Ecography 000: 000000, 2008
doi: 10.1111/j.2008.0906-7590.05336.x
# 2008 The Authors. Journal compilation # 2008 Ecography
Subject Editor: Douglas Kelt. Accepted 7 May 2008
Prairie dog presence affects occurrence patterns of disease vectors
on small mammals
R. Jory Brinkerhoff, Chris Ray, Bala Thiagarajan, Sharon K. Collinge, Jack F. Cully, Jr,
Brian Holmes and Kenneth L. Gage
R. J. Brinkerhoff (robert.brinkerhoff@colorado.edu) and C. Ray, Dept of Ecology and Evolutionary Biology, Univ. of Colorado, 334 UCB,
Boulder, CO 80309-0334, USA. B. Thiagarajan and J. F. Cully, Jr, Division of Biology, 204 Leasure Hall, Kansas State Univ., Manhattan,
KS 66056, USA. S. K. Collinge, Dept of Ecology and Evolutionary Biology and Environmental Studies Program, Univ. of Colorado, 334
UCB, Boulder, CO 80309-0334, USA. B. Holmes, 220 East Market Street, Meeker, CO 81641, USA. K. L. Gage, Bacterial Zoonoses
Branch, Division of Vector-Borne Infectious Diseases, Centers for Disease Control, Fort Collins, CO 80523, USA.
Wildlife disease is recognized as a burgeoning threat to imperiled species and aspects of host and vector community
ecology have been shown to have significant effects on disease dynamics. The black-tailed prairie dog is a species of
conservation concern that is highly susceptible to plague, a flea-transmitted disease. Prairie dogs (Cynomys) alter the
grassland communities in which they exist and have been shown to affect populations of small rodents, which
are purported disease reservoirs. To explore potential ecological effects of black-tailed prairie dogs on plague dynamics,
we quantified flea occurrence patterns on small mammals in the presence and absence of prairie dogs at 8 study areas
across their geographic range. Small mammals sampled from prairie dog colonies showed significantly higher flea
prevalence, flea abundance, and relative flea species richness than those sampled from off-colony sites. Successful plague
transmission likely is dependent on high prevalence and abundance of fleas that can serve as competent vectors. Prairie
dogs may therefore facilitate the maintenance of plague by increasing flea occurrence on potential plague reservoir species.
Our data demonstrate the previously unreported ecological influence of prairie dogs on vector species assemblages, which
could influence disease dynamics.
Dynamics and persistence of vector-borne infectious diseases depend on the communities of hosts and vectors in
which they occur (Keesing et al. 2006). Theoretical studies
of host-parasite systems indicate that host and parasite
population dynamics can determine whether or not a
parasite will establish and what conditions are necessary
for its persistence (Anderson and May 1978, Holt et al.
2003). Recent investigations have demonstrated that the
composition of the host community for a given pathogen or
vector can influence parasite establishment (Holt et al.
2003) and disease dynamics (Ostfeld and Keesing 2000,
Schmidt and Ostfeld 2001). It is less appreciated, however,
that certain members of the host community may directly
or indirectly influence vector prevalence and abundance on
other species (Collinge et al. 2008).
The black-tailed prairie dog Cynomys ludovicianus is an
excellent model for exploring effects of a disease host on
vector occurrence. Cynomys ludovicianus is highly susceptible to infection by the bacterium Yersinia pestis (Cully and
Williams 2001), a flea-transmitted pathogen that is thought
to be maintained by partially resistant rodents and their
fleas (Gage and Kosoy 2005). Prairie dog presence in
grassland ecosystems can influence plant and animal
community composition; prairie dogs alter soil properties
(Carlson and White 1987), change nutrient cycling
dynamics (Whicker and Detling 1988), and influence
both plant (Whicker and Detling 1988, Winter et al.
2002) and animal community structure (Smith and
Lomolino 2004, Collinge et al. 2008). In particular, prairie
dogs have been shown to significantly alter mammal species
assemblages (Agnew et al. 1986), though these effects may
not be generalizable across study systems. In some cases,
small mammal abundance is higher in the presence of
prairie dogs, though species richness is lower (Agnew et al.
1986, Cully et al. unpubl.). Other researchers, however,
have found contrasting patterns (Ceballos et al. 1999) or
have failed to find any relationship between prairie dog
presence and small mammal community composition
(Stapp 2007).
We evaluated the effect of prairie dog presence on
disease vector occurrence by comparing vector assemblages
on small mammals in the presence and absence of
C. ludovicianus across a wide geographical range (Fig. 1).
For the purposes of this study, we define ‘‘small mammals’’
Online Early (OE): 1-OE
Charles M. Russell National Wildlife Refuge, MT
Badlands National Park, SD
Thunder Basin National Grasslands, WY
Wind Cave National Park, SD
Boulder County, CO
Comanche National Grasslands, CO
Cimarron National Grasslands, KS
Janos, Chihuahua, MX
Figure 1. Map showing the approximate historical range of black-tailed prairie dogs (shaded region) and the locations of the 8 study
areas.
as non-prairie dog rodents that can be captured using 7.6 8.9 22.9 cm aluminum live traps. The likelihood of interand intraspecific Y. pestis transmission among mammals is
dependent on the prevalence and abundance of fleas
(Lorange et al. 2005) and may also be influenced by the
flea species assemblage, as flea species vary in their
competence as vectors (Perry and Fetherston 1997, Gage
and Kosoy 2005, Krasnov et al. 2006a). When highly
susceptible hosts, such as black-tailed prairie dogs, become
infected, an epizootic event may be triggered (Perry and
Fetherston 1997).
Prairie dog burrows provide habitat and refuge for a
wide variety of vertebrate and invertebrate species, including
arthropods (Bangert and Slobodchikoff 2006, Davidson
and Lightfoot 2007), herptiles (Shipley and Reading 2006),
birds (Smith and Lomolino 2004), and mammals (Agnew
et al. 1986, Shipley and Reading 2006, Collinge et al.
2008). Mammal burrows may serve to increase heterogeneity of microclimates, leading to higher overall arthropod species richness and diversity (Davidson and Lightfoot
2007). Fleas in particular may benefit from the stable
microclimate within a burrow as flea development and
survival are highly dependent on temperature and relative
humidity (Rust and Dryden 1997, Krasnov et al. 2001). If
the abundance and richness of fleas were higher on prairie
dog colonies, then small mammals on colonies would be
expected to carry more fleas and more flea species than
identical mammal species sampled at off-colony grassland
sites. Under this scenario, the transmission of flea-borne
diseases would be facilitated on prairie dog colonies for at
least 2 reasons. First, higher flea prevalence leads to more
frequent host-switching (Bossard 2006), increasing the
potential for interspecific pathogen transmission. Second,
associations among flea species tend to be facilitative rather
2-OE
than competitive (Brinkerhoff et al. 2006, Krasnov et al.
2006b), so an increase in flea species abundance and
richness should increase per-capita rates of flea-mediated
pathogen transmission as hosts acquire higher and more
speciose flea loads.
The specific role of fleas in the transmission of plague
among prairie dogs is unclear. The dominant paradigm for
flea-mediated plague transmission requires that a biofilm
blockage containing Y. pestis is formed in a flea’s proventriculus, causing regurgitation of subsequent blood meals,
thereby increasing the likelihood of Y. pestis transmission
(Gage and Kosoy 2005). However, Webb et al. (2006)
demonstrated with an epidemiological model that plague
epizootics in prairie dogs are not driven by blocked fleas.
Unblocked fleas are capable of spreading plague and earlyphase transmission by unblocked fleas may explain the
epizootic patterns that are observed in nature (Eisen et al.
2006, Wilder et al. 2008). Transmission models for
blocked and unblocked fleas indicate that higher flea
prevalence and abundance (Lorange et al. 2005, Eisen
et al. 2006) increase the likelihood of Y. pestis spread, yet
the effects of prairie dogs on flea occurrence are largely
unstudied. We explored the effects of prairie dogs on small
mammal flea assemblages by recording flea occurrence at
on- and off-prairie dog colony sites spanning the range of
C. ludovicianus in the western Great Plains of North
America. We examined patterns of flea prevalence, abundance, intensity, and relative species richness between
site types (on- versus off-colony) at 8 study areas across
the range of C. ludovicianus (Fig. 1). We also investigated
the similarity of flea communities among the 8 study areas
and modeled the similarity of flea assemblages as a function
of geographic distance.
Methods
Flea collection
We collected fleas from live-caught small mammals at 8
study areas: 1) Badlands National Park, South Dakota, 2)
Wind Cave National Park, South Dakota, 3) Thunder
Basin National Grasslands, Wyoming, 4) Comanche National Grasslands, Colorado, 5) Cimarron National Grasslands, Kansas, 6) Janos, Chihuahua, Mexico, 7) Boulder
County, Colorado, and 8) Charles M. Russell National
Wildlife Refuge, Montana (Fig. 1). Small mammal trapping
at all areas occurred between May and September 2003. At
each study area, trapping grids were set on active prairie dog
colonies (on-colony sites) and within similar grassland sites
located 5002000 m from prairie dog colonies (off-colony
sites). Similar numbers of on- and off-colony sites were
sampled, though replication varied among study areas; we
sampled 4 pairs of grids at study areas 1 and 2, 6 pairs at
areas 36, 20 pairs at area 7 and 25 on- and 30 off-colony
grids at area 8. We used square trapping grids at study
areas 17 consisting of 49 Sherman live-traps (7.6 8.9 22.9 cm; H. B. Sherman Traps, Tallahassee, FL) spaced at
20 m intervals. At area 8, a square trapping grid consisting
of 100 traps was used with traps placed at 10 m intervals.
All traps were set in the evening and checked between
06:00 and 10:00 the following morning. Grids at study
areas 16 were trapped for 3 successive nights and grids at
areas 7 and 8 were trapped for 4 successive nights. To
facilitate handling and collection of ectoparasites, we
anesthetized all captured animals using vaporized Isoflurane
(Halocarbon Products Corporation, River Edge, NJ).
Anesthesia was administered at areas 16 using SurgiVet
vaporizer (SurgiVet, Waukesha, WI). At areas 7 and 8, the
anesthetic was dispersed from wetted cottonballs placed
inside a transparent anesthetizing chamber. We collected
fleas both from the host’s body by brushing through the
pelage with a toothbrush (all areas) and from the anesthetizing chamber (areas 7 and 8 only) using forceps. Fleas
from each captured host were stored in a 2% saline solution
containing a small amount of the surfactant Tween
(polysorbate) 80. Fleas were identified to species using
keys presented in Hubbard (1947). In addition to ectoparasite data, we recorded host species identification, sex,
weight, and length measurements. We marked individuals
with either uniquely numbered aluminum eartags (study
areas 16) or with batch marks by shaving a patch of fur
from the hindquarters (areas 7 and 8).
Analytical methods
We calculated values for flea prevalence (proportion of hosts
infested), flea abundance (number of fleas divided by
number of hosts), and flea intensity (number of fleas
divided by number of infested hosts), as well as numbers of
flea and mammal species sampled at each study area by
averaging across trapping grids. To test for effects of prairie
dog presence and study area on flea occurrence, we used
mixed-model ANOVAs, each of which consisted of 3
independent variables: prairie dog presence or absence
(fixed, 2 levels), study area (random, 8 levels), and an
interaction term. We used separate tests for each dependent
variable: flea prevalence, flea abundance, flea intensity, and
the ratio of flea-to-mammal species richness at each
grid. The denominator degrees of freedom for each F-test
in the mixed-model ANOVAs were calculated using
Satterthwaite’s method (Satterthwaite 1946) in JMP 4.04
(SAS Inst., Cary, NC). Because latitude has been shown to
influence parasite occurrence (Lindenfours et al. 2007), we
used linear regression to test for influence of latitude on flea
and mammal species richness across our study areas. In
order to determine if flea species richness is a function of
mammal trapping effort, we regressed trapping effort
(number of trap-nights) against flea species richness at
each study area. To determine effects of colony presence
that may be independent of host species richness, we
calculated the ratio of flea species to small mammal species
from each of our trapping grids and compared these values
both among study areas and between on- and off-colony
sites. To control for differential effects of small rodent
species on flea occurrence, we tested for differences in flea
prevalence, abundance, and relative flea species richness on
the most commonly caught mammal species, Peromyscus
maniculatus, across the 8 study areas, and between on- and
off-colony sites. Peromyscus maniculatus did not always
occur at both on- and off-colony grids at each study area, so
mixed-model ANOVA was not applied. Instead, we used
2-sample t-tests to compare flea occurrence (prevalence,
abundance, and intensity) at on- and off-colony sites and
1-way ANOVA to compare flea occurrence on P. maniculatus across study areas. We used t-tests to account for
variation among study areas dues to differences in sampling
effort.
To compare flea species assemblages among our study
sites, we used Sorenson’s similarity index. We used a
randomized Monte-Carlo Mantel test to relate flea assemblage dissimilarity (1 S) and geographical distance. We
also used non-metric multidimensional scaling (NMS) to
graphically assess the similarity of flea assemblages among
study areas. The ordination was generated using the
Sorenson (Bray-Curtis) distance metric, beginning with a
random starting configuration of study areas and minimizing final stress (lack of fit) after 50 runs with the real data
set. Dimensionality was determined by comparison of the
ordination generated from real data to a randomized data
set generated by Monte Carlo simulation.
Results
We collected 2444 fleas representing 19 species from 2373
small mammals across the 8 study areas (Table 1). In
addition to capturing rodents, we also trapped juvenile
desert cottontails at study areas 7 and 8 (Supplementary
material, Table S1). Although traps were set overnight, we
trapped a number of diurnal rodent species, including 2
ground squirrel species and 1 chipmunk species (Supplementary material, Table S1). Absolute flea species richness
was highest at the CM Russell study area (12 species) and
lowest at the Janos study area (4 species). The number of
flea species collected from on- and off-prairie dog colony
grids was generally equivalent at each study area, though the
flea species composition varied depending on prairie dog
3-OE
466
377
843
4
32
412
44
6
5
2
1
60
224
1
8
8
29
7
45
158
1
31
1
70
7
113
5
17
1
1
1
52
5
77
279
2
28
55
24
1
15
207
15
156
363
6
164
3
1
1
3
10
4
380
1
4
8
22
12
27
4
3
6
5
27
13
0
1
2
6
2
0
4
5
4
24
110
1
2
2
26
1
86
160
10
202
15
0
17
11
Aetheca wagneri*
Amaradix euphorbi
Callistopsyllus deuterus
Callistopsyllus terinus
Cediopsylla inaequalis
Corrodopsylla curvata
Echidnophaga gallinacea
Epitedia wenmanni
Eumolpianus eumolpi*
Foxella ignota*
Malareus telchinus*
Meringis arachis
Meringis parkeri
Orchopeas leucopus*
O. sexdentatus*
Oropsylla hirsuta*
Peromyscopsylla hesperomys*
Pleochaetis exilis*
Thrassis fotus*
Total
Study area total
54
On
Off
On
39
10
1
1
9
21
3
17
1
2
3
14
On
Off
Off
On
2
6
270
1
395
24
353
36
133
125
158
Off
On
Off
On
Off
On
Off
On
Off
Russell (8)
Boulder (7)
Wind Cave (6)
Thunder Basin (5)
Janos (4)
Comanche (3)
Cimarron (2)
Badlands (1)
Flea species
Table 1. List of flea species collected from each study area. Asterisks indicate fleas that have been found naturally infected with Y. pestis (Pollitzer and Meyer 1961).
4-OE
presence or absence (Table 1). Although variable among our
study areas, trapping effort was not a significant predictor of
number of flea species sampled among our study areas
(linear regression, r2 0.34, p0.1). The variation in flea
collection techniques at study areas 7 and 8 did not result in
abnormally high flea prevalence or abundance (prevalence:
t 0.66, p0.51; abundance: t 0.89, p 0.38).
Flea prevalence and abundance, as well as the ratio of flea
species to small mammal species, differed significantly
among study areas (prevalence: F7, 7 5.78, p 0.017;
abundance: F7, 7 4.61, p0.031; flea-to-mammal species
ratio; F7, 7 5.94, p 0.016) and between on- and offcolony trapping locations (prevalence: F1, 13 9.64, p 0.008; abundance: F1, 13 13.16, p0.003; flea-to-mammal species ratio; F1, 13 7.92, p 0.015. Mean flea
intensity did not vary by site (F7, 7 1.88, p0.21) or as
a function of prairie dog presence (F1, 13 1.05, p0.33).
Flea prevalence and abundance, as well as the ratio of flea
species to small mammal species, were all significantly
higher in the presence of prairie dogs (Fig. 2). The
interaction between study area and prairie dog presence
did not significantly affect any dependent variable (prevalence: F7, 138 1.06, p 0.39; abundance: F7, 138 1.03,
p0.41; intensity: F7, 138 2.0, p0.06; flea-to-mammal
species ratio; F7, 138 1.17, p0.33). Latitude was not a
significant predictor of mammal species richness among our
study areas (adjusted r2 0.0, p 0.6) but was a significant
predictor of flea species richness (adjusted r2 0.44, p
0.045). The flea-to-mammal species richness ratio, however, was not significantly influenced by latitude (adjusted
r2 0.37, p0.07).
Peromyscus maniculatus occurred at all of our study areas
and at 136 of 159 trapping grids (65 on-colony grids and
71 off-colony grids). The relative abundance of P. maniculatus ranged from 0 to 95% among study areas (Table 3).
Averaged across study areas, flea prevalence, abundance, and
intensity were significantly higher on P. maniculatus
sampled at prairie dog colony sites (prevalence: t 2.26, p 0.026; abundance: t2.53, p 0.013;
intensity: t 2.13, p 0.035); the number of flea species
collected from P. maniculatus, however, did not vary
depending on prairie dog presence (number of flea species;
t 0.64, p0.52). Study area significantly was a
significant predictor of flea prevalence (F7, 128 3.64,
p0.001), abundance (F7, 128 3.19, p0.004), intensity
(F7, 128 3.32, p 0.002), as well as the number of
flea species sampled (F7, 128 6.16, pB0.001) from
P. maniculatus.
Sorenson’s similarity indices were lowest (0.11) between
the CM Russell (Montana) and Cimarron (Kansas) study
areas and were highest (0.92) between the Comanche
(Colorado) and Badlands (South Dakota) study areas. A
randomized Monte Carlo Mantel test indicated a significant
positive relationship between flea assemblage dissimilarity
and geographical distance (r 0.67, p0.005; Fig. 3).
Non-metric multidimensional scaling (NMS) resulted in a
2-dimensional representation of flea assemblages by study
area (Fig. 4). Ordination stress of the real data set was
reduced substantially after 16 iterations and reached its
minimum value of 2.89 after 39 iterations; ordinations with
stress values B5 are considered highly robust representations of the dataset (McCune and Grace 2002). R-squared
Figure 2. Differences in flea prevalence (a), flea abundance (b), flea intensity (c), and flea-to-mammal species ratio (d) between on-colony
and off-colony sites averaged across all trapping grids at all 8 study areas. Bars represent mean values; error bars represent standard error.
Statistical significance as described in the text is generated from mixed-model ANOVA analysis.
values between Sorenson’s distance and axes 1 and 2 were
0.179 and 0.754, respectively, and explain a total of 93% of
the variance between distance in the ordination space and
distance in the original data set.
Discussion
The presence of prairie dogs is significantly associated with
differences in metrics of flea occurrence on small mammals;
fleas were more prevalent and present in higher abundance
on small mammals associated with black-tailed prairie dog
colonies. Furthermore, relative flea species richness, measured as the ratio of flea to mammal species at a sampling
grid, was significantly higher in the presence of prairie dogs.
Given that plague, the disease caused by the bacterium
Yersinia pestis, is reliant on high levels of flea prevalence and
abundance for successful transmission (Lorange et al. 2005),
the presence of prairie dogs in grassland ecosystems may
affect disease dynamics in ways that increase the probability
of epizootic events. Dozens of flea species have been found
to be naturally infected with Y. pestis (Pollitzer and Meyer
1961, Gage and Kosoy 2005), including several which are
present in our study system (Table 1), and increased flea
abundance may be associated with higher rates of plague
transmission (Krasnov et al. 2006a). Thus, the ecological
effect of prairie dog colonies on small mammal fleas may
ultimately lead to higher probability and rate of plague
transmission to and among prairie dogs.
Potential causes of increased flea occurrence on
small mammals
The mechanisms by which prairie dog presence increases
flea prevalence, abundance, and relative species richness are
unclear, but may be related to the role of prairie dogs as
ecological engineers. Prairie dog burrows provide habitat
and refuge for other vertebrate species and the presence of
prairie dogs increases arthropod species richness in grassland
ecosystems (Davidson and Lightfoot 2007). Flea development and survival is highly sensitive to ambient conditions
such as temperature and relative humidity (Rust and
Dryden 1997, Krasnov et al. 2001) and the burrow network
created by prairie dogs may mediate microclimatic conditions in ways that are favorable to fleas (Krasnov et al.
1997).
Presence of prairie dogs may increase (Shipley and
Reading 2006) or decrease (Agnew et al. 1986) local small
mammal species diversity, although small mammal abundance in this study system is higher in the presence of
prairie dogs (Collinge et al. 2008). In this study system, the
higher overall abundance of rodents, including prairie dogs,
at prairie dog colony sites could result in higher flea
prevalence and abundance; increased overall host availability could lead to higher flea fitness and therefore greater flea
populations. However, this hypothesis contradicts previous
studies that show a negative or no relationship between
small mammal abundance and flea prevalence and abundance (Stanko et al. 2002, 2006). Such variation in results
could be due to differences in focal mammal communities;
social animals may be more likely to share ectoparasites than
non-social animals (Brown and Brown 1996), potentially
resulting in higher parasite prevalence and abundance. The
propensity of fleas to switch hosts is dependent on both flea
and host species identities and fleas are more likely to switch
among ecologically and taxonomically similar hosts (Traub
1985). Thus, the species composition of the local mammalian host community is likely to influence the rate at which
fleas parasitize non-characteristic hosts, potentially altering
flea prevalence and abundance.
In this study system, small mammal species richness
generally is lower at on-colony sites than at off-colony
sites (Collinge et al. 2008). Relative to small rodent species
richness, we have shown that flea species richness is
significantly higher in the presence of prairie dogs (Fig.
2). One potential explanation for this phenomenon is
that small rodents at prairie dog colony sites acquire prairie
5-OE
6-OE
Table 2. Numbers of rodents and fleas sampled at each study area. Flea occurrence metrics (prevalence, abundance, and intensity) are averaged across all on- or off-colony grids at each study area.
Badlands (1)
Number of rodents sampled
Number of rodent species sampled
Number of flea species sampled
Number of fleas collected
Mean flea prevalence
Mean flea abundance
Mean flea intensity
Cimarron (2)
Comanche (3)
Janos (4)
Thunder Basin (5)
Wind Cave (6)
Boulder (7)
Russell (8)
On
Off
On
Off
On
Off
On
Off
On
Off
On
Off
On
Off
On
Off
103
5
6
86
0.5
0.84
1.64
40
5
4
24
0.2
0.5
1.6
86
9
4
202
0.58
1.88
3.26
91
9
6
77
0.5
0.7
1.6
57
7
6
113
0.61
1.84
2.82
62
6
5
45
0.4
0.8
1.9
22
4
3
27
0.39
1.36
1.81
68
7
4
28
0.1
0.4
4.2
150
4
6
207
0.57
1.31
2.38
155
5
7
156
0.4
0.9
2
140
1
4
164
0.37
1.17
3.19
37
4
6
60
0.6
1.5
2.3
525
4
4
380
0.35
0.73
2.1
191
7
4
32
0.14
0.17
1.12
248
4
6
466
0.64
1.77
2.5
398
8
12
377
0.4
1
2
Table 3. Average flea prevalence, abundance, and intensity on Peromyscus maniculatus at each study area.
Number of P. maniculatus sampled
Relative abundance of P. maniculatus
Mean flea prevalence
Mean flea abundance
Mean flea intensity
Badlands (1)
Cimarron (2)
Comanche (3)
Janos (4)
Thunder Basin (5)
Wind Cave (6)
Boulder (7)
Russell (8)
On
Off
On
Off
On
Off
On
Off
On
Off
On
Off
On
Off
On
Off
78
0.76
0.53
1.02
1.89
22
0.6
0.18
0.38
1.0
19
0.22
0.17
0.36
32.0
27
0.30
0.39
0.74
2.0
1
0.02
1.0
1.0
1.0
33
0.53
0.30
0.64
1.66
0
0
0
0
0
2
0.03
0
0
0
48
0.32
0.53
1.32
2.5
55
0.35
0.36
0.94
2.5
51
0.36
0.39
1.26
3.55
22
0.59
0.75
1.54
2.04
497
0.95
0.32
0.68
1.7
117
0.61
0.19
0.22
1.18
220
0.89
0.60
1.54
2.15
342
0.86
0.41
0.89
1.89
Figure 3. Relationship between linear distance and flea community dissimilarity among the 8 study areas. Dissimilarity was
calculated as 1-S, where S is the Sorensen’s similarity index value
for each pair of study areas.
dog-specific fleas, which they would otherwise not encounter. Our data indicate that this is a plausible explanation; small rodents sampled from on-colony grids at 4
of our study areas harbored a total of 54 Oropsylla hirsuta,
the most common warm-season flea of C. ludovicianus
(Table 1). Oropsylla hirsuta is rarely collected from nonprairie dog mammal species (Brinkerhoff unpubl.) and
prairie dogs rarely acquire fleas typical of other mammal
species (Brinkerhoff et al. 2006). However, it is possible
that the relatively high mammal biomass associated with
prairie dog colonies makes these unusual host-switching
events slightly more common.
Because host sampling effort may confound measures of
parasite species richness (Guegan and Kennedy 1996),
Russell
1.0
Thunder Basin
Axis 2
Wind Cave
Boulder
0
Badlands
Comanche
Cimarron
-1.0
Janos
-2.0
1.0
0
-1.0
Axis 1
Figure 4. NMS ordination of pairwise similarity values generated
from flea species presence/absence data for each of the 8 study
areas. Study areas that are closer geographically have more similar
small mammal flea assemblages. Axes represent NMS scores for
each study area.
within-species measures of parasite richness and occurrence
may be more reliable than measures summed across
multiple host species (Stanko et al. 2002). Given that
sampling effort was not a predictor of flea species richness,
we are confident that our samples accurately represent the
flea species assemblages at each study area. However,
mammal species vary in their suitability as hosts for fleas
(Krasnov et al. 2004), so it is likely that variation in
mammal communities among our sites influences flea
occurrence. Analysis of the most frequently encountered
host in our study system, P. maniculatus, demonstrated that
flea prevalence and abundance on this species were
significantly higher on prairie dog colonies than at offcolony grassland sites even though the relative abundance of
P. maniculatus was highly variable across study areas (Table
3). The number of flea species collected from P. maniculatus, however, did not differ between on- and off-colony
sites. Although both prairie dog presence and study areas
were significantly associated with differences in flea occurrence on P. maniculatus, the probabilities associated with
these factors were lower for the latter than the former;
additionally, flea prevalence at 2 study areas (Cimarron and
Wind Cave) was greater on off-colony P. maniculatus,
suggesting that flea occurrence on this species is more
strongly influenced by locality than by the presence of
prairie dogs.
Consequences of high flea prevalence and abundance
Parasite intensity is positively related to consequences of
infestation. Although fleas tend not to cause direct mortality
of their hosts (Traub 1985), they are vectors of a variety of
pathogens (Shaw et al. 2004). High flea prevalence leads to
higher flea species exchange among hosts (Bossard 2006)
and a higher rate of flea species exchange could increase
the probability of inter-species pathogen transmission.
Because Y. pestis is a highly virulent pathogen and vector
competence often is very low, transmission is thought to
require high flea prevalence and abundance, even when
many susceptible hosts are available (Lorange et al. 2005).
Krasnov et al. (2006a) determined that there is a positive
relationship between the abundance of a flea species on its
host and its efficacy as a plague vector. Thus, the rapid
spread of plague among prairie dogs could be at least partly
due to the fact that flea prevalence and abundance on small
mammals at on-colony sites is inflated relative to off-colony
grassland sites.
Most North American flea species have traditionally
been considered to be poor vectors of plague because they
rarely form proventricular blockages (Pollitzer and Meyer
1961, Gage and Kosoy 2005). However, a number of flea
species, including Oropsylla hirsuta, have recently been
found to transmit Y. pestis without forming blockages
(Eisen et al. 2006, Wilder et al. 2008). Thus, traditional
assumptions about which fleas are effective plague vectors
may preclude complete understanding of plague transmission dynamics. It is likely that a number of small rodent flea
species may be competent plague vectors, spreading the
bacterium by way of early phase transmission (Eisen et al.
2006). If this is the case, increased flea prevalence and
abundance, irrespective of flea species identities, may lead to
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higher rates of plague transmission within and among
mammal species. The impact of plague on most wild
mammals in North America is unknown (Gage and Kosoy
2005), but it has dramatic negative effects on prairie dogs.
Plague spreads quickly among prairie dog colonies, results
in nearly 100% mortality (Biggins and Kosoy 2001, Cully
and Williams 2001), and reduces prairie dog genetic
variation (Trudeau et al. 2004). Cynomys ludovicianus
recently was removed from the candidate list of endangered
species (Anon. 2004) but it is still a species of conservation
concern given that the historical range occupied by this
species has been diminished by 98% in the last 100 yr
(Miller and Cully 2001).
Regional variation in flea occurrence
Flea prevalence, abundance, and relative flea species richness
on small mammal hosts varied significantly among our
study sites indicating that factors other than presence of
prairie dogs are important determinants of flea occurrence.
The mammal communities among the 8 study areas are
highly variable (Collinge et al. 2008; Supplementary
material, Table S1) and this variation is likely to account
for some of the spatial heterogeneity in flea assemblages
given that fleas tend to be strongly host-specific. However,
geographical distance also significantly influences flea
species assemblages in western North America (Fig. 3).
The fact that the NMS ordination closely mirrors the
geographical dispersion of the study area locations (Fig. 1,
4) suggests that factors associated with geography may be
determinants of flea species assemblages; flea species
assemblages are known to vary spatially due to factors
such as environmental conditions (Rust and Dryden 1997,
Krasnov et al. 1997) and host geographic range (Krasnov
et al. 2005).
Latitude was a significant predictor of flea, but not
mammal, species richness in this study system. This result
contrasts with the finding that primates at lower latitudes
showed higher diversity of protozoan parasites than primates at higher latitudes (Nunn et al. 2005) but is
consistent with the idea that flea assemblages vary spatially
depending on host community (Stanko et al. 2002), local
environmental conditions (Krasnov et al. 1997), or other
factors (Krasnov et al. 2005). It is possible that the variation
in flea collection techniques led to significant differences in
flea occurrence metrics, though substantial variation in flea
prevalence, abundance, and intensity was found among
study areas where methods were identical (Table 2). Given
the sensitivity of fleas to temperature and humidity, it is
reasonable to expect that temporal variation in sampling
could influence flea occurrence. Indeed, significant variation among study areas in flea occurrence could stem from
local climatological processes rather than inherent differences associated with each study area. However, with one
exception, each study area was sampled for a minimum of 7
weeks, which should have accounted for day-to-day
fluctuations in temperature and humidity. Study area 4
(Janos) was sampled for only 1 week and, as a result, the
sample size from this study area is relatively small (Table 2).
However, the flea occurrence metric values from this site are
within the range of values from all sites.
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We have demonstrated heretofore unrecognized associations between prairie dog presence and occurrence patterns
of small mammal fleas. The mechanistic link between
prairie dog presence and flea occurrence is unclear, though
we suggest that higher flea prevalence and abundance on
small mammals at prairie dog colony sites could affect
transmission dynamics of Y. pestis and other flea-borne
pathogens. Higher flea prevalence and abundance among
small mammals on prairie dog colonies may lead to
increased rates of host-switching by fleas (Bossard 2006)
and higher probability of plague transmission (Krasnov
et al. 2006a). In some systems, prairie dogs decrease small
mammal species diversity but increase overall small mammal abundance (Agnew et al. 1986, Ray and Collinge 2006,
Collinge et al. 2008). Given that the relative abundance of
particular pathogen hosts or reservoirs can influence the
force of pathogen transmission (Ostfeld and Keesing 2000,
Schmidt and Ostfeld 2001), the cumulative effects of prairie
dogs on small mammals and their fleas serves to alter the
dynamics of plague transmission and lead to epizootic
events.
Acknowledgements We thank the land management agencies that
granted us permission to perform the field work associated with
this study. These include the National Park Service, Boulder City
Open Space and Mountain Parks, Boulder County Parks and
Open Space, Jefferson County Open Space, and the Colorado
Division of Wildlife. In particular, we thank B. Kenner,
D. Roddy, D. Foster, D. Augustine, A. Chappell, T. Byer,
C. Lockerman, M. Brennan, B. Pritchett, and C. Richardson for
their logistical support. We would also like to thank our many
field assistants for their hard work, including W. Davis, C. Pope,
T. Johnson, B. Erie, M. Campbell, D. Stetson, D. Conlin, and
A. Markeson. This research was supported by grants from the
National Center for Environmental Research STAR program of
the US-EPA (R-82909101-0), the NSF/NIH joint program in
Ecology of Infectious Diseases (DEB-0224328), and the USGS
Species at Risk Program. Comments made by 3 anonymous
reviewers greatly improved this manuscript.
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Download the Supplementary material as file E5336 from
Bwww.oikos.ekol.lu.se/appendix .
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