2008 NORTHEASTERN NATURALIST 15(2):283–292 Ectoparasites of Small Mammals in Western Iowa Jonathan J. Storm1,2,* and Christopher M. Ritzi3 Abstract - We conducted a formal survey of small-mammal ectoparasite diversity in Iowa. We examined 166 small mammals and documented 54 species of parasitic arthropods present on 12 species of mammals. Ectoparasite species richness was greatest for Blarina brevicauda (northern short-tailed shrew), Microtus ochrogaster (prairie vole), Peromyscus maniculatus (deer mouse), and Peromyscus leucopus (white-footed mouse). Immature (larvae and nymphs) Dermacentor variabilis (American dog tick) were collected from P. leucopus, M. ochrogaster, Reithrodontomys megalotis (western harvest mouse), and Zapus hudsonius (meadow jumping mouse). The fleas Epitedia wenmanni and Orchopeas leucopus, potential vectors of sylvatic plague bacilli, were found on Mus musculus (house mouse), white-footed mouse, and deer mouse. We document 21 new ectoparasite host records for North America and 115 new host locality records for ectoparasites in Iowa. Introduction The distribution and host-specificity of ectoparasites of mammals is poorly known across much of North America (Whitaker et al. 1993). In particular, there have been few studies on ectoparasites of wild mammals in Iowa (Whitaker and Wilson 1974). Previously documented ectoparasites for Iowa are limited to 5 species of laelapid mites (Ewing 1925, Herrin 1970, Keegan 1946, Kietzmann and Kietzmann 1987), 1 species of listrophorid mite (Fain and Lukoschus 1984), 9 species of pygmephorid mites (Dastych et al. 1991, 1992), 2 species of macronyssid mites (Becker 1948, Ewing and Stover 1915, Ubelaker and Kunz 1971), 1 species of myobiid mite (Osborn 1896), 1 species of rhyncoptid mite, and 1 species of spinturnicid mite (Keegan 1943). Given the paucity of information on ectoparasite diversity, we conducted a detailed ectoparasite survey of wild mammals in Iowa. We sought to determine the species composition, host specificity, and infestation prevalence of parasitic and phoretic arthropods. In addition, we wished to determine the occurrence of potential vectors of zoonotic pathogens. Given that some ectoparasites are vectors of zoonotic agents and that some rodents are reservoirs for these pathogens, it is important to document host-parasite associations and infestation rates of ectoparasites on mammals. 1Department of Ecology and Organismal Biology, Indiana State University, Terre Haute, IN 47809. 2Current address - Division of Natural Sciences and Engineering, University of South Carolina Upstate, Spartanburg, SC 29303. 3Department of Biology, Box C-64, Sul Ross State University, Alpine, TX 79832 .*Corresponding author - jstorm@uscupstate.edu. 284 Northeastern Naturalist Vol. 15, No. 2 Methods Small mammals were collected using snap-back mousetraps on various dates during May–November of 2003, 2004, and 2005 in Dallas County, IA. Traps were baited with a mixture of peanut butter and rolled oats and placed in a variety of habitats, including fallow cornfields, woodland edges, and old fields. Upon collection, mammals were identified to species using Jones and Birney (1988) and placed in individual plastic bags. Specimens were kept frozen at the Indiana State University Vertebrate Museum (ISUVM) until further processing. Ectoparasites were also collected from frozen small-mammal carcasses provided by the Buena Vista University Vertebrate Museum. Ectoparasites were collected following the washing technique outlined in Whitaker et al. (1993). After washing, hosts were examined for residual ectoparasites using a stereomicroscope. Residual parasites were removed with forceps and mounted in PVA medium (BioQuip Products, Gardena, CA). Representative voucher specimens were slide-mounted as stated above. Parasites were identified using various keys, including Benton (1983), Herrin (1970), and Whitaker (1982), relevant primary literature for taxa recovered, and compared against a collection housed at the Jim V. Richerson Invertebrate Collection (JVRIC). Prevalence (percentage of host individuals infested) and mean intensity (number of ectoparasites per infested host) of ectoparasites were calculated following Bush et al. (1997). A literature search using Whitaker and Wilson (1974) and Web of Science indicated whether each ectoparasite species represented a new host record (i.e., first report of the parasite on the host) or a new host locality record for Iowa. Ectoparasite voucher specimens were deposited in the JVRIC, Sul Ross State University, Alpine, TX, and small mammal vouchers were deposited at the ISUVC, Terre Haute, IN. Results We collected ectoparasites from 166 individuals representing 12 species of small mammals in western Iowa (Appendix 1). Most mammals were collected in Dallas County, but additional individuals came from Adair, Buena Vista, Dickinson, Lyon, and Sac counties. The most common species examined were Blarina brevicauda Say (northern short-tailed shrew, n = 33), Peromyscus leucopus Rafinesque (white-footed mouse, n = 24), and Peromyscus maniculatus Wagner (deer mouse, n = 57). We collected 3265 arthropods representing 54 species of ectoparasites and phoretomorphs (Appendix 1). Hosts with the greatest ectoparasite species richness included northern short-tailed shrew (22 species of ectoparasites), Microtus ochrogaster Wagner (prairie vole; 17 species), deer mouse (16 species), and white-footed mouse (14 species). We documented 21 new host records and 115 new host locality records for ectoparasites of mammals 2008 J.J. Storm and C.M. Ritzi 285 in Iowa (Appendix 1). The most widely occurring ectoparasite was the fur mite Glycyphagus hypudaei Koch, which was found on 10 of the 12 host species. Other widely occurring ectoparasites included the mites Androlaelaps fahrenholzi Berlese (found on 8 species), Myocoptes musculinus Koch (7 species), Echinonyssus utahensis Allred and Beck (6 species), Euschoengastia peromysci Ewing (6 species), Myocoptes japonensis Radford (6 species), and Orycteroxenus soricis Oudemans (6 species). Discussion The most common ectoparasite collected was the mite Glycyphagus hypudaei, which is known from a wide variety of mammals in North America (Nims et al. 2004). Other commonly recovered ectoparasites (e.g. Androlaelaps fahrenholzi, Myocoptes musculinus, and Myocoptes japonensis) have previously been shown to be parasitic generalists that occur on a number of host species (Whitaker and Wilson 1974). Whether these species are truly polyxenous generalists, or whether they represent several morphologically cryptic host-specific species, has yet to be determined. An interesting difference between our study and most ectoparasite studies is the large proportion of small mites recovered (e.g., members of the Glycyphagidae, Myocoptidae, and Myobiidae). One reason for this could be the lengths of time between capture and processing, in which larger, more readily dispersing parasites abandon their host. Thus, prevalence and mean intensity for larger parasites in this study should be considered conservative. A second and more likely reason is the washing technique we used to recover ectoparasites. This method is often superior to the brushing method, which can underrepresent the proportion of small arthropods on the host (Whitaker et al. 1993). In addition, prevalence and mean intensity values for all parasites should be viewed with caution in some instances, as sample size was limited for some host species. Mus musculus L. (house mouse) lives near humans and can spread pathogens such as lymphocytic choriomeningitis virus (Childs et al. 1991), Rickettsia akari (Huebner et al. 1946), and Borrelia burgdorferi (Gern et al. 1998). We collected 9 species of ectoparasites from house mice, all of which were new host locality records and two of which (Glycyphagus hypudaei and Orycteroxenus soricis) are new host records. Although our sample size was small, the mange mite, Myocoptes musculinus, was much more prevalent in our study than previously found for wild house mice (Whitaker 1970). Mange mites can be common in laboratory colonies of house mice (Fain and Hyland 1970, Reeves and Cobb 2005), but are generally thought to have low prevalence among wild house mice. Mange mites were also collected from northern short-tailed shrews, prairie voles, Microtus pennsylvanicus Ord (meadow vole), Onychomys leucogaster Wied-Neuwied (northern grasshopper mouse), white-footed mice, and deer mice. 286 Northeastern Naturalist Vol. 15, No. 2 White-footed mice have previously been shown to harbor a diverse assemblage of ectoparasites (Ritzi and Whitaker 2003). Among the ectoparasites we collected was Dermacentor variabilis Say (American dog tick), a vector of the rickettsial agent of Rocky Mountain spotted fever in humans (Felz and Durden 1998). Immature stages of D. variabilis were also collected from Reithrodontomys megalotis Baird (western harvest mouse) and Zapus hudsonicus Zimmerman (meadow jumping mouse). None of these mammals are highly synanthropic; thus, the risk of acquiring zoonotic pathogens from these hosts is unlikely. The deer mouse is a potential reservoir of hantavirus and the plague bacillus in North America. We collected two species of fleas from deer mice, Epitedia wenmanni Rothschild and Orchopeas leucopus Baker, both of which are potential vectors of sylvatic plague (Eskey 1938). However, risk of plague is rare in Iowa, as most cases are reported from the southwestern United States (Gage et al. 1995). Acknowledgments We thank R. Lampe for providing specimens from Buena Vista University. R. Meraz and V. Sanchez processed filter papers and slide mounted specimens. All work was approved by the Indiana State University Animal Care and Use Committee. Funding was provided by the Sul Ross State University Faculty Enhancement Program. Literature Cited Becker, E.R. 1948. The occurrence of Rhipicephalus sanguineus and Liponyssus bacoti in Iowa. Proceedings of the Iowa Academy of Science 55:349–350. Benton, A.H. 1983. An illustrated key to the fleas of the eastern United States. Marginal Media, Fredonia, NY. 34 pp. Bush, A.O., K.D. Lafferty, J.M. Lotz, and A.W. Shostak. 1997. Parasitology meets ecology on its own terms. Margolis et al. revisited. Journal of Parasitology 83:575–583. Childs, J.E., G.E. Glass, T.G. Ksiazek, C.A. Rossi, J.G.B. Oro, and J.W. LeDuc. 1991. Human-rodent contact and infection with lymphocytic choriomeningitis and Seoul viruses in an inner-city population. American Journal of Tropical Medicine and Hygiene 44:117–121. Dastych, H., G. Rack, and N. Wilson. 1991. Notes on mites of the genus Pygmephorus (Acari: Heterostigmata) associated with North American mammals. Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut 88:161–174. Dastych, H., G. Rack, and N. Wilson. 1992. Notes on mites of the genus Pygmephorus (Acari: Heterostigmata) associated with North American mammals (Part II). Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut 89:141–156. Eskey, C.R. 1938. Fleas as vectors of plague. American Journal of Public Health 28:1305–1310. Ewing, H.E. 1925. New mites of the parasitic genus Haemogamasus Berlese. Proceedings of the Biological Society of Washington 38:137–143. 2008 J.J. Storm and C.M. Ritzi 287 Ewing, H.E., and A.J. Stover. 1915. New parasitic mites (Acarina). Entomological News 26:109–114. Fain, A., and K. Hyland. 1970. Notes on the Myocoptidae of North America with description of a new species on the eastern chipmunk, Tamias striatus Linnaeus. Journal of the New York Entomological Society 78:80–87. Fain, A., and F.S. Lukoschus. 1984. New observations on the genus Prolistophorus Fain, 1970 (Acari: Astigmata: Listrophoridae). Systematic Parasitology 6:161–185. Felz, M.W., and L.A. Durden. 1998. Identifying ticks: A pictorial guide. Patient Care 32:172–187. Gage, K.L., R.S. Ostfeld, and J.G. Olson. 1995. Nonviral vector-borne zoonoses associated with mammals in the United States. Journal of Mammalogy 76:695– 715. Gern, L., A. Estrada-Pena, F. Frandson, J.S. Gray, T.G.T. Jaenson, F. Jongejan, O. Kahl, E. Korenberg, R. Mehl, and P.A. Nuttall. 1998. European reservoir hosts of Borrelia burgdorferi sensu lato. Zentralblatt für Bakteriologie: International Journal of Medical Microbiology 287:196–204. Herrin, C.S. 1970. A systematic revision of the genus Hirstionyssus (Acari: Mesostigmata) of the nearctic region. Journal of Medical Entomology 7:391–437. Huebner, R.J., W.L. Jellison, and C. Pomerantz. 1946. Rickettsialpox: A newly recognized rickettsial disease IV. Isolation of a Rickettsia apparently identical with the causative agent of rickettsialpox from Allodermanyssus sanguineus, a rodent mite. Public Health Reports 61:1677–1682. Jones, J.K., and E.C. Birney. 1988. Handbook of Mammals of the North-Central States. University of Minnesota Press, Minneapolis, MN. 346 pp. Keegan, H.L. 1943. Some host records from the parasitological collection of the State University of Iowa. Bulletin of the Brooklyn Entomological Society 38:54–57. Keegan, H.L. 1946. Six new mites of the superfamily Parasitoidea. Transactions of the American Microscopical Society 65:69–77. Kietzmann, G.E., and E.A. Kietzmann. 1987. Parasites associated with thirteen-lined ground squirrels (Spermophilus tridecemlineatus (Mitchell)) from Ames, Iowa. Proceedings of the Iowa Academy of Science 94:22–23. Nims, T.N., L.A. Durden, and R.L. Nims. 2004. New state and host records for the phoretic fur mite, Glycyphagus hypudaei (Acari: Glycyphagidae). Journal of Entomological Science 39:470–471. Osborn, H. 1896. Insects Affecting Domestic Animals: An account of the Species of Importance in North America, with Mention of Related Forms Occurring on Other Animals. Division of Entomology, United States Department of Agriculture Bulletin 5(NS). Government Printing Office, Washington DC. 302 pp. Reeves, W.K., and K.D. Cobb. 2005. Ectoparasites of house mice (Mus musculus) from pet stores in South Carolina, USA. Comparative Parasitology 72:193–195. Ritzi, C.M., and J.O. Whitaker. 2003. Ectoparasites of small mammals from the Newport Chemical Depot, Vermillion County, Indiana. Northeastern Naturalist 10:149–158. Ubelaker, J.E., and T.H. Kunz. 1971. Parasites of the evening bat, Nycticeius humeralis, in Iowa. Texas Journal of Science 22:425–427. Whitaker, J.O. 1970. Parasites of feral house mouse, Mus musculus, in Vigo County, 288 Northeastern Naturalist Vol. 15, No. 2 Indiana. Proceedings of the Indiana Academy of Science 79:441–448. Whitaker, J.O. 1982. Ectoparasites of mammals of Indiana. Indiana Academy of Science Monograph No. 4. Indianapolis, IN. 240 pp. Whitaker, J.O., and N. Wilson. 1974. Host and distribution lists of mites (Acari) parasitic and phoretic, in the hair of wild mammals of North America, north of Mexico. American Midland Naturalist 91:1–67. Whitaker, J.O., W.J. Wrenn, and R.E. Lewis. 1993. Parasites, Pp. 386–478, In H.H. Genoways and J.H. Brown (Eds.). Biology of the Heteromyidae, Special Publications No. 10. The American Society of Mammalogists. 719 pp. 2008 J.J. Storm and C.M. Ritzi 289 Appendix 1. Ectoparasites and phoretic arthropods recovered from 12 species of small mammals in western Iowa, including number of specimens examined, total ectoparasites recovered, prevalence (percentage of individuals infested), and intensity (mean ectoparasites per infested host). R = number recovered, P = prevalence (%), and I = intensity (mean). Host (n) Ectoparasite R P I Blarina brevicauda (33) Androlaelaps fahrenholziA 114 39 8.8 Echinonyssus blarinae HerrinA 8 6 4.0 Echinonyssus utahensisB 7 3 7.0 Eulaelaps stabularis KochA 1 3 1.0 Haemogamasus liponyssoides EwingA 16 9 4.0 Cyrtolaelaps sp. 30 27 3.3 Euryparasitus sp. 2 6 1.0 Glycyphagus hypudaeiA 68 15 4.5 Orycteroxenus soricisA 254 36 21.2 Xenoryctes latiporus Fain and WhitakerA 1 3 1.0 Euschoengastia peromysciA 1 3 1.0 Neotrombicula fitchi LoomisA 1 3 1.0 Pygmephorus brevicaudae Smiley and WhitakerA 13 6 6.5 Pygmephorus designatus MahunkaB 93 8 31.0 Pygmephorus mahunkai Smiley and WhitakerB 7 3 3.5 Pygmephorus whitakeri Mahunka 19 18 3.2 Bakerdania sp. 1 3 1.0 Blarinobia simplex EwingA 34 15 6.8 Protomyobia americana Lukoschus et al.A 28 21 4.0 Myocoptes musculinusB 2 3 2.0 Corrodopsylla curvata RothschildA 1 3 1.0 Ctenophthalmus pseudagyrtes BakerA 5 9 1.6 Hoplopleura captiosa JohnsonA 1 3 1.0 Sorex cinereus (15) Androlaelaps fahrenholziA 2 13 1.0 Echinonyssus blarinaeB 2 13 1.0 Echinonyssus utahensisB 1 7 1.0 Cyrtolaelaps sp. 1 7 1.0 Glycyphagus hypudaeiA 1 7 1.0 Orycteroxenus soricisA 572 80 48.0 Pygmephorus designatusB 15 20 5.0 Blarinobia cryptotis McDanielA 1 7 1.0 Protomyobia claparedei PoppeA 12 27 3.0 Myocoptes japonensisB 1 7 1.0 Amorphacarus hengererorum JamesonA 1 7 1.0 Eptesicus fuscus (1) Steatonyssus occidentalis EwingA 7 100 7.0 290 Northeastern Naturalist Vol. 15, No. 2 Host (n) Ectoparasite R P I Microtus ochrogaster (9) Androlaelaps fahrenholziA 18 44 4.5 Echinonyssus utahensisA 1 11 1.0 Haemogamasus ambulans ThorellB 1 11 1.0 Laelaps kochi OudemansA 8 22 4.0 Cyrtolaelaps sp. 6 11 6.0 Euryparasitus sp. 1 11 1.0 Listrophorus synaptomys Fain et al.A 29 22 14.5 Glycyphagus hypudaeiA 75 44 18.8 Orycteroxenus soricisA 1 11 1.0 Euschoengastia peromysciA 77 44 19.3 Pygmephorus designatusB 5 33 1.7 Radfordia hylandi Fain and LukoschusA 21 44 5.3 Myocoptes japonensisA 5 22 2.5 Myocoptes musculinusA 34 33 11.3 Trichoecius tenax MichaelA 15 11 15.0 Hoplopleura acanthopus BurmeisterA 173 11 173.0 Dermacentor variabilisA 3 22 1.5 Microtus pennsylvanicus (4) Androlaelaps fahrenholziA 8 50 4.0 Laelaps alaskensis GrantA 10 25 10.0 Laelaps kochiA 7 50 3.5 Listrophorus mexicanus FainA 1 25 1.0 Glycyphagus hypudaeiA 9 50 4.5 Euschoengastia peromysciA 1 25 1.0 Neotrombicula fitchiA 2 25 2.0 Neotrombicula lipovsyi Brennan and WhartonA 63 25 63.0 Myocoptes japonensisA 7 50 3.5 Myocoptes musculinusA 3 25 3.0 Amorphacarus hengeroronumA 3 25 3.0 Mus musculus (7) Androlaelaps fahrenholziA 5 29 2.5 Echinonyssus butantanensis FonsecaA 1 14 1.0 Echinonyssus utahensisA 1 14 1.0 Glycyphagus hypudaeiB 2 14 2.0 Orycteroxenus soricisB 6 29 3.0 Myobia musculi SchrankB 51 29 25.5 Radfordia affinis PoppeA 13 43 4.3 Myocoptes musculinusA 30 43 10.0 Orchopeas leucopusA 1 14 1.0 Onychomys leucogaster (2) Glycyphagus hypudaeiA 29 100 14.5 Radfordia subuliger EwingA 13 100 6.5 Myocoptes musculinusA 1 50 1.0 Trichoecius tenaxB 64 100 32.0 2008 J.J. Storm and C.M. Ritzi 291 Host (n) Ectoparasite R P I Peromyscus leucopus (24) Androlaelaps fahrenholziA 51 67 3.2 Echinonyssus utahensisA 11 21 2.2 Glycyphagus hypudaeiA 93 42 9.3 Euschoengastia peromysciA 6 8 3.0 Neotrombicula fitchiA 1 4 1.0 Ripiaspichia americana EwingA 2 4 2.0 Radfordia subuligerA 20 29 2.9 Myocoptes japonensisA 17 8 8.5 Myocoptes musculinusA 44 42 4.4 Trichoecius tenaxB 3 4 3.0 Ctenophthalmus pseudagyrtesA 1 4 1.0 Epitedia wenmanniA 5 16 1.3 Orchopeas leucopusA 16 33 2.0 Dermacentor variabilisA 7 21 1.4 Peromyscus maniculatus (57) Androlaelaps fahrenholziA 58 32 3.2 Echinonyssus blarineaB 1 2 1.0 Echinonyssus utahensisA 111 53 3.7 Haemogamasus liponyssoidesA 1 2 1.0 Hypoaspis lubrica Oudemans and VoigtsA 1 2 1.0 Glycyphagus hypudaeiA 7 7 1.8 Orycteroxenus soricisB 297 7 74.3 Euschoengastia peromysciA 2 4 1.0 Myobia musculiA 1 2 1.0 Radfordia subuligerA 22 21 1.8 Myocoptes japonensisA 8 7 2.0 Myocoptes musculinusA 37 21 3.1 Trichoecius tenaxB 6 9 1.2 Hoplopleura hesperomydis OsbornA 110 44 4.4 Epitedia wenmanniA 6 9 1.2 Orchopeas leucopusA 20 21 1.7 Reithrodontomys megalotis (5) Cyrtolaelaps sp. 1 20 1.0 Glycyphagus hypudaeiA 1 20 1.0 Orycteroxenus soricisB 16 40 8.0 Euschoengastia peromysciA 2 20 2.0 Radfordia hylandiB 2 20 2.0 Radfordia subuligerA 1 20 1.0 Myocoptes japonensisB 2 20 2.0 Dermacentor variabilisA 1 20 1.0 292 Northeastern Naturalist Vol. 15, No. 2 Host (n) Ectoparasite R P I Spermophilus tridecemlineatus (7) Androlaelaps fahrenholzi 11 57 2.8 Haemogamasus liponyssoidesB 3 14 3.0 Macrocheles mesochthonius Krantz and WhitakerA 8 42 2.7 Lepidoglyphus hylandiA 35 42 11.7 Glycyphagus reticulosis Spika and GerritsA 7 29 3.5 Bakerdania sp. 5 14 5.0 Enderleinellus suturalis OsbornA 2 14 2.0 Opisocrostis bruneri BakerA 9 71 1.8 Zapus hudsonicus (2) Glycyphagus newyorkensis FainA 63 50 63.0 Radfordia ewingi FoxA 3 100 1.5 Dermacarus variabilisA 1 50 1.0 ANew host locality (Iowa) record. BNew host record.