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Kevin T. Shoemaker

Publications and source records attributed to Kevin T. Shoemaker.

11 recordsLinked to original sources

Common-garden experiment reveals outbreeding depression and region-of-origin effects on reproductive success in a frequently translocated tortoise

Human-mediated animal movement can expose wildlife populations to novel environments. Phenotypic plasticity can buffer against the challenges presented by novel environments, while adaptation to local ecosystems may limit resilience in novel ecosystems. Outbreeding depression during the mixing of disparate gene pools can also reduce reproductive success after long-distance movement. Here, we use a ‘common-garden’ population of gopher tortoises ( Gopherus polyphemus ), translocated from numerous sites across the state of Florida, USA, to a mitigation site in the north-west (panhandle) region to assess whether geographic origin, outbreeding effects, and behavioral plasticity influence reproductive success in this threatened keystone species. We found that females from north-east Florida produced clutches with lower hatching success than females from other regions. We detected regional differentiation in nest site selection behavior in the common environment of the translocation site, though these differences did not mediate the regional effect on hatching success. We also found evidence for outbreeding depression: hatching success declined with increasing parental geographic and genetic distances, dropping from 93% to 67% across the range of observed parental genetic distances. Together, these results suggest that newly admixed populations may suffer reproductive costs due to historical population differentiation, and that undetected outbreeding depression could significantly hamper conservation efforts for this species and others undergoing a variety of human-mediated movements.

Florida

Asymmetric mate preference and reproductive interference mediate climate-induced changes in mate availability in a small mammal hybrid zone

Range expansion and contraction are among the most common biotic responses to changing environmental conditions, yet much is to be learned about the mechanisms that underlie range-edge population dynamics, especially when those areas are points of secondary contact between closely related species. Here, we present field-measured parentage data that document the reproductive outcomes of changes in mate availability at a secondary contact zone between two species of woodrat in the genus Neotoma . Changes in mate availability resulted from drought-driven differential survival between the species and their hybrids. As the availability of conspecifc mates declined, rates of hybridization increased, leading to the accumulation of admixed individuals in the zone of contact. Patterns of reproductive success in the wild appear to be the result of a combination of both pre-mating isolation and post-zygotic selection resulting from genomic incompatibilities between the parental lineages. Evidence of asymmetric mate preference between the parental lineages came from both skewed reproductive output in the field and laboratory preference trials. Moreover, partial genomic incompatibility was evident from the near-zero reproductive success of F1 males and because nearly all surviving hybrids had one pure parent. Nonetheless, the high reproductive success of F1 females and backcrossing in both parental directions allow for introgression between the parental species. These findings reveal how climate change may alter evolutionary outcomes for species at the edge of their ranges through an interplay of behavioral, demographic, and genetic mechanisms.

California

Testosterone identifies hatchling sex for Mojave desert tortoises (Gopherus agassizii)

The threatened Mojave desert tortoise ( Gopherus agassizii ) exhibits temperature-dependent sex determination, and individuals appear externally sexually monomorphic until sexual maturity. A non-surgical sex identification method that is suitable for a single in situ encounter with hatchlings is essential for minimizing handling of wild animals. We tested (1) whether plasma testosterone quantified by enzyme-linked immunosorbent assay differentiated males from females in 0–3 month old captive hatchlings, and (2) whether an injection of follicle-stimulating hormone (FSH) differentially elevates testosterone in male hatchlings to aid in identifying sex. We validated sex by ceolioscopic (laparoscopic) surgery. We then fit the testosterone concentrations to lognormal distributions and identified the concentration below which individuals are more likely female, and above which individuals are more likely male. Using a parametric bootstrapping procedure, we estimated a 0.01–0.04% misidentification rate for naïve testosterone samples, and a 1.26–1.39% misidentification rate for challenged (post-FSH injection) testosterone samples. Quantification of plasma testosterone concentration from small volume (0.1 mL) blood samples appears to be a viable, highly accurate method to identify sex of 0–3 month old hatchlings and could be a valuable tool for conservation measures and investigation of trends and variation in sex ratios for in situ wild nests.

Scientific Reports

A big data–model integration approach for predicting epizootics and population recovery in a keystone species

Infectious diseases pose a significant threat to global health and biodiversity. Yet, predicting the spatiotemporal dynamics of wildlife epizootics remains challenging. Disease outbreaks result from complex nonlinear interactions among a large collection of variables that rarely adhere to the assumptions of parametric regression modeling. We adopted a nonparametric machine learning approach to model wildlife epizootics and population recovery, using the disease system of colonial black-tailed prairie dogs (BTPD, Cynomys ludovicianus ) and sylvatic plague as an example. We synthesized colony data between 2001 and 2020 from eight USDA Forest Service National Grasslands across the range of BTPDs in central North America. We then modeled extinctions due to plague and colony recovery of BTPDs in relation to complex interactions among climate, topoedaphic variables, colony characteristics, and disease history. Extinctions due to plague occurred more frequently when BTPD colonies were spatially clustered, in closer proximity to colonies decimated by plague during the previous year, following cooler than average temperatures the previous summer, and when wetter winter/springs were preceded by drier summers/falls. Rigorous cross-validations and spatial predictions indicated that our final models predicted plague outbreaks and colony recovery in BTPD with high accuracy (e.g., AUC generally >0.80). Thus, these spatially explicit models can reliably predict the spatial and temporal dynamics of wildlife epizootics and subsequent population recovery in a highly complex host–pathogen system. Our models can be used to support strategic management planning (e.g., plague mitigation) to optimize benefits of this keystone species to associated wildlife communities and ecosystem functioning. This optimization can reduce conflicts among different landowners and resource managers, as well as economic losses to the ranching industry. More broadly, our big data–model integration approach provides a general framework for spatially explicit forecasting of disease-induced population fluctuations for use in natural resource management decision-making.

Arizona, Colorado, Kansas, Montana, Nebraska, New

A comparison of non-surgical methods for sexing young gopher tortoises (Gopherus polyphemus)

Many turtle species have temperature-dependent sex determination (TSD), raising the prospect that climate change could impact population dynamics by altering sex ratios. Understanding how climate change will affect populations of animals with TSD requires a reliable and minimally invasive method of identifying the sexes of young individuals. This determination is challenging in many turtles, which often lack conspicuous external sexual dimorphism until years after hatching. Here, we explore four alternatives for sexing three age classes of captive-reared young gopher tortoises ( Gopherus polyphemus ), a terrestrial turtle of conservation concern native to the southeastern United States: (1) naive testosterone levels, (2) testosterone levels following a follicle stimulating hormone (FSH) challenge, (3) linear morphological measurements, and (4) geometric morphometrics. Unlike some other turtle species, male and female neonatal gopher tortoises have overlapping naive testosterone concentration distributions, justifying more complicated methods. We found that sex of neonates (<7 days old) is best predicted by a “random forest” machine learning model with naive testosterone levels and morphological measurements (8% out-of-bag error). Sex of hatchlings (4–8 months old) was predicted with 11% error using a simple threshold on naive testosterone levels, or with 4% error using a simple threshold on post-FSH testosterone levels. Sex of juveniles (approximately 3.5 years old) was perfectly predicted using a simple threshold on naive testosterone levels. Sexing hatchlings at >4 months of age is the easiest and most reliable non-surgical method for sex identification. Given access to a rearing facility and equipment to perform hormone assays, these methods have the potential to supplant laparoscopic surgery as the method of choice for sexing young gopher tortoises.

Georgia

Computed tomography for measuring body fat reserves in threatened Mohave desert tortoise (Gopherus agassizii)

Noninvasive methods for measuring fat reserves in both captive and free-ranging animals are important for monitoring individual and population health, but chelonian anatomy and physiology present challenges to accurate measurements. Standard field-based methods for assessing body condition in Mojave desert tortoises ( Gopherus agassizii ) involve the qualitative body condition score, which relies on the apparent height of the temporalis muscle relative to the sagittal crest (in addition to other characteristics) and quantitative body condition indices that measure relative mass at size. However, it is unclear how these metrics relate to body fat reserves in this species. The aims of this study were to (1) describe the use of noninvasive computed tomography in measuring body fat volume of Mojave desert tortoises, (2) describe the location of fat reserves, (3) investigate relationships between fat reserves and body condition score and body condition index, and (4) explore whether relative temporalis muscle depth, measured via computed tomography, correlates with body condition score. Body condition scores were assessed for eight captive Mojave desert tortoises prior to euthanasia, and computed tomography was performed postmortem to quantify fat volume and measure temporalis muscle depth. At necropsy, the distribution of fat was documented. Fat volume calculated by computed tomography ranged from 2.83 to 145.38 cm 3 (0.07–2.5% body volume). Neither qualitative body condition score nor quantitative body condition index was correlated with fat volume. Bladder content did not compromise body condition index. Body condition score was not correlated with relative temporalis muscle depth. Computed tomography is a noninvasive method for successfully identifying fat reserves and estimating total fat volume in Mojave desert tortoises. The lack of a relationship between computed tomography-determined metrics and commonly used body condition metrics indicates that computed tomography fills a critical gap in the health assessment tool kit for captive and free-ranging Mojave desert tortoises.

Journal of Zoo and Wildlife Medicine

Warming conditions boost reproductive output for a northern gopher tortoise population

The effects of climate change on at-risk species will depend on how life history processes respond to climate and whether the seasonal timing of local climate changes overlaps with species-specific windows of climate sensitivity. For long-lived, iteroparous species like gopher tortoises Gopherus polyphemus , climate likely has a greater influence on reproduction than on adult survival. Our objective was to estimate the timing, magnitude, and direction of climate-driven effects on gopher tortoise reproductive output using a 25 yr dataset collected in southeastern Georgia, USA, near the northern edge of the species’ range. We assessed the timing of climate effects on reproductive output (both probability of reproduction and clutch size) by fitting models with climate covariates (maximum temperature, precipitation, and temperature range) summarized at all possible time intervals (in 1 mo increments) within the 24 mo period prior to the summer census date. We then fit a final model of reproductive output as a function of the identified climate variables and time windows using a Bayesian mixture model. Probability of reproduction was positively correlated with the prior year’s April-May maximum temperature, and clutch size was positively correlated with the prior year’s June maximum temperature. April-May and June maximum temperatures have increased over the past 3 decades at the study site, which likely led to an increase in clutch size of approximately 1 egg (15% increase over a mean of 6.5 eggs). However, the net effect of climate change on gopher tortoise population dynamics will depend on whether there are opposing or reinforcing climate responses for other demographic rates.

Georgia

Integrating telemetry data at several scales with spatial capture–recapture to improve density estimates

Accurate population estimates are essential for monitoring and managing wildlife populations. Mark–recapture sampling methods have regularly been used to estimate population parameters for rare and cryptic species, including the federally listed Mojave desert tortoise ( Gopherus agassizii ); however, the methods employed are often plagued by violations of statistical assumptions, which have the potential to bias density estimates. By incorporating spatial information into conventional density estimation models, spatial capture–recapture (SCR) models can account for common assumption violations such as spatially heterogeneous detection probabilities and temporary emigration when animals leave plots during a survey. We conducted mark–recapture surveys at 10 1-km 2 plots in and adjacent to the Ivanpah Valley of California and Nevada from 2015 to 2019. Locality data were collected concurrently using radio-telemetry and GPS data loggers. GPS data demonstrated that desert tortoises frequently exhibited temporary emigration outside a plot during the survey periods, thereby complicating standard approaches for closed-model density estimation. We integrated mark–recapture survey data for subadults and adults at each plot with corresponding spatial capture locations and supplementary spatial data using a modified SCR model fitted in a Bayesian framework. We compared density estimates modeled with conventional non-spatial methods, as well as three SCR models based on symmetrical usage areas described by various levels and types of supplementary spatial data. The conventional model consistently resulted in inflated estimates of density while the SCR models allowed us to generate spatially corrected estimates for a species where detectability and densities are low. However, we found that if not properly specified, the temporal scale of supplementary data may result in an unintended source of bias in parameter estimates. Integrating spatial data over a larger temporal scale than mark–recapture surveys were conducted resulted in higher detection probabilities and lower density estimates, due to an overestimation of space use. Our results not only demonstrate the importance of accounting for spatial information but also the value of understanding the potential for bias when integrating multiple data sets at different temporal resolutions. The methods presented can be used to enhance monitoring efforts for the Mojave desert tortoise and other species where mark–recapture methods are used.

California, Nevada

Connectivity of Mojave Desert tortoise populations—Management implications for maintaining a viable recovery network

Executive Summary The historic distribution of Mojave desert tortoises ( Gopherus agassizii ) was relatively continuous across the range, and the importance of tortoise habitat outside of designated tortoise conservation areas (TCAs) to recovery has long been recognized for its contributions to supporting gene flow between TCAs and to minimizing impacts and edge effects within TCAs. However, connectivity of Mojave desert tortoise populations has become a concern because of recent and proposed development of large tracts of desert tortoise habitat that cross, fragment, and surround designated conservation areas. This paper summarizes the underlying concepts and importance of connectivity for Mojave desert tortoise populations by reviewing current information on connectivity and providing information to managers for maintaining or enhancing desert tortoise population connectivity as they consider future proposals for development and management actions. Maintaining an ecological network for the Mojave desert tortoise, with a system of core habitats (TCAs) connected by linkages, is necessary to support demographically viable populations and long-term gene flow within and between TCAs. There are four points for wildlife and land-management agencies to consider when making decisions that could affect connectivity of Mojave desert tortoise populations (for example, in updating actions in resource management plans or amendments that could help maintain or restore functional connectivity in light of the latest information): Management of all desert tortoise habitat for persistence and connectivity . Desert tortoise populations continue to decline within most TCAs, and it is unlikely that trends are better in populations outside protected areas. Fragmentation exacerbates negative population trends by breaking large continuous populations into smaller isolated populations. Connectivity within large populations can enhance resilience to localized disturbances due to rescue by neighboring individuals. In contrast, smaller fragmented populations are resistant to rescue by their isolation and thus could suffer irreversible declines to extirpation from a variety of threats and stochastic events. Enhanced threat reduction to reverse declines within TCAs and to maintain occupied habitat in the surrounding matrix would help reduce the variability in population growth rates and improve the resilience of protected populations even while implementing efforts to improve connectivity. Each TCA has unique strengths and weaknesses regarding its ability to support minimum sustainable populations based on areal extent and its ability to support population increases based on landscape connection with adjacent populations. Considering how proposed projects (inside or outside of TCAs) affect connectivity and the ability of TCAs to support at least 5,000 adult tortoises (the numerical goal for each TCA) could help managers to maintain the resilience of TCAs to population declines. The same project, in an alternative location, could have very different impacts on local and regional populations. For example, within the habitat matrix surrounding TCAs, narrowly delineated corridors may not allow for natural population dynamics if they do not accommodate overlapping home ranges along most of their widths so that tortoises reside, grow, find mates, and produce offspring that can replace older tortoises. In addition, most habitat outside TCAs may receive more surface disturbance than habitat within TCAs. Therefore, managing the entire remaining matrix of desert tortoise habitat for permeability may be better than delineating fixed corridors. These concepts apply, especially given uncertainty about long-term condition of habitat, within and outside of TCAs under a changing climate. Ultimately, questions such as “ What are the critical linkages that need to be protected ?” could be better framed as “ How can we manage the remaining habitat matrix in ways that sustain ecological processes and habitat suitability for special status species ?” Land-management decisions made in the context of the latter question may be more conducive to maintenance of a functional ecological network. Limitations on landscape-level disturbance across habitat managed for the desert tortoise Clearly delineating habitat linkages and differentiating them from non-delineated areas by the uses that are permitted or prohibited within them by specific management guidelines can help achieve functional connectivity. Such guidelines would be most effective if they considered and accounted for all surface disturbances (for example, temporary disturbances such as fiberoptic lines or off-highway vehicle routes, right-of-ways, utility-scale solar development, urbanization) to the extent possible. A weighted framework that varies with the permanence or severity of the disturbance, and can be additive to quantify cumulative effects, could be useful (Xiong, 2020). For example, minor roads can alter tortoise movements independently of other features (Peaden and others, 2017; Hromada and others, 2020), but if the isolated dirt road is accompanied by a powerline that encourages raven predation (Xiong, 2020), then the two features together may be additive. Ignoring minor or temporary disturbance on the landscape could result in a cumulatively large impact that is not explicitly acknowledged (Goble, 2009); therefore, understanding and quantifying all surface disturbance on a given landscape is prudent. In California, the Bureau of Land Management established 0.1–1.0 percent caps on new surface-disturbance for TCAs and mapped linkages that address the issues described in number 1 of this list. Nevada, Utah, and Arizona currently do not have surface-disturbance limits. Limits comparable to those in the Desert Renewable Energy Conservation Plan (DRECP) would be 0.5 percent within TCAs and 1 percent within the linkages modeled by Averill-Murray and others (2013). Limits in some areas of California within the Desert Renewable Energy Conservation Plan, such as Ivanpah Valley, are more restrictive, at 0.1 percent. Continuity across the state line in Nevada could be achieved with comparable limits in the adjacent portion of Ivanpah Valley, as well as the Greater Trout Canyon Translocation Area and the Stump Springs Regional Augmentation Site. These more restrictive limits would help protect remaining habitat in the major interstate connectivity pathway through Ivanpah Valley and focal areas of population augmentation that provide additional population connectivity along the western flank of the Spring Mountains. In a recent study that analyzed 13 years of desert tortoise monitoring data, nearly all desert tortoise observations were at sites in which 5 percent or less of the surrounding landscape within 1 kilometer was disturbed (Carter and others, 2020a). To help maintain tortoise habitability and permeability across all other non-conservation-designated tortoise habitat, all surface disturbance could be limited to less than 5-percent development per square kilometer because the 5-percent threshold for development is the point at which tortoise occupation drops precipitously (Carter and others, 2020a). However, although individual desert tortoises were observed at development levels up to 5 percent, we do not know the fitness or reproductive characteristics of these individuals. This level of development also may not allow for long-term persistence of healthy populations that are of adequate size needed for demographic or functional connectivity; therefore, a conservative interpretation suggests that, ideally, development could be lower. Lower development levels would be particularly useful in areas within the upper 5th percentile of connectivity values modeled by Gray and others (2019). Reducing ancillary threats in places where connectivity is restricted to narrow strips of habitat, for example, narrow mountain passes or vegetated strips between solar development, could enhance the functionality of these vulnerable linkages. In such areas, maintaining multiple, redundant linkages could further enhance overall connectivity. Minimization of mortality from roads and maximization of passage under roads . Roads pose a significant threat to the long-term persistence of local tortoise populations, and roads of high traffic volume lead to severe population declines, which ultimately fragments populations farther away from the roads. Three points (a.–c.) pertain to reducing direct mortality of tortoises on the many paved roads that cross desert tortoise habitat and to maintaining a minimal level of permeability across these roads: Tortoise-exclusion fencing tied into culverts, underpasses, overpasses, or other passages below roads in desert tortoise habitat, would limit vehicular mortality of tortoises and provide opportunities for movement across the roads. Installation of shade structures on the habitat side of fences installed in areas with narrow population-depletion zones would limit overheating of tortoises that may pace the fence. Passages below highways could be maintained or retrofitted to ensure safe tortoise access, for example, by filling eroded drop-offs or modifying erosion-control features such as rip-rap to make them safer and more passable for tortoises. Wildlife management agencies could work with transportation departments to develop construction standards that are consistent with hydrologic/erosion management goals, while also incorporating a design and materials consistent with tortoise survival and passage and make the standards widely available. The process would be most effective if the status of passages was regularly monitored and built into management plans. Healthy tortoise populations along fenced highways could be supported by ensuring that land inside tortoise-exclusion fences is not so degraded that it leads to degradation of tortoise habitat outside the exclusion areas. For example, severe invasive plant infestations inside a highway exclusion could cause an increase of invasive plants outside the exclusion area and degrade habitat; therefore, invasive plants inside road rights of way could be mown or treated with herbicide to limit their spread into adjacent tortoise habitat and minimize the risk of these plants carrying wildfires into adjacent habitat. Adaptation of management based on new information . Future research will continue to build upon and refine models related to desert tortoise population connectivity and develop new ones. New models could consider landscape levels of development and be constructed such that they share common foundations to support future synthesis efforts. If model development was undertaken in partnership with entities that are responsible for management of desert tortoise habitat, it would facilitate incorporation of current and future modeling results into their land management decisions. There are specific topics that may be clarified with further evaluation: The effects of climate change on desert tortoise habitat, distribution, and population connectivity; The effects of large-scale fires, especially within repeatedly burned habitat, on desert tortoise distribution and population connectivity; The ability of solar energy facilities or similar developments to support tortoise movement and presence by leaving washes intact; leaving native vegetation intact whenever possible, or if not possible, mowing the site, allowing vegetation to re-sprout, and managing weeds; and allowing tortoises to occupy the sites; and The design and frequency of underpasses necessary to maintain functional demographic and genetic connectivity across linear features, like highways.

Arizona, California, Nevada

‘Unscrambling’ the drivers of egg production in Agassiz’s desert tortoise: Climate and individual attributes predict reproductive output

ABSTRACT: The ‘bet hedging’ life history strategy of long-lived iteroparous species reduces short-term reproductive output to minimize the risk of reproductive failure over a lifetime. For desert-dwelling ectotherms living in variable and unpredictable environments, reproductive output is further influenced by precipitation and temperature via effects on food availability and limits on activity. We assembled multiple (n = 12) data sets on egg production for the threatened Agassiz’s desert tortoise Gopherus agassizii across its range and used these data to build a range-wide predictive model of annual reproductive output as a function of annual weather variation and individual-level attributes (body size and prior-year reproductive status). Climate variables were more robust predictors of reproductive output than individual-level attributes, with overall reproductive output positively related to prior-year precipitation and an earlier start to the spring activity season, and negatively related to spring temperature extremes (monthly temperature range in March-April). Reproductive output was highest for individuals with larger body sizes that reproduced in the previous year. Expected annual reproductive output from 1990-2018 varied from 2-5 to 6-12 eggs female -1 yr -1 , with a weak decline in expected reproductive output over this time (p = 0.02). Climate-driven environmental variation in expected reproductive output was highly correlated across all 5 Recovery Units for this species (Pearson’s r > 0.9). Overall, our model suggests that climate change could strongly impact the reproductive output of Agassiz’s desert tortoise, and could have a negative population-level effect if precipitation is significantly reduced across the species’ range as predicted under some climate models.

California, Arizona, Nevada, Utah

Developing population models with data from marked individuals

Population viability analysis (PVA) is a powerful tool for biodiversity assessments, but its use has been limited because of the requirements for fully specified population models such as demographic structure, density-dependence, environmental stochasticity, and specification of uncertainties. Developing a fully specified population model from commonly available data sources &ndash; notably, mark&ndash;recapture studies &ndash; remains complicated due to lack of practical methods for estimating fecundity, true survival (as opposed to apparent survival), natural temporal variability in both survival and fecundity, density-dependence in the demographic parameters, and uncertainty in model parameters. We present a general method that estimates all the key parameters required to specify a stochastic, matrix-based population model, constructed using a long-term mark&ndash;recapture dataset. Unlike standard mark&ndash;recapture analyses, our approach provides estimates of true survival rates and fecundities, their respective natural temporal variabilities, and density-dependence functions, making it possible to construct a population model for long-term projection of population dynamics. Furthermore, our method includes a formal quantification of parameter uncertainty for global (multivariate) sensitivity analysis. We apply this approach to 9 bird species and demonstrate the feasibility of using data from the Monitoring Avian Productivity and Survivorship (MAPS) program. Bias-correction factors for raw estimates of survival and fecundity derived from mark&ndash;recapture data (apparent survival and juvenile:adult ratio, respectively) were non-negligible, and corrected parameters were generally more biologically reasonable than their uncorrected counterparts. Our method allows the development of fully specified stochastic population models using a single, widely available data source, substantially reducing the barriers that have until now limited the widespread application of PVA. This method is expected to greatly enhance our understanding of the processes underlying population dynamics and our ability to analyze viability and project trends for species of conservation concern.

Biological Conservation