
453
Shenbrot G, Krasnov B, Khokhlova I, Demidova T, Fielden L
(2002) Habitat-dependent differences in architecture and
microclimate of the burrows of Sundevall’s jird (Meriones
crassus) (Rodentia: Gerbillinae) in the Negev Desert, Israel.
Journal of Arid Environments 51:265–279
Silverman J, Rust MK, Reierson DA (1981) Influence of temper-
ature and humidity on survival and development of the cat flea,
Ctenocephalides felis (Siphonaptera: Pulicidae). Journal of Med-
ical Entomology 18:35–78
Stapp P (1998) A reevaluation of the role of prairie dogs in great
plains grasslands. Conservation Biology 12:1253–1259
Stapp P, Antolin MF, Ball M (2004) Patterns of extinction in
prairie dog metapopulations: plague outbreaks follow El Nin
˜o
events. Pages 235–240 in Frontiers in Ecology and the Environ-
ment, Ecological Society of America.
Tripp DW, Gage KL, Montenieri JA, Antolin MF (2009) Flea
abundance on black-tailed prairie dogs (Cynomys ludovicianus)
increases during plague epizootics. Vector-Borne and Zoonotic
Diseases 9:313–321
Tripp DW, Rocke TE, Runge JP, Abbott RC, Miller MW (2017)
Burrow dusting or oral vaccination prevents plague-associated
prairie dog colony collapse. Ecohealth 14:451–462
USFWS (2013) Recovery plan for the black-footed ferret (Mustela
nigripes). U.S. Fish and Wildlife Service Region 6, Denver, CO,
USA. 157 pp. http://www.fws.gov/endangered/species/recovery-
plans.html
Wilder AP, Eisen RJ, Bearden SW, Montenieri JA, Tripp DW,
Brinkerhoff RJ, Gage KL, Antolin MF (2008) Transmission
efficiency of two flea species (Oropsylla tuberculata cynomuris
and Oropsylla hirsuta) involved in plague epizootics among
prairie dogs. Ecohealth 205–12. doi: https://doi.org/10.1007/s10
393-008-0165-1. Epub 2008 Mar 25. PMID: 18787922.
Williams ES, Mills K, Kwiatkowski DR, Thorne ET, Boerger-Fields
A (1994) Plague in a Black-footed Ferret (Mustela nigripes).
Journal of Wildlife Diseases 30:581–585
Williams SK, Schotthoefer AM, Montenieri JA, Holmes JL, Vetter
SM, Gage KL, Bearden SW (2013) Effects of low-temperature
flea maintenance on the transmission of Yersinia pestis by
Oropsylla montana.Vector Borne Zoonotic Diseases 13:468–748
Wilson LT, Barnett WW (1983) Degree-days: an aid in crop and
pest management. California Agriculture 37:4–7
Yeruham I, Rosen S, Hadani A (1989) Mortality in calves, lambs
and kids caused by severe infestation with the cat flea Cteno-
cephalides felis felis (Bouche
´, 1835) in Israel. Veterinary Para-
sitology 30:351–356
Potential Effects of Environmental Conditions on Prairie Dog Flea Development