The Parasitology of the Ground Squirrels of Western Utah

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 intestinal protozoa (except Coccidia), endoparasitic helminths and dipteran larvae, and ectoparasites. A complete list is included. The probable results of host post-Pleistocene migration on parasitism are described. Parasite-host interrelationships are discussed. A parasitological study of the ground squirrels (Spermophilus and Ammospermophilus) was conducted throughout the Bonneville Basin and surrounding mountains that make up the western half of Utah. Most of the six species included reach the limits of their geographical distribution in this region and represent the present state of the migration that has occurred since Pleistocene Lake Bonneville receded to form the present Great Salt Lake. The ranges of the species are, with several exceptions, allopatric, and provide a probable record of some host-restricted parasites carried in with host migrations as well as those acquired through interrelationships with other genera of mammals in the region. Included in the study were helminths, intestinal protozoa (excluding Currently U. S. Army Medical Corps. Coccidia), myiasis-producing Diptera larvae, and ectoparasites. Two extensive systematic and distributional studies of the hosts in Utah are those by Durrant (1952) and Hansen (1954). In addition to systematics, Hansen also reported on the parasitic fauna, especially the ectoparasites. Helminths of the antelope ground squirrel were reported by Grundmann (1957, 1958), and Frandsen and Grundmann (1961) published on the helminths of several additional host species. Doran (1954, 1955) compiled parasite lists for rodent species. Excellent publications on fleas that provide pertinent data are those of Stark (1958), Jellison (1945), Jellison et al. (1953), Hansen (1954), and Beck (1955). Sucking lice were reported 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 these studies are acknowledged in Table 1. Kirby and Honigberg (1949) and Evans (1955, 1956, 1957, 1959) studied the flagellates 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 one have been conducted in North America. Most of these have been concerned with defined categories of parasites such as helminths or protozoa, and none has covered as broad a range as the present study. The most extensive previous study was that of McLeod (1933) in Manitoba, Canada, which covered helminths and ectoparasites of three species of squirrels. Rausch and Tiner (1948) surveyed 325 sciurids from the North Central States. Voge (1956) published a summary of California nematode parasites. A number of parasite species reported in these publications also were found in the Bonneville Basin. Materials and Methods A total of 490 specimens was live-trapped or shot from 60 localities distributed over the 14 western counties of Utah extending from Boxelder and Summit on the north to Washington on the south. Trapsites ranged in elevation from 4,200 feet adjacent to the Great Salt Lake to 4,800 at the southern end of the Bonneville Basin floor. In the higher mountain ranges in and surrounding the basin, the study extended to 11,000 feet elevation. The sample included 181 rock squirrels, Spermophilus variegatus Utah Merriam; 100 golden mantled ground squirrels, S. lateralis lateralis (Say); 12 Belding squirrels, S. beldingi crebus Hall; 35 Uinta, S. armatus (Kennicott); 25 Townsend, S. townsendi mollis Kennicott; and 135 antelope ground squirrels, Ammospermophilus leucurus leucurus (Merriam). Animals removed from traps were placed in muslin bags for transport to the laboratory. Animals shot were also bagged to gain maximum recovery of ectoparasites. Live animals were etherized while still in the bags, and upon removal were combed, washed in detergent, and beaten to remove ectoparasites before autopsy. Before discarding, the carcass was placed in a bag and refrigerated at 36 F for 24 hr. This procedure caused the ectoparasites remaining to move to the hair tips where they could be collected. In the case of animals examined for protozoa, specimens were taken from the ileum, cecum, and colon immediately after the abdominal cavity was opened. Slide material was fixed in Schaudinn's and stained with iron hematoxylin. Tapeworms were relaxed in chloretone-saline solution, flattened, fixed in AFA, stained in acid alum carmine, and mounted. Nematodes were fixed either in hot 70% alcohol or in Kahle's, washed to remove the formaldehyde, and stored in 70% alcohol. Specimens were cleared in chlorolactophenol d'Amann for study and returned to storage in 70% alcohol. Examination for Trichinella spiralis was done by removing a sample of approximately 1.25 g of muscle tissue from the diaphragm, tongue, and leg muscles. The sample was cut into small pieces and subjected to digestion (Hoffman, 1956), at 37-39 C using a shaker. Fleas and ticks were prepared for mounting by being placed in warm 10% KOH for 2 hr, neutralized in acid alcohol, dehydrated in alcohol, and mounted in Hoyer's solution. Mites and lice were prepared in a similar manner omitting the KOH step. Host Distribution The six ground squirrel species are currently divided among three subgenera of Spermophilus and one of Ammospermophilus. The subgenus Spermophilus is represented by S. armatus, S. beldingi, and S. townsendi. The former two species are thought to have entered the Bonneville Basin region from the north and the northwest while townsendi invaded from the west (Hansen, 1954). S. beldingi has the most limited distribution in the region and occurs only in the Raft River Mountains located in the extreme northwest corner of Utah where the animal also reaches the most southern and eastern limits of its range. The habitat of the Belding ground squirrel is primarily the moist upland meadow. S. armatus inhabits the drier situations in mountains, foothills, and high valleys in the Wasatch and central mountain chain that forms the eastern rim of the Bonneville Basin. The range as it occurs marks both the western limit of migration in northern Utah with the southern limit being reached in Sevier County Copyright © 2011, The Helminthological Society of Washington 78 PROCEEDINGS OF THE HELMINTHOLOGICAL SOCIETY near the center of the state. These animals select cultivated fields and pastures around developed areas and are abundant in welldrained situations such as knolls and in man-constructed banks of canals, roads, and railroads. Where its habitat coincides with recreational areas, the species is a frequent inhabitant of garbage areas and campgrounds. Spcrmophilus townsendi mollis inhabits the northern three-fourths of the Bonneville Basin and is a desert valley form located in discrete population groups about moist areas such as springs and seeps. Townsendi range is allopatric in relation to its two closest relatives described above although farther north in Idaho there are limited areas of overlap with beldingi. The Townsend squirrel is closely associated in the habitat with the antelope ground squirrel, Ammospermophilus leucurus leucurus Merriam, that also inhabits the desert conditions of the basin and with whom it shares most of its parasites. The subgenus Otospermophilus is represented by S. variegatus utah Merriam. Rock squirrel distribution in Utah coincides with the distribution of the scrub oak, Quercus gambellii Nuttall, which the animal utilizes for its basic food resources. Rock squirrels have extended their distribution into some of the desert mountain ranges of the basin where it is usually the only squirrel present above the foothill habitat where one encounters the antelope ground squirrel. The rock squirrel, however, has extended its niche greatly by adapting to suburban and urban living in human communities. It has also moved into the niche afforded by forest service garbage dumps and campgrounds and by so doing has expanded both its population density and its parasite diversity. Rock squirrel range overlaps that of the golden mantled ground squirrel, S. lateralis lateralis Say, at elevations around 7,000 to 7,500 ft. S. variegatus reaches its northern limit near the Utah—Idaho border and is considered to have invaded the region from the south as ancient Lake Bonneville receded. The subgenus Callospermophilus has one representative, S. lateralis lateralis Say, in the region. The golden mantled ground squirrel is an inhabitant of canyon bottoms and suitable forested areas in the aspen-fir and spruce—fir belts from about 7,000 to 10,500 feet elevation. Colorado is considered to be the center of dispersal of this species and its migration into Utah has been from the east and north down the central mountain chain. The golden mantled ground squirrel had the lowest incidence of parasitism in the study group (7%) and, to date, only two parasite species have been present that have not been recovered from other ground squirrels. These are a larval tapeworm, Taenia mustelae Gmelin, and an adult of Cittotaenia. Ammospermophilus leucurus leucurus Merriam, the antelope ground squirrel, is the lone representative of its genus in the region. The species inhabits the dry desert of the basin floor and low foothills where the rainfall is less than 10 inches per year. Antelope ground squirrels favor rocky outcrops and vegetated dunes and do not extend above the pinyon pine-juniper region along hillsides. Parasitism was found to be more individualistic in this species than in other ground squirrels of the region, being approximated in this regard only by S. variegatus. The major species of helminth is Citellina triradiata Hall, present in 74.7% of specimens. Several additional species of nematodes, Spirura infundibuliformis McLeod, and a species of Subulura also appear to be restricted to this host. Discussion and Results It is interesting to note that S. townsendi, which occurs sympatrically with A. leucurus, also possesses Citellina triradiata as its major parasite rather than possessing the parasites of its two nearest relatives, S. armatus and S. beldingi. Townsend ground squirrels appear to be primarily vegetarian in diet and do not acquire the parasites requiring insect intermediate hosts found in A. leucurus. Townsend ground squirrels also have an activity period that varies greatly from that of S. armatus, S. beldingi, and A. leucurus in that these animals are active only from February to July after which they enter into a 71/£-month period of inactivity. This unique activity pattern, vegetarian diet, and independent migration into the area from the west has produced an almost totally different parasitic fauna in the Townsend squirrel than occurs in its two nearest relatives in the subgenus. Additional evidence that the Townsend squirrel has acCopyright © 2011, The Helminthological Society of Washington OF WASHINGTON, VOLUME 40, NUMBER 1, JANUARY 1973 79 Table 1. Parasite-host records for ground squirrels of Western Utah.* Parasite species PROTOZOA Rhizopoda: Entamoeba citelli Becker, 1926 Mastigophora: Chilomastix magna Becker, 1926 Hexamastix rnuris Wenrich, 1924 Hexamites teres Kirby and Honigberg, 1949 Monocercomonoides pilleata Kirby and Honigberg, 1949 M. robustus Gabel, 1954 Tritrichomonas muris Grassi, 1879 THEMATODA Brachylaimidae : Brachylaime microti Kniidenier and Gallecchio, 1959 CESTODA ( adult ) : Mesocestoididae : Mesocestoides corti Hoeppli, 1925 Anoplocephalidae : Cittotaenia sp. Hymenolepididae : Hi/menolepis citelli McLeod, 1933 Davaineidae: Raillietina retractilis Stiles, 1925 S ub ge nu s O to sp cr m op hi lu s Sp er m op hi lu s va ri eg at us