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Helminths of Squirrels (Sciuridae)

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Helminths of Squirrels (Sciuridae) Occasional Papers Museum of Texas Tech University Number 303 5 October 2011 HELMINT H S OF SQUIRRELS (SCIURIDAE ) FROM MONGOLIA DAVI D S. TINNIN , SUMIYA GANZORI G , AN D SCO tt L. GAR D NER ABSTRACT Two species of ground squirrels, Urocitellus undulatus and Spermophilus alashanicus, were collected and examined for parasites from two localities in Mongolia in 1999. A total of 24 individuals of U. undulatus were examined resulting in a total of six taxa of helminths found, including: Ascaris tarbagan, Physaloptera massino, Streptopharagus kutassi, Anoplocephaloides transversaria, Hymenolepis suslica, and Moniliformis sp. This represents four new species records and an additional host record for the country. Two individuals of S. alashanicus were examined and found to be uninfected. Key words.—acanthocephala, cestode, helminth, Mongolia, nematode, Spermophilus, squirrel, Urocitellus INTRODUCTION The geographic distribution of the long-tailed which some authors consider to be synonymous with ground squirrel, Urocitellus undulatus (Pallas 1778) C. marmotae; Mesocestoides sp.; and Moniliformis extends through a wide band of central Asia including moniliformis (Bremser 1811) (see Danzan 1978; Gan- suitable habitats in Kazakhstan across southern and zorig et al. 1988; Ganzorig et al. 1998; Ganzorig et eastern Siberia through Mongolia and into northern al. 2007). Tokobaev (1976) reports the finding of two China (Tinnin et al. 2002). Although patchy in occur- helminths, Trichuris citellorum (Kirshenblat 1939) and rence through this region, these squirrels are found in Ctenotaenia citelli, from Kazakhstan. great abundance in some areas with numerical densi- ties sometimes exceeding 18 individuals/hectare (ha) In contrast, there have been nine publications (Tinnin 2002) with some observers reporting very high that examined the parasite fauna of the long-tailed densities of “…hundreds all over the plains” (Allen ground squirrel in eastern Siberia, reporting 35 spe- 1940). cies of helminths. Six of these are surveys from the region of Lake Baikal (Machulskii 1958; Nadtochi et al. Published information on endoparasites of U. 1966; Eltyshev and Maklokova 1971; Eltyshev 1975; undulatus has also historically been patchy in time Shalaeva et al. 1987; Zhaltsanova and Shalaeva 1990). and space. In Mongolia, four species of helminths The three additional papers were each a single species have been reported from this host: Ctenotaenia mar- description from the regions of Tuva (Sulimov 1961a, motae (Frölich 1802); C. citelli (Kirshenblat 1939), 1961b) and Yakutsia (Ryzhikov 1956). 2 OCCASIONAL PA P ERS , MUSEUM OF TEXAS TEC H UNIVERSITY The Alashan ground squirrel, Spermophilus From 9 July through 2 August 1999, small mam- alashanicus Büchner 1888, in comparison has a rather mals were collected from 13 sites as part of a survey restricted range across the Ala Shan Mountains of of small mammal and parasite diversity in Mongolia northwestern China and the Gobi Altai Mountains of (Tinnin et al. 2002; Tinnin et al. 2008). The results southern Mongolia. However, the literature seems to of the examination for helminths of 24 individuals indicate that they have never previously been examined of Urocitellus undulatus and two individuals of S. for parasites. alashanicus are presented in this study. MATERIALS AND MET H ODS Squirrels were collected from two localities in for later examination for microfilariae or hemopro- Mongolia in July 1999. The first site, Ulaan Tsutgaalan tozoa, and fecal samples were collected for study of (46º47'13"N, 101º57'47"E; 1,850 m elevation), is lo- coccidia following the method of Vance and Duszynski cated in the Khangai Mountains of Övörkhangay Aimag (1985) and Gardner (1996). The complete GI tract (Province) in west central Mongolia. The surrounding was removed, and the liver, lungs, and the pleural area is rocky mountain steppe habitat cut through by and peritoneal cavities were examined for helminths. the Orkhon River. The river canyon (ca. 200 m wide Each organ was opened and examined separately for by 50 m deep) is steep sharply cut rock with a mixed helminths. Gastrointestinal tracts of eight individuals Pinus, Populus, and Larix forest along the riverbank. of U. undulatus were preserved in 70% ETOH until ex- At this site, 24 Urocitellus undulatus were collected amined in the Manter Laboratory of Parasitology. From and examined for parasites. The second site, Ulziyt complete field necropsies, parasite specimens were Uul (44º41'09"N, 102º00'57"E; 1,640 m elevation), is preserved in 10% formalin or 70% ETOH for study a small barren rocky hill in the arid Gobi Steppe north by light microscopy. Cestode specimens were stained of Arts Bogd Mountain. The area consists of sparse with carmine, mounted with damar gum and observed vegetation (Allium, Stipa, and Artemesia) and desert with a light microscope. Nematode specimens were pavement. Two individuals of S. alashanicus were preserved in 10% formalin cleared in lactophenol and examined for parasites from this locality. observed with a light microscope. Animals were processed immediately after Mammals used in this study have been deposited capture following standard protocols (Gardner 1996). in the Museum of Southwestern Biology (MSB) as Each animal was killed with chloroform, brushed, and reported by Tinnin et al. (2002). examined for ectoparasites, a blood smear was made RESULTS A total of six taxa of helminths was collected from Site of infection.—Small intestine. 16 of the 24 individuals of U. undulatus examined. Both of the individuals of S. alashanicus examined Prevalence and intensity.—6/24 (25%), 3.8 (1- were uninfected. Parasite, locality, and infection pa- 13). rameters for the U. undulatus specimens are outlined below. Specimens deposited.—HWML 62986, 62988, 62997, 63004, 66692, 66697, 66698, 66699, 66705. NEMATA Additional host from Mongolia.—Marmota si- Ascaris tarbagan Schulz 1931 birica (Radde 1862) from near Baruun-Urt, Sukhbaatar Aimag in eastern Mongolia (Meszaros 1974). Collection locality.—Ulaan Tsutgaalan. TINNIN ET AL .—HELMINT H S OF MONGOLIAN SQUIRRELS 3 Type host and type locality.—Marmota sibirica 1758); Meriones meridianus (Pallas 1773); Marmota from the vicinity of Chita, Russia (Schulz 1931). sibirica; Sciurus niger Linnaeus 1758; Urocitellus undulatus; Ictidomys tridecemlineatus (Mitchill 1821); Other reported hosts.—Ascaris tarbagan is Poliocitellus franklini (Sabine 1822); and Tamias si- common in marmots across central Asia and southern biricus (Laxmann 1769) (Morgan 1943; Chabaud 1956; Siberia. It has been reported from: Marmota menzbieri Yamaguti 1961; Skrjabin and Sobolev 1964; Tokobaev (Kashkarov 1925); M. caudata (Geoffroy 1844); M. 1976; Shalaeva et al. 1987; Zhaltsanova and Shalaeva baibacina Kastchenko 1889; and M. sibirica (Schulz 1990; Coyner et al. 1996). 1931) (Spasski et al. 1950; Machulskii 1958; Yamaguti 1961; Barus et al. 1970; Ismatov 1970; Tokobaev 1976; Geographic range.—This species has been re- Zhaltsanova and Shalaeva 1990). It also has been ported from across central Asia including Kazakhstan reported from M. monax (Linnaeus 1758) in Alaska and Uzbekistan (Skrjabin and Sobolev 1964; Tokobaev (Phillip 1938) and is commonly found in Urocitellus 1976), Russia (Morgan 1943; Yamaguti 1961; Shalaeva undulatus in Russia (Eltyshev and Maklokova 1971; et al. 1987; Zhaltsanova and Shalaeva 1990), and North Eltyshev 1975; Shalaeva et al. 1987; Zhaltsanova and America including Canada and Florida (Morgan 1943; Shalaeva 1990). Yamaguti 1961; Coyner et al. 1996). Geographic range.—This species has been Remarks.—Some authors believe that P. spini- reported from Afghanistan (Barus et al. 1970), Tadjik- cauda MacLeod 1933, the form found in I. tridecem- histan (Ismatov 1970), southern Kazakhstan (Spasski lineatus and P. franklini in North America, is a distinct et al. 1950), several locations in southern Russia in species (Chabaud 1956; Skrjabin and Sobolev 1964), the regions of Lake Baikal and Buryatia (Machulskii while others have recognized it as a synonym of P. 1958; Eltyshev and Maklokova 1971; Eltyshev 1975; massino (see Morgan 1943; Yamaguti 1961). Shalaeva et al. 1987; Zhaltsanova and Shalaeva 1990) into eastern Mongolia (Meszaros 1974). There is also Streptopharagus kutassi (Schulz 1927) Kirshenblat one report of this species from Alaska (Phillip 1938). 1949 (Syn. Arduenna kutassi Schulz 1927) Physaloptera massino Schulz 1926 Collection locality.—Ulaan Tsutgaalan. Collection locality.—Ulaan Tsutgaalan. Site of infection.—Small intestine and stomach. Site of infection.—Small intestine and stomach. Prevalence and intensity.—4/24 (16.7%), 16 Prevalence and intensity.—6/24 (25%), 4 (1- (1-49). 11). Specimens deposited.—HWML 62985, 66695, Specimens deposited.—HWML 62985, 66694, 66697, 66698, 66699, 66710. 66697, 66698, 66699, 66704, 66710, 66711, 66712. Additional host from Mongolia.—This represents Additional host from Mongolia.—This represents the first record for the country. the first record for the country. Type host and type locality.—Spermophilus pyg- Type host and type locality.—Mus musculus maeus (Pallas 1778) from Ukraine. Linnaeus 1758 from Bukhara, Uzbekistan (Morgan 1943). Other reported hosts.—Spermophilus pygmaeus; S. citellus (Linnaeus 1766); S. fulvus (Lichtenstein Other reported hosts.—Rhombomys opimus 1823); S. relictus (Kashkarov 1923); S. xanthoprym- (Lichtenstein 1823); Apodemus sylvaticus (Linnaeus nus (Bennet 1835); U. undulatus; Spermophilopsis 4 OCCASIONAL PA P ERS , MUSEUM OF TEXAS TEC H UNIVERSITY leptodactylus
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