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1 California Animal Health and Food Safety, San Bernardino Branch, School of Veterinary Medicine, University of California, Davis, California 92408, USA
2 Veterinary Medical Teaching Hospital, School of Veterinary Medicine. University of California, Davis, California 95616, USA
3 National Park Service, Santa Monica Mountains National Recreation Area, Thousand Oaks, California 91360, USA
4 California Animal Health and Food Safety Laboratory, Davis Branch, School of Veterinary Medicine, University of California, Davis, California 95616, USA
5 Wildlife Health Center, School of Veterinary Medicine, University of California, Davis, California 95616, USA
6 Corresponding author (email: fuzal{at}cahfs.ucdavis.edu)
ABSTRACT:
Two mountain lions (Puma con-color) were found dead in the Simi Hills area of southern California (Ventura County). Postmortem examination and toxicological analyses indicated that the cause of death was anticoagulant rodenticide intoxication. In addition, both lions had marked alopecia and skin crusts, caused by Notoedres cati. The diagnosis of notoedric mange was confirmed by histology and direct examination of mites obtained from skin scrapings of the two animals. Histologically, the affected skin showed acanthotic epidermis with parakeratosis and parasitic tunnels in the stratum corneum. This is the first report of the pathological changes associated with notoedric mange in free-ranging mountain lions.
Key words: Anticoagulant, mange, mountain lion, Notoedres cati.
Notoedric mange is a cutaneous disease of mammals caused by the mite Notoedres cati (Astigmata: Sarcoptidae). The condition has been described in felids (Young et al., 1972; Fletcher, 1978; Pence et al., 1982; Foley, 1991; Maehr et al., 1995; Pence et al., 1995; Scott et al., 2001), white-nosed coatis (Nasua narica) (Valenzuela et al., 2000), ring-tail cats (Bassariscus astutus; Klompen, 1992), masked palm civets (Paguma larvata; Hamir et al., 1993), and raccoons (Procyon lotor; Ninomiya and Ogata, 2002). Among felids, N. cati parasitism has been described in a 10-day-old Florida panther (Puma concolor coryi), an endangered subspecies of mountain lion (Puma concolor), which was recently incorporated into a captive breeding colony (Maehr et al., 1995). However, to the best of our knowledge, the pathological changes of this mite infestation have not been described in mountain lions. This report describes two cases of notoedric mange in free-ranging mountain lions in southern California.
Two radiocollared adult mountain lions (a male and a nonpregnant female) were found dead in the Simi Hills area of southern California (Ventura County). The Universal Transverse Mecator coordinates where the carcasses were found were X: 334,422 Y: 3784,646 (male) and X: 344,132 Y: 3791,074 (female). This area consists mostly of chaparral intermixed with occasional exotic grasslands, oak woodlands, and riparian woodlands. The date and time of death was unknown. The carcass of the male lion was frozen and maintained in that state until it was transported to the California Animal Health and Food Safety Laboratory in San Bernardino, California, and necropsied. A field necropsy was performed on the female lion and the whole head, hide, and a sample of liver from this animal were also frozen, and then submitted to the laboratory.
At the laboratory, the frozen carcass of the male lion and the specimens from the female lion were thawed at 4 C over a 48 hr period. A full necropsy was performed on the male lion, and the hide, head, and liver of the female animal were examined. Samples of liver, heart, lung, small and large intestine, kidney, and skeletal muscle from the male lion, and samples of brain and skin from both lions, were fixed in neutral buffered formalin overnight, embedded in paraffin wax, sectioned at 5 µm, and stained with hematoxylin and eosin (HE). Skin scrapings from both lions were obtained from the periphery of gross skin lesions of the head (see below), treated with 10% KOH, and prepared as whole mounts in lactophenol and Hoyer’s mounting media. One-half brain from each lion was collected and stored frozen until analyzed for cholinesterase activity using the Ellman procedure adapted to a 96-well microliter plate reader (Tor et al., 1994). The liver also was collected from each lion and stored frozen until processed for anticoagulant rodenticide screening by HPLC using both fluorescence and photodiode array detection. Brodifacoum, bromodiolone, chlorophacinone, coumachlor, difethialone, diphacinone, and warfarin were included in the screen.
Both carcasses were in a moderate state of post-mortem decomposition. The two animals had extensive multifocal to coalescing dermatitis involving the head (mostly face and ears), shoulders, and ventral aspects of forepaws (Fig. 1
). The affected skin was multifocally alopecic, had numerous nodules and was lichenified (Fig. 1). Large quantities of unclotted blood were present in the pleural, pericardial, and peritoneal cavities of both lions. In addition, the male lion had multiple subserosal hemorrhages (petechiae and ecchymoses) in thoracic and abdominal organs. Because of the extensive hemorrhages seen in both animals, an intensive search for traumatic injuries was performed, which included complete skinning of the carcasses, paramedial sectioning of the skull of both animals, and examination of most joints and spinal column of the male lion. However, no evidence of trauma was found in either of the two carcasses.
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). The epidermis was multifocally covered by thick, sometimes spongiform crusts composed of degenerate keratinocytes, blood, fibrin, neutrophils, lymphocytes, plasma cells, macrophages, and cellular debris with intralesional colonies of coccoid bacteria and nests of mites. The mites measured 110 µm by 33 µm and were ovoid, with spiny cuticles, striated skeletal muscle, and a hemocoelom. Parasitic tunnels were present within the stratum corneum (less commonly, within the stratum spinosum), often forming a crescent-shaped notch within which one to three mites could be found (Fig. 3). These epidermal tunnels occasionally extended to hair follicles, contained keratinocytes and cellular debris, and had parakeratosis and compression of the stratum basale. Occasionally, severely affected hair follicles had disrupted architecture, lost their hair shaft, and contained only cellular debris. Mild to moderate, multifocal, lymphoplasmacytic, occasionally neutrophilic perivascular infiltrates were present within the superficial dermis. The deep dermis was variably expanded by multifocally degenerate collagen (dermal scarring). In the ears, lesions were generally more severe on the outer pinna vs. the inner pinna.
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, 5, and 6) on all specimens observed, and mid-dorsal blunt dorsal spines were present (Fig. 6). Females lacked a mid-dorsal shield. The mites were thus identified as Notoedres cati (vs. Sarcoptes spp.) on the basis of these morphologic features (Flynn, 1973; McDaniel, 1979). Representative specimens have been deposited at the United States National Parasite Museum Collection with accession number 210A-17/18; 1181.
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Mountain lions are found throughout California, including many areas of southern California where large expanses of natural habitat remain. As human population size and development increase in southern California, mountain lions increasingly are living in proximity to people and their pets. Notoedres mites parasitize several mammalian species and, although the life cycle of this parasite is poorly understood, it has been established that the closely related Sarcoptes scabiei can live for as much as 3 wk off the host (Arlian et al., 1989). Sarcoptid mites are transmitted primarily by direct contact between animals or by contact with infested bedding or sites recently visited by infested animals.
Information about prevalence of notoedric mange in mountain lions in southern California is not available, but if the mites maintain a population in free-ranging mountain lions in the region, it is possible that the infestation is transmitted by direct contact between lions. Mountain lions eat a wide variety of mostly mammalian prey, including potential Notoedres hosts such as raccoons and ground squirrels (Spermophilus spp.), but in southern California, they generally prey on ungulates, especially mule deer (Odocoileus hemionus; Beier and Barrett 1993). Mountain lions in southern California occasionally kill and/ or eat domestic cats (unpubl. data), and infected cats can serve as a source of infection because notoedric mange is highly prevalent in domestic cats of southern California (Brooks, 2005). It is also possible that infected bobcats (Felis rufus) transmitted mites to these two lions because notoedric mange has been frequently diagnosed in bobcats in the area where these two mountain lions originated (National Park Service, unpubl. data). Wildlife managers need to be aware that notoedric mange could affect free-ranging mountain lions, particularly in southern California.
Notoedres cati excavates tunnels in the skin; this seem to vary between host species. In raccoons, tunnels are relatively shallow and are located between hair follicles (Webb, 1980), whereas tunnels in masked palm civets are located close to hair shafts and excavated along the hair follicles where the mites inhabit deep in the hair root, similarly to Demodex spp. mites (Hamir et al., 1993). In the mountain lions presented here, the tunnels were generally shallow and located between hair follicles, although rarely a few follicles were affected. In this regard, the lesions were similar to the shallow tunnels produced by S. scabei in different animal species (Ninomiya and Ogata, 2002; Webb, 1980)
The detection of multiple anticoagulant rodenticides in the liver from both mountain lions, along with the gross necropsy findings of large amounts of free, un-clotted blood in the pleural, pericardial and peritoneal cavities is indicative of anticoagulant rodenticide intoxication. Unfortunately, it was not possible to determine the source of exposure to the rodenticides in this case. It is possible that the lions ingested rodent baits directly, or that they were exposed indirectly via intoxicated prey. To the authors’ knowledge there are no currently available commercial products that contain more than one anticoagulant, which suggests that these animals had access to different baits, or to prey exposed to different rodenticides. Mountain lions are both predators and scavengers (Bauer et al., 2005), so they could have been intoxicated by eating live or dead prey. However, it seems unlikely that they would ingest baits intended for rodent control.
Sarcoptic mange has been documented as a cause of epizootic mortality in other wildlife, especially coyotes (Canis latrans; Pence et al., 1983), so further investigation is warranted to determine the extent and impact of N. cati infection in free-ranging mountain lions. We are not aware of any causal relationship between the occurrence of notoedric mange and anticoagulant exposure. However, a high prevalence of notoedric mange was detected concurrently with anticoagulant rodenticide exposure in a series of bobcats examined in the same general area (National Park Service, un-publ. data). Thus the relationship, if any, between mange and anticoagulant exposure warrants further investigation.
We thank S. Kwiek and E. J. Hurley for excellent technical assistance and S. Fitisemanu and C. Garcia for their patient secretarial work.
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Received for publication 1 April 2006.
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