Criticisms Biologically Unwarranted and Analytically Irrelevant: Reply to Rominger et al.

ABSTRACT The criticisms of Rominger et al. (2008) of our retrospective analysis of desert bighorn sheep (DBS; Ovis canadensis mexicana) dynamics in the San Andres Mountains of south-central New Mexico, USA, contained many biological errors and analytical oversights. Herein, we show that Rominger et al. (2008) 1) overstated both magnitude and potential effect of predator removal; 2) incorrectly claimed that our total precipitation (TP) model did not fit the data when TP correctly classed ≥66% of subsequent population increases and declines (P ≥0.063); 3) presented a necessary prerequisite of the exponential model (serial correlation between N_t and N_t+1) as the key relationship in the DBS data, when it merely reflected that DBS are strongly K-selected and was irrelevant to our hypothesis tests specific to factors affecting the instantaneous rate of population increase (r); 4) greatly oversimplified relationships among precipitation, arid environments, and DBS; and 5) advocated a time for collection of lamb/female (L/F) ratio data that was unrelated to any meaningful period in the biological year of DBS and consequently presented L/F ratio data unrelated to observed dynamics of DBS. In contrast, the L/F ratios used in Bender and Weisenberger (2005) correctly predicted annual changes and were correlated with long-term population rates of change.     

Comparison of Endocrine Response to Stress Between Captive-Raised and Wild-Caught Bighorn Sheep

ABSTRACT Stress hormones in Rocky Mountain bighorn sheep (Ovis canadensis canadensis), produced in response to environmental changes, road development, or high population density, may impact their immune systems to a threshold level that predisposes them to periodic, large-scale mortality. We compared the stress response to a novel environmental situation and repeated handling between bighorn sheep born and raised in captivity (CR) and bighorn sheep born in the wild (WC) and brought into captivity. We measured plasma epinephrine, norepinephrine, cortisol, and fecal glucocorticoid metabolites (FGM). Three weeks after each group's arrival we used a one-time drop-net event to elicit an acute stress response, and we collected blood samples from each sheep over 35 minutes, as well as one fecal sample. We collected blood and fecal samples from both groups on 7 other occasions over the subsequent 6 months. We also collected fecal samples from the pen at approximately 24-hour intervals for 3 days following every handling event to monitor the stress response to handling. We found that CR sheep had a stronger autonomic nervous system response than WC sheep, as measured by epinephrine and norepinephrine levels, but we found a very similar hypothalamic-pituitary–adrenal axis (HPA) response, measured by cortisol levels, to the acute stress event of a drop-net restraint. We also found that once the WC sheep had acclimated, as indicated by the return to the initial baseline FGM levels within 12 weeks, the CR and WC groups' HPA responses to sampling events were not significantly different from one another. Fecal samples can provide a noninvasive mechanism for managers to monitor baseline FGM for a given herd. Using long-term monitoring of FGM rather than values from a single point in time may allow managers to correlate these levels to outside influences on the herd and better understand the impacts of management changes, population density, or increased human developments on the health of the sheep population.     

Bighorn Sheep Response to Road-Related Disturbances in Rocky Mountain National Park,Colorado

ABSTRACT Bighorn sheep (Ovis canadensis) use of Sheep Lakes mineral site, Rocky Mountain National Park, Colorado, USA, has decreased since 1996. Officials were concerned that human disturbance may have been contributing to this decline in use. We evaluated effects of vehicular traffic and other road-related disturbance on bighorn use of Sheep Lakes in the summers of 2002 and 2003. We found that the time and number of attempts required by bighorn to reach Sheep Lakes was positively related to the number of vehicles and people present at Sheep Lakes. Further, the number of bighorn individuals and groups attempting to visit Sheep Lakes were negatively affected by disturbance associated with the site. The number of vehicles recorded the hour before bighorn tried to access Sheep Lakes best predicted an animal's failure to cross Fall River Road and reach Sheep Lakes. We conclude that human and road-related disturbance at Sheep Lakes negatively affected bighorn use of the mineral site. Because Sheep Lakes may be important for bighorn sheep, especially for lamb production and survival, the negative influence of disturbance may compromise health and productivity of the Mummy Range bighorn sheep.     

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.     

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.     

Elevation and connectivity define genetic refugia for mountain sheep as climate warms

Global warming is predicted to affect the evolutionary potential of natural populations. We assessed genetic diversity of 25 populations of desert bighorn sheep (Ovis canadensis nelsoni) in southeastern California, where temperatures have increased and precipitation has decreased during the 20th century. Populations in low-elevation habitats had lower genetic diversity, presumably reflecting more fluctuations in population sizes and founder effects. Higher-elevation habitats acted as reservoirs of genetic diversity. However, genetic diversity was also affected by population connectivity, which has been disrupted by human development. Restoring population connectivity may be necessary to buffer the effects of climate change on this desert-adapted ungulate.     

Relative allocation to horn and body growth in bighorn rams varies with resource availability

Males may allocate a greater proportion of metabolic resourcesto maintenance than to the development of secondary sexual characterswhen food is scarce, to avoid compromising their probabilityof survival. We assessed the effects of resource availabilityon body mass and horn growth of bighorn rams (Ovis canadensis)at Ram Mountain, Alberta, Canada over 30 years. The number ofadult ewes in the population tripled during our study, and theaverage mass of yearling females decreased by 13%. We used theaverage mass of yearling females as an index of resource availability.Yearling female mass was negatively correlated with the bodymass of rams of all ages, but it affected horn growth only duringthe first three years of life. Yearly horn growth was affectedby a complex interaction of age, body mass, and resource availability.Among rams aged 2–4 years, the heaviest individuals hadsimilar horn growth at high and at low resource availability,but as ram mass decreased, horn growth for a given body massbecame progressively smaller with decreasing resource availability.For rams aged 5–9 years, horn growth was weakly but positivelycorrelated with body mass, and rams grew slightly more hornfor a given body mass as resource availability decreased. Whenfood is limited, young rams may direct more resources to bodygrowth than to horn growth, possibly trading long-term reproductivesuccess for short-term survival. Although horn growth of olderrams appeared to be greater at low than at high resource availability,we found no correlation between early and late growth in hornlength for the same ram, suggesting that compensatory horn growthdoes not occur in our study population. Young rams with longerhorns were more likely to be shot by sport hunters than thosewith shorter horns. Trophy hunting could select against ramswith fast-growing horns.     

Selfish mothers: reproductive expenditure and resource availability in bighorn ewes

We present a marginal value model explaining intraspecific andinterspecific variation of mating systems in nonterritorialungulates. The model takes into account the simultaneous effectsof spatial and temporal distribution of females, female groupsize, male-male competition, female choice, and the operationalsex ratio (i.e., the proportion of estrous females). The modelpredicts that higher numbers of females per group increasesthe average exploitation time of such groups by males. An increasein female group density, operational sex ratio, and age-specificfighting success of males are predicted to reduce the averageexploitation time of female groups, leading to roving of males(i.e., moving between female groups). In contrast, an increasein die female rejection rate of males and in the time spentby males on nonmating activities (i. e., foraging, lying down,ruminating, migrating) are predicted to increase the averageexploitation time of female groups and to favor staying behaviorof males (i.e., defending a female group over a longer periodof time). Consequently, die model predicts that young maleswill tend to be "stayers," whereas middle-aged and old malesare expected to be "rovers." Model predictions were tested widifield data collected on muskoxen Ovibos moschatus in a naturalpopulation in west Greenland. Observed correlations betweenbull exploitation times of cow groups and the six above-mentionedsocial and environmental parameters were all in die predicteddirection and statistically significant in five of die six cases.Overall, 69% of die observed variation in exploitation timeof cow groups by males was explained by die model predictions.Stepwise regression suggested that, of die six parameters, variationin sex ratio (R² = .56) and time spent on nonmating activities(R² = .35) had the largest effects on male exploitation time.Also, die observed age-specific variation in bull exploitationtime of cow groups was as predicted.     

Disease and secondary sexual traits: effects of pneumonia on horn size of bighorn sheep

Secondary sexual traits (e.g., horns and antlers) have ecological and evolutionary importance and are of management interest for game species. Yet, how these traits respond to emerging threats like infectious disease remains underexplored. Infectious pneumonia threatens bighorn sheep (Ovis canadensis) populations across North America and we hypothesized it may also reduce horn growth in male sheep. We assess the effect of pneumonia on horn size in male bighorn sheep using 12 herd datasets from across the western United States that had horn growth and disease data. Disease resulted in 12–35% reduction in increment (yearly) length and 3–13% reduction in total horn length in exposed individuals. The disease effect was prolonged when pathogens continued to circulate in sheep populations. Further, disease likely delays the age at which horns reach ¾-curl and prevents achievement of full-curl. This is further evidenced with 6 of the 12 herds experiencing an increase in average age at harvest following die-off events.     

Early development, adult mass, and reproductive success in bighorn sheep

Despite considerable empirical and theoretical work on the individualand population consequences of early development, little isknown about the correlations between early mass and adult sizeor lifetime reproductive success of free-ranging mammals. Usinga 26-year study of bighorn sheep (Ovis canadensis), we examinedhow mass as a lamb and mass gain as a yearling affected adultmass for both sexes, horn length of males and lifetime reproductivesuccess of females at different population densities. Mass asa 3-week-old lamb was either weakly or not correlated withadult mass, horn length of adult males, or the number of lambsweaned over a ewe's lifetime. Weaning mass was correlated withmost of these variables when the number of ewes in the populationwas taken into account. When weaning mass was controlled throughpartial correlation, mass as a yearling was correlated with adult mass of ewes but not with ewe reproductive success orwith adult mass or horn length of rams. Lamb mass and numberof ewes explained more of the variance in adult characteristicsfor males than for females. Our results suggest that mass gainduring lactation, possibly but not necessarily related to theamount of maternal care received, affects adult mass and reproductive success. Females appear better able than males to compensatefor poor early development, likely by postponing their firstreproduction. Mass gain over several years and the number ofewes in the population strongly affect adult mass of both sexesand therefore can have profound effects on reproductive successof this long-lived species with a multi-year growth period.