The Parasitology of the Ground Squirrels of Western Utah - BioNames

76 PROCEEDINGS OF THE HELMINTHOLOGICAL SOCIETY

Literatur e CitedGlaser, R. W. 1940. The bacteria-free cultivation

of a nematode parasite. Proc. Soc. Exp. Biol.Med. 43: 512-514.

, and H. Fox. 1930. A nematode para-site of the Japanese beetle (Popillia japonicaNewm.). Science 71: 16-17.

Jackson, G. J. 1962. The parasitic nematode,Neoaplectana glaseri, in axenic culture. II .Initial results with defined media. Exp. Para-sit. 12: 25-32.—. 1966. Helminth physiology: stage andspecies differences in culture. Ann. N. Y.Acad. Sci. 139: 91-97.

. 1969. Nutritional control of nematodedevelopment. Adv. Exp. Med. & Biol. 3:333-341.

, and G. E. Moore. 1969. Infectivity

of nematodes, Neoaplectana species, for thelarvae of the weevil Hijlobius pales, afterrearing in species isolation. J. Invert. Pathol.14: 194-198.

Stoll, N. R. 1953. Continued infectivity forJapanese beetle grubs of Neoaplectana glaseri(Nematoda) after seven years axenic cultures.In J. Dayal and K. S. Singh (eds.), ThaparCommemoration Volume, p. 259-268. Univ.of Lucknow, India.

. 1959. Conditions favoring the axenicculture Neoaplectana glaseri, a nematode par-asite of certain insect grubs. Ann. N. Y.Acad. Sci. 77: 126-136.

Turco, C. P., S. H. Hopkins, and W. H.Thames, Jr. 1970. Susceptibility of fiveinsect pests to Neoaplectana glaseri Steiner,1929. J. Parasitol. 56: 277-280.

The Parasitology of the Ground Squirrels ofWestern Utah

ELRAY JENKINS* AND ALBERT W. GRUNDMANNDepartment of Biology, University of Utah

ABSTRACT: The parasitology of six species of ground squirrels (Spermophilus and Amrnospermophiliis)occupying the western half, or Bonneville Basin area, of Utah is reported. The study included intes-tinal protozoa (except Coccidia), endoparasitic helminths and dipteran larvae, and ectoparasites. Acomplete list is included. The probable results of host post-Pleistocene migration on parasitism aredescribed. Parasite-host interrelationships are discussed.

A parasitological study of the ground squir-rels (Spermophilus and Ammospermophilus)was conducted throughout the Bonneville Basinand surrounding mountains that make up thewestern half of Utah. Most of the six speciesincluded reach the limits of their geographicaldistribution in this region and represent thepresent state of the migration that has occurredsince Pleistocene Lake Bonneville receded toform the present Great Salt Lake. The rangesof the species are, with several exceptions,allopatric, and provide a probable record ofsome host-restricted parasites carried in withhost migrations as well as those acquiredthrough interrelationships with other genera ofmammals in the region. Included in the studywere helminths, intestinal protozoa (excluding

Currently U. S. Army Medical Corps.

Coccidia), myiasis-producing Diptera larvae,and ectoparasites.

Two extensive systematic and distributionalstudies of the hosts in Utah are those by Dur-rant (1952) and Hansen (1954). In additionto systematics, Hansen also reported on theparasitic fauna, especially the ectoparasites.Helminths of the antelope ground squirrel werereported by Grundmann (1957, 1958), andFrandsen and Grundmann (1961) publishedon the helminths of several additional hostspecies. Doran (1954, 1955) compiled para-site lists for rodent species.

Excellent publications on fleas that providepertinent data are those of Stark (1958),Jellison (1945), Jellison et al. (1953), Hansen(1954), and Beck (1955). Sucking lice werereported by Bell (1950) and Hansen (1954).Edmunds (1951) compiled a check list of the

Copyright © 2011, The Helminthological Society of Washington

OF WASHINGTON , VOLUME 40, NUMBER 1, JANUARY 1973 77

ticks of Utah. Data contributed by thesestudies are acknowledged in Table 1.

Kirby and Honigberg (1949) and Evans(1955, 1956, 1957, 1959) studied the flagel-lates of ground squirrels. Becker (1926a, b)described Entamoeba citelli. Dajani (1962)studied amoeba from a number of host species.

Several studies similar to the present onehave been conducted in North America. Mostof these have been concerned with definedcategories of parasites such as helminths orprotozoa, and none has covered as broad arange as the present study. The most extensiveprevious study was that of McLeod (1933) inManitoba, Canada, which covered helminthsand ectoparasites of three species of squirrels.Rausch and Tiner (1948) surveyed 325 sciuridsfrom the North Central States. Voge (1956)published a summary of California nematodeparasites. A number of parasite species re-ported in these publications also were foundin the Bonneville Basin.

Material s and MethodsA total of 490 specimens was live-trapped

or shot from 60 localities distributed over the14 western counties of Utah extending fromBoxelder and Summit on the north to Washing-ton on the south. Trapsites ranged in elevationfrom 4,200 feet adjacent to the Great SaltLake to 4,800 at the southern end of theBonneville Basin floor. In the higher mountainranges in and surrounding the basin, the studyextended to 11,000 feet elevation. The sampleincluded 181 rock squirrels, Spermophilusvariegatus Utah Merriam; 100 golden mantledground squirrels, S. lateralis lateralis (Say); 12Belding squirrels, S. beldingi crebus Hall; 35Uinta, S. armatus (Kennicott); 25 Townsend,S. townsendi mollis Kennicott; and 135 ante-lope ground squirrels, Ammospermophilusleucurus leucurus (Merriam).

Animals removed from traps were placedin muslin bags for transport to the laboratory.Animals shot were also bagged to gain maxi-mum recovery of ectoparasites. Live animalswere etherized while still in the bags, andupon removal were combed, washed in de-tergent, and beaten to remove ectoparasitesbefore autopsy. Before discarding, the carcasswas placed in a bag and refrigerated at 36 Ffor 24 hr. This procedure caused the ecto-

parasites remaining to move to the hair tipswhere they could be collected. In the case ofanimals examined for protozoa, specimenswere taken from the ileum, cecum, and colonimmediately after the abdominal cavity wasopened. Slide material was fixed in Schaudinn'sand stained with iron hematoxylin. Tapewormswere relaxed in chloretone-saline solution, flat-tened, fixed in AFA, stained in acid alumcarmine, and mounted. Nematodes were fixedeither in hot 70% alcohol or in Kahle's, washedto remove the formaldehyde, and stored in70% alcohol. Specimens were cleared inchlorolactophenol d'Amann for study and re-turned to storage in 70% alcohol.

Examination for Trichinella spiralis was doneby removing a sample of approximately 1.25 gof muscle tissue from the diaphragm, tongue,and leg muscles. The sample was cut intosmall pieces and subjected to digestion (Hoff-man, 1956), at 37-39 C using a shaker.

Fleas and ticks were prepared for mountingby being placed in warm 10% KOH for 2 hr,neutralized in acid alcohol, dehydrated inalcohol, and mounted in Hoyer's solution.Mites and lice were prepared in a similarmanner omitting the KOH step.

Host Distributio nThe six ground squirrel species are currently

divided among three subgenera of Spermophi-lus and one of Ammospermophilus. The sub-genus Spermophilus is represented by S.armatus, S. beldingi, and S. townsendi. Theformer two species are thought to have enteredthe Bonneville Basin region from the north andthe northwest while townsendi invaded fromthe west (Hansen, 1954). S. beldingi has themost limited distribution in the region and oc-curs only in the Raft River Mountains locatedin the extreme northwest corner of Utah wherethe animal also reaches the most southern andeastern limits of its range. The habitat of theBelding ground squirrel is primarily the moistupland meadow.

S. armatus inhabits the drier situations inmountains, foothills, and high valleys in theWasatch and central mountain chain that formsthe eastern rim of the Bonneville Basin. Therange as it occurs marks both the westernlimi t of migration in northern Utah with thesouthern limi t being reached in Sevier County



near the center of the state. These animalsselect cultivated fields and pastures arounddeveloped areas and are abundant in well-drained situations such as knolls and inman-constructed banks of canals, roads, andrailroads. Where its habitat coincides withrecreational areas, the species is a frequentinhabitant of garbage areas and campgrounds.

Spcrmophilus townsendi mollis inhabits thenorthern three-fourths of the Bonneville Basinand is a desert valley form located in discretepopulation groups about moist areas such assprings and seeps. Townsendi range is allo-patric in relation to its two closest relativesdescribed above although farther north inIdaho there are limited areas of overlap withbeldingi. The Townsend squirrel is closelyassociated in the habitat with the antelopeground squirrel, Ammospermophilus leucurusleucurus Merriam, that also inhabits the desertconditions of the basin and with whom itshares most of its parasites.

The subgenus Otospermophilus is repre-sented by S. variegatus utah Merriam. Rocksquirrel distribution in Utah coincides withthe distribution of the scrub oak, Quercusgambellii Nuttall, which the animal utilizes forits basic food resources. Rock squirrels haveextended their distribution into some of thedesert mountain ranges of the basin where itis usually the only squirrel present above thefoothill habitat where one encounters the ante-lope ground squirrel. The rock squirrel, how-ever, has extended its niche greatly by adaptingto suburban and urban living in human com-munities. It has also moved into the nicheafforded by forest service garbage dumps andcampgrounds and by so doing has expandedboth its population density and its parasitediversity. Rock squirrel range overlaps thatof the golden mantled ground squirrel, S.lateralis lateralis Say, at elevations around7,000 to 7,500 ft. S. variegatus reaches itsnorthern limi t near the Utah—Idaho borderand is considered to have invaded the regionfrom the south as ancient Lake Bonnevillereceded.

The subgenus Callospermophilus has onerepresentative, S. lateralis lateralis Say, in theregion. The golden mantled ground squirrelis an inhabitant of canyon bottoms and suitableforested areas in the aspen-fir and spruce—firbelts from about 7,000 to 10,500 feet elevation.

Colorado is considered to be the center of dis-persal of this species and its migration intoUtah has been from the east and north downthe central mountain chain. The goldenmantled ground squirrel had the lowest inci-dence of parasitism in the study group (7%)and, to date, only two parasite species havebeen present that have not been recoveredfrom other ground squirrels. These are a larvaltapeworm, Taenia mustelae Gmelin, and anadult of Cittotaenia.

Ammospermophilus leucurus leucurus Mer-riam, the antelope ground squirrel, is the lonerepresentative of its genus in the region. Thespecies inhabits the dry desert of the basinfloor and low foothills where the rainfall is lessthan 10 inches per year. Antelope groundsquirrels favor rocky outcrops and vegetateddunes and do not extend above the pinyonpine-juniper region along hillsides. Parasitismwas found to be more individualistic in thisspecies than in other ground squirrels of theregion, being approximated in this regard onlyby S. variegatus. The major species of helminthis Citellina triradiata Hall, present in 74.7%of specimens. Several additional species ofnematodes, Spirura infundibuliformis McLeod,and a species of Subulura also appear to berestricted to this host.

Discussion and ResultsIt is interesting to note that S. townsendi,

which occurs sympatrically with A. leucurus,also possesses Citellina triradiata as its majorparasite rather than possessing the parasitesof its two nearest relatives, S. armatus and S.beldingi. Townsend ground squirrels appearto be primarily vegetarian in diet and do notacquire the parasites requiring insect inter-mediate hosts found in A. leucurus. Townsendground squirrels also have an activity periodthat varies greatly from that of S. armatus, S.beldingi, and A. leucurus in that these animalsare active only from February to July afterwhich they enter into a 71/£-month period ofinactivity. This unique activity pattern, vege-tarian diet, and independent migration intothe area from the west has produced analmost totally different parasitic fauna in theTownsend squirrel than occurs in its twonearest relatives in the subgenus. Additionalevidence that the Townsend squirrel has ac-


OF WASHINGTON, VOLUME 40, NUMBER 1, JANUARY 1973 79

Table 1. Parasite-host records for ground squirrels of Western Utah.*

Parasite species

PROTOZOARhizopoda:

Entamoeba citelliBecker, 1926

Mastigophora:Chilomastix magna

Becker, 1926

Hexamastix rnurisWenrich, 1924

Hexamites teresKirby and Honigberg,1949

Monocercomonoidespilleata Kirby andHonigberg, 1949

M. robustus Gabel, 1954

Tritrichomonas murisGrassi, 1879

THEMATODABrachylaimidae :

Brachylaime microtiKniidenier andGallecchio, 1959

CESTODA ( adult ) :Mesocestoididae :

Mesocestoides cortiHoeppli, 1925

Anoplocephalidae :Cittotaenia sp.

Hymenolepididae :Hi/menolepis citelli

McLeod, 1933

Davaineidae:Raillietina retractilis

Stiles, 1925

Su

bg

en

us O

tosp

crm

op

hilu

sS

pe

rmo

ph

ilus

varie

ga

tus

Uta

h M

err

iam

Su

bg

en

us S

pe

rmo

ph

ilus

Sp

erm

op

hilu

s a

rma

tus

( Ke

nn

ico

tt )

I f 2

18/50:1: 9/16

6/50 6/16

10/50 5/16

1/16

28/50 15/16

6/50 7/16

9/50 13/16

4/154

1/154

4/154

5/154

Sp

erm

op

hilu

s b

eld

ing

icr

eb

us

Me

rria

m

Sp

erm

op

hilu

s to

wn

sen

di

mo

lis (

Ke

nn

ico

tt )

Su

bg

en

us C

allo

spe

rmo

ph

ilus

S. l

ate

ralis

la

tera

lis(S

ay)

3 4 5

3/5 8/20 15/38

3/38

1/5 4/38

X 1/38

4/5 4/20 20/38

1/5 5/38

3/5 4/20 12/38

4/100

2/100

Ge

nus

Am

mo

spe

rmo

ph

ilus

Am

mo

spe

rmo

ph

ilus le

ucu

rus

leu

curu

s M

err

iam

6

3/10

5/10

1/10

2/10

10/10

2/10

1/10

8/135

Previous reports in literature

Dajani, 1962 (It , 5, 6)

Evans, 1955 (6)

Kirby and Honigberg, 1949 (3,

Kirby and Honigberg, 1949 (3,

Kirby and Honigberg, 1949 (3,Evans, 1955 (6)

Kirby and Honigberg, 1949 ( 5 )Evans, 1955 (6)

Grundmann, 1958 (6)Hansen, 1954 (6)

5)

5)

5)

CESTODA (larval)Taeniidae:

Taenia hydatigenaPallas, 1866

2/154 2/135 Hansen, 1954 (1)Grundmann, 1958 (6)



Table 1 cont'd.

|-cs c

!seo, r^-i ^

2 3

r~ s

»"8 »";3 s e . ^ s . s3 _<«C/3 C/3 CO o IX! ft C/} (_)

Parasite species

2'. mustelaeGmelin, 1790

T. rifeyi Loewen, 1929

T. taxidicnsisSkinker, 1935

Cladotacnia globiferaBatsch, 1786

NEMATODATrichuridae:

Trichuris citelliChandler, 1945

Trichuris sp. (possiblyT. perognathi)

Capillarinae:Capillaria hepatica

Bancroft, 1843

Trichostrongylidae :Citellincma bifurcatum

Hall, 1916Ostertagia circumcincta

Stradelmann, 1894Trichostronglus

colubriformis Giles

Oxyuridae:Citellina triradiata

Hall, 1916

Syphacia citelliTiner and Rausch,1950

If 2 3 4 5 6 Previous reports i n literature

5/154 1/35 2/100

2/154 1/135 Grundmann, 1958 (6)

3/154

3/154

18/154

1/154

3/154

7/154 6/35 1/12

1/35 1/12

1/35 1/12 1/100

1/35 8/12 100/135 Grundmann, 1957 (6)

101/154 22/35 1/12 Tiner and Rausch, 1950 (2)

Spiruroidea:Rictulariidae:

Ritcularia coloradensisHall, 1916

Rictularia sp. (possiblyaffinis or splcndida)

Spiruridae:Spirura infundibuli-formis McLeod, 1933

Subuluridae:Subulura sp.

Physalopteridae:Physaloptera massino

Schultz, 1927

1/54

1/100

1/25

3(135 Grundmann, 1957 (6)

5/135

2/135

7/135 Grundmann, 1957 (6)

ACANTHOCEPHALA

Moniliformidae:Moniliformis clarki

Ward, 19171/154 1/100 2/135



Table 1 cont'd.

Parasite species

Su

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op

hilu

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pe

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ph

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va

rie

ga

tus

Uta

h M

err

iam

It

Su

bg

en

us S

pe

rmo

ph

ilus

Sp

erm

op

hilu

s a

rma

tus

( Ke

nn

ico

tt )

2

Sp

erm

op

hilu

s b

eld

ing

icre

bu

s M

err

iam

Sp

erm

op

hilu

s to

wtiscn

di

mo

lis (

Ke

nn

ico

tt)

Su

bg

en

us C

allo

sp

erm

op

hilu

sS

. la

tera

lis l

ate

ralis

(Sa

y)

3 4 5

Ge

nus

A

mm

osp

erm

op

hilu

sA

mm

osp

erm

op

hilu

s le

ucu

rus

leu

cu

rus M

err

iam

6 Previous reports in literature

AllTHBOPODAf

Siphonaptera:Fain. Hystrichopsyllidae

(Tiraboschi)

Subfam. HystrichopsyllinaeHystrichopsylla dippei

truncata HollandHystrichopsylla sp.Rhadinopsylla heiseri

(McCoy)

Subfam. NeopsyllinaeNeopsylla inopina

RothschildCatallagia decipiens

RothschildMcringis dipodomys KohlsM . parkeri Jordan

Subfam. AnomiopsyllinaeConorhinopsylla stanfordi

StewartMegarthroglossis smiti

MendezFam. Ceratophyllidae Dampf

Thrassis acamatusutahensis ( Wagner )

T. francisi francisi(Fox)

T. pandorae Jellison

T. petiolatus (Baker)T. bacchi caducus

( Jordan )T. b. gladiolus (Jordan)

T. b. consimilis StarkT. arizonensis arizonesis

(Baker)

Diamanus montanus(Baker)

Nosopsyllus fasciatus(Bosc)

Oropstjlla idahoensis(Baker)

O. rupcstrisOpisthocrostis

tubcrculatus (Baker)

4/61

3/61

X1/61

X

X

43/61

X

1/61

8/61

XX

X

1/14

3/14

X3/14

X

X

7/14

X

4/14

1/14

3/14

2/24

1/24

X

X 2/24

X 2/12 1/24X 2/24

X1/12 X

4/12 11/24

X 3/12 4/24

X 2/12 3/24

X

XX

1/14

XX

XX

X

10/14

2/14

6/14

Stark, 1958 (2)Stark, 1958 (2, 5)Hansen, 1954 (6)Stark, 1954 (6)

Hansen, 1954 (2)Stark, 1958 (2)

Stark, 1958 (1)Stark, 1958 (6)Stark, 1958 (6)

Stark, 1958 ( 4)

Stark, 1958 (6)

Hansen, 1954 (4)Stark, 1958 (1 ,2)

Stark, 1958 (1,2, 4, 6)Hansen, 1954 (2, 4)Stark, 1958 (1, 2, 4, 6)

Stark, 1958 (2)

Stark, 1958 ( 5, 6 )Hansen, 1954 (4, 6)Stark, 1958 (1, 2, 4, 6)Stark, 1958 (1, 6)

Stark, 1958 (2)

Hansen, 1954 (1, 2, 4, 5, 6)Stark, 1958 (1, 2, 5, 6)Stark, 1958 (1, 2)

Hansen, 1954 (2, 3, 4, 5)

Stark, 1958 (1, 2, 5, 6)

Hansen, 1954 (2, 3, 4, 6)Stark, 1958 (1, 2)



Table 1 cont'd.

Parasite species

O. t. cynomuris JellisonO. hirsutus (Baker)

O. labis (Jordan andRothschild)

Dactylopsljlla ignotautahensis (Wagner)

D. ignota apachina Fox

Orchopeas leucopus(Baker)

O. sexdentatus (Baker)Opisodasys keeni keeni

(Baker)Malareus bitterrootensis

( Dunn )

M. sinomus JordanMonopsljllus wagneri

wagneri Baker

Monopsljllus vision(Baker)

M. eumolpi (Rothschild)

M. e, cyrturus JordanMegabothris abantis

(Rothschild)Fain. Pulicidae Stephens

Subfam. PulicinaePulex sp. pos. irritansSubfam. SpilopsyllinaeEchidnophaga gallinacea

WestvvoodCediopsylla inaequalis

inaequalis (Baker)Hoplopsljlla anomalus

Baker

Phtheraptera : Fam .HematopinidaeEnderleinellus suturalis

OsbornEnderleinellus sp.Hoplopleura acanthopus

BurmeisterNeohaematopinus citcl-

linus FerrisN. laeviusculus Grube

Su

bg

en

us O

tosp

erm

op

hilu

sS

pe

rmo

ph

ilus

varie

ga

tus

uta

h M

err

iam

I t

X

X6/61

X2/61

X

X

X

X

25/61

12/61

Su

bg

en

us S

pe

rmo

ph

ilus

Sp

erm

op

hilu

s a

rma

tus

( Ke

nn

ico

tt )

2

XX

X

X

X

XX

2/14

1/14

1/14

X

6/14

Sp

erm

op

hilu

s b

eld

ing

icr

eb

us M

err

iam

Sp

erm

op

hilu

s to

wn

sen

di

mo

lis (

Ke

nn

ico

tt)

3 4

X

X

5/12

X

X X

Su

bg

en

us C

allo

spe

rmo

ph

ilus

S. l

ate

ralis

la

tera

lis(S

ay)

5

X

1/24

5/24

X

X

X

X

X

1/24

X

1/24

1/24

X

1/24

Ge

nus

A

mm

osp

erm

op

hilu

sA

mm

osp

erm

op

hilu

s le

ucu

rus

leu

curu

s M

err

iam

6

X

X

1/14

1/14

X

1/24

X

1/14

X

X1/14

Previous reports in literature

Stark, 1958 (1, 2)Hansen, 1954 (6)Stark, 1958 (2, 5)

Stark, 1958 (2, 4, 6)

Stark, 1958 (6)Stark, 1958 (1)

Stark, 1958 (1, 5)

Stark, 1958 (5)

Hansen, 1954 (2, 5, 6)Stark, 1958 (1, 2, 5)

Stark, 1958 (5)

Hansen, 1954 (2, 5)Stark, 1958 (1, 2, 5)Stark, 1958 (2)Stark, 1958 (2 ,5)

Hansen, 1954 (1)Stark, 1954 (6)Hansen, 1954 (1)Stark, 1958 (5)

Stark, 1958

Hansen, 1954 (2, 4, 5,Bell, 1950 (4, 5)

Bell, 1950 (2, 5)

Hansen, 1954 ( 6)Hansen, 1954 (1,2, 3,Bell, 1950 (2, 4, 5)

8)

4)

ACAHIN A

Suborder MesostigmataFain. Dermanyssidae

Kolenati



Table 1 cont'd.

0- 0,3 S

11

!»§ 3

0 C

"2£0 £7s §S I"-"5 - 5?

^'~a.0

as

3K

CO O

t™3 ^J

!|i

111

S S"S v§3 s~tO JX-iS tC JS.HH J ~

CO CO CO i

Parasite species If 2 3

Hirstionyssuscarniflex Koch X

H. incomptus Eadsand Hight

H. trlcanthus Koch XFam. Laelaptidae Berlese

Hypoaspis levicitlusEwing

Hacmolaclapsglasgowi Ewing 3/61 2/14

Haemolaelaps sp. 2/14Suborder TrombidiformesFam. Trombiculidae Ewing

Enschongastia sp. 2/61 1/14Trombicula sp. 1/61

ACARINA (ticks)Dermacentor andersoni

Stiles 23/61 9/14 XD. parumapertus

Neumann 2/61 2/14 1/5Ixodes marmotae

Cooley and Kohls 1/12I. sculptus Neumann X/. kingi Bishopp

INSECTAOrder Diptera(larvae determined tofamily with theexception of one case)

Anthomyidae 1/54Calliphoridae

Cecidomyidae Sp. ISp. II 1/154Sp. Il l

Hylemya Sp. ISp. IISp. Il lSp. IVSp. V 1/154Sp. VI 1/154Sp. VII 1/154Sp. VII I 1/135

Mycetophyllidae Sp. ISp. II

Muscidae 1/135Nitidylidae

Chijchramus adastrisPhoridae 1/154RhagoletisSarcophagidae 1/154

j^ .&> to co^o •%*>-

co S co

4 5

X

X 4/24

4/24

21/24

X

1/241/24

1/25

1/1001/100

2/100

1/1001/1001/1001/1001/100

2/100

1/100

2/100

2/100

§g|

o6 Previous reports in literature

Hansen, 1954 (2)

2/141/14 Hansen, 1954 (2)

Hansen, 1954 (5)

Hansen, 1954 ( 2 , 4 ,5)

Hansen, 1954 (5)X Hansen, 1954 (6)

Hansen, 1954 (1, 2, 3, 5)

X Hansen, 1954 (4, 6)Edmunds, 1948 (2)Hansen, 1954 (2, 3, 5)Edmunds, 1948 ( 2 )

1/14

1/135

1/135

* Includes data from all sources. Data contributed by the present study is expressed by number of infected animals overnumber processed. Records from literature only are represented by X and followed by reference.

f Host species are numbered to correspond to previous reports in literature in right-hand column.:;: Not all specimens were processed for protozoa and ectoparasites.



quired its parasites from its association withthe antelope ground squirrel is that a secondnematode, Physaloptera massino Shultz, is alsopresent in both but not in other ground squir-rels of the region.

Most of the helminths listed in Table 1 wererestricted to one or two species of groundsquirrels. Few are host-specific to the specieslisted except in this area, and the majorityhave a wide distribtuion in North America.Seven species were found to inhabit at leastthree of the six host species. Continued collec-tion wil l probably increase this number. Para-sites exhibiting broad host involvement inaddition to residence in ground squirrels are:Trematodes: Brachylaime microti Kruidinierand Gallecchio (ground squirrels, deer mice,and voles). Cestodes: Mesocestoides cortiHoeppli (ground squirrels, house mice, andcarnivores); Hymenolepis citelli McLeod(ground squirrels, deer mice, chipmunks,grasshopper mice, pocket gophers, and Ordkangaroo rats); Raillietina retractilis Stiles(ground squirrels, jack rabbits, and kangaroorats); larval Taenia mustelae Gmelin (groundsquirrels and deer mice). Nematodes: Capil-laria hepatica Bancroft (ground squirrels, deermice, pocket gophers, and voles); Citellonemabifurcation Hall (ground squirrels and mar-mots); Trichostrongylus colubriformis Giles(ground squirrels, sheep, goats, and cattle);Ostertagia circumcincta Stradelman (groundsquirrels, deer mice, chipmunks, tree squirrels,sheep, and goats); Physaloptera massino Shultz(ground squirrels, house mice); and Rictulariacoloradensis Hall (ground squirrels, deer mice,chipmunks, pocket mice, and weasels). Acan-thocephala: Monilijormis clarki Ward (groundsquirrels, deer mice, pocket gophers, chip-munks, and voles).

Special mention should be made of Trich-ostrongylus colubriformis and Ostertagia cir-cumcincta, both considered to be mainly para-sites of sheep and goats. It is likely thesespecies were introduced into the region alongwith sheep. These species probably weretransferred from sheep to ground squirrels inmountain habitats capable of sustaining thelif e history of the worms but not in deserthabitats used by sheep as winter range. Whatis important is that ground squirrels couldpossibly act as a reservoir of infection in suit-

able locations and complicate control measuresdesigned for sheep.

Why S. lateralis and S. variegatus have buttwo helminth species of a total of 21 in com-mon even though their habitats overlap canbe explained only through physiological andbehavioral differences resulting from speciation.However, both hosts share all of the protozoanspecies. It is easier to explain why A. leucurusand S. lateralis have two helminths in commonbecause one is a desert rodent and the lattera high-mountain resident. Moreover, bothcommon parasite species in this instance haveintermediate hosts that are burrow-dwellinginsects and are not restricted by altitudinaldifferences. S. armatus and S. beldingi havefour helminth species in common, but thesetwo hosts belong to the same subgenus andoccupy adjacent ranges.

Parasites suggesting specificity to genus ofhost are the following: Syphacia citelli (S.armatus, S. beldingi, and S. variegatus). Thisoxyurid has been previously reported by Tinerand Rausch (1950) from S. armatus in Wyo-ming and from S. variegatus by Kruidinierand Peebles in Arizona. Trichuris citelli (S.variegatus) has been previously reported fromS. beecheyii in California by Chandler (1945).Furthermore, in the total of 18 cases T. citelliwas never found as a single infection but wasalways accompanied by Syphacia citelli sug-gesting dependence on either previous or con-current infection with the latter species.

Infection rates were based on both the di-versity and number of parasite species presentin each host and the high incidence producedby principal species having highly developedpatterns of dissemination. Most heavily para-sitized were S. variegatus (70.5%), S. town-sendi (72%), and A. leucurus (71.5%). Thesewere followed by S. armatus (39.2%) and S.beldingi (42.8%). S. lateralis at 7.3% showedthe lowest parasitism. S. variegatus wouldreasonably be expected to have the highestrate in that it (1) has the largest number ofparasitic species, (2) has expanded its nicheto include urban and suburban habitat as wellas taking over the role of the Norway andbrown rat in recreational areas, (3) normallyinhabits the transitional habitat between desertand higher mountains where environmentalconditions are more variable and the commu-



nity consists of a greater number of species,and (4) is parasitized by an oxyurid species,Syphacia citelli Tiner and Rausch, that isextremely prevalent. In the case of S. town-sendi and A. leucurus leucurus, both desertforms, the high percentage of parasitism isassociated with the high incidence of Citellinatriradiata Hall, mediated by the variety andsuccession of food in a desert habitat that en-sures that fecal pellets will constitute a con-siderable part of the diet when other food isnot abundant.

Males of most of the host species showedhigher incidence of parasitism than females.Trapping success in S. variegatus yielded ap-proximately 40% males and 60% females ofwhich 35.6% of the former and 23.5% of thelatter were parasitized with one or more spe-cies. A similar situation was present in S.armatus where 41.6% of males and 33.3% offemales were infected. In S. lateralis, however,the majority of infections in males were casesof myiasis while females revealed Rictulariacoloradensis and Moniliformis clarki cases notrecovered from males, suggesting greater de-pendence of nesting females on burrow-in-habiting insects such as the camel cricket,Ceuthophilus utahensis, the natural host ofthese species. Lower infection rates in femalesalso may be due to sex-hormone-induced re-sistance as established by Mathies (1959) instudies with Aspiculuris tetraptera in mice.Testosterone in males is also known to enhancesusceptibility.

A trichinosis survey was conducted on 100selected specimens from the six host species.The bulk of the specimens (S. variegatus, S.armatus, and S. lateralis} were collected aboutcampgrounds and garbage disposal areas inthe Wasatch Mountains where a potential forinfection exists. Completely negative resultswere obtained but these results are not con-sidered conclusive because the specimens camefrom too limited a number of localities. How-ever, with the heavy visitor pressure nowpresent in most recreational areas and withthe present garbage disposal methods whereForest Service sanitaiy landfills are left ex-posed for long periods, it will be only a matterof time before T. spiralis is introduced. As faras is known, all ground squirrel species, withthe possible exception of S. townsendi, are sus-ceptible to infection.

Three protozoan species were present in allhost species. These were Entamoeba citelliBecker which is specific to ground squirrels.The flagellates, Monocercomoides pileata Kirbyand Honigberg, and Tritrichomonas murisGrassi, were also present in all host species.Additional study of the host species otherthan the antelope ground squirrel that wasthoroughly studied by Evans (1955, 1956,1959) might reveal that other protozoans listedmay also occur universally in ground squirrels.

Littl e host selectivity could be demonstratedin the ectoparasites recovered. Most have beenrecovered from rodent species other thanground squirrels and it appears that consider-able normal exchange occurs. Two species offlea, Opisthocrostis tuberculatus Baker andOropsylla idahoensis Baker, were present onall six hosts, although individuals of these spe-cies were not as numerous nor did they havethe incidence of parasitism that Diamanusmontanus Baker and Hoplopsyllus anomalusBaker had on five of the six hosts. Among thelice, only Neohematopinus laeviuscula Grubewas universal in distribution and quite numer-ous. Among the mites, the most frequentlyrecovered was Haemolaelaps glascowi Ewing.

In western Utah, the Rocky Mountainspotted fever tick, Dermacentor andersoniStiles, is generally present above 6,000 feet inelevation while D. parumapertus Neumann ispresent in the lower areas. These species lackhost specificity and the absence of either spe-cies on a host is due to altitudinal restriction.The restriction of Ixodes kingi to A. leucuruscould also be distributional.

The Diptera larvae recovered probablyrepresent accidental ingestion of fly-infestedfood while the host was feeding in garbagecans and dumps about forest recreation areas.It was not possible to establish that true myiasiswas present in these cases although a numberof the genera represented are known to as-sume this role. Adult flies were not rearedsince most specimens were preserved at thetime of collection.

AcknowledgmentsThe authors are indebted to Dr. Dorald M.

Allred, Department of Zoology and Entomol-ogy, Brigham Young University, for his assist-ance in determination of the Acarina; to M. B.


86 PROCEEDINGS OF THE HELMINTHOLOGICA L SOCIETY

Chitwood, Parasite Identification Laboratory,ARS-USDA, Beltsville, Md., for confirmationof Trichostrongylids; to Dr. Elmer Johnson,Ecodynamics of Utah, for aid in the determina-tion of ticks and lice; to C. W. Sabrosky, R. H.Foote, G. C. Steyskol, and W. H. Anderson,Insect Identification and Parasite IntroductionResearch Branch, USD A, U. S. National Mu-seum, for the identification of Diptera larvae.

Literatur e CitedBeck, D. E. 1955. Distribution studies of para-

sitic arthropods in Utah, determined as ac-tual and potential vectors of Rocky Mountainspotted fever and plague, with notes on vec-tor-host relationships. Brigham Young Uni-versity Sci. Bull. Ser. 1: 1-64.

Becker, E. R. 1926a. The flagellate fauna ofthe caecum of the striped ground squirrel,Citellus tridecemlineatus, with special refer-ence to Chilomastix magna sp. nov. Biol.Bull. 51: 287-298.

. 1926b. Endamoeba citelli sp. nov. fromthe striped ground squirrel, Citellus tridecem-lineatus, and the lif e history of its parasiteSphaerita endamoebae sp. nov. Biol. Bull.444: 454.

Bell, I. L. 1950. A study of sucking lice (Ano-plura) on rodents in Utah. Unpub. M.S.thesis, Univ. of Utah, 55 p.

Chandler, A. C. 1945. Trichuris species fromCalifornia rodents. J. Parasit. 31: 284-286.

Dajani, S. W. 1962. A study of the intestinalamoeba of some Utah rodents. M.S. thesis,University of Utah, 102 p.

Doran, D. J. 1954. A catalogue of the proto-zoa and helminths of North American ro-dents. 1. Protozoa and Acanthocephala. Am.Midi . Nat. 52: 118-128.

. 1955. A catalogue of the protozoa andhelminths of North American rodents. III .Nematoda. IV. Trematoda. Am. Midi. Nat.53: 162-175.

Durrani , S. D. 1952. Mammals of Utah, tax-onomy and distribution. Univ. of KansasPubl. Mus. Nat. Hist. 6: 1-549.

Edmunds, L. R. 1951. A check list of theticks of Utah. Pan Pacific Ent. 27: 23-26.

Evans, F. R. 1955. Survey of the caecal flagel-lates of the antelope ground squirrel, Citellusleucurus leucurus (Merriam). J. Protozool. 2(Suppl.): 1-2.

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Frandsen, J. C., and A. W. Grundmann.1961. Endoparasitism in isolated populationsof rodents of the Lake Bonneville Basin,Utah. J. Parasit. 47: 391-396.

Grundmann, A. W. 1957. Nematode parasitesof mammals of the Great Salt Lake Desertof Utah. J. Parasit. 43: 105-112.

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Hansen, R. M. 1954. Ground squirrels (Citel-lus) of Utah. Ph.D. thesis, Dept. of Zool.and Ent., Univ. of Utah, 197 p.

Hoffman, G. L. 1956. Medical parasitologylaboratory manual. Burgess, Minneapolis,Minn.

Jellison, W. L. 1945. Siphonaptera: the genusOropsylla in North America. J. Parasit. 31:83-97.

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McLeod, J. A. 1923. A parasitological surveyof the genus Citellus in Manitoba, Canada.J. Res. 9: 108-127.

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The Parasitology of the Ground Squirrels of Western Utah - BioNames

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