Phthiraptera: Trichodectidae): Occurrence of an Exotic Chewing Louse on Cervids in North America
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SAMPLING,DISTRIBUTION,DISPERSAL Bovicola tibialis (Phthiraptera: Trichodectidae): Occurrence of an Exotic Chewing Louse on Cervids in North America JAMES W. MERTINS,1 JACK A. MORTENSON,2,3 JEFFREY A. BERNATOWICZ,4 5 AND P. BRIGGS HALL J. Med. Entomol. 48(1): 1Ð12 (2011); DOI: 10.1603/ME10057 ABSTRACT Through a recent (2003Ð2007) survey of ectoparasites on hoofed mammals in western North America, a literature review, and examination of archived museum specimens, we found that the exotic deer-chewing louse, Bovicola tibialis (Piaget), is a long-term, widespread resident in the region. The earliest known collection was from Salt Spring Island, Canada, in 1941. We found these lice on the typical host, that is, introduced European fallow deer (Dama dama L.), and on Asian chital (Axis axis [Erxleben]), native Columbian black-tailed deer (Odocoileus hemionus columbianus [Ri- chardson]), and Rocky Mountain mule deer (O. h. hemionus [RaÞnesque]) ϫ black-tailed deer hybrids. Chital and the hybrid deer are new host records. All identiÞed hosts were known to be or probably were exposed to fallow deer. Geographic records include southwestern British Columbia, Canada; Marin and Mendocino Counties, California; Deschutes, Lincoln, and Linn Counties, Oregon; Yakima and Kittitas Counties, Washington; Curry County, New Mexico; and circumstantially, at least, Kerr County, Texas. All but the Canadian and Mendocino County records are new. Bovicola tibialis displays a number of noteworthy similarities to another exotic deer-chewing louse already established in the region, that is, Damalinia (Cervicola) sp., which is associated with a severe hair-loss syndrome in black-tailed deer. We discuss longstanding problems with proper identiÞcation of B. tibialis, the probability that it occurs even more widely in the United States, and the prospects for it to cause health problems for North American deer. Additional information gathered since our active survey estab- lishes further new distribution and host records for B. tibialis. KEY WORDS hair loss, exotic pediculosis of deer, EPOD, Dama dama, Odocoileus hemionus During a recent survey for exotic Asian chewing lice drome is characterized by a general decline in body known to be associated with a pathologic hair-loss condition and a loss of pelage, especially over the syndrome (HLS) in native deer in the North Ameri- thorax, ßanks, and hindquarters. The most severe cases can PaciÞc Northwest, we unexpectedly encountered may progress to morbidity and mortality. Victims are the widespread presence of Bovicola tibialis (Piaget) mostly young deer, especially does, and the syndrome (Phthiraptera: Trichodectidae), a European chewing is most evident in the winter and spring. HLS was louse parasite of fallow deer, Dama dama L. Some noted Þrst by wildlife biologists in Washington (Fo- infestations by B. tibialis now seem to be causing reyt et al. 2004), but deer showing similar signs soon deer-host hair loss much like that previously associ- appeared in Oregon, as well (Bildfell et al. 2004). ated with the Asian lice. The etiology of HLS is not well understood and may In the mid-1990s, native populations of the Colum- depend on the convergence of several predisposing bian black-tailed deer, Odocoileus hemionus columbia- factors (Bender and Hall 2004, Bildfell et al. 2004). nus (Richardson) (BTD), began to display signs of However, one consistent and possibly critical element mysterious and unprecedented hair loss. The syn- is the presence on affected animals of large popula- tions of chewing lice (Phthiraptera: Ischnocera: Tri- chodectidae). The lice in question were an undeter- 1 Corresponding author: United States Department of Agriculture, Animal and Plant Health Inspection Service, Veterinary Services, mined species of Damalinia (Cervicola), a subgenus of National Veterinary Services Laboratories, 1920 Dayton Avenue, artiodactyl parasites whose only known members are Ames, IA 50010 (e-mail: James.W.Mertins@ aphis.usda.gov). endemic to the Eastern Hemisphere. It follows, then, 2 United States Department of Agriculture, Animal and Plant that the lice are introduced exotics whose normal Health Inspection Service, Veterinary Services, 530 Center Street NE, Suite 335, Salem, OR 97301. hosts are some Old World artiodactyl, probably a 3 Oregon State University, Department of Fisheries and Wildlife, cervid, and BTD are aberrant, but acceptable hosts. 104 Nash Hall, Corvallis, OR 97331. Such colonizations of local vertebrate hosts by exotic 4 Washington Department of Fish and Wildlife, 1701 S. 24th Ave- parasites are prone to pathological outcomes (Bru- nue, Yakima, WA 98902. 5 Washington Department of Fish and Wildlife, 16018 Mill Creek netti and Cribbs 1971, Foreyt et al. 1986, Hoberg et al. Boulevard, Mill Creek, WA 98012. 2001), and we believe that naive, young, and winter- 2JOURNAL OF MEDICAL ENTOMOLOGY Vol. 48, no. 1 stressed BTD are particularly susceptible to attacks by slide-mounted archival specimens of cervid-chewing this Cervicola louse. Exploding populations of the lice lice with regional origins from entomological collec- are extremely irritating to the host victims, leading tions at the Spencer Entomological Collection (Uni- them to excessive grooming behavior that only exac- versity of British Columbia, Vancouver, BC, Canada) erbates extensive pelage damage already exacted by and the United States National Parasite Collection feeding activities of huge numbers of lice (Bildfell et (USNPC, United States Department of Agriculture al. 2004). [USDA], Agricultural Research Service, Beltsville, In an effort to assess the geographic extent, chro- MD). nological progression, and host speciÞcity of HLS and Parasite identiÞcations were done at the USDA, Cervicola sp. infestations, we extensively surveyed and National Veterinary Services Laboratories (NVSL, examined a variety of native and exotic artiodactyl Ames, IA). The great majority were made under a species for ectoparasites along the West Coast of dissecting microscope at magniÞcations up to ϫ60 by North America between 2003 and 2007. Incidental to J.W.M. using standard taxonomic reference guides. this effort, we encountered several other unusual par- The small number of borrowed slide-mounted louse asites, including the unexpected presence in several specimens was studied and identiÞed under a com- localities of another exotic cervid-chewing louse, B. pound microscope using differential interference con- tibialis, a speciÞc parasite of the European fallow deer. trast illumination at magniÞcations up to ϫ400. The In this study, we present information gathered on the basic references for chewing louse identiÞcations occurrence of B. tibialis in North America and pathol- were Lyal (1985), Werneck (1950), and Price et al. ogy circumstantially associated with its presence on (2003), supplemented by original descriptions, other native deer. descriptive literature, and reference specimens in the NVSL parasitology collection. For veriÞcation of sub- ject louse species identiÞcation, we borrowed and Materials and Methods studied voucher samples of B. tibialis collected on Between March 2003 and September 2007, we ac- free-ranging fallow deer in Europe from the entomol- quired, examined, and identiÞed Ϸ500 collections of ogy collection at the Natural History Museum (Lon- ectoparasites from various free-ranging and captive don, United Kingdom). We follow the supraspeciÞc artiodactyls in California, Oregon, Washington, and louse taxonomy proposed by Lyal (1985) and the British Columbia, Canada. Most of the host animals taxonomy of Pitra et al. (2004) and Groves (2005) for were BTD, but variable sample numbers came from cervids. mule deer (O. h. hemionus [RaÞnesque], MD), BTD ϫ For perspective and completeness, we reviewed, MD hybrid animals, Columbian white-tailed deer evaluated for validity, and summarized previously (Odocoileus virginianus leucurus [Douglas]), North- published citations mentioning the existence of exotic west white-tailed deer (O. virginianus ochrourus V. lice on cervid hosts in North America. Bailey), Roosevelt elk (Cervus canadensis roosevelti Representative vouchers of studied lice are retained Merriam), sika deer (C. nippon Temminck, sensu in the NVSL parasitology reference collection, or at lato), fallow deer, and chital (Axis axis [Erxleben]). A other listed institutions, with accession numbers as few examined samples came from captive aoudad given in the text and in Table 1. (Ammotragus lervia [Pallas]), greater kudu (Tragela- phus strepsiceros [Pallas]), and slender-horned gazelle Results (Gazella leptoceros Cuvier). Many of the parasite sam- ples were collected from targeted wild animals show- The general groups of ectoparasites collected from ing signs of HLS and killed (or anesthetized) by wild- the examined hosts comprised ticks (Acari: Ixodidae), life biologists for surveillance examination. Others chiggers (Acari: Trombiculidae), keds (Diptera: Hip- were collected during necropsies of animals opportu- poboscidae), ßeas (Siphonaptera: Pulicidae), sucking nistically found dead from road accidents or natural lice (Phthiraptera: Linognathidae), and chewing lice causes; from hunter-killed animals at check stations; or (Phthiraptera: Trichodectidae). We found among from captive/farmed animals harvested for commer- them a number of interesting parasite records and host cial purposes, dead of natural causes, or anesthetized relationships that will be detailed elsewhere, but in for examination. this study we present evidence we found that