You are on page 1of 10

VECTOR-BORNE DISEASES, SURVEILLANCE, PREVENTION

Arthropod Vectors and Vector-Borne Bacterial Pathogens


in Yosemite National Park
KATRYNA A. FLEER,1,2 PATRICK FOLEY,3 LEE CALDER,3

AND

JANET E. FOLEY1

J. Med. Entomol. 48(1): 101110 (2011); DOI: 10.1603/ME10040

ABSTRACT Ticks, eas, and vector-borne pathogens were surveyed in diverse small mammals in
Yosemite National Park, California, from 2005 to 2007. A total of 450 unique captures of small mammals
was collected during a 3-yr period and yielded 16 species of eas and 10 species of ticks, including
known vectors of Anaplasma phagocytophilum and Borrelia burgdorferi and plague. Serology was
performed for A. phagocytophilum, spotted fever group Rickettsia spp., B. burgdorferi, and Yersinia
pestis. A. phagocytophilum exposure was identied in 12.1% of all wild small mammals tested, with
seropositive animals in 10 species, notably Beldings ground squirrels (Spermophilus beldingi), jumping
mice (Zapus princeps), and voles (Microtus sp.). Spotted fever group Rickettsia spp. exposure was
detected in 13.9% of all small mammals tested, with seropositive animals in eight species. Additionally,
37.0% of rodents in ve species tested were seropositive for B. burgdorferi. No individuals were
seropositive for Y. pestis. No animals were polymerase chain reaction positive for any pathogen tested.
These results provide baseline data for future research and prediction of emerging vector-borne
disease in Yosemite National Park, as well as adding to the known ranges and host species for tick and
eas in California.
KEY WORDS Anaplasma phagocytophilum, Borrelia species, eas, plague, ticks

Ticks and eas serve as vectors for numerous bacterial


pathogens that can cause disease in domestic animals,
wildlife, and humans. Small mammals are common
reservoirs for many of these pathogens and are important in both intra- and interspecic pathogen transmission. Some important examples include the
causative agents of Lyme disease, relapsing fever, tularemia, Rocky Mountain spotted fever, Q fever, ehrlichiosis, anaplasmosis, babesiosis, and plague. Diseases such as plague and tularemia in novel areas could
be especially devastating to small mammal populations, as they cause acute illness and death in susceptible small mammal species (Gage and Kosoy 2005,
Foley and Nieto 2010).
Yosemite National Park (YNP) spanning Tuolumne,
Mariposa, and Madera Counties, California, is an area
that could be highly impacted by tick- and ea-borne
disease. The park has high biodiversity of both plant and
animal species, with 1,338 reported plant species (23% of
total species in California) and 42 small mammal species
(47% of total species in California) (Grinnell and Storer
1924, Jameson and Peters 1988, Botti 2001), a phenomenon likely the result of a combination of factors, including diverse soil types, temporal and spatial temper1 Department of Medicine and Epidemiology, School of Veterinary
Medicine, University of California, Davis, CA 95616.
2 Corresponding author: Department of Medicine and Epidemiology, School of Veterinary Medicine, University of California, Davis,
CA 95616 (e-mail: kaeer@ucdavis.edu).
3 Department of Biological Sciences, California State University,
Sacramento, CA 95819.

ature variations, and a wide elevational range (6004,000


m). Extremely high numbers of tourists (3.5 million/
yr) visit YNP yearly, including children and pets (NPS
2008). Additionally, a number of vulnerable mammal
species inhabit YNP, including pika (Ochotona princeps),
Mount Lyell shrew (Sorex lyellii), and Sierra Nevada
bighorn sheep (Ovis canadensis). Both visiting tourists
and resident animals may suffer as a result of vectorborne disease. Important zoonoses that are likely to be a
risk to humans include plague, which occurred in a human YNP in 1959 (Kartman et al. 1966), and relapsing
fever, reported in YNP in the early 1990s (Smith 1992).
Comprehensive studies of small mammals, ticks, and
eas have not been reported for YNP; thus, the potential
for vector-borne disease there is not known.
Baseline knowledge of ectoparasites and disease
present in an area is essential for predicting and monitoring future outbreaks and dangers to humans, domestic animals, and wildlife. Plague and tularemia in
particular could be important threats to vulnerable
species of wildlife. Further data will be useful for
tracking effects of potential changes in disease prevalence that could occur as functions of changes in
climate and land use. The specic goals of this study
were to identify and catalog ticks and eas in YNP that
could impact wildlife and domestic animals; report
exposure to and infection with vector-borne pathogens found in the small mammals, ticks, and eas; and
compare ea diversity from YNP with that reported in
other major California studies.

0022-2585/11/01010110$04.00/0 2011 Entomological Society of America

102

JOURNAL OF MEDICAL ENTOMOLOGY

Table 1.

Location of field sites in YNP, California

Site

Elevation

UTM (N)

UTM (E)

Foresta
Hodgdon Meadows
Crane Flats
Porcupine Creek
Tuolumne Meadows
Dana Meadows

1,200
1,200
1,800
2,400
2,800
3,000

374220
374748
374631
374803
375208
375414

1194516
1195151
1194750
1193437
1192121
1191504

UTM, universal transverse mercator.

Materials and Methods


Two habitat types (meadow and forest) at each of
ve different elevations (1,200; 1,800; 2,400; 2,800; and
3,000 m above sea level) were chosen in YNP (Table
1). Sites were constrained to be within 200 m of a road
and 50 m of a hiking trail, to have adjacent forest and
meadow, and to t elevation requirements. An additional site (Hodgdon Meadow at 1,200 m) was added
to increase our sample size of California ground squirrels (Spermophilus beecheyi). Primary vegetation at
1,200 1,800 m elevation consisted of Ponderosa pine
(Pinus ponderosa), forest, and mixed grass meadow. At
2,800 and 3,000 m above sea level, Ponderosa pines
were replaced by lodgepole pines (Pinus contortus).
Small mammals, ticks, and eas were surveyed in each
location monthly from June through September of
20052007 to evaluate disease diversity and prevalence. One hundred Sherman live traps containing a
small amount of polyester nesting material were deployed during each sampling event in the evening (50
in the forest and 50 in the meadow), baited with oats,
and checked rst thing in the morning. Traps were
partially covered with soil or plant material for protection and camouage. The location of each successful trap was obtained using a global positioning system
device. Twenty Tomahawk live traps were deployed
each morning, baited with a mixture of peanut butter
and oats, and reset after each successful capture until
the afternoon. Small mammals were removed from
traps; either manually restrained (squirrels and chipmunks) or anesthetized with an intramuscular injection of 100 mg/kg ketamine and 10 mg/kg xylazine
(other small mammals); and identied to species, age,
and sex. A quantity amounting to 0.25 ml of blood was
taken from the lateral saphenous vein of squirrels and
chipmunks; other small mammals were bled retroorbitally into 1.0-ml ethylenediaminetetraacetic acid
tubes (BD Biosciences, Franklin Lakes, NJ). Whole
blood samples in ethylenediaminetetraacetic acid
were kept cool for the day, and then frozen until
transfer to the University of California (Davis, CA)
where they were maintained in a 80C freezer until
processing. Each small mammal was marked with an
ear tag and then monitored for hemostasis and/or
recovery from anesthesia. When fully recovered, small
mammals were rereleased at the capture site. Ticks
were removed with forceps, and eas were removed
by combing small mammals over a white sheet; both
were preserved in 70% ethanol. Each ea was cleared
by incubating in dilute KOH for 24 h, dehydrated in

Vol. 48, no. 1

an ethanol series (75, 85, 95, and 100% for 30 min


each), and then mounted in Euparal (BioQuip, Rancho Dominguez, CA). Each ea was identied to species using western North American taxonomic keys
(Stark 1958, Hubbard 1947, Lewis et al. 1988). Often
an individual small mammal yielded a large number of
eas that tended to be identical; in these cases, a
random sample of three was processed, with the rest
saved in 70% ethanol to be evaluated in the future,
particularly for individual animals with multiple ea
species. Ticks were identied to sex, stage, and species
using a western North American taxonomic key (Furman and Loomis 1984). Blood samples were taken via
cardiocentesis from roadkill, when available.
Serology was performed to assay for antibodies and
presumptive exposure to infectious pathogens. Plasma
was separated by centrifugation at 3,000 rpm for 10
min. Anti-Yersinia spp. V-antigen immunoglobulin G
was detected in an enzyme-linked immunosorbent
assay format (Anderson et al. 1996). Indirect uorescent assay (IFA) was performed for Anaplasma phagocytophilum, spotted fever group (SFG) Rickettsia spp.,
and Borrelia burgdorferi. Plasma was diluted in phosphate-buffered saline (PBS) at 1/25; applied to A.
phagocytophilum, Rickettsia rickettsii, or B. burgdorferi
(Barlough et al. 1995) antigen slides (VMRD, Pullman,
WA); and incubated at 37C with moisture for 30 min.
Slides were then washed three times in PBS and incubated with uorescein isothiocyanate-labeled rabbit anti-rat immunoglobulin G heavy and light chain
antibodies (Kirkegaard & Perry Laboratories, Gaithersburg, MD) diluted in PBS at 1/30. Slides were
washed three additional times and, during the third
wash, incubated with two drops of eriochrome black
for 2 min. Positive (previously tested woodrats and
chipmunks) and negative (water and negative rodent
serum) controls were included in each run. Samples
were considered positive if strong uorescence was
detected at dilutions of at least 25. All animals captured
in 2005 and all except Peromyscus spp. from 2006 and
2007 were tested for exposure to A. phagocytophilum,
based on our extensive prior data (Foley et al. 2008)
and rst year study results showing that Peromyscus
spp. were rarely exposed to A. phagocytophilum. A
random sampling from each species (50% of each, to
minimize costs) was tested for SFG Rickettsia spp.
exposure for all years. Borrelia spp. exposure was assessed in all sciurids, except that a random subset of
20% of Spermophilus spp. was tested because this sample was so large compared with other species. All small
mammals captured in 2005 were tested for exposure to
Yersinia pestis.
All seropositive small mammals were assessed for active infection by polymerase chain reaction (PCR).
Blood was extracted using a kit (Qiagen, Valencia, CA),
and quantitative PCR for A. phagocytophilum (Drazenovich et al. 2006) and SFG Rickettsia spp. (Leutenegger et al. 1999, Adjemian et al. 2008) was performed, as
previously described. Quantitative PCR for B. burgdorferi was done using the following primers: 304f, 5-GTCACACTGGAACTGAGATACGGT-3, and 394r, 5AGTGTCGCTCCGTCAGGCT-3, and the universal

0
0
0
0
0
0
0
0
0
0
1
0
1
0
0
0
0
0
2
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
1
1
0
0
0
0
0
2
0
0
0
0
0
0
1
0
0
0
1
0
0
0
0
0
0
0
2
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
1
0
1
0
1
0
2
0
6
0
0
0
0
4
0
0
0
0
0
14
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
1
1
0
2
0
0
0
0
1
3
0
0
0
0
0
0
0
0
0
7
Chaetodipus californicus (1)
Glaucomys sabrinus (8)
Homo sapiens (2)
Microtus californicus (2)
Microtus longicaudus (8)
Microtus montanus (26)
Peromyscus boylii (1)
Peromyscus maniculatus (137)
Peromyscus truei (6)
Sorex lyelli (4)
Sorex trowbridgii (1)
Spermophilus beecheyi (32)
Spermophilus beldingi (126)
Tamias alpinus (1)
Tamias minimus (1)
Tamias speciosus (7)
Thomomys monticola (5)
Zapus princeps (25)
Total

0
0
0
0
0
0
1
3
0
0
0
0
1
0
0
0
0
0
5

Ixodes
woodi
Ixodes
spinipalpis
Ixodes
sculptus
Ixodes
pacificus
Ixodes
kingi
Ixodes
hearli
Ixodes
angustus
Haemaphysalis
leporispalustris
Dermacentor
sp.
Dermacentor
occidentalis

Number of individuals of each small mammal species infested with various species of ticks from YNP, California

A total of 415 unique captures of small mammals


from 16 species was trapped between June 2005 and
September 2007 during 62 trapping events (9,560 trap
periods). The most frequently caught animals were
deer mice (Peromyscus sp.) (38% of all unique captures), ground squirrels (Spermophilus sp.) (37%),
voles (Microtus sp.) (9%), jumping mice (Zapus sp.)
(6%), and chipmunks (Tamias sp.) (3%). Rarely captured species were shrews (Sorex lyelii and Sorex trowbridgii), pocket gophers (Thomomys monticola), and
pocket mice (Chaetodipus californicus). Roadkill collections resulted in one yellow-bellied marmot (Marmota flaviventris) and one western gray squirrel (Sciurus griseus).
Ten tick species were identied on small mammals
(Table 2), including all stages of Dermacentor occidentalis and Ixodes angustus. Otherwise, all ticks collected were immature stages. Beldings ground squirrels (Spermophilus beldingi) had the greatest tick
diversity with seven different species (Table 2).
Eleven small mammal species examined had at least
one tick species identied (Table 2).
D. occidentalis was the most common tick identied
(49%), and was found to infest four small mammal
species (Table 2). Eighty-two percent of D. occidentalis were found at 1,200 m elevation. Haemaphysalis
leporispalustris, Ixodes kingi, Ixodes hearlei, and Ixodes
spinipalpis were found only at 2,800 m.
The Yosemite eas and their hosts are shown in
Tables 3 and 4. Our survey identied 464 eas from 378
rodent and ve shrew individuals. The 18 host species
harbored 16 species of eas from three families, as
follows: Hystrichopsyllidae (four species), Leptopsyllidae (two species), and Ceratophyllidae (10 species).
North American deer mice (Peromyscus maniculatus),
the most frequently collected mammal, had high ea
diversity with 148 eas from six species. Beldings

Table 2.

Results

Tick species
richness

probe library (UPL) probe, GTCACACTGGAACTGAGATACGGTCCAGACTCNGACTCTACGG


AGGCAGCAGCTAA GAATCTTCCGCAATGGGCGANAGCCTGACGGAGCGACACT (N. Nieto, unpublished data). Each 12-l reaction contained 5 l of
DNA, 1 TaqMan Universal Master Mix (Applied
Biosystems, Foster City, CA), 2 nmol each primer, and
400 pmol probe. The thermocycling conditions consisted of 50C for 2 min, 95C for 10 min, and 40 cycles
at 95C for 15 s, followed by 60C for 1 min. For all PCR
reactions, samples were considered positive if they
had a cycle threshold value 40 and characteristic
amplication plots.
Data were maintained in Excel (Microsoft, Redmond, WA) and analyzed with the statistical package
R (R-Development Core Team, http://www.r-project.org). For all tests, the cutoff for statistical significance was P 0.05. Descriptive statistics were done
to summarize seroprevalence and PCR prevalence for
each pathogen. Prevalence odds ratios (ORs) and 95%
condence intervals (CI) for each disease risk factor
were estimated using logistic regression.

103

1
1
1
1
0
1
2
4
1
0
2
1
7
0
0
0
0
0
22

FLEER ET AL.: VECTOR-BORNE DISEASE IN YOSEMITE NATIONAL PARK

Small mammal species


(no. examined)

January 2011

0
0
0
0
0
0
10
0
0
0
0
1
0
0
0
0
0
0
0

Callistopsyllus
terinus
0
0
0
1
0
0
6
0
0
0
0
0
0
0
0
0
0
0
0

Catallagia
s. sculleri
0
0
0
0
0
0
0
0
2
0
0
0
0
0
0
0
0
0
0

Corrodopsylla curuata
obtusata
0
0
0
0
0
0
0
0
0
0
0
2
0
4
0
0
0
0
0

Eumolpianus
eutamiadis
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
3
0
0
1

Foxella ignotus
recula

Opisodasys
vesperalis

0
2
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0

Small mammal species


(no. examined)

Chaetodipus californicus (1)


Glaucomys sabrinus (8)
Microtus californicus (2)
Microtus longicaudus (8)
Microtus montanus (26)
Peromyscus boylii (1)
Peromyscus maniculatus (130)
Peromyscus truei (6)
Sorex lyelli (4)
Sorex trowbridgii (1)
Spermophilus beecheyi (32)
Spermophilus beldingi (126)
Tamias alpinus (1)
Tamias minimus (1)
Tamias speciosus (6)
Thomomys bottae (2)
Thomomys monticola (5)
Zapus princeps (25)
Unknown

0
0
0
0
0
0
0
0
0
0
56
0
0
0
0
0
0
0
0

Oropsylla
montana
0
0
0
0
0
0
0
0
0
0
0
13
1
0
0
0
0
0
0

Oropsylla
t. tuberculata
0
0
0
0
0
0
13
0
0
0
0
1
0
0
0
0
0
0
0

Peromyscopsyllus hesperonomys
adelpha

0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0

Peromyscopsylla
selenis

0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0

Hystrichopsylla dippiei
heotomae

0
0
0
0
0
0
0
0
0
0
0
35
0
0
0
0
0
0
0

0
2
0
3
3
0
6
0
2
0
2
10
1
1
1
1
0
2

Flea species
richness

0
2
0
0
0
0
0
0
0
0
0
3
0
0
0
0
0
0
0

Ceratophyllus ciliatus
mononis

Thrassis francisi
sierrae

0
0
0
9
38
0
1
0
0
0
0
3
0
0
0
0
0
3
0

Megabothris
abantis

JOURNAL OF MEDICAL ENTOMOLOGY

0
0
0
0
0
0
0
0
0
0
0
94
0
0
0
0
0
0
0

Oropsylla
idahoensis

Number of individuals of each small mammal species infested with various species of fleas from YNP, California

0
0
0
5
6
0
116
0
0
0
1
5
0
0
1
0
0
1
1

Chaetodipus californicus (1)


Glaucomys sabrinus (8)
Microtus californicus (2)
Microtus longicaudus (8)
Microtus montanus (26)
Peromyscus boylii (1)
Peromyscus maniculatus (137)
Peromyscus truei (6)
Sorex lyelli (4)
Sorex trowbridgii (1)
Spermophilus beecheyi (32)
Spermophilus beldingi (126)
Tamias alpinus (1)
Tamias minimus (1)
Tamias speciosus (7)
Thomomys bottae (2)
Thomomys monticola (5)
Zapus princeps (25)
Unknown

Table 4.

Aetheca
wagneri

Number of individuals of each small mammal species infested with various species of fleas from YNP, California

Small mammal species


(no. examined)

Table 3.

104
Vol. 48, no. 1

January 2011
Table 5.

FLEER ET AL.: VECTOR-BORNE DISEASE IN YOSEMITE NATIONAL PARK

105

Small mammal-flea surveys of large sample size or conducted proximal to YNP, California

Locality

No. rodents collected

No. rodent species

No. eas collected

No. ea species

Citation

Hastings Reserve
San Diego County
Chuchupate
Plumas County
Yosemite
Morro Bay
Sagehen
Lava Beds

2,204
2,207
1,563
2,423
408
295
89
382

14
17
10
4
16
10
5
15

22,087
11,984
2,277
1,417
462
180
39
779

23
22
18
19
15
10
5
21

Linsdale and Davis 1956


Lang 2004
Davis et al. 2002
Jameson and Brennan 1957
Stark 1970
Nieto et al. 2007
Adjemian et al. 2008
Stark and Kinney 1969

ground squirrels were also commonly collected and


rich in eas, as follows: 158 eas from 10 species. The
California ground squirrel was less common in traps
and had much lower ea diversity, 56 Oropsylla montana and one Aetheca wagneri. The montane vole (Microtus montanus) was the third most frequently collected mammal, but was host for only a single species
of ea, Megabothris abantis, of which 38 were collected.
The most commonly collected ea was A. wagneri,
with 116 individuals on deer mice, and 16 more individuals scattered across seven host species. O. montana
and Oropsylla idahoensis were common, but only on
ground squirrels. Thrassis francisi sierrae showed a
similar pattern with 35 eas found only on Beldings
ground squirrels. M. abantis was common on voles and,
to a lesser extent, Beldings ground squirrels.
We have identied eight additional large or nearby
ea surveys performed in California (Table 5). Stark
mentions collecting eas in YNP in his monograph on
Thrassis (Stark 1970). Surveys of eas targeting areas
near YNP were conducted in Plumas County (Jameson and Brennan 1957) and Sagehen Creek (Nevada
County) (Adjemian et al. 2008). Hubbard reviewed
California eas from his home base in Oregon (Hubbard 1943). A very thorough study was performed by
Linsdale and Davis at Hastings Reserve in the central
Coast Range (Linsdale and Davis 1956). Public healthoriented surveys were done in the San Diego mountains (Lang 2004) and the Transverse Ranges at Chuchupate (Davis et al. 2002). The eight studies of Table
5 differed in their focus and methodology. Hastings
included all available mammals. The Plumas study
primarily trapped rodents and shrews. Three of the
studies collected almost only rodents. Sample size
across all studies clearly affects ea diversity, but it is
noteworthy that the YNP ea fauna is almost as diverse
as the much larger samples of Plumas County and
Chuchupate. Several ea species were readily collected in Yosemite, but not in other large mammal-ea
surveys in California (Table 6), including Callistopsyllus terinus, T. francisi sierrae, O. idahoensis, Oropsylla tuberculata, and Eumolpianus eutamiadis. M.
abantis was common in YNP, but very rare in a Plumas
County study (Jameson and Brennan 1957). However,
the common vole and deer mouse ea Malaraeus
telchinus was not found at YNP. This absence is, however, consistent with other collections (Auguston
1942, Hubbard 1947). The woodrat ea Orchopeas
sexdentatus was not collected in part because, despite

the presence of active houses, woodrats did not enter


the traps.
In addition to evaluating ectoparasites at YNP, we
evaluated animals directly for exposure and infection
with vector-borne pathogens. We used the low cutoff
value of 1:25 to increase sensitivity with using nonspecies-specic conjugate. Anti-rat conjugate was
used because specic conjugate for the species collected was not available. Seroprevalence for A. phagocytophilum ranged across host species from 0 to 100%,
with yellow-bellied marmots having the highest seroprevalence and Beldings ground squirrels having the
most seropositive individuals (Table 7). Spotted fever
group Rickettsia spp. seroprevalence ranged from 0 to
100%. The highest seroprevalence was found in brush
mice (Peromyscus boylii), whereas North American
deer mice had the overwhelming majority of seropositive individuals (Table 7). Seroprevalence of Borrelia
sp. ranged from 0 to 86% across host species, with
lodgepole chipmunks (Tamias speciosus) having the
highest seroprevalence and Beldings ground squirrels
with the highest number of infected individuals. No
animals tested positive for Y. pestis. Additionally, no
animals tested PCR positive for any pathogen.
Prevalence ORs signicantly different from 1 were
not observed for seropositivity for A. phagocytophilum,
SFG Rickettsia spp., or Borrelia spp. for altitude, habitat, species, or gender. Seroprevalence among years
differed signicantly for A. phagocytophilum (OR
2.0, 95% CI 1.23.2, P 0.004), with the highest prevalence in 2005 of 28%, followed by seroprevalence of
0.4 and 5.6% in 2006 and 2007, respectively. Years also
differed signicantly for SFG Rickettsia spp. seroprevalence (prevalence OR 1.6, 95% CI 1.12.2, P
0.009), from 1.4% in 2005, increasing to 10.3 and 13.0%
in 2006 and 2007, respectively. When the 3 yr of data
were lumped, A. phagocytophilum seropositivity differed by month of capture (prevalence OR 3.7, 95%
CI 1.113.2, P 0.009). No seropositive animals were
detected in June, only two (1.5%) in July, and 39
(23.3%) in August.
Discussion
Vector-borne disease maintenance in nature requires complex interactions among small mammals,
ectoparasites, and other ecological factors. The rich
small mammal fauna in YNP hosts a diversity of ectoparasites and shows susceptibility to multiple important vector-borne pathogens.

106
Table 6.

JOURNAL OF MEDICAL ENTOMOLOGY

Vol. 48, no. 1

Fleas reported from eight small mammal surveys in California


Flea species

Corrodopsylla curvata obtusata


Carteretta carteri
Anomiopsyllus congruens
Anomiopsyllus nudatus nudatus
Callistopsyllus terinus
Megarthroglossus sp. near divisus
Megarthroglossus sp. (Lava Beds)
Megarthroglossus procus
Catallagia luski
Catallagia mathesoni
Catallgia sculleri
Delotelis hollandi
Epitedia scapani
Epitedia wenmanni
Phalacropsylla allos
Meringis cummingi
Meringis parkeri
Atyphloceras multidentatus
Atyphloceras longipalpus
Hystrichopsylla dippei neotomae
Hystrichopsylla occidentalis linsdalei
Hystrichopsylla occidentalis occidentalis
Corypsylla kohlsii
Corypsylla ornata
Nearctopsylla hamata
Neactopsylla princei
Rhadinopsylla (Micropsylla) sectilis
Rhadinopsylla (Rectofrontia) fraterna
Ctenocephalides canis
Ctenocephalides felis
Echidnophaga gallinosa
Pulex irritans/simulans
Hoplopsyllus anomalus
Hoplopsyllus foxi
Cediopsylla inaequalis
Leptopsylla segnis
Odontopsyllus dentatus
Peromyscopsylla selenis
Peromyscopsylla hesperomys
Nosopsyllus fasciatus
Thrassis acamantis howelli
Thrassis francisi rockwoodi
Thrassis francisi sierrae
Oropsylla idahoensis
Oropsylla montana
Oropsylla tuberculata
Dactopsylla bluei
Foxella ignota
Malaraeus sinomus
Malaraeus telchinus
Amaradix biterootensis
Opisodasys keeni
Opisodasys vesperalis
Opisodasys nesiotus
Orchopeas latens
Orchopeas leucopus
Orchopeas sexdentatus
Aetheca wagneri
Ceratophyllus ciliatus mononis
Eumolpianus fornacis
Eumolpianus eumolpi
Eumolpianus eutamiadis
Megabothris abantis
Total

Lava
beds

Plumas

Sagehen

Yosemite

Hastings

Morro
Bay

198
171
1

Chuchupate

23
257

San
Diego
29
at least 2
215

11
267

14
4
19
1
23

18
10
22
6

123
81
2
1
10

1
1
1

28
198

28

4
14

206
4

10

26
26

121

14

1
22
1
1
8
3

1
2

16

607
3
44
1
4

11
131

1
14

50

4
391
1
2,516
7
8
237

8,353
3
4
251
1

224

37

45

44
22

8,192

15

792

7,537

101
28
18
21

35
94
56
14
19

17
1
310

695

17
607
1,806

2
63

93

21

333

5
2
10

168
6

93
11

6
20

27

18

847

2
1,417

131
5

1,053
156

1
4
21

72

39

6
66
462

22,087

293
204

567
13

117
1
180

2,277

11,948

Total
0
227
194
472
12
267
14
4
20
124
112
2
1
11
18
70
22
460
30
1
137
22
1
0
1
8
20
2
0
4
998
1
10,924
13
56
490
2
16
498
22
101
28
35
112
16,618
14
19
626
0
3,007
1
315
2
27
11
4
2,102
609
36
189
51
6
68
39,257

Based on data from references listed in Table 4.

Small mammal species captured at each site were


expected based on previous studies in nearby locations in YNP (Grinnell and Storer 1924, Moritz 2007).

Howevshrews) are more amenable to trapping usinger,


small mammal diversity was likely underrepresented in
this study because trapping methods were limited to live

January 2011
Table 7.

FLEER ET AL.: VECTOR-BORNE DISEASE IN YOSEMITE NATIONAL PARK

107

Results of serology for vector-borne pathogens in wild rodents in YNP, California


A. phagocytophilum

Chaetodipus californicus
Glaucomys sabrinus
Marmota flaviventris
Microtus californicus
Microtus longicaudus
Microtus montanus
Peromyscus boylii
P. maniculatus
Peromyscus truei
Sciurus griseus
Spermophilus beecheyi
Spermophilus beldingi
Tamias alpinus
Tamias minimus
Tamias speciosus
Thomomys monticola
Zapus princeps
Total

Borrelia spp.

Rickettsia spp.

Yersinia spp.

No. positive

No. tested

No. positive

No. tested

No. positive

No. tested

No. positive

No. tested

0 (0%)
0 (0%)
1 (100%)
1 (50%)
3 (42.86)
6 (22.2)
0 (0%)
2 (1.53%)
0 (0%)
0 (0%)
1 (3.45%)
18 (18.56)
0 (0%)
0 (0%)
2 (28.57)
2 (40%)
6 (28.57)
42 (12.1%)

1
8
1
2
7
27
1
131
5
1
29
97
4
0
7
5
21
347

0 (0%)
3 (42.86%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
2 (25%)
8 (47.06)
1 (25%)
0 (0%)
6 (54.54%)
0 (0%)
0 (0%)
20 (37.03%)

0
7
1
0
0
0
0
0
0
1
8
17
8
1
11
0
0
54

0 (0%)
1 (16.67%)
0 (0%)
0 (0%)
1 (14.29%)
0 (0%)
1 (100%)
20 (28.57%)
0 (0%)
0 (0%)
4 (13.79%)
0 (0%)
0 (0%)
0 (0%)
3 (42.86%)
1 (20%)
3 (15.79%)
34 (13.93%)

1
6
1
1
7
24
1
70
5
1
29
62
5
0
7
5
19
244

0 (0%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)

1
2
1
0
7
10
0
24
4
0
11
30
0
0
1
3
5
99

traps, and some species (e.g., voles and shrews) are more
amenable to trapping using other methods such as pitfall
traps. YNP has 33 rodent and shrew species listed within
its boundaries (www.nps.gov/yose/naturescience/
mammal-species-list.htm). We captured 16 of these in
our study, as well as two species of shrews. We did not
capture the nonnative Rattus rattus, Mus musculus, and
Castor canadensis. Several large native rodents, Erethizon dorsatum, Aplodontia rufa, Neotoma cinerea, Neotoma macrotis, Marmota flaviventris, and Spermophilus
lateralis, as well as the arboreal squirrels Sciurus griseus
and Tamiasciurus douglassii, also avoided our traps,
which is a problem that previously has been reported
(Nieto and Foley 2008). Thus, the species included in
this study could have resulted in an underestimate of
ectoparasite numbers and diversity, as well as disease
prevalence. Beldings ground squirrel and deer mouse
abundance may have been overrepresented because
of large population size and ease of capture.
Overall tick numbers observed on small mammals
were relatively low compared with other sites in California (Nieto et al. 2007, Adjemian et al. 2008, Foley
et al. 2008). North American deer mice had greatest
tick loads, possibly because they are such common
generalists present at nearly every location. The high
tick diversity on Beldings ground squirrels was previously unreported (Furman and Loomis 1984), including many species of nidicolous ticks (I. angustus,
Ixodes hearli, I. kingi, I. spinipalpis, and Ixodes woodi).
Chipmunks had no evidence of ticks, in contrast to our
published data in the Coast Range Mountains (Nieto
and Foley 2009). This may be because many of the
sites we sampled were relatively dry and at higher
altitude, which are inappropriate conditions for many
ticks, or because chipmunk capture numbers were
low. Small numbers of human-biting ticks (Ixodes
pacificus, I. angustus, Dermacentor andersoni) were
recovered, suggesting a possible risk of some tickborne disease in humans and their pets. However,
further work to evaluate the role of nidicolous and
specialist ticks in disease ecology is warranted. Spe-

cically, many species of nidicolous ticks occurred on


rodents, but the relevance of most of these tick species
for vector-borne disease transmission is unknown. Importantly, prior research has documented roles for
several host specialist ticks in the ecology of R. rickettsii. For example, much work was done early in the
20th century to understand the ecology of Rocky
Mountain spotted fever (Parker 1923), and, in particular, the rabbit tick, H. leporispalustris, has been shown
to be a competent vector for some SFG rickettsiae
(Freitas et al. 2009, Parker 1923) even though American SFG rickettsiae from H. leporispalustris are generally minimally pathogenic.
YNP eas have been largely unstudied, with the
exception of Starks monograph on Thrassis in YNP
(Stark 1970). An analysis of his collection would
complement our study. Overall, the entire California ea fauna has received sporadic attention. California ea communities appear to be at the intersection of three ea faunas, as follows: a Pacic
Northwestern fauna well described in Lewis et al.
(1988), an intermontane fauna best examined in
Stark (1958), and a Southwestern fauna that still
needs attention. This can be seen roughly in Ceratophyllid distribution maps (Traub et al. 1983). For
example, the chipmunk ea Ceratophyllus ciliatus
mononis extends along the Sierra Nevada to desert
mountains in Southern California, whereas Eumolpianus c. protinus extends from northern California
to coastal Alaska, and Eumolpianus c. kincaidi inhabits Idaho and Utah. The pocket gopher ea Dactylopsylla bluei bluei is on the central California
coast, whereas Dactylopsylla b. psila is found near
Los Angeles and Las Vegas. Often the same ea
species occupies the Pacic Coast and interior
mountains such as the deer mouse ea Opisodasys
keeni, whereas Opisodasys nesiotus inhabits the central to southern California coast. Certainly there are
other eas in YNP besides those we assessed, as a
result of sampling size, season, and host targets, but

108

JOURNAL OF MEDICAL ENTOMOLOGY

our other data are consistent with very high ea


biodiversity.
The high abundance and diversity of ectoparasites
suggest a high risk of enzootic vector-borne disease. In
fact, data did reveal exposure to multiple vector-borne
pathogens, although in a few cases, imperfect sensitivity or specicity of the test was unfortunate. For all
serological assays, wildlife species-specic secondary
conjugates were not available and the use of anti-rat
antibodies could have resulted in some reduction of
sensitivity of the test. For the IFAs, we used a relatively concentrated secondary antibody for all host
species (based on our prior results and in-house protocols; data not shown), in part to maximize sensitivity
and for consistency in assays among species. Specicity would be unlikely to be affected, especially in light
of the complete lack of uorescence on negative controls. For the anti-Y. pestis enzyme-linked immunosorbent assay, a recombinant antigen was used in part
because of availability of the antigen and to allow us
to detect any F1-negative strains to which animals
could have been exposed. The sensitivity of this assay
for wildlife also was likely affected by the lack of
species-specic secondary antibodies. Thus, data for
these serological tests could potentially be underestimates of the actual prevalence.
A. phagocytophilum is a tick-vectored bacterial
pathogen that causes granulocytic anaplasmosis in humans, dogs, and horses (Madigan and Gribble 1987,
Dumler et al. 1995, Foley et al. 2001). Symptoms of
infection are often nonspecic, including fever and
thrombocytopenia, and can range from mild to severe
or fatal. A. phagocytophilum seroprevalence in this
study (12.1%) was comparable to other sites in California (Foley et al. 2008). It was interesting that the
prevalence increased so dramatically from June (0%)
to August (23%), suggesting that some important vector was infecting most individuals early to midsummer.
California tick species known to be competent for
transmitting A. phagocytophilum are I. pacificus (Richter et al. 1996) and I. spinipalpis (Zeidner et al. 2000),
both of which were collected in this study. There is
some speculation that I. angustus, a common tick species collected at all elevations and a known tick vector
for Lyme disease (Peavey et al. 2000), could also be
vector competent for A. phagocytophilum (Foley et al.
2008). Disease seroprevalence in this study was much
higher in locations with more I. angustus, suggesting
that this species may play a role in the cycle of this
pathogen in YNP. Ten small mammal species were
seropositive for this pathogen, although species per se
was not a statistically signicant risk factor for seropositivity. The upper value of 100% seropositivity is
biased because the only marmot tested was seropositive. It is not known whether other species of
Anaplasma exist that may cross-react with A. phagocytophilum in our serologic test, but it is interesting to
speculate that this may be true, because seropositive
individuals were found above the normal elevational
range for this pathogen. Further research should be
done to identify PCR or cell culture-positive individuals so a conrmatory DNA sequence can be obtained.

Vol. 48, no. 1

Tissue PCR may have been more sensitive than blood


PCR because infection in the blood may be intermittent, but could not be performed within the scope of
this study.
Spotted fever group Rickettsia spp., transmitted by
Dermacentor sp. tick vectors, are rickettsial pathogens
that cause disease in humans, dogs, and occasionally
cats. R. rickettsii is the causative agent of Rocky Mountain spotted fever, the most common rickettsial pathogen in North America (Adjemian et al. 2009), but
several nonpathogenic rickettsias (e.g., R. montana, R.
peacockii, R. rhipicephali) also exist that may crossreact in the IFA test used in this study (Marshall et al.
2003). Moreover, a commonly detected Rickettsia sp.
in D. occidentalis, designated 364D, has been shown
recently to cause disease in people (Shapiro et al.
2010). Further species differentiation can be attained
with PCR, but because no samples were PCR positive
for SFG Rickettsia spp., we could not distinguish between different species. Dermacentor sp. ticks were
collected at most locations with animals seropositive
for SFG Rickettsia spp., but were occasionally found in
locations where no seropositive individuals were collected. The upper value of 100% seropositivity is biased because the only brush deer mouse tested was
seropositive. Further research should also be done in
YNP to identify PCR and tissue culture-positive animals, to elucidate which SFG Rickettsia sp. is involved
in this location and potentially provide bacterial isolates for further study.
Borrelia spp. in California can roughly be divided
into two main groups, as follows: relapsing fever Borrelia spp., which are vectored by soft ticks or lice and
cause undulating fever eventually leading to central
nervous system involvement; and B. burgdorferi sensu
lato, hard tick-vectored spirochete bacterial pathogens that cause u-like symptoms and thrombocytopenia in humans, dogs, cats, and potentially other
wildlife species. B. burgdorferi sensu stricto causes
Lyme disease, the most common vector-borne disease
in North America. Lyme disease is treatable in acute
stages, but can become chronic and debilitating if left
untreated. Chronic symptoms can include arthritis,
nervous system disorders, and gastrointestinal disease
(Brown and Lane 1992). Certain species of Borrelia
that cause relapsing fever (e.g., B. hermsii, B. parkeri,
B. turicatae, B. duttonii) can cross-react with B. burgdorferi in our IFA test, but specicity of this test also
is low because of reaction with heat shock and other
host proteins (Bruckbauer et al. 1992, Magnarelli et al.
1987). Because no samples were PCR positive, further
species differentiation could not be achieved, but
based on the location and elevation of seropositive
animals, it is possible that some of these animals were
exposed to a relapsing fever Borrelia sp., especially
because chipmunks are the known reservoir for relapsing fever in California (Dworkin et al. 2002).
Although plague is endemic in several montane
communities of California (Davis et al. 2002, Adjemian
et al. 2006, Foley and Foley 2010), it was not apparent
in YNP. Key factors that maintain plague are a controversial, ecologically complicated problem (Gage

January 2011

FLEER ET AL.: VECTOR-BORNE DISEASE IN YOSEMITE NATIONAL PARK

and Kosoy 2005), but there is some evidence that a


higher diversity rodent-ea community is important,
at least in California (Foley et al. 2007, Foley and Foley
2010). More specically, diversity increases plague
persistence because of the availability of new susceptible rodents at different times during the year (host
phenological variation), additional potential hosts
(host abundance), and plague transmission-competent eas with multiple hosts (vector exibility).
Plague is known to be present in YNP based on an
earlier case report (Nelson 1980, Smith 1994). Given
the fairly high rodent and ea diversity of Yosemite,
we might expect a higher prevalence of plague in the
current study. The lack of plague could be the result
of test insensitivity, a local historic accident by which
infection in local populations we sampled had recently
become extinct and not yet been reintroduced, or lack
of detection with our sample size if prevalence was
low. Alternatively, there could be some consistent
homogenizing factor (such as highly mobile carnivores) that has deprived YNP of the structural heterogeneity needed for endemicity.
Overall, YNP shows evidence of exposure to at least
three important vector-borne pathogens, which has
important implications for public health and conservation medicine. The high ea and tick diversity on
seropositive hosts would suggest ongoing enzootic disease in sylvatic cycles that are poorly understood.
More research dening competent vectors and reservoirs for these pathogens, and conrming the identities of Borrelia spp. and SFG Rickettsia spp., is warranted. Nevertheless, in this study, we establish
important baseline data for vectors and pathogens in
YNP.
Acknowledgments
We thank Jennifer Dike, Haleh Siahpolo, Jennifer Glavis,
and Jeff Maurer for support of eld work; Niki Drazenovich,
Nathan Nieto, Nat Lim, Jennifer Gorman, Joy Worth, and
Raymond Wong for assistance in the laboratory; and Jan
VanWagtendonk for assistance with housing and background
literature access. This work was supported by the Geraldine
R. Dodge Foundation and the University of California Davis
Center for Vector-Borne Disease.

References Cited
Adjemian, J., E. Girvetz, and J. Foley. 2006. Analysis of the
GARP modeling approach for predicting the distributions
of eas implicated as vectors of plague, Yersinia pestis, in
California. J. Med. Entomol. 43: 93103.
Adjemian, J. Z., M. K. Adjemian, P. Foley, B. B. Chomel, R. W.
Kasten, and J. E. Foley. 2008. Evidence of multiple zoonotic agents in a wild rodent community in the eastern
Sierra Nevada. J. Wildl. Dis. 44: 737742.
Adjemian, J., J. Krebs, E. Mandel, and J. McQuiston. 2009.
Spatial clustering by disease severity among reported
Rocky Mountain spotted fever cases in the United States,
20012005. Am. J. Trop. Med. Hyg. 80: 7277.
Anderson, G. W., Jr., S. E. Leary, E. D. Williamson, R. W.
Titball, S. L. Welkos, P. L. Worsham, and A. M. Friedlander. 1996. Recombinant V antigen protects mice
against pneumonic and bubonic plague caused by F1-

109

capsule-positive and -negative strains of Yersinia pestis.


Infect. Immun. 64: 4580 4585.
Auguston, G. F. 1942. Ectoparasite-host records from the
Sierran region of east central California. Bull. South. Calif.
Acad. Sci. 40: 146 157.
Barlough, J. E., J. E. Madigan, E. DeRock, and J.D.a.J. Bakken.
1995. Protection against Ehrlichia equi is conferred by
prior infection with the human granulocytotropic Ehrlichia (HGE agent). J. Clin. Microbiol. 33: 33333334.
Botti, S. J. 2001. An Illustrated Flora of Yosemite National
Park. Yosemite Association/Heyday Books.
Brown, R. N., and R. S. Lane. 1992. Lyme disease in California: a novel enzootic transmission cycle of Borrelia
burgdorferi. Science 256: 1439 1442.
Bruckbauer, H. R., V. Preac-Mursic, R. Fuchs, and B. Wilske.
1992. Cross-reactive proteins of Borrelia burgdorferi.
Eur. J. Clin. Microbiol. Infect. Dis. 11: 224 232.
Davis, R. M., R. T. Smith, M. B. Madon, and E. Sitko-Cleugh.
2002. Flea, rodent, and plague ecology at Chuchupate
Campground, Ventura County, California. J. Vector Ecol.
27: 107127.
Drazenovich, N. L., R. N. Brown, and J. E. Foley. 2006. Use
of real-time quantitative PCR targeting the msp2 protein
gene to identify cryptic Anaplasma phagocytophilum infections in wildlife and domestic animals. Vector Borne
Zoonotic Dis. 6: 8390.
Dumler, S. J., K. M. Asanovich, J. S. Bakken, P. Richter, R.
Kimsey, and J. E. Madigan. 1995. Serologic cross-reactions among Ehrlichia equi, Ehrlichia phagocytophila, and
human granulocytic Ehrlichia. J. Clin. Microbiol. 33:
1098 1103.
Dworkin, M. S., P. C. Shoemaker, C. L. Fritz, M. E. Dowell,
and D. E. Anderson, Jr. 2002. The epidemiology of tickborne relapsing fever in the United States. Am. J. Trop.
Med. Hyg. 66: 753758.
Foley, P., and J. Foley. 2010. Modeling SIR dynamics and
plague persistence in California rodent-ea communities.
Vector Borne Zoonotic Dis. 10(1): 59 67.
Foley, J. E., and N. C. Nieto. 2010. Tularemia. Vet. Microbiol. 140: 332338.
Foley, J. E., P. Foley, and J. E. Madigan. 2001. The distribution of granulocytic Ehrlichia seroreactive dogs in California. Am. J. Vet. Res. 62: 1599 1605.
Foley, J. E., J. Zipser, B. Chomel, E. Girvetz, and P. Foley.
2007. Modeling plague persistence in host-vector communities in California. J. Wildl. Dis. 43: 408 424.
Foley, J. E., N. C. Nieto, J. Adjemian, H. Dabritz, and R. N.
Brown. 2008. Anaplasma phagocytophilum infection in
small mammal hosts of Ixodes ticks, western United States.
Emerg. Infect. Dis. 14: 11471150.
Freitas, L. H., J. L. Faccini, and M. B. Labruna. 2009. Experimental infection of the rabbit tick, Haemaphysalis
leporispalustris, with the bacterium Rickettsia rickettsii,
and comparative biology of infected and uninfected tick
lineages. Exp. Appl. Acarol. 47: 321345.
Furman, D. P., and E. C. Loomis. 1984. The Ticks of California (Acari: Ixodida). University of California Press,
Berkeley, CA.
Gage, K., and M. Kosoy. 2005. Natural history of plague:
perspectives from more than a century of research. Annu.
Rev. Entomol. 50: 505528.
Grinnell, J., and T. I. Storer. 1924. Animal Life in the Yosemite. University of California Press, Berkeley, CA.
Hubbard, C. 1943. The eas of California. Pacic University
Bulletin 39: 112.
Hubbard, C. 1947. Fleas of Western North America.
Hafner, New York, NY.

110

JOURNAL OF MEDICAL ENTOMOLOGY

Jameson, E. W., and J. M. Brennan. 1957. An environmental


analysis of some ectoparasites of small forest animals in
the Sierra Nevada, California. Ecol. Monogr. 27: 4554.
Jameson, E. J., and H. Peters. 1988. California Mammals.
University of California Press, Berkeley, CA.
Kartman, L., M. I. Goldenberg, and W. Hubbert. 1966. Recent observations on the epidemiology of plague in the
United States. Am. J. Public Health 56: 1554 1569.
Lang, J. 2004. Rodent-ea-plague relationships at the higher
elevations of San Diego County. J. Vector Ecol. 29: 236
247.
Leutenegger, C. M., N. Pusterla, C. N. Mislin, R. Weber, and
H. Lutz. 1999. Molecular evidence of coinfection of
ticks with Borrelia burgdorferi sensu lato and the human
granulocytic ehrlichiosis agent in Switzerland. J. Clin.
Microbiol. 37: 3390 3391.
Lewis, R., J. Lewis, and C. Maser. 1988. The Fleas of the
Pacic Northwest. Oregon State University Press, Corvallis, OR.
Linsdale, J., and B. Davis. 1956. Taxonomic appraisal and
occurrence of eas at the Hastings Reservation in Central
California. Univ. Calif. Publ. Zool. 54: 293370.
Madigan, J. E., and D. Gribble. 1987. Equine ehrlichiosis in
northern California: 49 cases (1968 1981). J. Am. Vet.
Med. Assoc. 190: 445 448.
Magnarelli, L., J. Anderson, and R. Johnson. 1987. Crossreactivity in serological tests for Lyme disease and other
spirochetal infections. J. Infect. Dis. 156: 183188.
Marshall, G., G. Stout, R. Jacobs, G. Schutze, H. Paxton, S.
Buckingham, J. DeVincenzo, M. Jackson, V. S. Joaquin, S.
Standaert, and C. Woods. 2003. Antibodies reactive to
Rickettsia rickettsii among children living in the southeast
and south central regions of the United States. Arch.
Pediatr. Adolesc. Med. 157: 443 448.
Moritz, C. 2007. Final Report: A Re-survey of the Historic
Grinnell-Storer Vertebrate Transect in Yosemite National Park, California. Sierra Nevada Network, Berkeley,
CA.
[NPS] National Park Service. 2008. Yosemite National Park
Statistics.
(http://www.nps.gov/yose/naturescience/
park-statistics.htm).
Nelson, B. 1980. Plague studies in California: the roles of
various species of sylvatic rodents in plague. Proc. Vertebr. Pest Conf. 9: 89 96.
Nieto, N. C., and J. E. Foley. 2008. Evaluation of squirrels
(Rodentia: Sciuridae) as ecologically signicant hosts for
Anaplasma phagocytophilum in California. J. Med. Entomol. 45: 763769.
Nieto, N. C., and J. E. Foley. 2009. Reservoir competence of
the redwood chipmunk (Tamias ochrogenys) for
Anaplasma phagocytophilum. Vector Borne Zoonotic Dis.
9: 573577.

Vol. 48, no. 1

Nieto, N., P. Foley, L. Calder, H. Dabritz, J. Adjemian, P. A.


Conrad, and J. Foley. 2007. Ectoparasite diversity and
exposure to vector-borne disease agents in wild rodents
in central coastal California. J. Med. Entomol. 44: 328
335.
Parker, R. 1923. Transmission of Rocky Mountain spotted
fever rickettsiae from the rabbit tick Haemaphysalis leporis-palustris Packard. Public Health Rep. 66: 455 463.
Peavey, C. A., R. S. Lane, and T. Damrow. 2000. Vector
competence of Ixodes angustus (Acari: Ixodidae) for Borrelia burgdorferi sensu stricto. Exp. Appl. Acarol. 24:
77 84.
Richter, P. J., R. B. Kimsey, J. E. Madigan, J. E. Barlough, J. S.
Dumler, and D. L. Brooks. 1996. Ixodes pacificus (Acari:
Ixodidae) as a vector of Ehrlichia equi (Rickettsiales:
Ehrlichieae). J. Med. Entomol. 33: 15.
Shapiro, M. R., C. L. Fritz, K. Tait, C. D. Paddock, W. L.
Nicholson, K. F. Abramowicz, S. E. Karpathy, G. A. Dasch,
J. W. Sumner, P. V. Aden et al. 2010. Rickettsia 364D: a
newly recognized cause of eschar-associated illness in
California. Clin. Infect. Dis. 50(4): 541548.
Smith, C. R. 1992. Rodent disease implications associates
with campgrounds and public use areas in California, pp.
258 260. In J. E. Borrecco and R. E. Marsh (eds.), Proceedings of the Fifteenth Vertebrate Pest Conference,
Newport Beach, CA. University of California, Davis, CA.
Smith, C. R. 1994. Wild carnivores as plague indicators in
California: a cooperative interagency disease surveillance
program, pp. 192199. In W. Halverson and A. Crabb
(eds.), Proceedings of the Sixteenth Vertebrate Pest Conference, Santa Clara, CA. University of California, Davis,
CA.
Stark, H. 1958. The Siphonaptera of Utah: Their Taxonomy,
Distribution, Host Relations, and Medical Importance.
U.S. Department of Health, Education, and Welfare,
Communicable Disease Center, Atlanta, GA.
Stark, H. 1970. A Revision of the Flea Genus Thrassis Jordan
1933 with Observations on Ecology and Relationship to
Plague. University of California Press, Berkeley, CA.
Stark, H., and A. Kinney. 1969. Abundance of rodents and
eas as related to plague in Lava Beds National Monument, California. J. Med. Entomol. 6: 287294.
Traub, R., M. Rothschild, and J. Haddow. 1983. The Ceratophyllidae: Key to the Genera and Host Relationships.
Academic, London, United Kingdom.
Zeidner, N. S., T. R. Burkot, R. Massung, W. L. Nicholson,
M. C. Dolan, J. S. Rutherford, B. J. Biggerstaff, and G. O.
Maupin. 2000. Transmission of the agent of human granulocytic ehrlichiosis by Ixodes spinipalpis ticks: evidence
of an enzootic cycle of dual infection with Borrelia burgdorferi in Northern Colorado. J. Infect. Dis. 182: 616 619.
Received 17 February 2010; accepted 2 September 2010.