Chronic wasting disease prions in mule deer interdigital glands.

Chronic wasting disease (CWD) is a geographically expanding, fatal neurodegenerative disease in cervids. The disease can be transmitted directly (animal-animal) or indirectly via infectious prions shed into the environment. The precise mechanisms of indirect CWD transmission are unclear but known sources of the infectious prions that contaminate the environment include saliva, urine and feces. We have previously identified PrPC expression in deer interdigital glands, sac-like exocrine structures located between the digits of the hooves. In this study, we assayed for CWD prions within the interdigital glands of CWD infected deer to determine if they could serve as a source of prion shedding and potentially contribute to CWD transmission. Immunohistochemical analysis of interdigital glands from a CWD-infected female mule deer identified disease-associated PrPCWD within clusters of infiltrating leukocytes adjacent to sudoriferous and sebaceous glands, and within the acrosyringeal epidermis of a sudoriferous gland tubule. Proteinase K-resistant PrPCWD material was amplified by serial protein misfolding cyclic amplification (sPMCA) from soil retrieved from between the hoof digits of a clinically affected mule deer. Blinded testing of interdigital glands from 11 mule deer by real-time quake-induced conversion (RT-QuIC) accurately identified CWD-infected animals. The data described suggests that interdigital glands may play a role in the dissemination of CWD prions into the environment, warranting future investigation.

Cellular prion protein distribution in the vomeronasal organ, parotid, and scent glands of white-tailed deer and mule deer.

Chronic wasting disease (CWD) is a contagious and fatal transmissible spongiform encephalopathy affecting species of the cervidae family. CWD has an expanding geographic range and complex, poorly understood transmission mechanics. CWD is disproportionately prevalent in wild male mule deer and male white-tailed deer. Sex and species influences on CWD prevalence have been hypothesized to be related to animal behaviours that involve deer facial and body exocrine glands. Understanding CWD transmission potential requires a foundational knowledge of the cellular prion protein (PrPC) in glands associated with cervid behaviours. In this study, we characterized the presence and distribution of PrPC in six integumentary and two non-integumentary tissues of hunter-harvested mule deer (Odocoileus hemionus) and white-tailed deer (O. virginianus). We report that white-tailed deer expressed significantly more PrPC than their mule deer in the parotid, metatarsal, and interdigital glands. Females expressed more PrPC than males in the forehead and preorbital glands. The distribution of PrPC within the integumentary exocrine glands of the face and legs were localized to glandular cells, hair follicles, epidermis, and immune cell infiltrates. All tissues examined expressed sufficient quantities of PrPC to serve as possible sites of prion initial infection, propagation, and shedding.

The effect of terrain and female density on survival of neonatal white-tailed deer and mule deer fawns.

Juvenile survival is a highly variable life-history trait that is critical to population growth. Antipredator tactics, including an animal's use of its physical and social environment, are critical to juvenile survival. Here, we tested the hypothesis that habitat and social characteristics influence coyote (Canis latrans) predation on white-tailed deer (Odocoileus virginianus) and mule deer (O. hemionus) fawns in similar ways during the neonatal period. This would contrast to winter when the habitat and social characteristics that provide the most safety for each species differ. We monitored seven cohorts of white-tailed deer and mule deer fawns at a grassland study site in Alberta, Canada. We used logistic regression and a model selection procedure to determine how habitat characteristics, climatic conditions, and female density influenced fawn survival during the first 8 weeks of life. Fawn survival improved after springs with productive vegetation (high integrated Normalized Difference Vegetation Index values). Fawns that used steeper terrain were more likely to survive. Fawns of both species had improved survival in years with higher densities of mule deer females, but not with higher densities of white-tailed deer females, as predicted if they benefit from protection by mule deer. Our results suggest that topographical variation is a critical resource for neonates of many ungulate species, even species like white-tailed deer that use more gentle terrain when older. Further, our results raise the possibility that neonatal white-tailed fawns may benefit from associating with mule deer females, which may contribute to the expansion of white-tailed deer into areas occupied by mule deer.

Deer mothers are sensitive to infant distress vocalizations of diverse mammalian species.

Acoustic structure, behavioral context, and caregiver responses to infant distress vocalizations (cries) are similar across mammals, including humans. Are these similarities enough for animals to respond to distress vocalizations of taxonomically and ecologically distant species? We show that mule deer (Odocoileus hemionus) and white-tailed deer (Odocoileus virginianus) mothers approach a speaker playing distress vocalizations of infant marmots (Marmota flaviventris), seals (Neophoca cinerea and Arctocephalus tropicalis), domestic cats (Felis catus), bats (Lasionycteris noctivagans), humans (Homo sapiens), and other mammals if the fundamental frequency (F0) falls or is manipulated to fall within the frequency range in which deer respond to young of their own species. They did not approach to predator sounds or to control sounds having the same F0 but a different structure. Our results suggest that acoustic traits of infant distress vocalizations that are essential for a response by caregivers, and a caregiver's sensitivity to these acoustic traits, may be shared across diverse mammals.

Fundamental frequency is key to response of female deer to juvenile distress calls.

Considerable attention is currently devoted to understanding acoustic mechanisms underlying animal responses to heterospecific vocalizations. A further complication ensues when the response of two species is asymmetrical. For example, white-tailed deer females approach a speaker only when it plays distress calls of conspecific fawns. Mule deer females approach when hearing distress calls of either white-tailed deer or mule deer. We hypothesized that selective species such as white-tailed deer respond to traits distinctive of their species and less-discriminating species such as mule deer respond to traits shared across species. Through an acoustic analysis of neonatal distress calls of six ungulate species, we found that mean and maximum fundamental frequency (F0) enabled the greatest statistical discrimination, and the pattern of frequency modulation (FM) was shared across species. Contrary to our initial hypothesis, playback experiments revealed that females of the two species respond similarly to manipulation of F0 and FM. F0 was critical to the response of females from both species, which tolerated the same relative F0 variation (approx. 0.6-1.4× the mean F0 for conspecific fawns). This discovery suggests that mule deer females only appear less discriminating because they are tuned to the higher F0 of mule deer distress calls (964 Hz vs. 546 Hz), resulting in a larger absolute response range that encompasses the F0 produced by white-tailed deer fawns. We propose that animals will have larger absolute response ranges, and therefore appear to be less discriminating, when they belong to a species that produces higher F0 calls.

Cervids with different vocal behavior demonstrate different viscoelastic properties of their vocal folds.

The authors test the hypothesis that vocal fold morphology and biomechanical properties covary with species-specific vocal function. They investigate mule deer (Odocoileus hemionus) vocal folds, building on, and extending data on a related cervid, the Rocky Mountain elk (Cervus elaphus nelsoni). The mule deer, in contrast to the elk, is a species with relatively little vocal activity in adult animals. Mule deer and elk vocal folds show the typical three components of the mammalian vocal fold (epithelium, lamina propria and thyroarytenoid muscle). The vocal fold epithelium and the lamina propria were investigated in two sets of tensile tests. First, creep rupture tests demonstrated that ultimate stress in mule deer lamina propria is of the same magnitude as in elk. Second, cyclic loading tests revealed similar elastic moduli for the vocal fold epithelium in mule deer and elk. The elastic modulus of the lamina propria is also similar between the two species in the low-strain region, but differs at strains larger than 0.3. Sex differences in the stress-strain response, which have been reported for elk and human vocal folds, were not found for mule deer vocal folds. The laminae propriae in mule deer and elk vocal folds are comparatively large. In general, a thick and uniformly stiff lamina propria does not self-oscillate well, even when high subglottic pressure is applied. If the less stiff vocal fold seen in elk is associated with a differentiated lamina propria it would allow the vocal fold to vibrate at high tension and high subglottic pressure. The results of this study support the hypothesis that viscoelastic properties of vocal folds varies with function and vocal behavior.

Prey behavior, age-dependent vulnerability, and predation rates.

Variation in the temporal pattern of vulnerability can provide important insights into predator-prey relationships and the evolution of antipredator behavior. We illustrate these points with a system that has coyotes (Canis latrans) as a predator and two species of congeneric deer (Odocoileus spp.) as prey. The deer employ different antipredator tactics (aggressive defense vs. flight) that result in contrasting patterns of age-dependent vulnerability in their probability of being captured when encountered by coyotes. We use long-term survival data and a simple mathematical model to show that (1) species differences in age-dependent vulnerability are reflected in seasonal predation rates and (2) seasonal variation in prey vulnerability and predator hunt activity, which can be associated with the availability of alternative prey, interact to shape seasonal and annual predation rates for each prey species. Shifting hunt activity from summer to winter, or vice versa, alleviated annual mortality on one species and focused it on the other. Our results indicate that seasonal variation in prey vulnerability and hunt activity interact to influence the impact that a predator has on any particular type of prey. Furthermore, these results indicate that seasonal variation in predation pressure is an important selection pressure shaping prey defenses.

Fight or flight? Antipredator behavior and the escalation of coyote encounters with deer.

It is well known that prey of different size and morphology often use different antipredator strategies. The prevailing notion is that this occurs because size, morphology and weaponry determine the relative effectiveness of alternative strategies, and nowhere is this assumption more entrenched than in our view of the basic decision to stay, fight or flee. Here, we use observations of coyote (Canis latrans) packs hunting deer in winter to show that two ungulates of similar size and morphology, white-tailed deer (Odocoileus virginianus) and mule deer (O. hemionus), use different antipredator strategies when encountered or attacked. Mule deer typically responded by holding their ground and aggressively defending conspecifics, and were at high risk of being attacked and killed if they fled or were undefended. White-tails always fled when pursued or attacked by coyotes. Coyotes pursued fewer white-tails than mule deer they encountered regardless of prey response. Once pursued or attacked, white-tails faced a risk of attack and capture, respectively, that was intermediate between the high and low risk mule deer groups. The overall risk of capture per encounter for white-tails was similar to that facing mule deer that confronted coyotes, which was much lower than risk facing mule deer that fled and were undefended. Contextual variables such as the opportunity to improve one's position by joining another group, moving to rugged terrain, or the presence of companions that are willing to provide defense may explain why a mixed strategy is maintained in mule deer, despite the apparently detrimental effects of flight. These examples illustrate the value of including prey behavior in models of hunting success in so far as prey defenses may not be coupled with differences in size and morphology.