Journal of Wildlife Diseases, 46(2), 2010, pp. 585–590 # Wildlife Disease Association 2010

New Records of Hair Follicle (Demodecidae) from North American Cervidae

Clifford E. Desch,1 John J. Andrews,2 Laurie A. Baeten,3,8 Zach Holder,4 Jenny G. Powers,5 Duane Weber,6 and Lora R. Ballweber7,9 1 Department of Ecology and Evolutionary Biology, University of Connecticut–Hartford Campus, 85 Lawler Road, West Hartford, Connecticut 06117, USA; 2 Colorado State University, Western Slope Veterinary Diagnostic Laboratory, Grand Junction, Colorado 80154, USA; 3 Colorado Division of Wildlife, Wildlife Research Center, Fort Collins, Colorado 80526, USA; 4 Colorado Division of Wildlife, 7405 Highway 50, Salida, Colorado 81201, USA; 5 Biological Resource Management Division, National Park Service, Fort Collins, Colorado 80525, USA; 6 Wind Cave National Park, Hot Springs, South Dakota 57747, USA; 7 Parasitology, Colorado State University Veterinary Diagnostic Laboratory, Fort Collins, Colorado, 80523-1644; 8 Current address: Colorado State University Veterinary Diagnostic Laboratory, Fort Collins, Colorado, 80523-1644, USA; 9 Corresponding Downloaded from http://meridian.allenpress.com/jwd/article-pdf/46/2/585/2241480/0090-3558-46_2_585.pdf by guest on 27 September 2021 author (email: [email protected])

ABSTRACT: Individuals of three species of pilosebaceous complex, most likely indi- cervids, with varying degrees of alopecia, were cates that these mites co-evolved with the examined for ectoparasites: Rocky Mountain hair follicle (Nutting, 1985; Bukva, 1991). elk (Cervus elaphus nelsoni) and mule deer (Odocoileus hemionus hemionus) in Colorado Thus, their association with is an and white-tailed deer (Odocoileus virginianus) ancient one, and the genus is in South Dakota. Hair follicle mites were most likely a monophyletic group. recovered and identified as Demodex kutzeri, Demodectic mites are highly special- a species originally described from the Euro- ized for their microhabitat, the hair follicle pean red deer (Cervus elaphus, from Austria) and the sika deer (Cervus nippon pseudaxis, complex; this specialization includes min- captive in Germany). These findings expand the iaturization and an extreme reduction of geographic range of D. kutzeri to North legs and setation. Most adult Demodex are America and extend its host range to include cigar-shaped and 100–300 mm long. Ex- the genus Odocoileus. Thus, the host range for cept for salivary glands, internal organs are D. kutzeri spans two subfamilies of cervids. Additionally, D. kutzeri was identified in unpaired. The adult legs are reduced to material from a white-tailed deer collected in three short, movable segments, and the South Carolina in 1971, indicating this parasite largest setae, the supracoxal spines, typi- has been present, but unrecognized, on US cally are only 2–3 mmlong.These cervids for some time. reductions result in a paucity of characters Key words: Cervus elaphus, Demodex kutzeri, Demodex odocoilei, ectoparasites, host suitable for . specificity, Odocoileus hemionus, Odocoileus Until the 1980s, all described Demodex virginianus, synhospitalic. species were from taxonomically disparate hosts, with each species being The hair follicle mites of the genus morphologically distinct; thus, it was Demodex, first described from humans presumed that the hair follicle mites were (Simon, 1842), are now known to infest host-species specific. Over the past 25 yr, host species in three of seven marsupial this strict host specificity has been chal- orders and in 11 of 18 eutherian orders. lenged by the discovery of instances of a This range of host orders encompasses (morpho) species of Demodex on multiple 97% of all living mammalian species. host species. These examples include Currently, 88 species of Demodex have Demodex sabani, hosted by seven species been described from 83 host species, with of Malaysian rats in five genera (Desch et over half the mite species from just two al., 1984); Demodex nanus from the brown host orders, the rodents (28 mite species rat, Rattus norvegicus and the black rat, from 29 host species) and the chiropterans Rattus rattus (Desch, 1987); and Demodex (17 mite species from 13 host species). kutzeri from the European red deer, This widespread occurrence of Demodex Cervus elaphus and the sika deer, Cervus throughout the class Mammalia, and their nippon pseudaxis (Bukva, 1987). specialization for inhabiting the host’s Thorough ectoparasite surveys of mam-

585 586 JOURNAL OF WILDLIFE DISEASES, VOL. 46, NO. 2, APRIL 2010 mals reveal that many host species harbor 1987). Demodex kutzeri was described two or three species of Demodex. In every from European red deer from Austria such instance, these synhospitalic Demo- and a captive sika deer in Berlin, Germany dex species (Eichler, 1966 and modified (Bukva, 1987). We document D. kutzeri by Nutting, 1985) are morphologically (originally considered restricted to Eur- distinct. The synhospitalic species occupy asia) from three cervid species in North different microhabitats on the skin (e.g., America. on the domestic cat, Felis catus, Demodex Two hunter-harvested , one cati resides in the hair follicles and mule deer and one Rocky Mountain elk

Demodex gatoi in the epidermal pits; (Cervus elaphus nelsoni), from Colorado Downloaded from http://meridian.allenpress.com/jwd/article-pdf/46/2/585/2241480/0090-3558-46_2_585.pdf by guest on 27 September 2021 Desch and Stewart, 1999); on the pter- were acquired from the southwestern opodid blossom-bat, Macroglossus mini- portion of the state. The game manage- mus, from Australia, Demodex macroglossi ment units (GMU) from which they were inhabits the hair follicles (Desch, 1981) harvested are given (Table 1); however, and Demodex bicaudatus is restricted to the precise location at which each the meibomian glands (Kniest and Lu- was taken is unknown. The white-tailed koschus, 1981). Triads of synhospitalic deer was collected by personnel of the species of Demodex are known from cattle, National Park Service in Wind Cave Bos taurus (Bukva, 1986), European red National Park, South Dakota (43u349N, deer (Bukva and Preisler, 1988), sheep, 103u299W). Although the mule deer ex- Ovis aries (Bukva, 1990a), and the domes- hibited patchy alopecia, the elk was tic cat (Desch and Stewart, 1999). The described as normal in appearance. The brown rat hosts a tetrad of synhospitalic white-tailed deer was described as being Demodex (Bukva, 1995). in very poor condition and missing large Demodex odocoilei from the white- patches of hair (Fig. 1). Further histories tailed deer, Odocoileus virginianus, was and diagnostic test results are presented in the first hair follicle mite described from a Table 1. In addition, mites collected from North American cervid and is associated a hunter-harvested white-tailed deer in with sporadic cases of mange in this host. Orange County, South Carolina in 1971 Infested white-tailed deer have been were available for examination. Histologic reported from the southeastern and north- techniques and procedures for examining central United States (Desch and Nutting, mites were as described (Desch and 1974; Jacques et al., 2001; Turner and Nutting, 1974; Jacques et al., 2001). Cano, 2008). The known geographic and Mites from all four animals were host distribution has expanded with the identified as D. kutzeri (Fig. 2) and were confirmation of D. odocoilei infesting the only species present in the Colorado Columbian black-tailed deer, Odocoileus and South Carolina cervids. This extends hemionus columbianus, in eastern Oregon the range of D. kutzeri to North America and Washington (Bildfell et al., 2004). and to the host genus Odocoileus. Given Nymphal mites, morphologically compat- the previous examples of a single (mor- ible with D. odocoilei, were reported from pho) species of Demodex infesting multi- a mule deer, O. hemionus hemionus,in ple, closely related host species, it is not Saskatchewan, Canada (Gentes et al., surprising that D. kutzeri occurs on 2007). European red deer and Rocky Mountain Although Demodex have been known to elk. However, it is unexpected that D. infest a variety of Eurasian cervids for kutzeri also parasitized O. virginianus and more than 120 yr, D. kutzeri is the only O. hemionus, in that these two host species from this region to be satisfactorily species are in different subfamilies. described in all life stages from a correctly The family Cervidae arose in the Late and positively identified host (Bukva, Miocene (7.7–9.6 mya) in central Asia and a TABLE 1. Pertinent history and diagnostic test results from three cervids harbo ring demodectic mites.

Mule deer Elk White-tailed deer

Origin GMU 072 b ; Colorado, collected 29 GMU 61 b ; Colorado, collected 6 Wind Cave National Park, South Dakota; collected 9 October 2006 November 2007 April 2009 Sex and age Mature male, age unknown Yearling female 3-yr-old male Body condition Normal; occasional areas of alopecia Normal Emaciated; ex tensive alopecia of ventral abdomen, hindquarters Chronic wasting Not detected Test not performed Not detected disease Skin: macroscopic Generalized thickening of the skin with Multiple, large ( ,2 mm) nodules Generalized alopecia, extending in front from shoul- patchy alopecia and moist crusts; present on cut section ders to carpi, in hindquarters to hocks, and on multiple, large nodules ( ,1 mm) ventral abdomen present on cut section Skin: microscopic Markedly dilated follicular structures Markedly dilated follicular structures Markedly dilated follicular structures packed with packed with mites; moderate, mixed packed with mites; mild mites; mild inflammation—multinucleated giant inflammatory cell infiltrates encircling lymphoplasmacytic infiltrate in cells, lymphocytes, and plasma cells and macro- many affected follicles; abundant keratin connective tissue surrounding phages (or both)—encircling many affected folli- debris and inflammatory crusts cover the follicles; mild inflammatory changes cles; mites occasionally present in dermis, sur- epidermal surfaces; bacterial colonies in present within overlying superficial rounded by multinucleated giant cells, plasma surface crusts but no fungal organisms dermis cells, and lymphocytes detected in surface or follicular structures

Other testing or Not performed Not performed Extensive serous atrophy of fat; lymph nodes n ormal, 587 COMMUNICATIONS SHORT comments not active; spleen normal; epizootic hemorrhagic disease serology: negative; parasites, external: Dermacentor albipictus ; Lipoptena depressa de- pressa ; parasites, internal: strongyles (31 eggs/ gram) a Hunter-killed white-tailed deer from South Carolina not included due to l ack of available information.

b See http://wildlife.state.co.us/Hunting/GMUnitMaps.htm for Game Man agement Unit maps. Downloaded from http://meridian.allenpress.com/jwd/article-pdf/46/2/585/2241480/0090-3558-46_2_585.pdf by guest on 27 September 2021 September 27 on guest by http://meridian.allenpress.com/jwd/article-pdf/46/2/585/2241480/0090-3558-46_2_585.pdf from Downloaded 588 JOURNAL OF WILDLIFE DISEASES, VOL. 46, NO. 2, APRIL 2010 Downloaded from http://meridian.allenpress.com/jwd/article-pdf/46/2/585/2241480/0090-3558-46_2_585.pdf by guest on 27 September 2021

FIGURE 1. White-tailed deer from South Dakota exhibiting extensive alopecia of lateral thigh and ventral abdomen associated with hair follicle mites (Demodex kutzeri). diverged there into major lineages (Gil- bert et al., 2006). Based on the results of a study of mitochondrial and nuclear DNA from 25 cervid species, Gilbert et al. (2006) proposed a new classification of FIGURE 2. Demodex kutzeri, wet mount of follic- Cervidae with two subfamilies, Cervinae ular material from an elk. Bar550 mm. (including elk and red deer) and Capreo- linae (including mule deer and white- An alternative explanation for the pres- tailed deer). The tribe Odocoleini, within ence of D. kutzeri on multiple host species the Capreolinae, arose in the Early could be that the mites in North America Pliocene and migrated to North America are not D. kutzeri, but are morphologically 4.2–5.7 mya. Even though Cervinae and indistinguishable from D. kutzeri.Al- Capreolinae diverged in the Early Plio- though possible, our current understand- cene, both subfamilies are hosts for D. ing of the species distribution of Demodex kutzeri. This likely indicates that the (based on morphologic criteria) and the cervid pilosebaceous complex is a stable concept of synhospitality leads to the habitat with little selection pressure to identification of D. kutzeri. bring about change in mite morphology, In addition to D. kutzeri, the white- even though the mites on different host tailed deer from South Dakota also harbored species are reproductively isolated. Be- D. odocoilei. Thus, D. kutzeri and D. odocoilei cause hair follicle mites are transferred appear to be synhospitalic. It remains to be between hosts by direct physical contact determined whether or not they occupy (mating, nursing, mutual grooming; see different microhabitats, as has been de- Bukva, 1990b), it is unlikely that interspe- scribed for other synhospitalic species. cific host transfer accounts for the occur- Lesions of demodicosis in cervids vary rence of D. kutzeri on multiple host from mild to moderate alopecia, with or species. without associated inflammation (Fig. 3A), SHORT COMMUNICATIONS 589 Downloaded from http://meridian.allenpress.com/jwd/article-pdf/46/2/585/2241480/0090-3558-46_2_585.pdf by guest on 27 September 2021

FIGURE 3. Gross and histologic features of demodicosis in cervids. (A) Follicle packed with mites and no associated inflammatory response (white-tailed deer). Bar5200 mm. (B) Cross-section of skin showing nodules (arrows) and surface crusts (mule deer). Bar5500 mm. (C) Mite fragment in dermis surrounded by multinucleated giant cell (white-tailed deer). Bar550 mm. (D) Ruptured follicle releasing mites into dermis with mixed inflammatory response (white-tailed deer). Bar5200 mm. to alopecia characterized by nodular Clinical demodicosis is considered to be dermatitis (Fig. 3B), purulent folliculitis, a secondary disorder in which the baseline and mixed inflammation within the sur- parasite population expands as a result of rounding dermis (Fig. 3C). Variable num- poor host nutrition, immunosuppression, bers of mites are found in affected or concomitant disease (see Gentes et al., follicles. Inflamed follicles may rupture, 2007). Other than the presence of mites, releasing mites and inflammatory cells into no other health issues could be identified the surrounding dermis (Fig. 3D), which in the mule deer or the elk (Table 1). Data may result in discrete pyogranulomas were not available on the white-tailed deer (Desch and Nutting, 1974; Bukva, 1987; from South Carolina. However, demodec- Bildfell et al., 2004; Gentes et al., 2007). tic mites were not the only parasites Nodular dermatitis tends to be associated present in the white-tailed deer from with D. kutzeri, but not with D. odocoilei South Dakota. (Dermacentor albi- (Desch and Nutting, 1974; Bukva, 1987). pictus), keds (Lipoptena depressa de- The lesions in the mule deer and elk pressa), and strongylid nematodes were reported here are consistent with previous also present. Parasitism, combined with reports of D. kutzeri-associated nodular the nutritional challenges of winter, may dermatitis, while the lesions in the white- have contributed to immunosuppression, tailed deer may reflect the mixed D. resulting in overt demodicosis in this kutzeri and D. odocoilei infestation. animal. Alternatively, the presence of 590 JOURNAL OF WILDLIFE DISEASES, VOL. 46, NO. 2, APRIL 2010 multiple ectoparasites (Demodex spp. and ———. 1987. Redescription of Demodex nanus Dermacentor albipictus) capable of caus- (: Demodicidae) from Rattus norvegicus and R. rattus (Rodentia). Journal of Medical ing alopecia may have resulted in more- Entomology 24: 19–23. extensive hair loss than either parasite ———, AND W. B. NUTTING. 1974. Demodex would have produced alone. odocoilei sp. nov. from the white-tailed deer, The authors thank Daniel Licht for the Odocoileus virginianus. Canadian Journal of photograph used in Fig. 1 and Terry Zoology 52: 785–789. 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