A spatially explicit hierarchical model to characterize population viability.

Many of the processes that govern the viability of animal populations vary spatially, yet population viability analyses (PVAs) that account explicitly for spatial variation are rare. We develop a PVA model that incorporates autocorrelation into the analysis of local demographic information to produce spatially explicit estimates of demography and viability at relatively fine spatial scales across a large spatial extent. We use a hierarchical, spatial, autoregressive model for capture-recapture data from multiple locations to obtain spatially explicit estimates of adult survival (ϕad ), juvenile survival (ϕjuv ), and juvenile-to-adult transition rates (ψ), and a spatial autoregressive model for recruitment data from multiple locations to obtain spatially explicit estimates of recruitment (R). We combine local estimates of demographic rates in stage-structured population models to estimate the rate of population change (λ), then use estimates of λ (and its uncertainty) to forecast changes in local abundance and produce spatially explicit estimates of viability (probability of extirpation, Pex ). We apply the model to demographic data for the Sonoran desert tortoise (Gopherus morafkai) collected across its geographic range in Arizona. There was modest spatial variation in λ^ (0.94-1.03), which reflected spatial variation in ϕ^ad (0.85-0.95), ϕ^juv (0.70-0.89), and ψ^ (0.07-0.13). Recruitment data were too sparse for spatially explicit estimates; therefore, we used a range-wide estimate ( R^  = 0.32 1-yr-old females per female per year). Spatial patterns in demographic rates were complex, but ϕ^ad , ϕ^juv , and λ^ tended to be lower and ψ^ higher in the northwestern portion of the range. Spatial patterns in Pex varied with local abundance. For local abundances >500, Pex was near zero (<0.05) across most of the range after 100 yr; as abundances decreased, however, Pex approached one in the northwestern portion of the range and remained low elsewhere. When local abundances were <50, western and southern populations were vulnerable (Pex  > 0.25). This approach to PVA offers the potential to reveal spatial patterns in demography and viability that can inform conservation and management at multiple spatial scales, provide insight into scale-related investigations in population ecology, and improve basic ecological knowledge of landscape-level phenomena.

Spatial and temporal variation in survival of a rare reptile: a 22-year study of Sonoran desert tortoises.

Although many species may be vulnerable to changes in climate, forecasting species-level responses can be challenging given the array of physiological, behavioral, and demographic attributes that might be affected. One strategy to improve forecasts is to evaluate how species responded to climatic variation in the past. We used 22 years of capture-recapture data for Sonoran desert tortoises (Gopherus morafkai) collected from 15 locations across their geographic range in Arizona to evaluate how environmental factors affected spatial and temporal variation in survival. Although rates of annual survival were generally high ([Formula: see text] = 0.92), survival of adults decreased with drought severity, especially in portions of their range that were most arid and nearest to cities. In three locations where large numbers of carcasses from marked tortoises were recovered, survival of adults was markedly lower during periods of severe drought ([Formula: see text] = 0.77-0.81) compared to all other periods ([Formula: see text] = 0.93-0.98). Assuming continued levels of dependency of humans on fossil fuels, survival of adult tortoises is predicted to decrease by an average of 3 % during 2035-2060 relative to survival during 1987-2008 in 14 of the 15 populations we studied. This decrease could reduce persistence of tortoise populations, especially in arid portions of their range. Temporal and spatial variation in drought conditions are important determinants of survival in adult desert tortoises.

A strategy for prioritizing threats and recovery actions for at-risk species.

Ensuring the persistence of at-risk species depends on implementing conservation actions that ameliorate threats. We developed and implemented a method to quantify the relative importance of threats and to prioritize recovery actions based on their potential to affect risk to Mojave desert tortoises (Gopherus agassizii). We used assessments of threat importance and elasticities of demographic rates from population matrix models to estimate the relative contributions of threats to overall increase in risk to the population. We found that urbanization, human access, military operations, disease, and illegal use of off highway vehicles are the most serious threats to the desert tortoise range-wide. These results suggest that, overall, recovery actions that decrease habitat loss, predation, and crushing will be most effective for recovery; specifically, we found that habitat restoration, topic-specific environmental education, and land acquisition are most likely to result in the greatest decrease in risk to the desert tortoise across its range. In addition, we have developed an application that manages the conceptual model and all supporting information and calculates threat severity and potential effectiveness of recovery actions. Our analytical approach provides an objective process for quantifying threats, prioritizing recovery actions, and developing monitoring metrics for those actions for adaptive management of any at-risk species.

Response to Comment on "Individual heterozygosity predicts translocation success in threatened desert tortoises".

Hansson et al argue that our main finding could provide an overly simplistic metric for maximizing genetic rescue. They agree that translocating the most genetically diverse individuals led to a large increase in translocated tortoise survival, but recommend instead moving individuals that have low genetic load and the greatest representation of metapopulation diversity. Their recommendation is based on specific model assumptions and fitness effects that are often unknown and are not generalizable to many endangered species applications.

Response to Comment on "Individual heterozygosity predicts translocation success in threatened desert tortoises".

Hedrick brings up several potential concerns that he feels challenge or limit our main finding. Hedrick does not comment on our empirical results, but rather argues that several factors may confound or invalidate our conclusion. Many of these concerns focus on unknown ecological aspects of the translocated tortoises, but we believe there is no reason to conclude that they bias the results or interpretation as presented in our original paper.

ASSESSMENT OF DISEASE RISK ASSOCIATED WITH POTENTIAL REMOVAL OF ANTHROPOGENIC BARRIERS TO MOJAVE DESERT TORTOISE (GOPHERUS AGASSIZII) POPULATION CONNECTIVITY.

The Mojave Desert tortoise (Gopherus agassizii), federally listed as threatened, has suffered habitat loss and fragmentation due to human activities. Upper respiratory tract disease (URTD), a documented health threat to desert tortoises, has been detected at the Large-Scale Translocation Study Site (LSTS) in southwestern Nevada, US, a fenced recipient site for translocated animals. Our study aimed to 1) estimate prevalence of URTD and Mycoplasma infection at LSTS and three nearby unfenced sites; 2) assess whether Mycoplasma infection status was associated with developing clinical signs of URTD; and 3) determine whether such an association differed between LSTS and unfenced areas. We sampled 421 tortoises in 2016 to describe the current status of these populations. We evaluated three clinical signs of URTD (nasal discharge, ocular discharge, nasal erosions) and determined individual infection status for Mycoplasma agassizii and Mycoplasma testudineum by quantitative PCR and enzyme-linked immunosorbent assay. In 2016, LSTS had the highest prevalence of M. agassizii (25.0%; 33/132), M. testudineum (3.0%; 4/132), and URTD clinical signs (18.9%; 25/132). Controlling for other factors, clinical sign(s) were positively associated with M. agassizii infection (odds ratio [OR]=7.7, P=0.001), and this effect was similar among study sites (P>0.99). There was no association with M. testudineum status (P=0.360). Of the 196 tortoises in a longitudinal comparison of 2011-14 with 2016, an estimated 3.2% converted from M. agassizii-negative to positive during the study period, and incidence was greater at LSTS (P=0.002). Conversion to positive M. agassizii status was associated with increased incidence of clinical signs in subsequent years (OR=11.1, P=0.018). While M. agassizii and URTD are present outside the LSTS, there is a possibility that incidence of Mycoplasma infection and URTD would increase outside LSTS if these populations were to reconnect. Population-level significance of this risk appears low, and any risk must be evaluated against the potential long-term benefits to population viability through increased connectivity.

Individual heterozygosity predicts translocation success in threatened desert tortoises.

Anthropogenic environmental modification is placing as many as 1 million species at risk of extinction. One management action for reducing extinction risk is translocation of individuals to locations from which they have disappeared or to new locations where biologists hypothesize they have a good chance of surviving. To maximize this survival probability, the standard practice is to move animals from the closest possible populations that contain presumably related individuals. In an empirical test of this conventional wisdom, we analyzed a genomic dataset for 166 translocated desert tortoises (Gopherus agassizii) that either survived or died over a period of two decades. We used genomic data to infer the geographic origin of translocated tortoises and found that individual heterozygosity predicted tortoise survival, whereas translocation distance or geographic unit of origin did not. Our results suggest a relatively simple indicator of the likelihood of a translocated individual's survival: heterozygosity.

Using incidental mark-encounter data to improve survival estimation.

Obtaining robust survival estimates is critical, but sample size limitations often result in imprecise estimates or the failure to obtain estimates for population subgroups. Concurrently, data are often recorded on incidental reencounters of marked individuals, but these incidental data are often unused in survival analyses.We evaluated the utility of supplementing a traditional survival dataset with incidental data on marked individuals that were collected ad hoc. We used a continuous time-to-event exponential survival model to leverage the matching information contained in both datasets and assessed differences in survival among adult and juvenile and resident and translocated Mojave desert tortoises (Gopherus agassizii).Incorporation of the incidental mark-encounter data improved precision of all annual survival point estimates, with a 3.4%-37.5% reduction in the spread of the 95% Bayesian credible intervals. We were able to estimate annual survival for three subgroup combinations that were previously inestimable. Point estimates between the radiotelemetry and combined datasets were within |0.029| percentage points of each other, suggesting minimal to no bias induced by the incidental data.Annual survival rates were high (>0.89) for resident adult and juvenile tortoises in both study sites and for translocated adults in the southern site. Annual survival rates for translocated juveniles at both sites and translocated adults in the northern site were between 0.73 and 0.76. At both sites, translocated adults and juveniles had significantly lower survival than resident adults. High mortality in the northern site was driven primarily by a single pulse in mortalities.Using exponential survival models to leverage matching information across traditional survival studies and incidental data on marked individuals may serve as a useful tool to improve the precision and estimability of survival rates. This can improve the efficacy of understanding basic population ecology and population monitoring for imperiled species.

The evolution of different maternal investment strategies in two closely related desert vertebrates.

We compared egg size phenotypes and tested several predictions from the optimal egg size (OES) and bet-hedging theories in two North American desert-dwelling sister tortoise taxa, Gopherus agassizii and G. morafkai, that inhabit different climate spaces: relatively unpredictable and more predictable climate spaces, respectively. Observed patterns in both species differed from the predictions of OES in several ways. Mean egg size increased with maternal body size in both species. Mean egg size was inversely related to clutch order in G. agassizii, a strategy more consistent with the within-generation hypothesis arising out of bet-hedging theory or a constraint in egg investment due to resource availability, and contrary to theories of density dependence, which posit that increasing hatchling competition from later season clutches should drive selection for larger eggs. We provide empirical evidence that one species, G. agassizii, employs a bet-hedging strategy that is a combination of two different bet-hedging hypotheses. Additionally, we found some evidence for G. morafkai employing a conservative bet-hedging strategy. (e.g., lack of intra- and interclutch variation in egg size relative to body size). Our novel adaptive hypothesis suggests the possibility that natural selection favors smaller offspring in late-season clutches because they experience a more benign environment or less energetically challenging environmental conditions (i.e., winter) than early clutch progeny, that emerge under harsher and more energetically challenging environmental conditions (i.e., summer). We also discuss alternative hypotheses of sexually antagonistic selection, which arise from the trade-offs of son versus daughter production that might have different optima depending on clutch order and variation in temperature-dependent sex determination (TSD) among clutches. Resolution of these hypotheses will require long-term data on fitness of sons versus daughters as a function of incubation environment, data as yet unavailable for any species with TSD.