Evaluating apparent competition in limiting the recovery of an endangered ungulate

Predation can disproportionately affect endangered prey populations when generalist predators are numerically linked to more abundant primary prey. Apparent competition, the term for this phenomenon, has been increasingly implicated in the declines of endangered prey populations. We examined the potential for apparent competition to limit the recovery of Sierra Nevada bighorn sheep (Ovis canadensis sierrae), an endangered subspecies under the US Endangered Species Act. Using a combination of location, demographic, and habitat data, we assessed whether cougar (Puma concolor) predation on endangered bighorn sheep was a consequence of their winter range overlap with abundant mule deer (Odocoileus hemionus). Consistent with the apparent competition hypothesis, bighorn sheep populations with higher spatial overlap with deer exhibited higher rates of cougar predation which had additive effects on adult survival. Bighorn sheep killed by cougars were primarily located within deer winter ranges, even though those areas constituted only a portion of the bighorn sheep winter ranges. We suspect that variation in sympatry between bighorn sheep and deer populations was largely driven by differences in habitat selection among bighorn sheep herds. Indeed, bighorn sheep herds that experienced the highest rates of predation and the greatest spatial overlap with deer also exhibited the strongest selection for low elevation habitat. Although predator-mediated apparent competition may limit some populations of bighorn sheep, it is not the primary factor limiting all populations, suggesting that the dynamics of different herds are highly idiosyncratic. Management plans for endangered species should consider the spatial distributions of key competitors and predators to reduce the potential for apparent competition to hijack conservation success.     

Desert bighorn sheep mortality due to presumptive type C botulism in California

During a routine telemetry flight of the Mojave Desert (California, USA) in August 1995, mortality signals were detected from two of 12 radio-collared female desert bighorn sheep (Ovis canadensis) in the vicinity of Old Dad Peak in San Bernardino County (California). A series of field investigations determined that at least 45 bighorn sheep had died near two artificial water catchments (guzzlers), including 13 bighorn sheep which had presumably drowned in a guzzler tank. Samples from water contaminated by decomposing bighorn sheep carcasses and hemolyzed blood from a fresh bighorn sheep carcass were tested for the presence of pesticides, heavy metals, strychnine, blue-green algae, Clostridium botulinum toxin, ethylene glycol, nitrates, nitrites, sodium, and salts. Mouse bioassay and enzyme-linked immunosorbent assay detected type C botulinum toxin in the hemolyzed blood and in fly larvae and pupae. This, coupled with negative results from other analyses, led us to conclude that type C botulinum poisoning was most likely responsible for the mortality of bighorn sheep outside the guzzler tank.     

Desert bighorn sheep habitat selection,group size,and mountain lion predation risk

Bighorn sheep (Ovis canadensis) evolved for thousands of years in the presence of numerous predators, including mountain lions (Puma concolor). Bighorn sheep have presumably developed predator avoidance strategies; however, the effectiveness of these strategies in reducing risk of mountain lion predation is not well understood. These strategies are of increasing interest because mountain lion predation on bighorn sheep has been identified as a leading cause of mortality in some sheep populations. Therefore, we investigated how mountain lions affect both bighorn sheep habitat selection and risk of mortality in Arizona, USA. We used 2 approaches to investigate the predator-prey relationship between mountain lions and bighorn sheep. We fit 103 bighorn sheep (81 females and 22 males) with global positioning system radio-collars in 2 Arizona populations from 2013 to 2017, and used a negative binomial resource selection probability function to evaluate whether bighorn sheep selected for habitat features in accordance with presumed predator avoidance strategies, including terrain ruggedness, slope, topographic position, and horizontal obstruction, in 2 seasons (winter and summer). We then estimated how habitat features such as terrain ruggedness, slope, horizontal obstruction, and group size, influence the risk of mortality due to mountain lion predation using an Andersen-Gill proportional hazards model. Generally, both sexes selected areas with lower horizontal obstruction and intermediate ruggedness and slope, but selection patterns differed between seasons and sexes. The use of more rugged areas and steeper slopes decreased the risk of mortality due to mountain lion predation, consistent with presumed predator avoidance strategies. Increased group size decreased risk of bighorn sheep mortality due to mountain lion predation but this effect became marginal at approximately 10 individuals/group. We did not identify a relationship between horizontal obstruction and bighorn sheep mortality risk. Our findings can be used in habitat and population management decisions such as the prioritization of habitat restoration sites or selection of translocation sites. In addition, we suggest that augmentation of low-density bighorn sheep populations may reduce mountain lion predation risk by increasing group size, and that releasing large groups of bighorn sheep in population augmentation and reintroduction efforts may help to reduce mountain lion predation.     

Hemorrhagic disease in bighorn sheep in Arizona

Two bighorn sheep from Arizona (USA) were submitted for necropsy. One was a Rocky Mountain bighorn (Ovis canadensis canadensis) and the other was a desert bighorn (Ovis canadensis mexicana). Both had lesions consistent with those of hemorrhagic disease (HD). Epizootic hemorrhagic disease virus (EHDV) type-2 and bluetongue virus (BTV) type-17, respectively, were isolated from the sheep tissues. To our knowledge, HD caused by either EHDV or BTV infection has not been documented previously in Arizona bighorn sheep.     

Weaning Conflict in Desert and Mountain Bighorn Sheep (Ovis canadensis): An Ecological Interpretation

Field data on weaning behavior in bighorn sheep (Ovis canadensis) were collected from populations in British Columbia, southern California, and one transplanted from the original B.C. study site to eastern Oregon. These areas were designated mountain, desert, and transplant, respectively. Seasons that were energetically stressful to lactating ewes were predicted. Summers were implicated for desert ewes; winters for ewes in colder and more seasonal northern environments. Although the temporal distribution of milk available to lambs varied between the three study populations, ewes generally weaned their lambs prior to the onset of the predicted stressful periods. In the desert, weaning occurred more abruptly than it did in the two more northern populations. The evolution of weaning strategies is discussed in subspecies of bighorn sheep based on proximate and ultimate factors.     

Using Genetic Tools to Track Desert Bighorn Sheep Colonizations

ABSTRACT Understanding colonization is vital for managing fragmented populations. We employed mitochondrial DNA haplotypes and 14 microsatellite (nuclear DNA) markers to infer the origins of newly established populations of desert bighorn sheep (Ovis canadensis nelsoni) and to assess loss of genetic diversity during natural colonizations. We used haplotype distribution, F-statistics, Bayesian population clustering, and assignment tests to infer source populations for 3 recent colonies and identified a previously undetected colonization from multiple source populations. Allelic richness declined in 3 of 4 colonies in comparison to the primary source populations, but not as much as has been reported for translocated populations. Heterozygosity declined in only one colony. We also demonstrated that both native and translocated desert bighorn sheep have naturally recolonized empty habitats and suggest that colonization may partially offset population extinction in the region as long as connectivity is maintained. Genetic techniques and mitochondrial DNA haplotypes we described will allow managers to determine the origins of future colonizations by bighorn sheep in California, USA, and prioritize protection of linkages between known sources and colonies.     

The rise and fall of psoroptic scabies in bighorn sheep in the San Andres Mountains, New Mexico

Between 1978 and 1997, a combination of psoroptic scabies (Psoroptes spp.), mountain lion (Puma concolor) predation, and periodic drought reduced a population of native desert bighorn sheep (Ovis canadensis) in the San Andres Mountains (SAM), New Mexico, from >200 individuals to a single ewe. In 1999, this ewe was captured, ensured to be Psoroptes-free, and released back into the SAM. Eleven radio-collared rams were translocated from the Red Rock Wildlife Area (RRWA) in New Mexico into the SAM range and monitored through 2002 to determine whether Psoroptes spp. mites were still in the environment. None of these sentinel rams acquired scabies during this period, and no additional native sheep were found to be present in the range. In 2002, 51 desert bighorn sheep were translocated into the SAM from the Kofa National Wildlife Refuge in Arizona (n = 20) and the RRWA in New Mexico (n = 31). Twenty-one bighorn sheep have died in the SAM since that time, but Psoroptes spp. mites have not been detected on any of these animals, nor have they been found on mule deer (Odocoileus hemionus) sampled since 2000. We conclude that psoroptic scabies is no longer present in the San Andres bighorn sheep population and that psoroptic scabies poses a minimal to nonexistent threat to the persistence of this population at this time.     

Biochemical and hematologic reference intervals for free-ranging desert bighorn sheep

Over 200 clinically normal desert bighorn sheep (Ovis canadensis) from multiple geographic areas were sampled utilizing a uniform protocol. The goals of this study were to develop comprehensive reference intervals for hematologic and biochemical analytes using central 90th percentile nonparametric analyses. Adult female sheep had greater erythrocyte mass (hemoglobin and hematocrit) compared with adult male sheep. Young animals < or = 1-yr-old had greater erythrocyte mass (hemoglobin, hematocrit and red blood cell count), higher alkaline phosphatase activity, and lower serum protein and globulin concentrations compared with adult animals. Because of the large sample size, wide geographic range, and uniform sample and handling protocol in this study, these reference intervals should be robust and applicable to other free-ranging desert bighorn sheep populations.     

Ecology of gastropod and bighorn sheep hosts of lungworm on isolated, semiarid mountain ranges in Utah, USA

Isolated, nonmigratory populations of bighorn sheep (Ovis canadensis) may experience high exposure to lungworms (Protostrongylus spp.) through a build-up of fecal material. However, semiarid climates may hinder lungworm transmission by limiting terrestrial gastropods, the intermediate hosts. We assessed potential for lungworm transmission, documented occurrence of transmission, and identified habitat types where transmission was likely to occur on ranges of two recently introduced populations of bighorn sheep in northern Utah. Gastropods were collected weekly on Antelope Island and the Newfoundland Mountains, May-August 2001-02, from each of the four major habitat types (riparian, rock, desert shrub, and grass). Distribution of 113 bighorn sheep groups was observed, and 421 fecal pellet groups were collected to estimate lungworm levels. A total of 1,595 gastropods representing five genera were collected from both ranges. Vallonia made up 85% of all gastropods collected. Of 980 gastropods collected on Antelope Island in 2002, only Vallonia were found infected with protostrongylid-type larvae (10 of 980=1%). Lungworm prevalence in bighorn fecal samples was 97% on Antelope Island and 90% on the Newfoundland Mountains. Lungworm prevalence in lambs indicated lungworm transmission was occurring on Antelope Island. Lungworm transmission was likely occurring in riparian habitat due to abundant gastropods, presence of infected gastropods, and reliance by bighorn sheep on few water sources. Differences in spatial distribution between ram and nursery groups may partly explain higher fecal larvae counts in nursery than in ram groups. We suggest lungworm levels in bighorn sheep on semiarid ranges may increase in dry years as bighorn sheep concentrate use on fewer perennial water sources.     

Comparing contemporary models to traditional indices to estimate abundance of desert bighorn sheep

Aerial surveys for large ungulates produce count data that often underrepresent the number of animals. Errors in count data can lead to erroneous estimates of abundance if they are not addressed. Our objective was to address imperfect detection probability by developing a framework that produces realistic and defensible estimates of bighorn sheep (Ovis canadensis) abundance. We applied our framework to a population of desert bighorn sheep (O. c. nelsoni) in the Great Basin, Nevada, USA. We captured and marked 24 desert bighorn sheep with global positioning system (GPS)-collars and then conducted helicopter surveys naïve to the locations of collared animals. We developed a Bayesian integrated data model to leverage information from telemetry data, helicopter survey counts, and habitat characteristics to estimate abundance while accounting for availability and perception probability (i.e., detection given availability). Distance to ridgeline, terrain ruggedness, tree cover, and slope influenced perception probability of sheep given they were viewable from the helicopter. There was also annual variation in perception probability (2018: median = 0.64, credible interval [CrI] = 0.37–0.87; 2019: median = 0.81, CrI = 0.49–0.97). The abundance estimates from the integrated data model decreased from 2018 (594; 95% CrI = 537–656) to 2019 (487; 95% CrI = 436–551). In addition, accounting for availability and imperfect perception resulted in greater estimates of abundance compared to traditional directed search methods, which were 340 for 2018 and 320 for 2019. Our modeling framework can be used to generate more defensible population estimates of bighorn sheep and other large mammals that have been surveyed in a similar manner.     

Potential Foraging Decisions by a Desert Ungulate to Balance Water and Nutrient Intake in a Water-Stressed Environment

Arid climates have unpredictable precipitation patterns, and wildlife managers often provide supplemental water to help desert ungulates endure the hottest, driest periods. When surface water is unavailable, the only source of water for ungulates comes from the forage they consume, and they must make resourceful foraging decisions to meet their requirements. We compared two desert bighorn sheep (Ovis canadensis nelsoni) populations in Arizona, USA: a treatment population with supplemental water removed during treatment, and a control population. We examined whether sheep altered their seasonal diets without supplemental water. We calculated water and nutrient intake and metabolic water production from dry matter intake and forage moisture and nitrogen content, to determine whether sheep could meet their seasonal daily water and nutrient requirements solely from forage. Diets of sheep were higher in protein (all seasons) and moisture (autumn and winter) during treatment compared to pretreatment. During treatment, sheep diet composition was similar between the treatment and control populations, which suggests, under the climatic conditions of this study, water removal did not influence sheep diets. We estimated that under drought conditions, without any surface water available (although small ephemeral potholes would contain water after rains), female and male sheep would be unable to meet their daily water requirements in all seasons, except winter, when reproductive females had a nitrogen deficit. We determined that sheep could achieve water and nutrient balances in all seasons by shifting their total diet proportions by 8–55% from lower to higher moisture and nitrogen forage species. We elucidate how seasonal forage quality and foraging decisions by desert ungulates allow them to cope with their xeric and uncertain environment, and suggest that, with the forage conditions observed in our study area during this study period, providing supplemental water during water-stressed periods may not be necessary for desert bighorn sheep.     

Genetic variation and population structure in desert bighorn sheep: implications for conservation

Bighorn sheep populations experienced a drastic reduction in both distribution and abundance until the advent of modern wildlife management, where improving viability of extant populations and translocating animals into historical habitat range have been the most important management policies. The fact that subspecies relationships among bighorn are ambiguous,together with the importance of selecting appropriate source stock and the expense of translocation projects, makes an understanding of subspecies relationships and genetic variation, within and between populations, important for the management and conservation of this species. In this study, genetic variation in 279 bighorn sheep from 13 study sites in Arizona, California, New Mexico and Alberta, Canada were examined by analyzing ten microsatellite loci to determine interpopulation differentiation and relationships between closely related taxa. All populations contained a substantial amount of genetic variation. Genetic differences between populations were large and roughly proportional to geographic distance. The significance of this to desert subspecies relationships and management is discussed.     

New ruminant hosts and wider geographic range identified for Babesia odocoilei (Emerson and Wright 1970)

Babesia odocoilei was found to infect two previously unknown host species, desert bighorn sheep (Ovis canadensis nelsoni) and musk oxen (Ovibos moschatus), both of which are members of the family Bovidae. Previously, B. odocoilei has been reported in only Cervidae hosts. New geographic regions where B. odocoilei infections have not been reported previously include Pennsylvania and New York, where fatal babesiosis has occurred in reindeer (Rangifer tarandus tarandus); New Hampshire, where elk (Cervus elaphus canadensis) have been affected; and California, home of the infected desert bighorn sheep. Infection with B. odocoilei in these hosts was confirmed by parasite small subunit ribosomal RNA gene sequence analysis. A serosurvey for B. odocoilei antibody activity in New Hampshire showed prevalence rates of 100% at two elk farms and 12% at another farm. Control of potential vector ticks, Ixodes scapularis, especially when translocating livestock, is imperative to prevent outbreaks of babesiosis in managed herds of potential host species.     

A field laparotomy technique for observing the reproductive tract of free-ranging desert bighorn sheep (Ovis canadensis cremnobates)

A surgical procedure was developed to observe the reproductive tract of free-ranging desert bighorn sheep (Ovis canadensis cremnobates) ewes. Ventral laparotomies were performed on 37 bighorn ewes (ages: lamb — 9 years of age), 24 of which were unilaterally ovariectomized. A second laparotomy was done on 31 ewes. Diazepam (1.5 mg/kg) was injected intramuscularly as a preanesthetic followed by 5 mg etorphine hydrochloride (M99) for restraint and anesthesia. Atropine sulfate (0.03 mg/kg) was used to control hypersalivation and bronchial mucus secretion. Diazepam was evaluated as a preanesthetic on a control group of 42 ewes not submitted to surgery. Pretreatment with diazepam significantly (P < 0.001) reduced the induction time of the anesthetic. All bighorn sheep subjected to surgery recovered without postoperative complications. Ambulation time was similar whether or not diazepam was used as a preanesthetic. Subsequent reproductive performance and mortality rates were similar to those bighorn sheep in the remaining population.     

Habitat use by desert bighorn sheep during lambing

Habitat used for predator escape may be a factor limiting restoration of desert bighorn sheep (Ovis canadensis mexicana) in small mountain ranges in New Mexico. Female bighorn sheep seek isolation in discrete areas for parturition. Although parturition sites are used only for <3 days they play an important role in neonate survival. We compared habitat characteristics at pre-parturition (n = 21), parturition (n = 38), random (n = 38), and post-parturition sites (n = 21). At each site we calculated distance to steep terrain, elevation, ruggedness, slope, and visibility. Parturition and post-parturition sites were higher in elevation and more rugged than sites used during pre-parturition. Post-parturition sites were closer to terrain with 100% slope than the pre-parturition or parturition sites. Post-parturition sites had higher visibility and steeper slopes than the pre-parturition sites. Parturition sites were steeper, higher in elevation, more rugged, and had lower visibility than the random sites. Fidelity to parturition sites was observed on 1 of 38 occasions. Because lambing sites are used for short periods they are poorly understood and often ignored by land managers. Additional research is recommended in other desert bighorn sheep populations to understand better and predict habitat use during the lambing period.     

Infectious keratoconjunctivitis in bighorn sheep, Silver Bell Mountains, Arizona, USA

An infectious keratoconjunctivitis (IKC) epizootic in bighorn sheep (Ovis canadensis) occurred in the Silver Bell Mountains, Arizona, USA, from 1 December 2003 to 31 March 2004. We used standard culture methods and polymerase chain reaction (PCR) amplification of the 16S rRNA gene to test for the causative agents of IKC and other diseases reported to be associated with bighorn sheep populations. All bighorn sheep and domestic goat test results were negative except for Mycoplasma spp. and Branhamella spp. The culture and PCR results differed. Conjunctival swabs from four of 19 IKC-affected bighorn sheep tested by culture were positive for Mycoplasma spp., whereas 22 of 22 bighorn sheep samples tested by PCR were positive for Mycoplasma spp. None of 13 domestic goats tested positive by culture for Mycoplasma spp., whereas five of 16 tested positive by PCR. Three of 16 domestic goats and seven of 24 IKC-affected bighorn sheep tested positive for Branhamella spp. by culture. Bighorn sheep began showing clinical signs of IKC between 21 and 28 days following initial detection of domestic goats in bighorn sheep habitat. The IKC epizootic lasted 122 days, and individual bighorn sheep were blind for an average of 38.4 days. Given the clear potential for disease transmission to bighorn sheep, we recommend that land managers not allow the pasturing of domestic goats near occupied bighorn sheep habitat.     

Further studies on the evolution of land and freshwater nemerteans: generic relationships among the paramonostiliferous taxa

The costs and benefits of fighting in bovids are high in terms of injury and reproductive success, respectively. The breakage of a horn would curtail reproductive success permanently. Therefore, the horns of bovids should include sufficient material so that they are strong enough to be unlikely to break in fighting but without being too heavy to carry around. The forces developed during fighting were measured in a computerized analysis of film of blackbuck and bighorn sheep. All possible modes of failure were investigated using a mechanical analysis to see how the horns are most likely to fail.
The maximum possible force developed during fighting is 3400 N for the bighorn sheep and 456 N for the blackbuck. Bending stress, shear stress, deflection, strain energy and critical crack lengths were calculated for the horns of these two bovids. Horns are most likely to fail in bending as indicated by safety factors. Most of the force is taken in compression due to the curvature of horns. Shear stresses are insignificant and deflections are negligible during the most forceful encounters.
The safety factor in bending of the horn of the bighorn sheep is greater (10) than that of the horn of the blackbuck (3.4) because the forces are probably more variable and unpredictable in the fighting of the former.
All of the energy of fighting is absorbed by the body musculature because horns store less than 1% of the energy produced in fighting as strain energy when they bend. Cracks and scratches mustbe more than 60% of the transverse basal dimensions of horns in order for there to be catastrophic failure at the maximum stresses developed during fighting.
The horns of the blackbuck and the bighorn sheep appear to be minimum weight structures given the variability of the forces acting on them and are unlikely to break in fighting given the forces calculated from the analyses of films.     

A genome-wide set of SNPs detects population substructure and long range linkage disequilibrium in wild sheep

The development of genomic resources for wild species is still in its infancy. However, cross-species utilization of technologies developed for their domestic counterparts has the potential to unlock the genomes of organisms that currently lack genomic resources. Here, we apply the OvineSNP50 BeadChip, developed for domestic sheep, to two related wild ungulate species: the bighorn sheep (Ovis canadensis) and the thinhorn sheep (Ovis dalli). Over 95% of the domestic sheep markers were successfully genotyped in a sample of fifty-two bighorn sheep while over 90% were genotyped in two thinhorn sheep. Pooling the results from both species identified 868 single-nucleotide polymorphisms (SNPs), 570 were detected in bighorn sheep, while 330 SNPs were identified in thinhorn sheep. The total panel of SNPs was able to discriminate between the two species, assign population of origin for bighorn sheep and detect known relationship classes within one population of bighorn sheep. Using an informative subset of these SNPs (n=308), we examined the extent of genome-wide linkage disequilibrium (LD) within one population of bighorn sheep and found that high levels of LD persist over 4 Mb.