arthropod vectors and vector-borne bacterial pathogens

VECTOR-BORNE DISEASES, SURVEILLANCE, PREVENTION

Arthropod Vectors and Vector-Borne Bacterial Pathogensin Yosemite National Park

KATRYNA A. FLEER,1,2 PATRICK FOLEY,3 LEE CALDER,3 AND JANET E. FOLEY1

J. Med. Entomol. 48(1): 101Ð110 (2011); DOI: 10.1603/ME10040

ABSTRACT Ticks, ßeas, and vector-borne pathogens were surveyed in diverse small mammals inYosemite National Park, California, from 2005 to 2007. A total of 450 unique captures of small mammalswas collected during a 3-yr period and yielded 16 species of ßeas and 10 species of ticks, includingknown vectors of Anaplasma phagocytophilum and Borrelia burgdorferi and plague. Serology wasperformed for A. phagocytophilum, spotted fever group Rickettsia spp., B. burgdorferi, and Yersiniapestis. A. phagocytophilum exposure was identiÞed in 12.1% of all wild small mammals tested, withseropositive animals in 10 species, notably BeldingÕs ground squirrels (Spermophilus beldingi), jumpingmice (Zapus princeps), and voles (Microtus sp.). Spotted fever group Rickettsia spp. exposure wasdetected in 13.9% of all small mammals tested, with seropositive animals in eight species. Additionally,37.0% of rodents in Þve species tested were seropositive for B. burgdorferi. No individuals wereseropositive forY. 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-bornedisease in Yosemite National Park, as well as adding to the known ranges and host species for tick andßeas in California.

KEY WORDS Anaplasma phagocytophilum, Borrelia species, ßeas, plague, ticks

Ticks and ßeas serve as vectors for numerous bacterialpathogens that can cause disease in domestic animals,wildlife, and humans. Small mammals are commonreservoirs for many of these pathogens and are im-portant in both intra- and interspeciÞc pathogen trans-mission. Some important examples include thecausative agents of Lyme disease, relapsing fever, tu-laremia, Rocky Mountain spotted fever, Q fever, ehr-lichiosis, anaplasmosis, babesiosis, and plague. Dis-eases such as plague and tularemia in novel areas couldbe especially devastating to small mammal popula-tions, as they cause acute illness and death in suscep-tible small mammal species (Gage and Kosoy 2005,Foley and Nieto 2010).

Yosemite National Park (YNP) spanning Tuolumne,Mariposa, and Madera Counties, California, is an areathat could be highly impacted by tick- and ßea-bornedisease. The park has high biodiversity of both plant andanimal species, with 1,338 reported plant species (23% oftotal species in California) and 42 small mammal species(47% of total species in California) (Grinnell and Storer1924, Jameson and Peters 1988, Botti 2001), a phenom-enon likely the result of a combination of factors, in-cluding diverse soil types, temporal and spatial temper-

aturevariations,andawideelevational range(600Ð4,000m). Extremely high numbers of tourists (�3.5 million/yr) visit YNP yearly, including children and pets (NPS2008). Additionally, a number of vulnerable mammalspecies inhabitYNP, includingpika(Ochotonaprinceps),Mount Lyell shrew (Sorex lyellii), and Sierra Nevadabighorn sheep (Ovis canadensis). Both visiting touristsand resident animals may suffer as a result of vector-borne disease. Important zoonoses that are likely to be arisk to humans include plague, which occurred in a hu-man YNP in 1959 (Kartman et al. 1966), and relapsingfever, reported in YNP in the early 1990s (Smith 1992).Comprehensive studies of small mammals, ticks, andßeas have not been reported for YNP; thus, the potentialfor vector-borne disease there is not known.

Baseline knowledge of ectoparasites and diseasepresent in an area is essential for predicting and mon-itoring future outbreaks and dangers to humans, do-mestic animals, and wildlife. Plague and tularemia inparticular could be important threats to vulnerablespecies of wildlife. Further data will be useful fortracking effects of potential changes in disease prev-alence that could occur as functions of changes inclimate and land use. The speciÞc goals of this studywere to identify and catalog ticks and ßeas in YNP thatcould impact wildlife and domestic animals; reportexposure to and infection with vector-borne patho-gens found in the small mammals, ticks, and ßeas; andcompare ßea diversity from YNP with that reported inother major California studies.

1 Department of Medicine and Epidemiology, School of VeterinaryMedicine, University of California, Davis, CA 95616.

2 Corresponding author: Department of Medicine and Epidemiol-ogy, School of Veterinary Medicine, University of California, Davis,CA 95616 (e-mail: kaß[email protected]).

3 Department of Biological Sciences, California State University,Sacramento, CA 95819.

0022-2585/11/0101Ð0110$04.00/0 � 2011 Entomological Society of America

Materials and Methods

Two habitat types (meadow and forest) at each ofÞve different elevations (1,200; 1,800; 2,400; 2,800; and3,000 m above sea level) were chosen in YNP (Table1). Sites were constrained to be within 200 m of a roadand 50 m of a hiking trail, to have adjacent forest andmeadow, and to Þt elevation requirements. An addi-tional site (Hodgdon Meadow at 1,200 m) was addedto increase our sample size of California ground squir-rels (Spermophilus beecheyi). Primary vegetation at1,200Ð1,800 m elevation consisted of Ponderosa pine(Pinus ponderosa), forest, and mixed grass meadow. At2,800 and 3,000 m above sea level, Ponderosa pineswere replaced by lodgepole pines (Pinus contortus).Small mammals, ticks, and ßeas were surveyed in eachlocation monthly from June through September of2005Ð2007 to evaluate disease diversity and preva-lence. One hundred Sherman live traps containing asmall amount of polyester nesting material were de-ployed during each sampling event in the evening (50in the forest and 50 in the meadow), baited with oats,and checked Þrst thing in the morning. Traps werepartially covered with soil or plant material for pro-tection and camoußage. The location of each success-ful trap was obtained using a global positioning systemdevice. Twenty Tomahawk live traps were deployedeach morning, baited with a mixture of peanut butterand oats, and reset after each successful capture untilthe afternoon. Small mammals were removed fromtraps; either manually restrained (squirrels and chip-munks) or anesthetized with an intramuscular injec-tion of 100 mg/kg ketamine and 10 mg/kg xylazine(other small mammals); and identiÞed to species, age,and sex. A quantity amounting to 0.25 ml of blood wastaken from the lateral saphenous vein of squirrels andchipmunks; other small mammals were bled retro-orbitally into 1.0-ml ethylenediaminetetraacetic acidtubes (BD Biosciences, Franklin Lakes, NJ). Wholeblood samples in ethylenediaminetetraacetic acidwere kept cool for the day, and then frozen untiltransfer to the University of California (Davis, CA)where they were maintained in a �80�C freezer untilprocessing. Each small mammal was marked with anear tag and then monitored for hemostasis and/orrecovery from anesthesia. When fully recovered, smallmammals were rereleased at the capture site. Tickswere removed with forceps, and ßeas were removedby combing small mammals over a white sheet; bothwere preserved in 70% ethanol. Each ßea was clearedby incubating in dilute KOH for 24 h, dehydrated in

an ethanol series (75, 85, 95, and 100% for 30 mineach), and then mounted in Euparal (BioQuip, Ran-cho Dominguez, CA). Each ßea was identiÞed to spe-cies using western North American taxonomic keys(Stark 1958, Hubbard 1947, Lewis et al. 1988). Oftenan individual small mammal yielded a large number ofßeas that tended to be identical; in these cases, arandom sample of three was processed, with the restsaved in 70% ethanol to be evaluated in the future,particularly for individual animals with multiple ßeaspecies. Ticks were identiÞed to sex, stage, and speciesusing a western North American taxonomic key (Fur-man and Loomis 1984). Blood samples were taken viacardiocentesis from roadkill, when available.

Serology was performed to assay for antibodies andpresumptive exposure to infectious pathogens. Plasmawas separated by centrifugation at 3,000 rpm for 10min. Anti-Yersinia spp. V-antigen immunoglobulin Gwas detected in an enzyme-linked immunosorbentassay format (Anderson et al. 1996). Indirect ßuores-cent assay (IFA) was performed forAnaplasmaphago-cytophilum, spotted fever group (SFG)Rickettsia spp.,and Borrelia burgdorferi. Plasma was diluted in phos-phate-buffered saline (PBS) at 1/25; applied to A.phagocytophilum, Rickettsia rickettsii, orB. burgdorferi(Barlough et al. 1995) antigen slides (VMRD, Pullman,WA); and incubated at 37�C with moisture for 30 min.Slides were then washed three times in PBS and in-cubated with ßuorescein isothiocyanate-labeled rab-bit anti-rat immunoglobulin G heavy and light chainantibodies (Kirkegaard & Perry Laboratories, Gaith-ersburg, MD) diluted in PBS at 1/30. Slides werewashed three additional times and, during the thirdwash, incubated with two drops of eriochrome blackfor 2 min. Positive (previously tested woodrats andchipmunks) and negative (water and negative rodentserum) controls were included in each run. Sampleswere considered positive if strong ßuorescence wasdetectedatdilutionsof at least 25.All animals capturedin 2005 and all except Peromyscus spp. from 2006 and2007 were tested for exposure to A. phagocytophilum,based on our extensive prior data (Foley et al. 2008)and Þrst year study results showing that Peromyscusspp. were rarely exposed to A. phagocytophilum. Arandom sampling from each species (�50% of each, tominimize costs) was tested for SFG Rickettsia spp.exposure for all years. Borrelia spp. exposure was as-sessed in all sciurids, except that a random subset of20% of Spermophilus spp. was tested because this sam-ple was so large compared with other species. All smallmammals captured in 2005 were tested for exposure toYersinia pestis.

All seropositive small mammals were assessed for ac-tive infection by polymerase chain reaction (PCR).Blood was extracted using a kit (Qiagen, Valencia, CA),and quantitative PCR for A. phagocytophilum (Dra-zenovich et al. 2006) and SFGRickettsia spp. (Leuteneg-ger et al. 1999, Adjemian et al. 2008) was performed, aspreviously described. Quantitative PCR for B. burgdor-feri was done using the following primers: 304f, 5�-GT-CACACTGGAACTGAGATACGGT-3�, and 394r, 5�-AGTGTCGCTCCGTCAGGCT-3�, and the universal

Table 1. Location of field sites in YNP, California

Site Elevation UTM (N) UTM (E)

Foresta 1,200 37�42�20� 119�45�16�Hodgdon Meadows 1,200 37�47�48� 119�51�51�Crane Flats 1,800 37�46�31� 119�47�50�Porcupine Creek 2,400 37�48�03� 119�34�37�Tuolumne Meadows 2,800 37�52�08� 119�21�21�Dana Meadows 3,000 37�54�14� 119�15�04�

UTM, universal transverse mercator.

102 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 48, no. 1

probe library (UPL) probe, GTCACACTGGAACT-GAGATACGGTCCAGACTCNGACTCTACGGAGGCAGCAGCTAA GAATCTTCCGCAATGGGCG-ANAGCCTGACGGAGCGACACT (N. Nieto, unpub-lished data). Each 12-�l reaction contained 5 �l ofDNA, 1� TaqMan Universal Master Mix (AppliedBiosystems, Foster City, CA), 2 nmol each primer, and400 pmol probe. The thermocycling conditions con-sisted of 50�C for 2 min, 95�C for 10 min, and 40 cyclesat 95�C for 15 s, followed by 60�C for 1 min. For all PCRreactions, samples were considered positive if theyhad a cycle threshold value �40 and characteristicampliÞcation plots.

Data were maintained in Excel (Microsoft, Red-mond, WA) and analyzed with the statistical package“R” (R-Development Core Team, http://www.r-pro-ject.org). For all tests, the cutoff for statistical signif-icance was P 0.05. Descriptive statistics were doneto summarize seroprevalence and PCR prevalence foreach pathogen. Prevalence odds ratios (ORs) and 95%conÞdence intervals (CI) for each disease risk factorwere estimated using logistic regression.

Results

A total of 415 unique captures of small mammalsfrom 16 species was trapped between June 2005 andSeptember 2007 during 62 trapping events (9,560 trapperiods). The most frequently caught animals weredeer mice (Peromyscus sp.) (38% of all unique cap-tures), ground squirrels (Spermophilus sp.) (37%),voles (Microtus sp.) (9%), jumping mice (Zapus sp.)(6%), and chipmunks (Tamias sp.) (3%). Rarely cap-tured species were shrews (Sorex lyelii and Sorex trow-bridgii), pocket gophers (Thomomys monticola), andpocket mice (Chaetodipus californicus). Roadkill col-lections resulted in one yellow-bellied marmot (Mar-mota flaviventris) and one western gray squirrel (Sciu-rus griseus).

Ten tick species were identiÞed on small mammals(Table 2), including all stages of Dermacentor occi-dentalis and Ixodes angustus. Otherwise, all ticks col-lected were immature stages. BeldingÕs ground squir-rels (Spermophilus beldingi) had the greatest tickdiversity with seven different species (Table 2).Eleven small mammal species examined had at leastone tick species identiÞed (Table 2).D. occidentaliswas the most common tick identiÞed

(49%), and was found to infest four small mammalspecies (Table 2). Eighty-two percent of D. occiden-talis were found at 1,200 m elevation. Haemaphysalisleporispalustris, Ixodes kingi, Ixodes hearlei, and Ixodesspinipalpis were found only at 2,800 m.

The Yosemite ßeas and their hosts are shown inTables 3 and 4. Our survey identiÞed 464 ßeas from 378rodent and Þve shrew individuals. The 18 host speciesharbored 16 species of ßeas from three families, asfollows: Hystrichopsyllidae (four species), Leptopsyl-lidae (two species), and Ceratophyllidae (10 species).North American deer mice (Peromyscusmaniculatus),the most frequently collected mammal, had high ßeadiversity with 148 ßeas from six species. BeldingÕs

Tab

le2

.N

umbe

rof

indi

vidu

als

ofea

chsm

all

mam

mal

spec

ies

infe

sted

wit

hva

riou

ssp

ecie

sof

tick

sfr

omY

NP

,C

alif

orni

a

Sm

all

mam

mal

speci

es

(no.exa

min

ed)

Dermacentor

occidentalis

Dermacentor

sp.

Haemaphysalis

leporispalustris

Ixodes

angustus

Ixodes

hearli

Ixodes

kingi

Ixodes

pacificus

Ixodes

sculptus

Ixodes

spinipalpis

Ixodes

woodi

Tic

ksp

eci

es

rich

ness

Chaetodipuscalifornicus

(1)

10

00

00

00

00

1Glaucomyssabrinus

(8)

00

01

00

00

00

1Homosapiens

(2)

20

00

00

00

00

1Microtuscalifornicus

(2)

00

01

00

00

00

1Microtuslongicaudus

(8)

00

00

00

00

00

0Microtusmontanus

(26)

00

02

00

00

00

1Peromyscusboylii

(1)

01

00

00

10

00

2Peromyscusmaniculatus

(137

)1

31

60

00

00

04

Peromyscustruei

(6)

30

00

00

00

00

1Sorexlyelli

(4)

00

00

00

00

00

0Sorextrowbridgii

(1)

00

00

00

10

01

2Spermophilusbeecheyi

(32)

00

00

00

01

00

1Spermophilusbeldingi

(126

)0

10

41

10

11

17

Tamiasalpinus

(1)

00

00

00

00

00

0Tamiasminimus

(1)

00

00

00

00

00

0Tamiasspeciosus

(7)

00

00

00

00

00

0Thomomysmonticola

(5)

00

00

00

00

00

0Zapusprinceps

(25)

00

00

00

00

00

0T

ota

l7

51

141

12

21

222

January 2011 FLEER ET AL.: VECTOR-BORNE DISEASE IN YOSEMITE NATIONAL PARK 103

Tab

le3

.N

umbe

rof

indi

vidu

als

ofea

chsm

all

mam

mal

spec

ies

infe

sted

wit

hva

riou

ssp

ecie

sof

fleas

from

YN

P,

Cal

ifor

nia

Sm

all

mam

mal

speci

es

(no.exa

min

ed)

Aetheca

wagneri

Callistopsyllus

terinus

Catallagia

s.sculleri

Corrodopsyllacuruata

obtusata

Eumolpianus

eutamiadis

Foxellaignotus

recula

Hystrichopsylladippiei

heotomae

Megabothris

abantis

Ceratophyllusciliatus

mononis


(1)

00

00

00

00

0Glaucomyssabrinus

(8)

00

00

00

00

2Microtuscalifornicus

(2)

00

00

00

00

0Microtuslongicaudus

(8)

50

10

00

09

0Microtusmontanus

(26)

60

00

00

038

0Peromyscusboylii

(1)

00

00

00

00

0Peromyscusmaniculatus

(137

)11

610

60

01

01

0Peromyscustruei

(6)

00

00

00

00

0Sorexlyelli

(4)

00

02

00

00

0Sorextrowbridgii

(1)

00

00

00

00

0Spermophilusbeecheyi

(32)

10

00

00

00

0Spermophilusbeldingi

(126

)5

10

02

01

33

Tamiasalpinus

(1)

00

00

00

00

0Tamiasminimus

(1)

00

00

40

00

0Tamiasspeciosus

(7)

10

00

00

00

0Thomomysbottae

(2)

00

00

03

00

0Thomomysmonticola

(5)

00

00

00

00

0Zapusprinceps

(25)

10

00

00

03

0U

nkn

ow

n1

00

00

10

00

Tab

le4

.N

umbe

rof

indi

vidu

als

ofea

chsm

all

mam

mal

spec

ies

infe

sted

wit

hva

riou

ssp

ecie

sof

fleas

from

YN

P,

Cal

ifor

nia

Sm

all

mam

mal

speci

es

(no.exa

min

ed)

Opisodasys

vesperalis

Oropsylla

idahoensis

Oropsylla

montana

Oropsylla

t.tuberculata

Peromyscopsyllushesperonomys

adelpha

Peromyscopsylla

selenis

Thrassisfrancisi

sierrae

Fle

asp

eci

es

rich

ness


(1)

00

00

00

00

Glaucomyssabrinus

(8)

20

00

00

02

Microtuscalifornicus

(2)

00

00

00

00

Microtuslongicaudus

(8)

00

00

00

03

Microtusmontanus

(26)

00

00

01

03

Peromyscusboylii

(1)

00

00

00

00

Peromyscusmaniculatus

(130

)0

00

013

00

6Peromyscustruei

(6)

00

00

00

00

Sorexlyelli

(4)

00

00

00

02

Sorextrowbridgii

(1)

00

00

00

00

Spermophilusbeecheyi

(32)

00

560

00

02

Spermophilusbeldingi

(126

)0

940

131

035

10Tamiasalpinus

(1)

00

01

00

01

Tamiasminimus

(1)

00

00

00

01

Tamiasspeciosus

(6)

00

00

00

01

Thomomysbottae

(2)

00

00

00

01

Thomomysmonticola

(5)

00

00

00

00

Zapusprinceps

(25)

00

00

00

02

Unknown

00

00

00

0


ground squirrels were also commonly collected andrich in ßeas, as follows: 158 ßeas from 10 species. TheCalifornia ground squirrel was less common in trapsand had much lower ßea diversity, 56 Oropsylla mon-tana and one Aetheca wagneri. The montane vole (Mi-crotus montanus) was the third most frequently col-lected mammal, but was host for only a single speciesof ßea, Megabothris abantis, of which 38 were col-lected.

The most commonly collected ßea was A. wagneri,with 116 individuals on deer mice, and 16 more indi-viduals scatteredacross sevenhost species.O.montanaand Oropsylla idahoensis were common, but only onground squirrels. Thrassis francisi sierrae showed asimilar pattern with 35 ßeas found only on BeldingÕsground squirrels.M.abantiswas common on voles and,to a lesser extent, BeldingÕs ground squirrels.

We have identiÞed eight additional large or nearbyßea surveys performed in California (Table 5). Starkmentions collecting ßeas in YNP in his monograph onThrassis (Stark 1970). Surveys of ßeas targeting areasnear YNP were conducted in Plumas County (Jame-son and Brennan 1957) and Sagehen Creek (NevadaCounty) (Adjemian et al. 2008). Hubbard reviewedCalifornia ßeas from his home base in Oregon (Hub-bard 1943). A very thorough study was performed byLinsdale and Davis at Hastings Reserve in the centralCoast Range (Linsdale and Davis 1956). Public health-oriented surveys were done in the San Diego moun-tains (Lang 2004) and the Transverse Ranges at Chu-chupate (Davis et al. 2002). The eight studies of Table5 differed in their focus and methodology. Hastingsincluded all available mammals. The Plumas studyprimarily trapped rodents and shrews. Three of thestudies collected almost only rodents. Sample sizeacross all studies clearly affects ßea diversity, but it isnoteworthy that the YNP ßea fauna is almost as diverseas the much larger samples of Plumas County andChuchupate. Several ßea species were readily col-lected in Yosemite, but not in other large mammal-ßeasurveys in California (Table 6), including Callistop-syllus terinus, T. francisi sierrae, O. idahoensis, Orop-sylla tuberculata, and Eumolpianus eutamiadis. M.abantiswas common in YNP, but very rare in a PlumasCounty study (Jameson and Brennan 1957). However,the common vole and deer mouse ßea Malaraeustelchinuswas not found at YNP. This absence is, how-ever, consistent with other collections (Auguston1942, Hubbard 1947). The woodrat ßea Orchopeassexdentatuswas not collected in part because, despite

the presence of active houses, woodrats did not enterthe traps.

In addition to evaluating ectoparasites at YNP, weevaluated animals directly for exposure and infectionwith vector-borne pathogens. We used the low cutoffvalue of 1:25 to increase sensitivity with using non-species-speciÞc conjugate. Anti-rat conjugate wasused because speciÞc conjugate for the species col-lected was not available. Seroprevalence forA. phago-cytophilum ranged across host species from 0 to 100%,with yellow-bellied marmots having the highest sero-prevalence and BeldingÕs ground squirrels having themost seropositive individuals (Table 7). Spotted fevergroup Rickettsia spp. seroprevalence ranged from 0 to100%. The highest seroprevalence was found in brushmice (Peromyscus boylii), whereas North Americandeer mice had the overwhelming majority of seropos-itive individuals (Table 7). Seroprevalence of Borreliasp. ranged from 0 to 86% across host species, withlodgepole chipmunks (Tamias speciosus) having thehighest seroprevalence and BeldingÕs ground squirrelswith the highest number of infected individuals. Noanimals tested positive for Y. pestis. Additionally, noanimals tested PCR positive for any pathogen.

Prevalence ORs signiÞcantly different from 1 werenot observed for seropositivity forA.phagocytophilum,SFG Rickettsia spp., or Borrelia spp. for altitude, hab-itat, species, or gender. Seroprevalence among yearsdiffered signiÞcantly for A. phagocytophilum (OR 2.0, 95% CI 1.2Ð3.2, P 0.004), with the highest prev-alence in 2005 of 28%, followed by seroprevalence of0.4 and 5.6% in 2006 and 2007, respectively. Years alsodiffered signiÞcantly for SFG Rickettsia spp. sero-prevalence (prevalence OR 1.6, 95% CI 1.1Ð2.2, P0.009), from 1.4% in 2005, increasing to 10.3 and 13.0%in 2006 and 2007, respectively. When the 3 yr of datawere lumped, A. phagocytophilum seropositivity dif-fered by month of capture (prevalence OR 3.7, 95%CI 1.1Ð13.2, P 0.009). No seropositive animals weredetected in June, only two (1.5%) in July, and 39(23.3%) in August.

Discussion

Vector-borne disease maintenance in nature re-quires complex interactions among small mammals,ectoparasites, and other ecological factors. The richsmall mammal fauna in YNP hosts a diversity of ec-toparasites and shows susceptibility to multiple im-portant vector-borne pathogens.

Table 5. Small mammal-flea surveys of large sample size or conducted proximal to YNP, California

Locality No. rodents collected No. rodent species No. ßeas collected No. ßea species Citation

Hastings Reserve 2,204 14 22,087 23 Linsdale and Davis 1956San Diego County 2,207 17 11,984 22 Lang 2004Chuchupate 1,563 10 2,277 18 Davis et al. 2002Plumas County 2,423 4 1,417 19 Jameson and Brennan 1957Yosemite 408 16 462 15 Stark 1970Morro Bay 295 10 180 10 Nieto et al. 2007Sagehen 89 5 39 5 Adjemian et al. 2008Lava Beds 382 15 779 21 Stark and Kinney 1969


Small mammal species captured at each site wereexpected based on previous studies in nearby loca-tions in YNP (Grinnell and Storer 1924, Moritz 2007).

Howevshrews) are more amenable to trapping usinger,small mammal diversity was likely underrepresented inthis study because trapping methods were limited to live

Table 6. Fleas reported from eight small mammal surveys in California

Flea speciesLavabeds

Plumas Sagehen Yosemite HastingsMorroBay

ChuchupateSan

DiegoTotal

Corrodopsylla curvata obtusata 0Carteretta carteri 198 29 227Anomiopsyllus congruens 171 23 at least 2 194Anomiopsyllus nudatus nudatus 257 215 472Callistopsyllus terinus 1 11 12Megarthroglossus sp. near divisus 267 267Megarthroglossus sp. (Lava Beds) 14 14Megarthroglossus procus 4 4Catallagia luski 19 1 20Catallagia mathesoni 1 123 124Catallgia sculleri 23 81 7 1 112Delotelis hollandi 2 2Epitedia scapani 1 1Epitedia wenmanni 10 1 11Phalacropsylla allos 18 18Meringis cummingi 10 28 28 4 70Meringis parkeri 22 22Atyphloceras multidentatus 6 198 206 10 26 14 460Atyphloceras longipalpus 4 26 30Hystrichopsylla dippei neotomae 1 1Hystrichopsylla occidentalis linsdalei 121 2 14 137Hystrichopsylla occidentalis occidentalis 22 22Corypsylla kohlsii 1 1Corypsylla ornata 0Nearctopsylla hamata 1 1Neactopsylla princei 8 8Rhadinopsylla (Micropsylla) sectilis 3 1 16 20Rhadinopsylla (Rectofrontia) fraterna 2 2Ctenocephalides canis 0Ctenocephalides felis 4 4Echidnophaga gallinosa 607 391 998Pulex irritans/simulans 1 1Hoplopsyllus anomalus 8,353 5 50 2,516 10,924Hoplopsyllus foxi 3 3 7 13Cediopsylla inaequalis 44 4 8 56Leptopsylla segnis 251 2 237 490Odontopsyllus dentatus 1 1 2Peromyscopsylla selenis 4 11 1 16Peromyscopsylla hesperomys 131 3 14 224 37 45 44 498Nosopsyllus fasciatus 22 22Thrassis acamantis howelli 101 101Thrassis francisi rockwoodi 28 28Thrassis francisi sierrae 35 35Oropsylla idahoensis 18 94 112Oropsylla montana 21 5 56 8,192 15 792 7,537 16,618Oropsylla tuberculata 14 14Dactopsylla bluei 17 2 19Foxella ignota 19 607 626Malaraeus sinomus 0Malaraeus telchinus 17 695 1,806 63 93 333 3,007Amaradix biterootensis 1 1Opisodasys keeni 310 5 315Opisodasys vesperalis 2 2Opisodasys nesiotus 21 6 27Orchopeas latens 10 1 11Orchopeas leucopus 4 4Orchopeas sexdentatus 168 1,053 21 293 567 2,102Aetheca wagneri 6 93 6 131 156 204 13 609Ceratophyllus ciliatus mononis 11 20 5 36Eumolpianus fornacis 72 117 189Eumolpianus eumolpi 27 18 5 1 51Eumolpianus eutamiadis 6 6Megabothris abantis 2 66 68Total 847 1,417 39 462 22,087 180 2,277 11,948 39,257

Based on data from references listed in Table 4.


traps, andsomespecies(e.g., voles andshrews)aremoreamenable to trapping using other methods such as pitfalltraps. YNP has 33 rodent and shrew species listed withinits boundaries (www.nps.gov/yose/naturescience/mammal-species-list.htm). We captured 16 of these inour study, as well as two species of shrews. We did notcapture the nonnativeRattus rattus,Musmusculus, andCastor canadensis. Several large native rodents,Erethi-zon dorsatum, Aplodontia rufa, Neotoma cinerea, Neo-tomamacrotis, Marmota flaviventris, and Spermophiluslateralis,as well as the arboreal squirrelsSciurus griseusand Tamiasciurus douglassii, also avoided our traps,which is a problem that previously has been reported(Nieto and Foley 2008). Thus, the species included inthis study could have resulted in an underestimate ofectoparasite numbers and diversity, as well as diseaseprevalence. BeldingÕs ground squirrel and deer mouseabundance may have been overrepresented becauseof large population size and ease of capture.

Overall tick numbers observed on small mammalswere relatively low compared with other sites in Cal-ifornia (Nieto et al. 2007, Adjemian et al. 2008, Foleyet al. 2008). North American deer mice had greatesttick loads, possibly because they are such commongeneralists present at nearly every location. The hightick diversity on BeldingÕs ground squirrels was pre-viously unreported (Furman and Loomis 1984), in-cluding 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 ourpublished data in the Coast Range Mountains (Nietoand Foley 2009). This may be because many of thesites we sampled were relatively dry and at higheraltitude, which are inappropriate conditions for manyticks, or because chipmunk capture numbers werelow. Small numbers of human-biting ticks (Ixodespacificus, I. angustus, Dermacentor andersoni) wererecovered, suggesting a possible risk of some tick-borne disease in humans and their pets. However,further work to evaluate the role of nidicolous andspecialist ticks in disease ecology is warranted. Spe-

ciÞcally, many species of nidicolous ticks occurred onrodents, but the relevance of most of these tick speciesfor vector-borne disease transmission is unknown. Im-portantly, prior research has documented roles forseveral host specialist ticks in the ecology of R. rick-ettsii. For example, much work was done early in the20th century to understand the ecology of RockyMountain spotted fever (Parker 1923), and, in partic-ular, the rabbit tick,H. leporispalustris,hasbeenshownto be a competent vector for some SFG rickettsiae(Freitas et al. 2009, Parker 1923) even though Amer-ican SFG rickettsiae from H. leporispalustris are gen-erally minimally pathogenic.

YNP ßeas have been largely unstudied, with theexception of StarkÕs monograph on Thrassis in YNP(Stark 1970). An analysis of his collection wouldcomplement our study. Overall, the entire Califor-nia ßea fauna has received sporadic attention. Cal-ifornia ßea communities appear to be at the inter-section of three ßea faunas, as follows: a PaciÞcNorthwestern fauna well described in Lewis et al.(1988), an intermontane fauna best examined inStark (1958), and a Southwestern fauna that stillneeds attention. This can be seen roughly in Cera-tophyllid distribution maps (Traub et al. 1983). Forexample, the chipmunk ßea Ceratophyllus ciliatusmononis extends along the Sierra Nevada to desertmountains in Southern California, whereas Eumol-pianus c. protinus extends from northern Californiato coastal Alaska, and Eumolpianus c. kincaidi in-habits Idaho and Utah. The pocket gopher ßea Dac-tylopsylla bluei bluei is on the central Californiacoast, whereas Dactylopsylla b. psila is found nearLos Angeles and Las Vegas. Often the same ßeaspecies occupies the PaciÞc Coast and interiormountains such as the deer mouse ßea Opisodasyskeeni,whereasOpisodasys nesiotus inhabits the cen-tral to southern California coast. Certainly there areother ßeas in YNP besides those we assessed, as aresult of sampling size, season, and host targets, but

Table 7. Results of serology for vector-borne pathogens in wild rodents in YNP, California

A. phagocytophilum Borrelia spp. Rickettsia spp. Yersinia spp.

No. positive No. tested No. positive No. tested No. positive No. tested No. positive No. tested

Chaetodipus californicus 0 (0%) 1 0 (0%) 0 0 (0%) 1 0 (0%) 1Glaucomys sabrinus 0 (0%) 8 3 (42.86%) 7 1 (16.67%) 6 0 (0%) 2Marmota flaviventris 1 (100%) 1 0 (0%) 1 0 (0%) 1 0 (0%) 1Microtus californicus 1 (50%) 2 0 (0%) 0 0 (0%) 1 0 (0%) 0Microtus longicaudus 3 (42.86) 7 0 (0%) 0 1 (14.29%) 7 0 (0%) 7Microtus montanus 6 (22.2) 27 0 (0%) 0 0 (0%) 24 0 (0%) 10Peromyscus boylii 0 (0%) 1 0 (0%) 0 1 (100%) 1 0 (0%) 0P. maniculatus 2 (1.53%) 131 0 (0%) 0 20 (28.57%) 70 0 (0%) 24Peromyscus truei 0 (0%) 5 0 (0%) 0 0 (0%) 5 0 (0%) 4Sciurus griseus 0 (0%) 1 0 (0%) 1 0 (0%) 1 0 (0%) 0Spermophilus beecheyi 1 (3.45%) 29 2 (25%) 8 4 (13.79%) 29 0 (0%) 11Spermophilus beldingi 18 (18.56) 97 8 (47.06) 17 0 (0%) 62 0 (0%) 30Tamias alpinus 0 (0%) 4 1 (25%) 8 0 (0%) 5 0 (0%) 0Tamias minimus 0 (0%) 0 0 (0%) 1 0 (0%) 0 0 (0%) 0Tamias speciosus 2 (28.57) 7 6 (54.54%) 11 3 (42.86%) 7 0 (0%) 1Thomomys monticola 2 (40%) 5 0 (0%) 0 1 (20%) 5 0 (0%) 3Zapus princeps 6 (28.57) 21 0 (0%) 0 3 (15.79%) 19 0 (0%) 5Total 42 (12.1%) 347 20 (37.03%) 54 34 (13.93%) 244 0 (0%) 99


our other data are consistent with very high ßeabiodiversity.

The high abundance and diversity of ectoparasitessuggest a high risk of enzootic vector-borne disease. Infact, data did reveal exposure to multiple vector-bornepathogens, although in a few cases, imperfect sensi-tivity or speciÞcity of the test was unfortunate. For allserological assays, wildlife species-speciÞc secondaryconjugates were not available and the use of anti-ratantibodies could have resulted in some reduction ofsensitivity of the test. For the IFAs, we used a rela-tively concentrated secondary antibody for all hostspecies (based on our prior results and in-house pro-tocols; data not shown), in part to maximize sensitivityand for consistency in assays among species. SpeciÞc-ity would be unlikely to be affected, especially in lightof the complete lack of ßuorescence on negative con-trols. For the anti-Y. pestis enzyme-linked immunosor-bent assay, a recombinant antigen was used in partbecause of availability of the antigen and to allow usto detect any F1-negative strains to which animalscould have been exposed. The sensitivity of this assayfor wildlife also was likely affected by the lack ofspecies-speciÞc secondary antibodies. Thus, data forthese serological tests could potentially be underes-timates of the actual prevalence.A. phagocytophilum is a tick-vectored bacterial

pathogen that causes granulocytic anaplasmosis in hu-mans, dogs, and horses (Madigan and Gribble 1987,Dumler et al. 1995, Foley et al. 2001). Symptoms ofinfection are often nonspeciÞc, including fever andthrombocytopenia, and can range from mild to severeor fatal. A. phagocytophilum seroprevalence in thisstudy (12.1%) was comparable to other sites in Cali-fornia (Foley et al. 2008). It was interesting that theprevalence increased so dramatically from June (0%)to August (23%), suggesting that some important vec-tor was infecting most individuals early to midsummer.California tick species known to be competent fortransmittingA. phagocytophilum are I. pacificus (Rich-ter et al. 1996) and I. spinipalpis (Zeidner et al. 2000),both of which were collected in this study. There issome speculation that I. angustus, a common tick spe-cies collected at all elevations and a known tick vectorfor Lyme disease (Peavey et al. 2000), could also bevector competent forA. phagocytophilum (Foley et al.2008). Disease seroprevalence in this study was muchhigher in locations with more I. angustus, suggestingthat this species may play a role in the cycle of thispathogen in YNP. Ten small mammal species wereseropositive for this pathogen, although species per sewas not a statistically signiÞcant risk factor for sero-positivity. The upper value of 100% seropositivity isbiased because the only marmot tested was seropos-itive. It is not known whether other species ofAnaplasma exist that may cross-react with A. phago-cytophilum in our serologic test, but it is interesting tospeculate that this may be true, because seropositiveindividuals were found above the normal elevationalrange for this pathogen. Further research should bedone to identify PCR or cell culture-positive individ-uals so a conÞrmatory DNA sequence can be obtained.

Tissue PCR may have been more sensitive than bloodPCR because infection in the blood may be intermit-tent, but could not be performed within the scope ofthis study.

Spotted fever group Rickettsia spp., transmitted byDermacentor sp. tick vectors, are rickettsial pathogensthat cause disease in humans, dogs, and occasionallycats.R. rickettsii is the causative agent of Rocky Moun-tain spotted fever, the most common rickettsial patho-gen in North America (Adjemian et al. 2009), butseveral nonpathogenic rickettsias (e.g.,R. montana, R.peacockii, R. rhipicephali) also exist that may cross-react 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 shownrecently to cause disease in people (Shapiro et al.2010). Further species differentiation can be attainedwith PCR, but because no samples were PCR positivefor SFG Rickettsia spp., we could not distinguish be-tween different species. Dermacentor sp. ticks werecollected at most locations with animals seropositivefor SFGRickettsia spp., but were occasionally found inlocations where no seropositive individuals were col-lected. The upper value of 100% seropositivity is bi-ased because the only brush deer mouse tested wasseropositive. Further research should also be done inYNP to identify PCR and tissue culture-positive ani-mals, to elucidate which SFG Rickettsia sp. is involvedin this location and potentially provide bacterial iso-lates for further study.Borrelia spp. in California can roughly be divided

into two main groups, as follows: relapsing fever Bor-relia spp., which are vectored by soft ticks or lice andcause undulating fever eventually leading to centralnervous system involvement; and B. burgdorferi sensulato, hard tick-vectored spirochete bacterial patho-gens that cause ßu-like symptoms and thrombocyto-penia in humans, dogs, cats, and potentially otherwildlife species. B. burgdorferi sensu stricto causesLyme disease, the most common vector-borne diseasein North America. Lyme disease is treatable in acutestages, but can become chronic and debilitating if leftuntreated. Chronic symptoms can include arthritis,nervous system disorders, and gastrointestinal disease(Brown and Lane 1992). Certain species of Borreliathat cause relapsing fever (e.g., B. hermsii, B. parkeri,B. turicatae, B. duttonii) can cross-react with B. burg-dorferi in our IFA test, but speciÞcity of this test alsois low because of reaction with heat shock and otherhost proteins (Bruckbauer et al. 1992, Magnarelli et al.1987). Because no samples were PCR positive, furtherspecies differentiation could not be achieved, butbased on the location and elevation of seropositiveanimals, it is possible that some of these animals wereexposed to a relapsing fever Borrelia sp., especiallybecause chipmunks are the known reservoir for re-lapsing fever in California (Dworkin et al. 2002).

Although plague is endemic in several montanecommunities of California (Davis et al. 2002, Adjemianet al. 2006, Foley and Foley 2010), it was not apparentin YNP. Key factors that maintain plague are a con-troversial, ecologically complicated problem (Gage


and Kosoy 2005), but there is some evidence that ahigher diversity rodent-ßea community is important,at least in California (Foley et al. 2007, Foley and Foley2010). More speciÞcally, diversity increases plaguepersistence because of the availability of new suscep-tible rodents at different times during the year (hostphenological variation), additional potential hosts(host abundance), and plague transmission-compe-tent ßeas with multiple hosts (vector ßexibility).

Plague is known to be present in YNP based on anearlier case report (Nelson 1980, Smith 1994). Giventhe fairly high rodent and ßea diversity of Yosemite,we might expect a higher prevalence of plague in thecurrent study. The lack of plague could be the resultof test insensitivity, a local historic accident by whichinfection in local populations we sampled had recentlybecome extinct and not yet been reintroduced, or lackof detection with our sample size if prevalence waslow. Alternatively, there could be some consistenthomogenizing factor (such as highly mobile carni-vores) that has deprived YNP of the structural heter-ogeneity needed for endemicity.

Overall, YNP shows evidence of exposure to at leastthree important vector-borne pathogens, which hasimportant implications for public health and conser-vation medicine. The high ßea and tick diversity onseropositive hosts would suggest ongoing enzootic dis-ease in sylvatic cycles that are poorly understood.More research deÞning competent vectors and reser-voirs for these pathogens, and conÞrming the identi-ties of Borrelia spp. and SFG Rickettsia spp., is war-ranted. Nevertheless, in this study, we establishimportant baseline data for vectors and pathogens inYNP.

Acknowledgments

We thank Jennifer Dike, Haleh Siahpolo, Jennifer Glavis,and Jeff Maurer for support of Þeld work; Niki Drazenovich,Nathan Nieto, Nat Lim, Jennifer Gorman, Joy Worth, andRaymond Wong for assistance in the laboratory; and JanVanWagtendonk for assistance with housing and backgroundliterature access. This work was supported by the GeraldineR. Dodge Foundation and the University of California DavisCenter for Vector-Borne Disease.

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Received 17 February 2010; accepted 2 September 2010.


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