Muscleworms, Parelaphostrongylus andersoni (Nematoda: Protostrongylidae), discovered in Columbia white-tailed deer from Oregon and Washington: implications for biogeography and host associations

Parelaphostrongylus andersoni is considered a characteristic nematode infecting white-tailed deer (Odocoileus virginianus). Host and geographic distribution for this parasite, however, remain poorly defined in the region of western North America. Fecal samples collected from Columbia white-tailed deer (O. v. leucurus) in a restricted range endemic to Oregon and Washington, USA, were examined for dorsal-spined larvae characteristic of many protostrongylid nematodes. Multilocus DNA sequence data (internal transcribed spacer 2 and cytochrome c oxidase subunit 1) established the identity and a new record for P. andersoni in a subspecies of white-tailed deer previously unrecognized as hosts. Populations of P. andersoni are now recognized along the basin of the lower Columbia River in Oregon and Washington and from south-central Oregon on the North Umpqua River. Current data indicate a potentially broad zone of sympatry for P. andersoni and Parelaphostrongylus odocoilei in the western region of North America, although these elaphostrongylines seem to be segregated, respectively, in white-tailed deer or in black-tailed and mule deer (Odocoileus hemionus) at temperate latitudes. The geographic range for P. andersoni in white-tailed deer is extended substantially to the west of the currently defined limit in North America, and we confirm an apparently extensive range for this elpahostrongyline. These observations are explored in the broader context of host and geographic associations for P. andersoni and related elaphostrongylines in North American cervids.     

Geographic distribution of the muscle-dwelling nematode Parelaphostrongylus odocoilei in North America, using molecular identification of first-stage larvae

Molecular identification of dorsal-spined larvae (DSL) from fecal samples indicates that the protostrongylid parasite Parelaphostrongylus odocoilei occupies a broader geographic range in western North America than has been previously reported. We analyzed 2,124 fecal samples at 29 locations from thinhorn sheep (Ovis dalli dalli and O. d. stonei), bighorn sheep (Ovis canadensis canadensis and O. c. californiana), mountain goats (Oreamnos americanus), woodland caribou (Rangifer tarandus caribou), mule deer (Odocoileus hemionus hemionus), and black-tailed deer (O. h. columbianus). The DSL were recovered from populations of thinhorn sheep south, but not north, of the Arctic Circle, and they were not recovered from any of the bighorn sheep populations that we examined. In total, DSL were recovered from 20 locations in the United States and Canada (Alaska, Yukon Territory, Northwest Territories, British Columbia, Alberta, and California). The DSL were identified as P. odocoilei by comparing sequences of the second internal transcribed spacer (ITS2) region of ribosomal RNA among 9 protostrongylid species validated by adult comparative morphology. The ITS2 sequences were markedly different between Parelaphostrongylus and other protostrongylid genera. Smaller fixed differences served as diagnostic markers for the 3 species of Parelaphostrongylus. The ITS2 sequences (n = 60) of P. odocoilei were strongly conserved across its broad geographic range from California to Alaska. Polymorphism at 5 nucleotide positions was consistent with multiple copies of the ITS2 within individual specimens of P. odocoilei. This work combines extensive fecal surveys, comparative morphology, and molecular diagnostic techniques to describe comprehensively the host associations and geographic distribution of a parasitic helminth.     

Hair-loss syndrome in black-tailed deer of the Pacific Northwest

A widespread hair-loss syndrome (HLS) has affected Columbian black-tailed deer (Odocoileus hemionus columbianus) in western Oregon and Washington (USA) since 1996. In order to better characterize the condition, 21 HLS-affected black-tailed deer (BTD) were necropsied, and body condition, parasite burdens, and significant lesions were noted. All deer were in poor body condition, and at least 17 had severe internal parasite burdens. A consistent finding was the presence of large numbers of chewing lice, identified as an indeterminate species of Damalinia (Cervicola). Four animals were infested with intrafollicular Demodex sp., the first report of this genus of mites in BTD. We postulate that the hair loss is largely due to ectoparasitism by a species of chewing louse that represents a new pathogen for BTD. This loss of pelage also may be an important contributor to the poor body condition of these animals.     

Resource partitioning between sympatric columbian white-tailed and black-tailed deer in western Oregon

We studied resource partitioning between sympatric populations of Columbian white-tailed (CWTD; Odocoileus virginianus leucurus) and black-tailed (BWTD) deer (O. odocoileus hemionus columbianus) in western Oregon to understand potential mechanisms of coexistence. We used horseback transects to describe spatial distributions, population overlap, and habitat use for both species, and we studied diets with microhistological analysis of fecal samples. Distribution patterns indicated that white-tailed and black-tailed deer maintained spatial separation during most seasons with spatial overlap ranging from 5%–40% seasonally. Coefficients of species association were negative, suggesting a pattern of mutual avoidance. White-tailed deer were more concentrated in the southern portions of the study area, which was characterized by lower elevations, more gradual slopes, and close proximity to streams. Black-tailed deer were more wide ranging and tended to occur in the northern portions of the study area, which had higher elevations and greater topographical variation. Habitat use of different vegetative assemblages was similar between white-tailed and black-tailed deer with overlap ranging from 89%–96% seasonally. White-tailed deer used nearly all habitats available on the study area except those associated with conifers. White-tailed deer used oak-hardwood savanna shrub, open grassland, oak-hardwood savanna, and riparian habitats the most. Black-tailed deer exhibited high use for open grassland and oak-hardwood savanna shrub habitats and lower use of all others. The 2 subspecies also exhibited strong seasonal similarities in diets with overlap ranging from 89% to 95%. White-tailed deer diets were dominated by forbs, shrubs, grasses, and other food sources (e.g., nuts and lichens). Columbian black-tailed deer diets were dominated mostly by forbs and other food sources. Seasonal diet diversity followed similar patterns for both species with the most diverse diets occurring in fall and the least diverse diets in spring. High overlap in habitat use and diets resulted in high trophic overlap (81–85%) between white-tailed and black-tailed deer; however, the low spatial overlap reduced the potential for exploitative competition but may have been indicative of inference competition between the species. Diverse habitat and forage opportunities were available on the study area due to heterogeneous landscape characteristics, which allowed ecological separation between white-tailed and black-tailed deer despite similarities in diets and habitat use. We make several recommendations for management of CWTD, a previously threatened species, based on the results of our study. © 2011 The Wildlife Society.     

Winter fawn survival in black-tailed deer populations affected by hair loss syndrome

Overwinter fawn mortality associated with hair loss syndrome (HLS) is anecdotally thought to be important in declines of Columbian black-tailed deer (Odocoileus hemionus columbianus) populations in Washington and Oregon (USA). We determined prevalence of HLS in black-tailed deer, September and April fawn:doe ratios, and minimum overwinter survival rates of fawns for selected game management units (GMUs) in western Washington from 1999 to 2001. Prevalence of HLS ranged from 6% to 74% in fawns and 4% to 33% in does. Minimum fawn survival ranged from 0.56 to 0.83 and was unrelated to prevalence of HLS in either does (r=0.005, P=0.991) or fawns (r=-0.215, P=0.608). The prevalence of HLS in either does or fawns was also unrelated to either fall fawn:doe ratios (HLS does: r=-0.132, P=0.779; HLS fawns: r=0.130, P=0.760) or spring fawn:doe ratios (HLS does: r=-0.173, P=0.711; HLS fawns: r=-0.020, P=0.963). However, the prevalence of HLS in does and fawns was strongly related (r=0.942, P=0.002), and GMUs with high prevalence of HLS had lower deer population densities (fawns: r=-0.752, P=0.031; does: r=-0.813, P=0.026). Increased overwinter mortality of fawns because of HLS was not supported by our data. Decreased production of fawns, increased summer mortality of fawns, or both were seen in six of eight study GMU-year combinations. Observed rates of productivity and minimum fawn survival were inadequate to maintain population size in five of eight study GMU-year combinations, assuming an annual doe survival rate of 0.75. The influence of deer condition and population health on adult survival, fawn production, preweaning fawn survival, parasitism, and prevalence of HLS in both fawns and adults need to be clarified to identify what factors are limiting black-tailed deer productivity.     

Evaluation of ivermectin for treatment of hair loss syndrome in black-tailed deer

Since 1997, numerous Columbian black-tailed deer (Odocoileus hemionus columbianus) in western Washington (USA) have developed a hair loss syndrome that often preceded emaciation, debilitation, pneumonia, and death. To study this syndrome, eight affected free-ranging Columbian black-tailed deer fawns were captured from western Washington in February 1999 to determine the effect of ivermectin treatment. Fecal examinations indicated that the internal parasites were Dictyocaulus viviparus, Parelaphostrongylus sp., Trichuris sp., Moniezia sp., Eimeria spp., and gastrointestinal strongyles. Biting lice (Tricholipeurus parallelus) were observed on all deer, with up to 5 lice/cm(2) on the index areas counted. Three deer were treated with ivermectin subcutaneously at doses between 0.2 and 1.3 mg/kg of body weight monthly for four consecutive months, and five control deer received no anthelmintic treatment. Complete blood counts, parasite evaluations, weight gains, and hair loss evaluations were used to assess effectiveness of treatment. Two untreated deer died during the experiment compared with no deaths among the three treated deer. Treated deer gained significantly more weight (P<0.05) than the untreated deer (22.4 vs. 12.6 kg, respectively) that survived the experiment, had significantly fewer parasite eggs and larvae (P<0.05) in feces and significantly fewer nematodes (P<0.05) at necropsy, and regrew their hair at a faster rate than untreated deer. Lice and all nematode eggs and larval stages in feces were eliminated or greatly reduced following treatment. On the basis of these data, excessive louse populations, gastrointestinal nematodes, and the lung-worms Parelaphostrongylus sp. and D. viviparus, might be important predisposing factors for this hair loss condition and death of affected animals.     

Serological evidence of California serogroup virus activity in Oregon

We wished to demonstrate evidence of the presence of California serogroup viruses in Oregon and to test for the presence of certain other arboviruses in large ungulates. Blood samples from black-tailed deer (Odocoileus hemionus columbianus), mule deer (O. hemionus hemionus), and Roosevelt elk (Cervus elaphus roosevelti) from nine counties in Oregon were tested by serum-dilution plaque reduction neutralization for antibody to California serogroup viruses, including snowshoe hare, California encephalitis, and Jamestown Canyon, as well as to Cache Valley (Bunyamwera serogroup) and Klamath, an ungrouped rhabdovirus. Of 132 samples tested, 60 (46%) were found to be seropositive at a dilution of greater than or equal to 1:10 for at least one of the five different arboviruses. Forty (30%) samples contained antibody to more than one arbovirus, and 15 samples (11%) contained antibody to all five. Of these 15, 14 were from 75 black-tailed deer sera collected in Lincoln County, Oregon. Seropositivity rates for black-tailed deer ranged from 23% to 35%, with all five arboviruses represented. Positive reactions for all five arboviruses were represented among mule deer sera at rates from 5% to 29%. Elk sera were found to be positive for four of the viruses (none for Klamath virus). Although Cache Valley and Klamath viruses have been reported from Oregon, these data represent the first evidence of a California serogroup virus in the state.     

Parelaphostrongylus odocoilei: Life cycle in experimentally infected cervids including the mule deer, Odocoileus h. hemionus

The life cycle of a metastrongyloid nematode, Parelaphostrongylus odocoilei, was successfully completed in three members of the Cervidae: mule deer (Odocoileus h. hemionus), black-tailed deer (O. h. columbianus), and moose (Alces alces andersoni). The terrestrial gastropod, Triodopsis multilineata, was the experimental intermediate host. White-tailed deer (O. virginianus dacotensis) were refractory to infection. The prepatent period of P. odocoilei was significantly shorter in mule deer (X = 53 days) than in the black-tailed deer or moose. There was an inverse relationship between the size of the infective inoculum and the duration of the prepatent period of P. odocoilei in mule deer, but not in black-tailed deer. The duration and intensity of larval production of P. odocoilei were higher in mule deer than in the other hosts. Peak larval production in the feces (approximately 14,000 larvae/g) of mule deer was in excess of previous reports for elaphostrongyline nematodes, regardless of the size of the infective inoculum. Daily larval production, estimated at 3 to 4 × 10⁶ larvae/day, was six times higher than estimates for other elaphostrongylines. The duration of patency was not clearly established, but three mule deer and one black-tailed deer passed larvae for 12, 18, 24, and 18 months, respectively. On the basis of the reduced prepatent period and increased length and intensity of larval production, O. h. hemionus is considered the primary host of P. odocoilei.     

The modified card agglutination test: an accurate tool for detecting anaplasmosis in Columbian black-tailed deer

Inoculation of susceptible calves confirmed that the modified card agglutination test accurately detected the anaplasmosis infection status of each of 35 Columbian black-tailed deer (Odocoileus hemionus columbianus). Anaplasma marginale, and specific antibodies, were demonstrated only in calves which received blood from deer that were positive by the card test. The modified card agglutination testing of deer serum was performed in the manner recommended for testing cattle serum with bovine-origin antigen and bovine serum factor.     

Demodicosis in a mule deer (Odocoileus hemionus hemionus) from Saskatchewan, Canada

Infestation of deer with Demodex spp. mites has been described in white-tailed deer (Odocoileus virginianus) and in Columbian black-tailed deer (Odocoileus hemionus columbianus) in North America, as well as in four species of deer in Europe. We describe Demodex sp. infestation in an adult female mule deer (Odocoileus hemionus hemionus) with skin lesions found dead near Saskatoon, Saskatchewan, Canada. This is believed to be the first report of demodicosis in mule deer.     

Endogenous type C RNA virus of Odocoileus hemionus, a mammalian species of New World origin.

Type C RNA viruses have been isolated from several Old World vertebrates, and an even larger number of Old World species have been shown to contain endogenous viral genetic sequences. The present report describes the first isolation of type C virus endogenous to a species originating in the New World. This virus, isolated from cells of the Columbian black-tailed deer, Odocoileus hemionus, is shown to possess genetic sequences in common with DNA of its species of origin. While it shares biochemical and immunologic characteristics with other mammalian type C viruses, its immunologic properties readily distinguish it from known endogenous viruses.     

New host and geographic records for two protostrongylids in Dall's sheep.

Biodiversity survey and inventory have resulted in new information on the distribution of Protostrongylidae in Dall's sheep (Ovis dalli dalli) from the Northwest Territories (NT, Canada) and from Alaska (AK, USA). In 1998, Parelaphostrongylus odocoilei adults were found for the first time in the skeletal muscles of Dall's sheep in the Mackenzie Mountains (NT). Adult P. odocoilei were associated with petechial and ecchymotic hemorrhages and localized myositis; eggs and larvae in the lungs were associated with diffuse granulomatous pneumonia. Experimental infections of the slugs Deroceras laeve and Deroceras reticulatum with dorsal-spined first-stage larvae assumed to be P. odocoilei, from ground-collected feces from Dall's sheep in the Mackenzie Mountains, yielded third-stage larvae by at least 28 (in D. laeve) and 48 (in D. reticulatum) days post-infection. Third-stage larvae emerged from D. laeve between days 19 and 46 post-infection and emergence occurred both at room temperature and at 10 to 12 C. Protostrongylus stilesi were definitively identified from the lungs of Dall's sheep collected in the Mackenzie Mountains, NT in 1998. Specimens collected from sheep in the Mackenzie Mountains, NT in 1971-72, and the Alaska Range, AK in 1972 were also confirmed as P. stilesi. Lung pathology associated with adults, eggs, and larvae of P. stilesi was similar to that described in bighorn sheep (Ovis canadensis). Concurrent infections with P. odocoilei and P. stilesi in a single host have not been previously reported.     

Modeling Black-Tailed Deer Population Dynamics Using Structured and Unstructured Approaches

Abstract: We used cohort analysis to reconstruct the female segment of a Columbian black-tailed deer (Odocoileus hemionus columbianus) population from 1979 to 2000 in the western Cascades of Washington, USA. We used reconstructed population estimates and age class representations to analyze relationships between population change and female density, forage availability, and weather influences. We applied stage structured and unstructured modeling approaches and used information-theoretic methods to select the best models. We used habitat covariates to develop predictive functions for fertility and survival parameters in structured models. The best structured and unstructured models were composed of combinations of factors including population density, forage availability, and winter weather. Structured and unstructured models could assist with management of black-tailed deer by providing the ability to predict deer population change given covariate values.     

Comparative studies of Babesia spp. from white-tailed and sika deer

Babesia odocoilei from white-tailed deer (Odocoileus virginianus) in Texas (USA) and B. capreoli isolated from sika deer (Cervus nippon) in Ireland were compared morphologically and antigenically. Babesia odocoilei and B. capreoli paired pyriforms resembled each other closely when in sika deer, but B. odocoilei pyriforms in white-tailed deer were slightly different. Babesia odocoilei in white-tailed deer also differed from B. odocoilei and B. capreoli in sika deer in the frequency of its developmental forms. Indirect immunofluorescence antibody test titres showed that there was some antigen cross-reactivity, but not as much as between B. capreoli and the bovine parasite, B. divergens. The Babesia spp. from deer that we studied appear to be distinct but related species. The low infectivity of B. odocoilei for a splenectomised sika deer suggests that sika deer in North America are probably not very susceptible to this parasite in the wild.     

Protostrongylid parasites and pneumonia in captive and wild thinhorn sheep (Ovis dalli)

We describe health significance of protostrongylid parasites (Parelaphostrongylus odocoilei and Protostrongylus stilesi) and other respiratory pathogens in more than 50 naturally infected Dall's sheep (Ovis dalli dalli) from the Mackenzie Mountains, Northwest Territories (1998-2002) as well as in three Stone's sheep (O. d. stonei) experimentally infected with P. odocoilei (2000-2002). Histological lesions in the brain and distribution of P. odocoilei in the muscles of experimentally and naturally infected sheep were consistent with a previously hypothesized "central nervous system to muscle" pattern of migration for P. odocoilei. Dimensions of granulomas associated with eggs of P. odocoilei and density of protostrongylid eggs and larvae in the cranial lung correlated with intensity of larvae in feces, and all varied with season of collection. Prevalence of P. stilesi based on the presence of larvae in feces underestimated true prevalence (based on examination of lungs) in wild Dall's sheep collected in summer and fall. Similarly, counts of both types of protostrongylid larvae in feces were unreliable indicators of parasitic infection in wild Dall's sheep with concomitant bacterial pneumonia associated with Arcanobacterium pyogenes, Pasteurella sp., and Mannheimia sp. Diffuse, interstitial pneumonia due to P. odocoilei led to fatal pulmonary hemorrhage and edema after exertion in one experimentally infected Stone's sheep and one naturally infected Dall's sheep. Bacterial and verminous pneumonia associated with pathogens endemic in wild Dall's sheep in the Mackenzie Mountains caused sporadic mortalities. There was no evidence of respiratory viruses or bacterial strains associated with domestic ruminants, from which this population of wild sheep has been historically isolated.     

Parelaphostrongylus odocoilei (Nematoda: Protostrongylidae) and a protostrongylid nematode in woodland caribou (Rangifer tarandus caribou) of Alberta, Canada

Two size-groups of dorsal-spined, first-stage, nematode larvae were found in feces of woodland caribou, Rangifer tarandus caribou (Gmelin), in Alberta from 1976-1982. Larvae from caribou feces in northeastern Alberta were 451 +/- 17 micrograms in length, while those from west-central Alberta were 362 +/- 18 micrograms in length. Larvae collected from west-central Alberta developed to the infective stage, experimentally, in the terrestrial gastropod Triodopsis multilineata (Say) and were infective to captive mule deer fawns, Odocoileus H. hemionus (Rafinesque). Adult nematodes, identified as Parelaphostrongylus odocoilei (Hobmaier and Hobmaier, 1934), were recovered from the skeletal muscles of the mule deer.     

Bionomics of larvae of Parelaphostrongylus odocoilei (Nematoda: Protostrongylidae) in experimentally infected gastropod intermediate hosts

Parelaphostrongylus odocoilei is a protostrongylid parasite that has recently been recognized at several locations in sub-Arctic, but not Arctic, North America. We investigated factors that may determine the distribution of P. odocoilei, including suitable gastropod intermediate hosts, temperature requirements for larval development in gastropods, and larval emergence facilitating overwinter transmission. We collected and experimentally infected gastropods from a site in the sub-Arctic where P. odocoilei is at the northern limit of its distribution. Deroceras laeve, Catinella sp., and Euconulus cf fulvus, but not members of the Pupillidae, were suitable intermediate hosts. We describe bionomics of larvae of P. odocoilei in D. laeve and Catinella sp. Infective larvae emerged from all slugs (D. laeve) and 60% of Catinella sp. snails, and emergence from D. laeve was intensity dependent. Emerged infective larvae survived up to 6 mo under conditions approximating that of the subnivean environment. In D. laeve, there was a direct relationship between temperature and development rate of larvae of P. odocoilei. Larvae of P. odocoilei did not develop to infective stage below the theoretical threshold (8.5 C), and required a minimum of 163 degree days to complete development. These developmental parameters can be incorporated into a model to predict larval development in the field. Knowledge of the factors influencing larval bionomics provides the foundation for predicting temporal and spatial patterns of parasite distribution, abundance, and transmission.     

Spirochetes in mammals and ticks (Acari: Ixodidae) from a focus of Lyme borreliosis in California

In northern California, antibodies to Borrelia burgdorferi were detected in 58 of 73 (79%), and spirochetemias in one of 26 (4%) black-tailed jackrabbits (Lepus californicus californicus), by indirect and direct immunofluorescence, respectively. Five species of ticks (Dermacentor occidentalis, D. parumapertus, Ixodes neotomae, I. pacificus, and Haemaphysalis leporispalustris) were collected from rabbits. Two of these species of ticks were found to contain spirochetes; two of 10 (20%) I. neotomae and two of 174 (1%) H. leporispalustris. A strain of B. burgdorferi was recovered from I. neotomae. One infected H. leporispalustris female passed spirochetes via eggs to about 67% of her progeny. The widespread distribution of the black-tailed jackrabbit, its infestation by at least four ticks (D. occidentalis, D. parumapertus, I. neotomae, and I. pacificus) known to be infected naturally with B. burgdorferi, and the high prevalence of spirochetal antibody in this lagomorph suggest that it might be useful as a sentinel for surveillance of Lyme borreliosis. Spirochetes were detected in 15% of 40 Columbian black-tailed deer (Odocoileus hemionus columbianus) by direct immunofluorescence bound with a Borrelia-specific monoclonal antibody (H9724), but not with a monoclonal antibody (H5332) specific for B. burgdorferi. The geographical overlap of different borreliae in ticks that bite wildlife such as deer may confound spirochetal serosurveys, and underscores the need for more specific serologic tests than those currently available.