Paul M. Lukacs

Review of capture-recapture methods applicable to noninvasive genetic sampling

The use of noninvasive genetic sampling to identify individual animals for capture–recapture studies has become widespread in the past decade. Strong emphasis has been placed on the field protocols and genetic analyses with fruitful results. Little attention has been paid to the capture–recapture application for this specific type of data beyond stating the effects of assumption violations. Here, we review the broad class of capture–recapture methods that are available for use with DNA‐based capture–recapture data, noting the array of biologically interesting parameters such as survival, emigration rates, state transition rates and the finite rate of population change that can be estimated from such data. We highlight recent developments in capture–recapture theory specifically designed for noninvasive genetic sampling data.

Estimating population size from DNA-based closed capture-recapture data incorporating genotyping error

Animal identification based on DNA samples and microsatellite genotypes is widely used for capture-recapture studies (Woods et al. 1999, Boulanger et al. 2003, Eggert et al. 2003). The method shows promise in field protocols (Woods et al. 1999) and potentially minimal error rates in the DNA analysis (Paetkau 2003). Some studies show much higher error rates in individual identification (Creel et al. 2003). There will be some level of uncertainty, although in some situations the uncertainty level is small, in the identification of individuals from microsatellite genotypes. Closed-population capture-recapture analysis has received substantial attention over the past century. More recently, it has been extended to conditional likelihood parameterizations that allow individual covariates to better estimate capture probability (Huggins 1989, 1991) and mixture models to estimate population size in the presence of individual heterogeneity in capture probability (Norris and Pollock 1996, Pledger 2000). The major focus of research has been developing methods to handle varying capture probability. Any methods developed in the future will also have to account for varying capture probability to obtain robust estimates of population size. While DNA-based capture-recapture studies and standard tagging studies share several common characteristics, they differ in others. In a standard tagging study, the researcher attaches a unique tag to the animal and keeps a list of tags that have been used. In a DNA-based study, the genotype of the individual acts as the tag. Therefore, all individuals are tagged prior to the beginning of the study. Unfortunately, the researcher does not know what genotypes exist in the population and must obtain samples from the animals to extract DNA. In a standard tagging study, if a tag is read that does not match one known to be in the population, the researcher knows that the tag was incorrectly read and then either rereads the tag or ignores the observation. In DNA-based studies, the researcher does not have the luxury of immediately knowing which genotypes may be incorrect. Thus, a new form of sampling uncertainty is introduced. For both standard tagging and DNA-based studies, capture probability is <1.0. This necessitates a way to infer what portion of the population is not captured in order to determine the total population size. For a DNAbased study, capture probability is a combination of the probability of encountering a sample (hair, scat, feather, etc.) and the probability that the sample yields a sufficient quantity and quality DNA to amplify and genotype. Current closed-population capture-recapture analysis for estimating population size assumes an animals mark is permanent and read correctly when the animal is captured (Otis et al. 1978). The use of genotype based identification can meet these assumptions in some situations, but the cost may be high. The cost comes in 2 pieces that clearly interact: (1) the monetary cost of analyzing the DNA and (2) the information loss when discarding samples that contain some degree of uncertainty in their identification. For example, the protocol described by Paetkau (2003) places a high emphasis on certainty of the genotype of the sample. In doing so, a large number of samples may have to be culled during the analysis. It may be beneficial to allow a small degree of uncertainty in the identification of a sample, perhaps 1-5%, if such a tradeoff would 1 E-mail: plukacs@cnr.colostate.edu

Lions and Prions and Deer Demise

Background Contagious prion diseases – scrapie of sheep and chronic wasting disease of several species in the deer family – give rise to epidemics that seem capable of compromising host population viability. Despite this prospect, the ecological consequences of prion disease epidemics in natural populations have received little consideration. Methodology/Principal Findings Using a cohort study design, we found that prion infection dramatically lowered survival of free-ranging adult (>2-year-old) mule deer (Odocoileus hemionus): estimated average life expectancy was 5.2 additional years for uninfected deer but only 1.6 additional years for infected deer. Prion infection also increased nearly fourfold the rate of mountain lions (Puma concolor) preying on deer, suggesting that epidemics may alter predator–prey dynamics by facilitating hunting success. Despite selective predation, about one fourth of the adult deer we sampled were infected. High prevalence and low survival of infected deer provided a plausible explanation for the marked decline in this deer population since the 1980s. Conclusion Remarkably high infection rates sustained in the face of intense predation show that even seemingly complete ecosystems may offer little resistance to the spread and persistence of contagious prion diseases. Moreover, the depression of infected populations may lead to local imbalances in food webs and nutrient cycling in ecosystems in which deer are important herbivores.

Camouflage mismatch in seasonal coat color due to decreased snow duration

Most examples of seasonal mismatches in phenology span multiple trophic levels, with timing of animal reproduction, hibernation, or migration becoming detached from peak food supply. The consequences of such mismatches are difficult to link to specific future climate change scenarios because the responses across trophic levels have complex underlying climate drivers often confounded by other stressors. In contrast, seasonal coat color polyphenism creating camouflage against snow is a direct and potentially severe type of seasonal mismatch if crypsis becomes compromised by the animal being white when snow is absent. It is unknown whether plasticity in the initiation or rate of coat color change will be able to reduce mismatch between the seasonal coat color and an increasingly snow-free background. We find that natural populations of snowshoe hares exposed to 3 y of widely varying snowpack have plasticity in the rate of the spring white-to-brown molt, but not in either the initiation dates of color change or the rate of the fall brown-to-white molt. Using an ensemble of locally downscaled climate projections, we also show that annual average duration of snowpack is forecast to decrease by 29–35 d by midcentury and 40–69 d by the end of the century. Without evolution in coat color phenology, the reduced snow duration will increase the number of days that white hares will be mismatched on a snowless background by four- to eightfold by the end of the century. This novel and visually compelling climate change-induced stressor likely applies to >9 widely distributed mammals with seasonal coat color.

Evaluating Dependence Among Mule Deer Siblings in Fetal and Neonatal Survival Analyses

Abstract The assumption of independent sample units is potentially violated in survival analyses where siblings comprise a high proportion of the sample. Violation of the independence assumption causes sample data to be overdispersed relative to a binomial model, which leads to underestimates of sampling variances. A variance inflation factor, c, is therefore required to obtain appropriate estimates of variances. We evaluated overdispersion in fetal and neonatal mule deer (Odocoileus hemionus) datasets where more than half of the sample units were comprised of siblings. We developed a likelihood function for estimating fetal survival when the fates of some fetuses are unknown, and we used several variations of the binomial model to estimate neonatal survival. We compared theoretical variance estimates obtained from these analyses with empirical variance estimates obtained from data-bootstrap analyses to estimate the overdispersion parameter, c. Our estimates of c for fetal survival ranged from 0.678 to 1.118, which indicate little to no evidence of overdispersion. For neonatal survival, 3 different models indicated that ranged from 1.1 to 1.4 and averaged 1.24–1.26, providing evidence of limited overdispersion (i.e., limited sibling dependence). Our results indicate that fates of sibling mule deer fetuses and neonates may often be independent even though they have the same dam. Predation tends to act independently on sibling neonates because of dam–neonate behavioral adaptations. The effect of maternal characteristics on sibling fate dependence is less straightforward and may vary by circumstance. We recommend that future neonatal survival studies incorporate additional sampling intensity to accommodate modest overdispersion (i.e., = 1.25), which would facilitate a corresponding adjustment in a model selection analysis using quasi-likelihood without a reduction in power. Our computational approach could be used to evaluate sample unit dependence in other studies where fates of individually marked siblings are monitored.

EPIDEMIC PASTEURELLOSIS IN A BIGHORN SHEEP POPULATION COINCIDING WITH THE APPEARANCE OF A DOMESTIC SHEEP

A pneumonia epidemic reduced bighorn sheep (Ovis canadensis) survival and recruitment during 1997–2000 in a population comprised of three interconnected wintering herds (Kenosha Mountains, Sugarloaf Mountain, Twin Eagles) that inhabited the Kenosha and Tarryall Mountain ranges in central Colorado, USA. The onset of this epidemic coincided temporally and spatially with the appearance of a single domestic sheep (Ovis aires) on the Sugarloaf Mountain herds winter range in December 1997. Although only bighorns in the Sugarloaf Mountain herd were affected in 1997–98, cases also occurred during 1998–99 in the other two wintering herds, likely after the epidemic spread via established seasonal movements of male bighorns. In all, we located 86 bighorn carcasses during 1997–2000. Three species of Pasteurella were isolated in various combinations from affected lung tissues from 20 bighorn carcasses where tissues were available and suitable for diagnostic evaluation; with one exception, β-hemolytic mannheimia (Pasteurella) haemolytica (primarily reported as biogroup 1G or 1αG) was isolated from lung tissues of cases evaluated during winter 1997–98. The epidemic dramatically lowered adult bighorn monthly survival in all three herds; a model that included an acute epidemic effect, differing between sexes and with vaccination status, that diminished linearly over the next 12 mo best represented field data. In addition to the direct mortality associated with epidemics in these three herds, lamb recruitment in years following the pneumonia epidemic also was depressed as compared to years prior to the epidemic. Based on observations presented here, pasteurellosis epidemics in free-ranging bighorn sheep can arise through incursion of domestic sheep onto native ranges, and thus minimizing contact between domestic and bighorn sheep appears to be a logical principle for bighorn sheep conservation.

Noninvasive Estimation of Black Bear Abundance Incorporating Genotyping Errors and Harvested Bear

Abstract Estimating black bear (Ursus americanus) population size is a difficult but important requirement when justifying harvest quotas and managing populations. Advancements in genetic techniques provide a means to identify individual bears using DNA contained in tissue and hair samples, thereby permitting estimates of population abundance based on established mark–capture–recapture methodology. We expand on previous noninvasive population-estimation work by geographically extending sampling areas (36,848 km2) to include the entire Northern Lower Peninsula (NLP) of Michigan, USA. We selected sampling locations randomly within biologically relevant bear habitat and used barbed wire hair snares to collect hair samples. Unlike previous noninvasive studies, we used tissue samples from harvested bears as an additional sampling occasion to increase recapture probabilities. We developed subsampling protocols to account for both spatial and temporal variance in sample distribution and variation in sample quality using recently published quality control protocols using 5 microsatellite loci. We quantified genotyping errors using samples from harvested bears and estimated abundance using statistical models that accounted for genotyping error. We estimated the population of yearling and adult black bears in the NLP to be 1,882 bears (95% CI = 1,389–2,551 bears). The derived population estimate with a 15% coefficient of variation was used by wildlife managers to examine the sustainability of harvest over a large geographic area.

Effects of Radiomarking on Prairie Falcons: Attachment Failures Provide Insights About Survival

Abstract From 1999–2002, we attached satellite-received platform transmitter terminals (PTTs) to 40 adult female prairie falcons (Falco mexicanus) on their nesting grounds in the Snake River Birds of Prey National Conservation Area (NCA) in southwest Idaho. We used 3 variations of a backpack harness design that had been used previously on raptors. Each radiomarked falcon also received a color leg band with a unique alphanumeric code. We monitored survival of birds using radiotelemetry and searched for marked birds on their nesting grounds during breeding seasons after marking. Because 6 falcons removed their harnesses during the first year, we were able to compare survival rates of birds that shed PTTs with those that retained them. We describe a harness design that failed prematurely as well as designs that proved successful for long-term PTT attachment. We resighted 21 marked individuals on nesting areas 1–5 years after they were radiomarked and documented 13 mortalities of satellite-tracked falcons. We used a Cormack-Jolly-Seber model to estimate apparent survival probability based on band resighting and telemetry data. Platform transmitter terminals had no short-term effects on falcons or their nesting success during the nesting season they were marked, but birds that shed their transmitters increased their probability of survival. Estimated annual survival for birds that shed their transmitters was 87% compared to 49% for birds wearing transmitters. We discuss possible reasons for differences in apparent survival rates and offer recommendations for future marking of falcons.

Relative influence of human harvest, carnivores, and weather on adult female elk survival across western North America

Summary 1. Well-informed management of harvested species requires understanding how changing ecological conditions affect demography and population dynamics, information that is lacking for many species. We have limited understanding of the relative influence of carnivores, harvest, weather and forage availability on elk Cervus elaphus demography, despite the ecological and economic importance of this species. We assessed adult female survival, a key vital rate for population dynamics, from 2746 radio-collared elk in 45 populations across western North America that experience wide variation in carnivore assemblage, harvest, weather and habitat conditions. 2. Proportional hazard analysis revealed that ‘baseline’ (i.e. not related to human factors) mortality was higher with very high winter precipitation, particularly in populations sympatric with wolves Canis lupus. Mortality may increase via nutritional stress and heightened vulnerability to predation in snowy winters. Baseline mortality was unrelated to puma Puma concolor presence, forest cover or summer forage productivity. 3. Cause-specific mortality analyses showed that wolves and all carnivore species combined had additive effects on baseline elk mortality, but only reduced survival by <2%. When human factors were included, ‘total’ adult mortality was solely related to harvest; the influence of native carnivores was compensatory. Annual total mortality rates were lowest in populations sympatric with both pumas and wolves because managers reduced female harvest in areas with abundant or diverse carnivores.

Snowshoe hares display limited phenotypic plasticity to mismatch in seasonal camouflage

As duration of snow cover decreases owing to climate change, species undergoing seasonal colour moults can become colour mismatched with their background. The immediate adaptive solution to this mismatch is phenotypic plasticity, either in phenology of seasonal colour moults or in behaviours that reduce mismatch or its consequences. We observed nearly 200 snowshoe hares across a wide range of snow conditions and two study sites in Montana, USA, and found minimal plasticity in response to mismatch between coat colour and background. We found that moult phenology varied between study sites, likely due to differences in photoperiod and climate, but was largely fixed within study sites with only minimal plasticity to snow conditions during the spring white-to-brown moult. We also found no evidence that hares modify their behaviour in response to colour mismatch. Hiding and fleeing behaviours and resting spot preference of hares were more affected by variables related to season, site and concealment by vegetation, than by colour mismatch. We conclude that plasticity in moult phenology and behaviours in snowshoe hares is insufficient for adaptation to camouflage mismatch, suggesting that any future adaptation to climate change will require natural selection on moult phenology or behaviour.