ALCES VOL. 48, 2012 HENNINGSEN ET AL. – ELAEOPHORA IN WYOMING

DISTRIBUTION AND PREVALENCE OF ELAEOPHORA SCHNEIDERI IN MOOSE IN WYOMING

John C. Henningsen1, Amy L. Williams1,2, Cynthia M. Tate3, Steve A. Kilpatrick1,4, and W. David Walter5

1Wyoming Game and Fish Department, PO Box 67, Jackson, Wyoming 83001, USA; 3Wyoming Game and Fish Department- Wildlife Diseases Laboratory, 1174 Snowy Range Road, Laramie, Wyoming 82070, USA; 5USDA/APHIS/WS National Wildlife Research Center, 4101 LaPorte Avenue, Fort Collins, Colorado 80521, USA.

ABSTRACT: Elaeophora schneideri causes disease in aberrant hosts such as moose. Documented E. schneideri infections in moose are relatively rare, yet noteworthy enough that individual cases describ- ing morbidity and mortality have been the norm for reporting. Surveillance efforts for E. schneideri in Wyoming moose in the 1970s found zero cases, but since 2000 several moose in Wyoming discovered dead or showing clinical signs of elaeophorosis have been found infected with E. schneideri. In 2009 we searched for worms in the carotid arteries of 168 hunter-harvested moose from across Wyoming to determine the prevalence and distribution of E. schneideri in moose; 82 (48.8%; 95% CI: 41.4-56.3%) were positive for E. schneideri. Prevalence did not differ between sexes or among age classes but there was difference in prevalence among herd units (range = 5-82.6%). Intensity of infection (range = 1-26 worms) did not differ between sexes, among age classes, or among herd units. Our findings indicate that moose do not succumb to the parasite to the extent previously thought. Prevalence and intensity were constant across age classes, suggesting that infected moose are surviving and an acquired, immunological resistance to further infection develops. In addition, moose might sometimes act as natural hosts to the parasite, as indicated by 1) high prevalence of infection in moose in areas where sympatric had much lower prevalence of infection, and 2) preliminary necropsy findings that revealed microfilariae in skin samples from 3 moose. However, negative impacts to moose and moose populations cannot be ruled out entirely, as this study was limited to apparently healthy hunter-harvested . While moose appear to often survive infection with E. schneideri, prevalence of ~50% is still cause for concern because it is unknown to what extent this parasite causes subclinical effects in moose that might impact recruitment or productivity. Subsequent research on moose herds where E. schneideri occurs should consider the effects of elaeophorosis and attempt to clarify its role.

ALCES VOL. 48: 35-44 (2012)

Key words: Alces alces, arterial worm, disease, Elaeophora schneideri, elaeophorosis, moose, para- site, Wyoming.

Elaeophora schneideri is a filarioid Adcock 1971). Microfilariae then migrate that lives in the cephalic arteries to the capillaries in the dermis of the host’s of mule deer (Odocoileus hemionus) (Hibler face and forehead where they are taken up et al. 1970) and black-tailed deer (O. hemio- in the blood meal of the intermediate host. nus columbianus) (Weinmann et al. 1973). Horse flies (Family Tabanidae) of the genera Adult in the arteries of deer give , , and (Hibler et birth to live young - microfilariae (Hibler and al. 1970, Clark and Hibler 1973, Espinosa 2Present address: University of Wyoming, Department of Veterinary Sciences, 1174 Snowy Range Road, Laramie, Wyoming 82070, USA. 4Present address: Conservation Research Center of Teton Science Schools, 700 Coyote Canyon, Jack- son, Wyoming 83001, USA. 35 ELAEOPHORA IN WYOMING MOOSE – HENNINGSEN ET AL. ALCES VOL. 48, 2012

1983) are intermediate hosts of the parasite. (Matthews, 2012). Transmission of the third stage infective to In Wyoming moose both the prevalence of the vertebrate host occurs after E. schneideri infection and the parasite’s geographic extent larvae develop in the horse fly vector for 2-3 appear to have undergone a recent, notable weeks (Hibler and Adcock 1971, Hibler and increase. In 1973-74 Worley (1975) exam- Metzger 1974, Davies 1979). ined 74 apparently healthy, hunter-harvested Development of E. schneideri in the de- moose: 69 from Teton and Fremont Counties in finitive host has been described previously northwestern Wyoming, and 5 from Park and (Weinmann et al. 1973, Hibler and Metzger Gallatin Counties in southwestern Montana. 1974). Less is known about development No Wyoming moose and only 3 of 5 Montana of E. schneideri in aberrant hosts but patho- moose were infected with worms in the carotid genesis usually stems from the parasite’s arteries. Presumably, low prevalence of E. delayed migration through the host body or schneideri in Wyoming led Hibler (1982) to complications from circulatory impairment believe elaeophorosis was of minimal impor- (i.e., elaeophorosis; Adcock and Hibler 1969, tance to Wyoming and moose. Hibler and Metzger 1974, Anderson 2001). Whereas E. schneideri has been docu- Gross clinical signs of infection among aber- mented consistently in small numbers of mule rant hosts range from dry gangrene of nose and deer and elk in Wyoming since 1967 (H. E. ear tips and antler malformations, to blindness, Edwards, WGFD, unpublished data), the first central nervous system damage, and death. infected moose was not identified until much Documented aberrant hosts of E. schneideri later. Within 2 weeks in January 2000, 2 moose are moose (Alces alces), elk (Cervus elaphus), were euthanized by WGFD field personnel in white-tailed deer (O. virginianus), bighorn Fremont County (central Wyoming) because (Ovis canadensis), and domestic (Boyce they were lethargic or walking in circles and et al. 1999, Anderson 2001). showed signs of impaired vision; illness in each E. schneideri is widespread across North of those cases was attributed to elaeophorosis America occurring in mule deer in Nebraska (W. E. Cook, unpublished report). In 2008 a (McKown et al. 2007), South Dakota (Jacques 3-yr-old cow moose in western Wyoming was et al. 2004), Utah (Pederson et al. 1985), Texas euthanized because of its abnormal behavior (Pence and Gray 1981), Colorado, and New (lack of fear, blindness, and loss of motor Mexico (Davies 1979). It has been docu- skills). Upon gross examination, a heavy load mented in white-tailed deer in Arizona (Hibler of worms (30-50) was found in the carotid 1982), Texas (Waid et al. 1984), and several arteries and its clinical signs were attributed southeastern states (Prestwood and Ridgeway to elaeophorosis (C. M. Tate, WGFD, unpub- 1972). Infected elk have been reported from lished report). Oklahoma, New Mexico, Arizona, Colorado, The WGFD and the Wyoming State Vet- and Wyoming (Hibler 1982). erinary Lab (WSVL) increased opportunistic The first documented E. schneideri infec- surveillance of moose in 2008. Animals found tions in moose were in Montana (Worley et al. dead, euthanized due to illness, and road-kills (1972). Subsequently, its presence in small were examined for E. schneideri; several numbers of moose was documented in Utah were found infected with E. schneideri. Most (Jensen et al. 1982), Colorado (Madden et positive cases were from animals discovered al. 1991),Washington (Pessier et al. 1998), dead or showing clinical signs of illness, and and Wyoming in 2000 (W. E. Cook, Wyo- pathology associated with E. schneideri was ming Game and Fish Department [WGFD], implicated in several cases. unpublished report), and Oregon in 2010 In order to survey moose for E. schneideri

36 ALCES VOL. 48, 2012 HENNINGSEN ET AL. – ELAEOPHORA IN WYOMING MOOSE more uniformly across Wyo- ming, a rigorous plan was devel- oped to establish baseline data on prevalence and distribution A of E. schneideri by surveying hunter-harvested moose during the 2009 hunting season. To our knowledge, this was the most comprehensive and widespread effort to date for surveillance of E. schneideri in moose.

STUDY AREA Brimeyer and Thomas (2004) described the history and status of moose in Wyoming through the early 2000s. Moose in Wyoming occupy 3 distinct ranges: 1) Bighorn Mountain Range in north-central Wyo- ming, 2) the Snowy Range and Sierra Madre Ranges of south- east and south-central Wyoming, B and 3) western Wyoming among comparatively connected moun- tain ranges from the Utah border north through Yellowstone Na- tional Park (Fig. 1a). Moose in Wyoming are managed as 11 herd units (herds) comprising discrete populations for which migration among adjacent herds is thought to account for <10% of a herd population. These herds are further divided into 43 hunt areas to provide flexibility for hunting seasons; begin and end dates of hunting seasons vary among areas. The WGFD has a statewide population objective Fig. 1. A) Moose herd units that hunter-harvested moose were of 14,630 moose (post-hunt), collected and sampled for Elaeophora schneideri in 2009 in yet population estimates are Wyoming, USA. B) Intensity of Elaeophora schneideri found considered relatively unreliable in carotid arteries categorized as none (●), low (○), moderate or completely lacking in most (○), and high (○) in hunter-harvested moose by herd unit in herds (Thomas 2008). 2009 in Wyoming, USA.

37 ELAEOPHORA IN WYOMING MOOSE – HENNINGSEN ET AL. ALCES VOL. 48, 2012

METHODS classes and herds; Fisher’s exact test was used We examined hunter-harvested moose for to test for differences between pairs of herds the presence of immature or adult worms in the when contingency tables had ≤5 observations terminal portion of the common carotid arteries in ≥1 cell. Because of the small number and in some instances the proximal portion of of examined animals from individual age the internal maxillary arteries (hereafter field classes, 4 combined age classes were created examinations). Many field examinations were (1, 2-4, 5-7, ≥ 8) for statistical comparisons. conducted at hunter check stations and during Likewise, some adjacent herds (Jackson and opportunistic field checks of successful hunt- Targhee, Lincoln and Uinta) were combined ers. Field examinations also took place when to obtain adequate sample sizes for analyses. hunters brought heads of harvested moose to Some herds were dropped from analyses be- WGFD regional offices, taxidermists, or meat cause they had both small sample sizes and processors. were too geographically separate to justify Incisor teeth were collected from harvest- merging. Because intensity was recorded as ed moose for aging by cementum annuli. The a categorical variable, chi-square was used to specific ages obtained via cementum annuli test for differences in intensity among sexes, are reported in whole years (i.e., yearling is age classes, and herds. Statistical significance 1). Successful development and migration of was set at P ≤0.05 for all tests. Calculations E. schneideri to the carotid arteries of moose were accomplished using SIGMAPLOT 11 would be expected to take 5-6 months (Hibler (Systat Software, San Jose, CA.). and Metzger 1974), thus nematodes would not be expected in the carotids until typically De- RESULTS cember. Thus field examinations as conducted Prevalence in this study could not adequately diagnose The reported harvest in fall 2009 was 548 infections in calves, and surveillance of calves moose (394 adult males, 135 adult females, was not included in this study. and 19 calves); 126 males and 42 females Intensity of infection with worms (Bush et were examined for E. schneideri from 1 al. 1987) was recorded as 1 of 3 categories: 1-6, September-14 November (Table 1), or 31% 7-13, and ≥14. These categories were based of adult females and 32% of adult males in on intensities observed previously in moose the harvest. E. schneideri was present in the from Wyoming and other states (Worley et al. carotid arteries of 48.8% of all moose ≥1 yr 1972, Worley 1975, Madden et al. 1991). In of age (95% CI: 41.4-56.3). Exactly 50% of addition to examining for the presence of E. males (95% CI: 41.4-58.6%) and 45.2% of schneideri, visual signs of elaeophorosis (e.g., females were infected (95% CI: 31.2-60.1%); cropped ears, necrotized tissues, lesions, or prevalence did not differ by sex (χ2 = 0.127; malformed antlers) were recorded. P = 0.72). The number of females checked in each herd was small, but prevalence did Statistical Analysis not appear to differ between sexes within any Prevalence was based on the total num- individual herd. Thus, we combined sexes for ber of positive individuals; 95% confidence statistical comparisons of prevalence among intervals (CI) around these proportions were age classes and herds. calculated based on the binomial distribution Ages were obtained from 151 of 168 (Rózsa et al. 2000). Fisher’s exact test was moose: 9 were yearlings, 54 were 2-4 years used to test for homogeneity in prevalence old, 71 were 5-7 years old, and 17 were ≥8 between sexes. Chi-square was used to test years. The infection rate was 56% in yearlings for homogeneity in prevalence among age (95% CI = 26.6-81.2%), 43% in 2-4 year olds

38 ALCES VOL. 48, 2012 HENNINGSEN ET AL. – ELAEOPHORA IN WYOMING MOOSE

Table 1. Prevalence of Elaeophora schneideri in hunter-harvested moose, Wyoming, USA, 2009. No. moose with differing intensities of infection Herd No. No. % infected No worms Low Moderate High examined infected (prevalence) (1-6) (7-13) (≥14) Absaroka 1 0 0 1 0 0 0 Big Horns 20 1 5 19 0 1 0 Dubois 1 0 0 1 0 0 0 Jackson 10 6 60 4 6 0 0 Lander 4 0 0 4 0 0 0 Lincoln 13 5 38.5 8 2 2 1 Snowy Range1 23 19 82.6 4 13 4 1 Sublette 90 47 52.2 43 21 18 8 Targhee 3 2 66.7 1 1 1 0 Uinta 3 2 66.7 1 1 0 1 Total 168 82 48.8 86 44 26 11 1Includes 1 found positive for E. schneideri for which number of worms was not recorded. (95% CI = 30.3-55.8%), 56% in 5-7 year olds Intensity (95% CI = 44.8-67.3%), and 41% in those ≥8 Of the 82 positive cases, we found 44, 26, years (95% CI = 21.6-64.0%). There were and 11 moose with low, moderate, and high no statistical differences in prevalence of E. E. Schneideri intensity, respectively (Table 1); schneideri among age classes (χ2 = 2.420; intensity was not recorded for 1 positive indi- df = 3; P = 0.490). vidual. The greatest number of worms counted Moose from 10 herds were checked for in any moose was 26. Parasite intensity was E. schneideri (Table 1). To obtain adequate similar between sexes (χ2 = 0.564; df = 2; P = sample size for statistical comparison, the 0.754) and among age classes (χ2 = 4.177; df adjacent Jackson and Targhee herds, and the = 6; P = 0.653). A low-intensity worm burden Lincoln and Uinta herds were combined; the was most common in all age classes, ranging Absaroka, Dubois, and Lander herds were from 40-71%. None of the age classes had a dropped because of low sample sizes and large number of high-intensity worm loads. geographic separation (Table 1). Prevalence High-intensity infections were not observed was different geographically (χ2 = 27.082, df in the 7 infected moose in the oldest age class = 4, P < 0.001). The lowest prevalence oc- (≥8 years). curred in the Bighorn herd (5%; 95% CI = Although prevalence was high in Snowy 0-25.4%) and was lower than that in the other Range moose, most (74%) had low-intensity 4 herds in the analysis. The Snowy Range infections (Fig. 1b). Similarly, most posi- herd had the highest prevalence (82.6%; 95% tive individuals in the Jackson-Targhee herd CI = 62.3-93.6%) which was higher than in (88%) had low-intensity infections. The the Bighorns, Lincoln-Uinta (43.8%; 95% CI only infected moose found in the Bighorns = 23.1-66.8%), and Sublette herds (52.2%; had a moderate-intensity infection (Table 95% CI = 42.0-62.2%), but not different than 1). The pattern of intensity was reversed in in the Jackson-Targhee herds (61.5%; 95% the Lincoln-Uinta and Sublette herds; more CI = 35.4-82.4%). individuals had moderate and high intensities than low intensities. However, patterns of intensity were not different among herd units

39 ELAEOPHORA IN WYOMING MOOSE – HENNINGSEN ET AL. ALCES VOL. 48, 2012

(χ2 = 11.950; df = 8; P = 0.153). ~10% prevalence of E. schneideri in mule deer in a portion of the area comprising the Clinical Signs Jackson, Targhee, and Sublette moose herds When possible, tissues were examined (J. C. Henningsen, unpublished data). It may for gross evidence of damage as a result of be that prevalence of E. schneideri in mule infection by E. schneideri. More thorough deer is too low in Wyoming to generate >90% examinations only occurred after heads had prevalence in moose; however, the Snowy been prepared for taxidermy or when hunters Range had 82.6% prevalence. donated their antlerless specimens. Of the 31 It has long been believed that deer are infected moose that were thoroughly exam- the only competent definitive hosts for E. ined, 10 showed visual signs of elaeophorosis: schneideri (Anderson 2001). However, 7 displayed cropped or hardened ears, 1 had some researchers (Worley et al. 1972, Mad- antler malformation, and 2 had cropped ears den et al. 1991) found gravid adult female and antler malformation. Three of the 10 worms in moose suggesting that they may moose with visual signs had low-intensity be competent hosts. Histopathologic and infections, 4 had moderate-intensity, and 3 laboratory evidence from 3 different cases in high-intensity infections. our study support the idea that moose are a competent host for E. schneideri: 1) several DISCUSSION microfilariae associated with an adult female Prevalence of E. schneideri in Wyoming worm were in a cross-section of formalin-fixed moose was much higher than anticipated. carotid artery, 2) several microfilariae were in Documented infections in moose have been a section of formalin-fixed skin overlying the fairly rare and noteworthy enough that indi- mandibular artery at the jugular notch of the vidual cases have been the norm for report- mandible, and 3) one dead was ing (Worley et al. 1972, Jensen et al. 1982, in an overnight saline soak of fresh forehead Madden et al. 1991, Pessier et al. 1998). The skin. Although not definitive, our evidence prevalence reported here is probably biased suggests that moose are competent hosts for low because only the main cephalic arteries E. schneideri reproduction and transmission. were examined for worms, yet post-mortem If this is the case, prevalence in mule deer and migration of worms occurs (Adcock and Hibler spatial overlap with infected mule deer could 1969). Furthermore, there was potential for be less influential in determiningE. schneideri false negatives because the length of the carotid prevalence in moose. artery was often short and compromised from We can only speculate about the increased hunter processing; there was no corresponding prevalence of E. schneideri in Wyoming moose risk of false positives. over recent decades. Because elaeophorosis Prevalence of E. schneideri in adult mule was perceived to have no effect on Wyoming deer has been 100% in certain local populations ungulate populations, there is inconsistent in the southwestern United States (Hibler and historical data to make inferences. Numerous Adcock 1971). Prevalence has been as high as case reports have expanded our knowledge of 93% in elk (Hibler et al. 1969, Davies 1979); the general distribution of E. schneideri, but high prevalence in elk occurs only in areas recent reports have not attempted to describe where mule deer also have high prevalence the ecology of E. schneideri and explain of infection. Our study focused solely on observed prevalence in wildlife (e.g., Davies moose so we have no analogous surveillance 1979). Prevalence of the disease is presum- data from deer and moose for comparison. ably related to the density of definitive hosts However, opportunistic sampling indicated as well as the abundance of tabanid vectors.

40 ALCES VOL. 48, 2012 HENNINGSEN ET AL. – ELAEOPHORA IN WYOMING MOOSE

Tabanid populations can be highly variable Madden et al. 1991, Pessier et al. 1998). As was among years depending on weather condi- demonstrated in elk (Adcock and Hibler 1969, tions, because temperature and precipitation Hibler and Adcock 1971, Hibler and Metzger influence the timing of fly emergence, seasonal 1974), pathogenic effects of E. schneideri on longevity, and total population size (Pence moose are more complex than a simple linear 1991). Thus gradual climate change has or threshold response by the host to number been attributed with observed and predicted of worms. Complications from infection increases in the effects of vector-borne para- could arise at a number of critical stages in sites (Patz et al. 1996, Hoberg et al. 2008, the life cycle of the parasite. Even slightly Laaksonen and Oksanen 2009). We might compromised basic functions resulting from have either conducted our surveillance when impaired blood flow such as vision, hearing, stochastic weather conditions were temporar- mastication, smell, and brain function could ily conducive for high E. schneideri transmis- expose individuals to malnutrition, predation, sion and/or prevalence, or changing conditions and ultimately lower survival and reproduc- over decades has lead to higher prevalence tion. While the maximum number of worms of E. schneideri. Determining the vectors of found in a hunter-harvested moose in our study E. schneideri in Wyoming and subsequently was 26, preliminary necropsies of symptom- confirming the impacts of temperature and atic moose have sometimes revealed double precipitation on those vectors will require that intensity (J. C. Henningsen, unpublished further research. data). Additionally, while none of the ≥8-yr- For the same reasons prevalence varies old moose had high-intensity infections, this over time, it can exhibit high spatial variability. may have been an artifact of low sample size. We found higher than expected prevalence Limiting surveillance to hunter-harvested among most herds; the Snowy Range and Big- moose possibly eliminates important cases horns stood out as having especially high and from consideration. Comprehensive surveil- low prevalence, respectively. Moose habitat lance that includes sick and dead moose with use and behavior could differ across herds in subsequent histopathologic examinations will ways that affect sympatry with mule deer or be valuable in elucidating impacts of this susceptibility to horse flies (Davies 1979). parasite on individual moose. Domestic livestock grazing adds another Prevalence in our study was consistent layer of complexity. Livestock could either across age classes. We interpret this to mean increase horse fly populations and exacerbate that moose of all ages are equally susceptible the transmission potential among wildlife, to infection and that infection does not affect or dilute the effect because tabanids would survival differently across ages. Constant prey on domestic animals instead of wildlife intensity of E. schneideri across ages of (Davies 1979). Further research is needed checked moose might additionally indicate a to fully understand the spatial dynamics of mechanism limiting worm burdens in moose. elaeophorosis in moose and other species in Perhaps individuals that tolerate initial infec- Wyoming. tion acquire some immunity against further On a more basic level, the effects of infection; Hibler and Metzger (1974) sug- elaeophorosis on individual moose remain gested as much for infected elk. Immune unknown. The high prevalence of apparently protection has been demonstrated in other healthy infected moose suggests elaeophorosis ungulate-nematode systems involving long- is often not debilitating to this host. Yet E. lived adult worms. Parelaphostrongylus schneideri has been implicated in morbidity or tenuis intensities in white-tailed deer are mortality in several cases (Worley et al. 1972, constrained across age classes (Slomke et

41 ELAEOPHORA IN WYOMING MOOSE – HENNINGSEN ET AL. ALCES VOL. 48, 2012 al. 1995) and Prestwood and Nettles (1977) histopathologic and laboratory work. We demonstrated white-tailed deer acquire im- are grateful to C. Hibler, Associate Editor B. munity to additional P. andersoni infections. McLaren, and reviewers E. Addison and M. This hypothesis presumes E. schneideri are Lankester for improving the manuscript. long-lived; however, it is unknown how long E. schneideri can live in moose. Other filarioid REFERENCES nematodes live in their definitive hosts from Ad c o c k , J. L., and C. P. Hi b l e r . 1969. Vas- 2->10 years (review by Gems 2000). cular and neuro-ophthalmic pathology of Alternatively, constant E. schneideri elaeophorosis in elk. Pathologia Veteri- prevalence and intensities with increasing age naria 6: 185-213. of moose might simply reflect new infections An d e r s o n , R. C. 2001. Filarioid nematodes. occurring at a rate that essentially replace those Pages 342-356 in W. M. Samuel, M. J. mature nematodes that die naturally. Under Pybus, and A. A. Kocan, editors. Parasitic this scenario, immune protection would not Diseases of Wild Mammals. Iowa State be perfect and new infections would continue University, Ames, Iowa, USA. through life at some rate that is tolerated by the Bo y c e , W., A. Fi s h e r , H. Pr o v e n c i o , E. host. On the other hand, pathologies arising Ro m i n g e r , J. Th i l s t e d , and M. Ah l m . from dead nematodes in the vascular system 1999. Elaeophorosis in (Adcock and Hibler 1969) would be incon- in New Mexico. Journal of Wildlife sistent with a hypothesis where moose can Diseases 35: 786-789. survive unaffected beyond the lifespan of the Br i m e y e r , D. G., and T. P. Th o m a s . 2004. adult parasite. Thus this hypothesis presumes History of moose management in Wyo- moose can tolerate not only live parasites, but ming and recent trends in Jackson Hole. individuals that die within their vascular sys- Alces 40: 133-143. tem. Regardless of the mechanism, constant Bu s h , A. O., K. D. La f f e r t y , J. M. Lo t z , and intensity and prevalence across age classes A. W. Sh o s t a k . 1987. Parasitology meets indicate infected moose are surviving, hence ecology on its own terms: Margolis et al. mortality caused by E. schneideri is lower revisited. The Journal of Parasitology than previously suggested. 83: 575-583. While moose might not overtly succumb Cl a r k , G. G., and C. P. Hi b l e r . 1973. Horse to elaeophorosis to the extent previously flies and Elaeophora schneideri in the Gila thought, prevalence of 50% is still cause for National Forest, New Mexico. Journal concern. At high prevalence, even a moderate of Wildlife Diseases 9: 21-25. proportion of infected individuals suffering Da v i e s , R. B. 1979. The ecology of Elaeo- from subclinical effects might impact recruit- phora schneideri in Vermejo Park, New ment or productivity at the population level. Mexico. Ph.D. Dissertation, Colorado Subsequent research on moose herds where State University, Fort Collins, Colorado, E. schneideri is present should consider the USA. effects of elaeophorosis and attempt to clarify Es p i n o s a , R. H. 1983. Tabanid vectors of the its role in moose population dynamics. arterial nematode, Elaeophora schneideri, in southwestern Montana. M.S. Thesis, ACKNOWLEDGEMENTS Montana State University, Bozeman, The WGFD Moose Working Group was Montana, USA. integral in designing the survey, and numerous Hi b l e r , C. P. 1982. Elaeophorosis. Pages WGFD field personnel conducted the field 214-218 in E. T. Thorne, N. Kingston, examinations. T. Cornish was integral in the W. R. Jolley, and R. C. Bergstrom, edi-

42 ALCES VOL. 48, 2012 HENNINGSEN ET AL. – ELAEOPHORA IN WYOMING MOOSE

tors. Diseases of Wildlife in Wyoming. and review of the vector-borne nematode Wyoming Game and Fish Department, Setaria tundra in Finnish cervids. Alces Cheyenne, Wyoming, USA. 45: 81-84. _____, and J. L. Ad c o c k . 1971. Elaeophorosis. Ma d d e n , D. J., T. R. Sp r a k e r , and W. J. Ad r i a n . Pages 263-278 in J. W. Davis and R. C. 1991. Elaeophora schneideri in moose Anderson, editors. Parasitic Diseases of (Alces alces) from Colorado. Journal of Wild Mammals. Iowa State University, Wildlife Diseases 27: 340-341. Ames, Iowa, USA. Ma t t h e w s , P. E. 2012. History and status of _____, _____, R. W. Da v i s , and Y. Z. Ab- moose in Oregon. Alces 48: 63-66. d e l b a k i . 1969. Elaeophorosis in deer McKo w n , R. D., M. C. St e r n e r , and D. W. and elk in the Gila Forest, New Mexico. Oa t e s . 2007. First observation of Elaeo- Bulletin of the Wildlife Disease Associa- phora schneideri Wehr and Dikmans, tion 5: 27-30. 1935 (Nematoda: Filariidae) in mule _____, _____, G. H. Ga t e s , and R. Wh i t e . deer from Nebraska. Journal of Wildlife 1970. Experimental infection of domestic Diseases 43: 142-144. sheep and mule deer with Elaeophora sch- Pa t z , J. A., P. R. Ep s t e i n , T. A. Bu r k e , and J. neideri Wehr and Dikmans, 1935. Journal M. Ba l b u s . 1996. Global climate change of Wildlife Diseases 6: 110-111. and emerging infectious diseases. Journal _____, and C. J. Me t z g e r . 1974. Morphol- of the American Medical Association 275: ogy of the larval stages of Elaeophora 217-223. schneideri in the intermediate and de- Pe d e r s o n , J. C., L. A. Je n s e n , and F. L. An d e r - finitive hosts with some observations on s e n . 1985. Prevalence and distribution their pathogenesis in abnormal definitive of Elaeophora schneideri Wehr and Dik- hosts. Journal of Wildlife Diseases 10: mans, 1935 in mule deer in Utah. Journal 361-369. of Wildlife Diseases 21: 66-67. Ho b e r g , E. P., L. Po l l e y , E. J. Je n k i n s , and Pe n c e , D. B. 1991. Elaeophorosis in wild S. J. Ku t z . 2008. Pathogens of domestic ruminants. Bulletin of the Society for and free-ranging ungulates: global climate Vector Ecology 16: 149-160. change in temperate to boreal latitudes _____, and G. G. Gr a y . 1981. Elaeophoro- across North America. Review Scienti- sis in and mule deer from fique et Technique-International Office the Texas Panhandle. Journal of Wildlife of Epizootics 27: 511-528. Diseases 17: 49-56. Ge m s , D. 2000. Longevity and ageing in Pe s s i e r , A. P., V. T. Ha m i l t o n , W. J. Fo r e y t , parasitic and free-living nematodes. S. Pa r i s h , and T. L. McEl w a i n . 1998. Biogerontology 1: 289-307. Probable elaeophorosis in a moose (Alces Ja c q u e s , C. N., J. A. Je n k s , D. T. Ne l s o n , T. alces) from eastern Washington state. J. Zi m m e r m a n , and M. C. St e r n e r . 2004. Journal of Veterinary Diagnostic Inves- Elaeophorosis in free-ranging mule deer tigation 10: 82-84. in South Dakota. Prairie Naturalist 36: Pr e s t w o o d , A. K., and V. F. Ne t t l e s . 1977. 251-54. Repeated low-level infection of white- Je n s e n , L. A., J. C. Pe d e r s o n , and F. L. An- tailed deer with Parelaphostrongylus d e r s e n . 1982. Prevalence of Elaeophora andersoni. Journal of Parasitology 58: schneideri and Onchocerca cervipedis in 897-902. mule deer from central Utah. Great Basin _____, and T. R. Ri d g e w a y . 1972. Elaeophoro- Naturalist 42: 351-352. sis in white-tailed deer of the Southeastern La a k s o n e n , S., and A. Ok s a n e n . 2009. Status USA.: Case report and distribution. Jour-

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nal of Wildlife Diseases 8: 233-236. We i n m a n n , E. J., J. R. An d e r s o n , W. M. Lo n - Ró z s a , L., J. Re i c z i g e l , and G. Ma j o r o s . 2000. g h u r s t , and G. Co n n o l l y . 1973. Filarial Quantifying parasites in samples of hosts. worms of Columbian black-tailed deer in Journal of Parasitology 86: 228-232. California 1. Observations in the verte- Sl o m k e , A. M., M. W. La n k e s t e r , and W. brate host. Journal of Wildlife Diseases J. Pe t e r s o n . 1995. Infrapopulation 9: 213-220. dynamics of Parelaphostrongylus tenuis Wo r l e y , D. E. 1975. Observations on epi- in white-tailed deer. Journal of Wildlife zootiology and distribution of Elaeophora Diseases 31: 125-135. schneideri in Montana ruminants. Journal Th o m a s , T. P. 2008. Moose population man- of Wildlife Diseases 11: 486-488. agement recommendations. Wyoming _____, C. K. An d e r s o n , and K. R. Gr e e r . Game and Fish Department, Cheyenne, 1972. Elaeophorosis in moose from Wyoming, USA. Montana. Journal of Wildlife Diseases Wa i d , D. D., R. J. Wa r r e n , and D. B. Pe n c e . 8: 242-244. 1984. Elaeophora schneideri Wehr and Dikmans, 1935 in white-tailed deer from the Edwards Plateau of Texas. Journal of Wildlife Diseases 20: 342-345.

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