Journal of Wildlife Diseases, 35(4), 1999, pp. 786–789 ᭧ Wildlife Disease Association 1999

Elaeophorosis in Bighorn in New Mexico

Walter Boyce,1,7 Amy Fisher,2 Henry Provencio,3 Eric Rominger,4 John Thilsted,5 and Mike Ahlm61Department of Pathology, Microbiology, and Immunology, University of California, One Shields Ave., Davis, California 95616, USA; 2 New Mexico Department of Game and Fish, P.O. Box 25112, Santa Fe, New Mexico 87504, USA; 3 Henry Provencio, Turner Endangered Species Fund, Armendaris Ranch, HC 32 Box 191, Truth or Consequences, New Mexico 87901, USA; 4 Department of Biology, University of New Mexico, P.O. Box 704, Santa Fe, New Mexico 87504, USA; 5 New Mexico Department of Agriculture, Veterinary Diagnostic Ser- vices, P.O. Box 4700, 700 Camino de Salud NE, Albuquerque, New Mexico 87196-4700, USA; 6 Department of Fishery and Wildlife Science, New Mexico State University, P.O. Box 30003, MSC 4901, Las Cruces, New Mexico 88003-8003, USA; 7 Corresponding author (e-mail: [email protected]).

ABSTRACT: Two (Ovis canaden- tured at Red Rock (New Mexico; sis) in New Mexico (USA) were found to be 32Њ42Ј17ЉN, 108Њ44Ј21ЉW), were translo- naturally infected with Elaeophora schneideri. An adult ram examined in 1997 in the Fra Cris- cated to the Fra Cristobal Mountains tobal Mountains had 26 in the ca- (New Mexico; 33Њ22Ј30ЉN, 107Њ07Ј30ЉW), rotid and iliac arteries, and microfilariae were to reestablish a permanent population in present in the skin, nasal mucosa, brain, and what was presumably historic range. Phys- lungs. This ram was markedly debilitated prior ical examination at the time of capture did to euthanasia and extensive crusty, scabby le- sions were observed on its head. In 1998, a not reveal clinical signs or lesions sugges- yearling ewe found dead adjacent to Watson tive of clinical disease, with the exception Mountain near the Gila Wilderness area was of one that had a healing ulcer on found to have 13 nematodes present in its its lip and another that had an apparent heart. This is the first report of E. schneideri in chronic abscess on its dorsal rump. No bighorn sheep, and we suggest that bighorn sheep are susceptible to E. schneideri infection ticks or mites were found on the integu- wherever they coexist with (Odoco- ment or in the ear canal of any of the an- ileus hemionus hemionus) and appropriate ta- imals. banid vectors. All translocated ewes (n ϭ 24) and rams Key Words: Case report, Elaeophora ϭ schneideri, bighorn sheep, Ovis canadensis, (n 13) were fitted with drop-off radi- mule deer, Tabanidae ocollars, and the rams also had passive in- tegrative transponder (PIT) tags (Destron- The Elaeophora schneideri Fearing, St. Paul, Minnesota, USA) placed normally parasitizes mule deer (Odoco- in their horns. By November 1997, the ileus hemionus hemionus) and black-tailed herd had increased to 43 through deer (O. h. columbianus) in the western the recruitment of lambs, despite the fact United States (Weinmann et al., 1973; that several adults had been killed by Hibler et al., 1974). It has been reported mountain lions (Puma concolor). On 4 No- also from atypical hosts including (Cer- vember 1997 a ram in the Fra Cristobal vus elaphus), (Alces alces), barbary Mountains was observed to be in poor sheep (Ammotragus lervia), domestic condition with skin lesions affecting much sheep (Ovis aries), and (Cervus of its face and head. The animal’s right eye nippon) (Adcock and Hibler, 1969; Worley, was swollen closed and there was a fluid 1975; Robinson et al., 1978; Pence and discharge from that eye and the external Gray, 1981; Madden et al., 1991). This re- nares. Over the next few weeks, new scab- port describes the initial detection of two like lesions appeared at the base of both cases in bighorn sheep (Ovis canadensis) horns and the animal’s condition deterio- in New Mexico (USA) by field biologists, rated. At the same time, three other ani- and the subsequent confirmation of E. mals in the herd with similar skin lesions schneideri infection following necropsy were observed to scratch their heads and and parasitologic examination. ears using their hooves. In October 1995, 37 bighorn sheep cap- The ram was euthanized by gunshot in

786 SHORT COMMUNICATIONS 787 the late afternoon on 2 December 1997 plasma cells into the dermis. There were and transported to the New Mexico De- scattered microfocal areas of necrosis and partment of Agriculture Veterinary Diag- microfilariae present in some of these foci. nostic Services Laboratory (Albuquerque, Microscopic examination of the nasal New Mexico, USA). The next day a com- plaques seen during gross necropsy re- plete necropsy was performed and repre- vealed a dense infiltration of mixed inflam- sentative tissues from all major organs matory cells, microfocal areas of necrosis, were fixed in 10% neutral buffered for- and rare degenerating microfilariae. Ex- malin. A PIT tag recovered from one horn amination of multiple sections of lung re- confirmed that the ram was originally vealed numerous vessel-associated infil- translocated to the Fra Cristobal Moun- trates of inflammatory cells, and degener- tains from Red Rock in 1995 (he had lost ate microfilariae were present in the lu- his drop-off radiocollar). Gross examina- men of scattered pulmonary arterioles and tion revealed multiple, raised, crusty skin capillaries. Multifocal inflammatory cell in- lesions on the forehead region, around the filtrates were found in the meninges, and base of the horns, and on the inner surface thick perivascular cuffs composed primar- of the pinnae of the ears. No mites or ticks ily of plasma cells and lymphocytes were were found in or around these lesions. The found in all major areas of the brain. De- largest lesion was about 5 cm in diameter, generate microfilariae were found in small and the skin in affected areas was about vessels scattered throughout the brain. twice normal thickness. Lesions on the The eyes and associated optic nerves and forehead extended from the horns to the vessels were not examined histologically. external nares, and the general appearance The second case of elaeophorosis was of these lesions was remarkably similar to detected in October 1998 when a yearling that described and photographed in bar- ewe was found dead near Watson Moun- bary sheep affected by elaeophorosis tain in western New Mexico (33Њ05Ј25ЉN (Pence and Gray, 1981). Twenty-four nem- 108Њ31Ј44ЉW). This ewe was a member of atodes, ranging from 4 to 10 cm in length, a small herd of resident bighorn sheep es- were found in the carotid arteries and a tablished in the Turkey Creek area by single nematode was found in each of the translocations from Banff National Park two iliac arteries. These nematodes were (Alberta, Canada) in 1964. The cause of identified as E. schneideri (Hibler and Ad- death could not be determined, but gross cock, 1968), and representative specimens examination of the heart revealed 13 nem- have been deposited in the U.S. National atodes, ranging in length from 4 to 11 cm, Parasite Collection (Beltsville, Maryland, that were subsequently identified as E. USA; USNPC No. 87636). Multiple raised schneideri (USNPC No. 88758). Carotid yellow-white plaques were found in the arteries, skin and other organs were not nasal mucosa covering the turbinates. No available for detailed parasitologic exami- dipterous larvae (e.g., Oestrus ovis) were nation. However, the biologist who found found in the nasal cavity or frontal sinus. the ewe noted that additional nematodes No gross lesions were found in the lungs, (not collected) were protruding from ar- kidneys, spleen, gastrointestinal tract, or teries in the neck when he cut off the brain. ewe’s head. Elaeophora schneideri adults Formalin-fixed tissues were embedded are typically found in the carotid arteries, in paraffin, sectioned at 4 ␮m, stained with and the presence of nematodes in the hematoxylin and eosin, and examined for heart may have resulted from postmortem microscopic lesions. Sections of skin from migration. Based on examination of the the head revealed focal erosion and ulcer- two female worms found in the heart, we ation and a dense infiltration of macro- concluded that this may have been a pre- phages, eosinophils, lymphocytes, and patent infection since undeveloped eggs 788 JOURNAL OF WILDLIFE DISEASES, VOL. 35, NO. 4, OCTOBER 1999 rather than microfilaria were present in and Hibler, 1973). In 1997 and 1998 bi- the uteri. ologists monitoring bighorn sheep in the Mule deer and black-tailed deer are Fra Cristobal Mountains observed mule considered the normal definitive hosts for deer within 200 m of bighorn sheep on E. schneideri in the western United States over 20 occasions, and Ͼ100 deer were and typically do not exhibit clinical signs counted during ground surveys of the of infection (Weinmann et al., 1973; Hib- range. In addition, in 1997 biting flies fre- ler et al., 1974). In contrast, several other quently attacked both humans and bighorn wild and domestic ruminants have been sheep in the spring and summer months. found to be clinically affected including We speculate that the nearby Elephant elk, moose, , domestic Butte Reservoir (Ͻ10 km away on the Rio sheep, and sika deer (Adcock and Hibler, Grande River) may have created appro- 1969; Worley, 1975; Robinson et al., 1978; priate habitat for the production of large Pence and Gray, 1981; Madden et al., numbers of competent vectors, and that 1991). The presence of E. schneideri in the resident mule deer population has the adult ram and yearling ewe examined served as a reservoir of infection for the in this study clearly indicates that bighorn newly established bighorn sheep popula- sheep are susceptible to elaeophorosis. tion. Additionally, conditions also may be However, it is surprising that this is the favorable for E. schneideri transmission to first time E. schneideri has been found in bighorn sheep in other areas such as the bighorn sheep. Bighorn sheep are inten- Red Rock facility where bighorn sheep, sively managed and it seems likely that the mule deer, and tabanid vectors all co-oc- lesions caused by elaeophorosis would cur. have been detected previously if clinical It remains to be demonstrated what ef- infection was present. In fact, in Novem- fect elaeophorosis has on the fitness and ber 1997 (prior to finding E. schneideri in viability of bighorn sheep populations. We any bighorn sheep) we also captured and encourage other investigators to examine examined 47 additional bighorn sheep at bighorn sheep for characteristic lesions Red Rock, and 7 bighorn sheep in the Tur- and the presence of E. schneideri in the key Creek herd. None of these animals heart and arteries. Although E. schneideri were observed to have lesions consistent microfilariae are not likely to be found in with elaeophorosis; however, we did not the blood, we have successfully used the examine skin biopsies for the presence of methods of Weinmann et al. (1973) to iso- microfilariae and thus we could not detect late microfilariae from skin punch biopsies subclinical infections. Although specula- of infected deer. In the absence of a se- tive, it is possible that E. schneideri infec- rologic assay, the collection and analysis of tions have not been detected previously in skin biopsies during routine capture op- bighorn sheep because heavily infected erations may provide the best approach for animals are likely to die. expanding our knowledge of the distribu- The occurrence of E. schneideri in atyp- tion and prevalence of E. schneideri infec- ical hosts such as bighorn sheep is likely tion in bighorn sheep. to be restricted to areas where there are adequate densities of deer definitive hosts LITERATURE CITED and tabanid vectors (Clark and Hibler, ADCOCK, J. L., AND C. P. HIBLER. 1969. Vascular 1973; Worley, 1975). These conditions and neuro-ophthalmic pathology of elaeophoro- clearly exist for the Turkey Creek herd lo- sis in elk. Pathologia Veterinaria 6: 185–213. cated near to the Gila Wilderness area CLARK, G. G., AND C. P. HIBLER. 1973. Horse flies and Elaeophora schneideri in the Gila National where E. schneideri infections in elk, mule Forest, New Mexico. Journal of Wildlife Diseas- deer, and tabanid vectors have been well- es 9: 21–25. documented (Hibler et al., 1968; Clark HIBLER, C. P., AND J. L. ADCOCK. 1968. Redescrip- SHORT COMMUNICATIONS 789

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