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Climatic variation and tortoise survival: has a desert species met its match?

While demographic changes in short-lived species may be observed relatively quickly in response to climate changes, measuring population responses of long-lived species requires long-term studies that are not always available. We analyzed data from a population of threatened Agassiz’s desert tortoises (Gopherus agassizii) at a 2.59 km 2 study plot in the Sonoran Desert ecosystem of Joshua Tree National Park, California, USA from 1978 to 2012 to examine variation in apparent survival and demography in this long-lived species. Transect-based, mark-recapture surveys were conducted in 10 of those years to locate living and dead tortoises. Previous modeling suggested that this area would become unsuitable as tortoise habitat under a warming and drying climate scenario. Estimated adult population size declined greatly from 1996 to 2012. The population appeared to have high apparent survival from 1978 to 1996 but apparent survival decreased from 1997 to 2002, concurrent with persistent drought. The best model relating apparent survivorship of tortoises ≥18 cm over time was based on a three year moving average of estimated winter precipitation. The postures and positions of a majority of dead tortoises found in 2012 were consistent with death by dehydration and starvation. Some live and many dead tortoises found in 2012 showed signs of predation or scavenging by mammalian carnivores. Coyote (Canis latrans) scats and other evidence from the site confirmed their role as tortoise predators and scavengers. Predation rates may be exacerbated by drought if carnivores switch from preferred mammalian prey to tortoises during dry years. Climate modeling suggests that the region will be subjected to even longer duration droughts in the future and that the plot may become unsuitable for continued tortoise survival. Our results showing wide fluctuations in apparent survival and decreasing tortoise density over time may be early signals of that possible outcome.

California

Breeding site heterogeneity reduces variability in frog recruitment and population dynamics

Environmental stochasticity can have profound effects on the dynamics and viability of wild populations, and habitat heterogeneity provides one mechanism by which populations may be buffered against the negative effects of environmental fluctuations. Heterogeneity in breeding pond hydroperiod across the landscape may allow amphibian populations to persist despite variable interannual precipitation. We examined recruitment dynamics over 10 yr in a high-elevation Columbia spotted frog ( Rana luteiventris ) population that breeds in ponds with a variety of hydroperiods. We combined these data with matrix population models to quantify the consequences of heterogeneity in pond hydroperiod on net recruitment (i.e. number of metamorphs produced) and population growth rates. We compared our heterogeneous system to hypothetical homogeneous environments with only ephemeral ponds, only semi-permanent ponds, and only permanent ponds. We also examined the effects of breeding pond habitat loss on population growth rates. Most eggs were laid in permanent ponds each year, but survival to metamorphosis was highest in the semi-permanent ponds. Recruitment success varied by both year and pond type. Net recruitment and stochastic population growth rate were highest under a scenario with homogeneous semi-permanent ponds, but variability in recruitment was lowest in the scenario with the observed heterogeneity in hydroperiods. Loss of pond habitat decreased population growth rate, with greater decreases associated with loss of permanent and semi-permanent habitat. The presence of a diversity of pond hydroperiods on the landscape will influence population dynamics, including reducing variability in recruitment in an uncertain climatic future.

Montana

Population declines lead to replicate patterns of internal range structure at the tips of the distribution of the California red-legged frog ( Rana draytonii )

Demographic declines and increased isolation of peripheral populations of the threatened California red-legged frog ( Rana draytonii ) have led to the formation of internal range boundaries at opposite ends of the species’ distribution. While the population genetics of the southern internal boundary has been studied in some detail, similar information is lacking for the northern part of the range. In this study, we used microsatellite and mtDNA data to examine the genetic structuring and diversity of some of the last remaining R. draytonii populations in the northern Sierra Nevada, which collectively form the northern external range boundary. We compared these data to coastal populations in the San Francisco Bay Area, where the species is notably more abundant and still exists throughout much of its historic range. We show that ‘external’ Sierra Nevada populations have lower genetic diversity and are more differentiated from one another than their ‘internal’ Bay Area counterparts. This same pattern was mirrored across the distribution in California, where Sierra Nevada and Bay Area populations had lower allelic variability compared to those previously studied in coastal southern California. This genetic signature of northward range expansion was mirrored in the phylogeography of mtDNA haplotypes; northern Sierra Nevada haplotypes showed greater similarity to haplotypes from the south Coast Ranges than to the more geographically proximate populations in the Bay Area. These data cast new light on the geographic origins of Sierra Nevada R. draytonii populations and highlight the importance of distinguishing the genetic effects of contemporary demographic declines from underlying signatures of historic range expansion when addressing the most immediate threats to population persistence. Because there is no evidence of contemporary gene flow between any of the Sierra Nevada R. draytonii populations, we suggest that management activities should focus on maintaining and creating additional ponds to support breeding within typical dispersal distances of occupied habitat.

Biological Conservation

Animal reintroductions: an innovative assessment of survival

Quantitative evaluations of reintroductions are infrequent and assessments of milestones reached before a project is completed, or abandoned due to lack of funding, are rare. However, such assessments, which are promoted in adaptive management frameworks, are critical. Quantification can provide defensible estimates of biological success, such as the number of survivors from a released cohort, with associated cost per animal. It is unlikely that the global issues of endangered wildlife and population declines will abate, therefore, assurance colonies and reintroductions are likely to become more common. If such endeavors are to be successful biologically or achieve adequate funding, implementation must be more rigorous and accountable. We use a novel application of a multistate, robust design capture-recapture model to estimate survival of reintroduced tadpoles through metamorphosis (i.e., the number of individuals emerging from the pond) and thereby provide a quantitative measure of effort and success for an "in progress" reintroduction of toads. Our data also suggest that tadpoles released at later developmental stages have an increased probability of survival and that eggs laid in the wild hatched at higher rates than eggs laid by captive toads. We illustrate how an interim assessment can identify problems, highlight successes, and provide information for use in adjusting the effort or implementing a Decision-Theoretic adaptive management strategy.

Biological Conservation

Establishing endangered species recovery criteria using predictive simulation modeling

Listing a species under the Endangered Species Act (ESA) and developing a recovery plan requires U.S. Fish and Wildlife Service to establish specific and measurable criteria for delisting. Generally, species are listed because they face (or are perceived to face) elevated risk of extinction due to issues such as habitat loss, invasive species, or other factors. Recovery plans identify recovery criteria that reduce extinction risk to an acceptable level. It logically follows that the recovery criteria, the defined conditions for removing a species from ESA protections, need to be closely related to extinction risk. Extinction probability is a population parameter estimated with a model that uses current demographic information to project the population into the future over a number of replicates, calculating the proportion of replicated populations that go extinct. We simulated extinction probabilities of piping plovers in the Great Plains and estimated the relationship between extinction probability and various demographic parameters. We tested the fit of regression models linking initial abundance, productivity, or population growth rate to extinction risk, and then, using the regression parameter estimates, determined the conditions required to reduce extinction probability to some pre-defined acceptable threshold. Binomial regression models with mean population growth rate and the natural log of initial abundance were the best predictors of extinction probability 50 years into the future. For example, based on our regression models, an initial abundance of approximately 2400 females with an expected mean population growth rate of 1.0 will limit extinction risk for piping plovers in the Great Plains to less than 0.048. Our method provides a straightforward way of developing specific and measurable recovery criteria linked directly to the core issue of extinction risk. Published by Elsevier Ltd.

Biological Conservation

Potential reduction in terrestrial salamander ranges associated with Marcellus shale development

Natural gas production from the Marcellus shale is rapidly increasing in the northeastern United States. Most of the endemic terrestrial salamander species in the region are classified as ‘globally secure’ by the IUCN, primarily because much of their ranges include state- and federally protected lands, which have been presumed to be free from habitat loss. However, the proposed and ongoing development of the Marcellus gas resources may result in significant range restrictions for these and other terrestrial forest salamanders. To begin to address the gaps in our knowledge of the direct impacts of shale gas development, we developed occurrence models for five species of terrestrial plethodontid salamanders found largely within the Marcellus shale play. We predicted future Marcellus shale development under several scenarios. Under scenarios of 10,000, 20,000, and 50,000 new gas wells, we predict 4%, 8%, and 20% forest loss, respectively, within the play. Predictions of habitat loss vary among species, but in general, Plethodon electromorphus and Plethodon wehrlei are predicted to lose the greatest proportion of forested habitat within their ranges if future Marcellus development is based on characteristics of the shale play. If development is based on current well locations, Plethodon richmondi is predicted to lose the greatest proportion of habitat. Models showed high uncertainty in species’ ranges and emphasize the need for distribution data collected by widespread and repeated, randomized surveys.

Biological Conservation

Quantification of eDNA shedding rates from invasive bighead carp Hypophthalmichthys nobilis and silver carp Hypophthalmichthys molitrix

Wildlife managers can more easily mitigate the effects of invasive species if action takes place before a population becomes established. Such early detection requires sensitive survey tools that can detect low numbers of individuals. Due to their high sensitivity, environmental DNA (eDNA) surveys hold promise as an early detection method for aquatic invasive species. Quantification of eDNA amounts may also provide data on species abundance and timing of an organism’s presence, allowing managers to successfully combat the spread of ecologically damaging species. To better understand the link between eDNA and an organism’s presence, it is crucial to know how eDNA is shed into the environment. Our study used quantitative PCR (qPCR) and controlled laboratory experiments to measure the amount of eDNA that two species of invasive bigheaded carps ( Hypophthalmichthys nobilis and Hypophthalmichthys molitrix ) shed into the water. We first measured how much eDNA a single fish sheds and the variability of these measurements. Then, in a series of manipulative lab experiments, we studied how temperature, biomass (grams of fish), and diet affect the shedding rate of eDNA by these fish. We found that eDNA amounts exhibit a positive relationship with fish biomass, and that feeding could increase the amount of eDNA shed by ten-fold, whereas water temperature did not have an effect. Our results demonstrate that quantification of eDNA may be useful for predicting carp density, as well as densities of other rare or invasive species.

Biological Conservation

The effect of dilution and the use of a post-extraction nucleic acid purification column on the accuracy, precision, and inhibition of environmental DNA samples

Isolation of environmental DNA (eDNA) is an increasingly common method for detecting presence and assessing relative abundance of rare or elusive species in aquatic systems via the isolation of DNA from environmental samples and the amplification of species-specific sequences using quantitative PCR (qPCR). Co-extracted substances that inhibit qPCR can lead to inaccurate results and subsequent misinterpretation about a species’ status in the tested system. We tested three treatments (5-fold and 10-fold dilutions, and spin-column purification) for reducing qPCR inhibition from 21 partially and fully inhibited eDNA samples collected from coastal plain wetlands and mountain headwater streams in the southeastern USA. All treatments reduced the concentration of DNA in the samples. However, column purified samples retained the greatest sensitivity. For stream samples, all three treatments effectively reduced qPCR inhibition. However, for wetland samples, the 5-fold dilution was less effective than other treatments. Quantitative PCR results for column purified samples were more precise than the 5-fold and 10-fold dilutions by 2.2× and 3.7×, respectively. Column purified samples consistently underestimated qPCR-based DNA concentrations by approximately 25%, whereas the directional bias in qPCR-based DNA concentration estimates differed between stream and wetland samples for both dilution treatments. While the directional bias of qPCR-based DNA concentration estimates differed among treatments and locations, the magnitude of inaccuracy did not. Our results suggest that 10-fold dilution and column purification effectively reduce qPCR inhibition in mountain headwater stream and coastal plain wetland eDNA samples, and if applied to all samples in a study, column purification may provide the most accurate relative qPCR-based DNA concentrations estimates while retaining the greatest assay sensitivity.

Biological Conservation

Activity-specific ecological niche models for planning reintroductions of California condors (Gymnogyps californianus)

Ecological niche models can be a useful tool to identify candidate reintroduction sites for endangered species but have been infrequently used for this purpose. In this paper, we (1) develop activity-specific ecological niche models (nesting, roosting, and feeding) for the critically endangered California condor ( Gymnogyps californianus ) to aid in reintroduction planning in California, Oregon, and Washington, USA, (2) test the accuracy of these models using empirical data withheld from model development, and (3) integrate model results with information on condor movement ecology and biology to produce predictive maps of reintroduction site suitability. Our approach, which disentangles niche models into activity-specific components, has applications for other species where it is routinely assumed (often incorrectly) that individuals fulfill all requirements for life within a single environmental space. Ecological niche models conformed to our understanding of California condor ecology, had good predictive performance when tested with data withheld from model development, and aided in the identification of several candidate reintroduction areas outside of the current distribution of the species. Our results suggest there are large unoccupied regions of the California condor’s historical range that have retained ecological features similar to currently occupied habitats, and thus could be considered for future reintroduction efforts. Combining our activity-specific ENMs with ground reconnaissance and information on other threat factors that could not be directly incorporated into empirical ENMs will ultimately improve our ability to select successful reintroduction sites for the California condor.

California, Oregon, Washington

Heterogeneous movement of insectivorous Amazonian birds through primary and secondary forest: A case study using multistate models with radiotelemetry data

Given rates of deforestation, disturbance, and secondary forest accumulation in tropical rainforests, there is a great need to quantify habitat use and movement among different habitats. This need is particularly pronounced for animals most sensitive to disturbance, such as insectivorous understory birds. Here we use multistate capture–recapture models with radiotelemetry data to determine the successional stage at which within-day movement probabilities of Amazonian birds in secondary forest are similar to those in primary forest. We radio-tracked three common understory insectivore species in primary and secondary forest at the Biological Dynamics of Forest Fragments project near Manaus, Brazil: two woodcreepers, Glyphorynchus spirurus ( n = 19) and Xiphorhynchus pardalotus ( n = 18), and the terrestrial antthrush Formicarius colma ( n = 19 ) . Forest age was a strong predictor of fidelity to a given habitat. All three species showed greater fidelity to primary forest than to 8–14-year-old secondary forest, indicating the latter’s relatively poor quality. The two woodcreeper species used 12–18-year-old secondary forest in a manner comparable to continuous forest, but F . colma avoided moving even to 27–31-year-old secondary forest—the oldest at our site. Our results suggest that managers concerned with less sensitive species can assume that forest reserves connected by 12–18-year-old secondary forest corridors are effectively connected. On the other hand, >30 years are required after land abandonment before secondary forest serves as a primary forest-like conduit for movement by F . colma ; more sensitive terrestrial insectivores may take longer still.

Manaus

Avoidance of unconventional oil wells and roads exacerbates habitat loss for grassland birds in the North American great plains

Oil development in the Bakken shale region has increased rapidly as a result of new technologies and strong demand for fossil fuel. This region also supports a particularly high density and diversity of grassland bird species, which are declining across North America. We examined grassland bird response to unconventional oil extraction sites (i.e. developed with hydraulic fracturing and horizontal drilling techniques) and associated roads in North Dakota. Our goal was to quantify the amount of habitat that was indirectly degraded by oil development, as evidenced by patterns of avoidance by birds. Grassland birds avoided areas within 150 m of roads (95% CI: 87–214 m), 267 m of single-bore well pads (95% CI: 157–378 m), and 150 m of multi-bore well pads (95% CI: 67–233 m). Individual species demonstrated variable tolerance of well pads. Clay-colored sparrows ( Spizella pallida ) were tolerant of oil-related infrastructure, whereas Sprague's pipit ( Anthus spragueii ) avoided areas within 350 m (95% CI: 215–485 m) of single-bore well pads. Given these density patterns around oil wells, the potential footprint of any individual oil well, and oil development across the region, is greatly multiplied for sensitive species. Efforts to reduce new road construction, concentrate wells along developed corridors, combine numerous wells on multi-bore pads rather than build many single-bore wells, and to place well pads near existing roads will serve to minimize loss of suitable habitat for birds. Quantifying environmental degradation caused by oil development is a critical step in understanding how to better mitigate harm to wildlife populations.

Biological Conservation

The rapid return of marine-derived nutrients to a freshwater food web following dam removal

Dam removal is increasingly being recognized as a viable river restoration action. Although the main beneficiaries of restored connectivity are often migratory fish populations, little is known regarding recovery of other parts of the freshwater food web, particularly terrestrial components. We measured stable isotopes in key components to the freshwater food web: salmon, freshwater macroinvertebrates and a river specialist bird, American dipper ( Cinclus mexicanus ), before and after removal of the Elwha Dam, WA, USA. Less than a year after dam removal, salmon returned to the system and released marine-derived nutrients (MDN). In that same year we documented an increase in stable-nitrogen and carbon isotope ratios in American dippers. These results indicate that MDN from anadromous fish, an important nutrient subsidy that crosses the aquatic–terrestrial boundary, can return rapidly to food webs after dams are removed which is an important component of ecosystem recovery.

Washington

Book review: Bats: A world of science and mystery.

This book has something for everyone, from casual seekers of fascinating eye candy to professional scientists interested in the latest discoveries. Without losing sight of how mysterious bats remain despite decades of research, the authors deftly introduce readers to bats and the people who study them. The book is nice to look at, easy to understand, and interesting in many ways. These stories stick in the reader's memory long after being read—a sign of great scientific communication. Review info: Bats: A world of science and mystery. By M. Brock Fenton, Nancy B. Simmons (Eds.), 2015. ISBN 978-0226065120, 240 pp.

Biological Conservation

Migratory corridors of adult female Kemp’s ridley turtles in the Gulf of Mexico

For many marine species, locations of migratory pathways are not well defined. We used satellite telemetry and switching state-space modeling (SSM) to define the migratory corridor used by Kemp's ridley turtles (Lepidochelys kempii) in the Gulf of Mexico. The turtles were tagged after nesting at Padre Island National Seashore, Texas, USA from 1997 to 2014 (PAIS; n = 80); Rancho Nuevo, Tamaulipas, Mexico from 2010 to 2011 (RN; n = 14); Tecolutla, Veracruz, Mexico from 2012 to 2013 (VC; n = 13); and Gulf Shores, Alabama, USA during 2012 (GS; n = 1). The migratory corridor lies in nearshore Gulf of Mexico waters in the USA and Mexico with mean water depth of 26 m and a mean distance of 20 km from the nearest mainland coast. Migration from the nesting beach is a short phenomenon that occurs from late-May through August, with a peak in June. There was spatial similarity of post-nesting migratory pathways for different turtles over a 16 year period. Thus, our results indicate that these nearshore Gulf waters represent a critical migratory habitat for this species. However, there is a gap in our understanding of the migratory pathways used by this and other species to return from foraging grounds to nesting beaches. Therefore, our results highlight the need for tracking reproductive individuals from foraging grounds to nesting beaches. Continued tracking of adult females from PAIS, RN, and VC nesting beaches will allow further study of environmental and bathymetric components of migratory habitat and threats occurring within our defined corridor. Furthermore, the existence of this migratory corridor in nearshore waters of both the USA and Mexico demonstrates that international cooperation is necessary to protect essential migratory habitat for this imperiled species.

Gulf of Mexico

Understanding environmental DNA detection probabilities: A case study using a stream-dwelling char Salvelinus fontinalis

Environmental DNA sampling (eDNA) has emerged as a powerful tool for detecting aquatic animals. Previous research suggests that eDNA methods are substantially more sensitive than traditional sampling. However, the factors influencing eDNA detection and the resulting sampling costs are still not well understood. Here we use multiple experiments to derive independent estimates of eDNA production rates and downstream persistence from brook trout ( Salvelinus fontinalis ) in streams. We use these estimates to parameterize models comparing the false negative detection rates of eDNA sampling and traditional backpack electrofishing. We find that using the protocols in this study eDNA had reasonable detection probabilities at extremely low animal densities (e.g., probability of detection 0.18 at densities of one fish per stream kilometer) and very high detection probabilities at population-level densities (e.g., probability of detection > 0.99 at densities of ≥ 3 fish per 100 m). This is substantially more sensitive than traditional electrofishing for determining the presence of brook trout and may translate into important cost savings when animals are rare. Our findings are consistent with a growing body of literature showing that eDNA sampling is a powerful tool for the detection of aquatic species, particularly those that are rare and difficult to sample using traditional methods.

Montana

Impacts of climate change and renewable energy development on habitat of an endemic squirrel, Xerospermophilus mohavensis , in the Mojave Desert, USA

Predicting changes in species distributions under a changing climate is becoming widespread with the use of species distribution models (SDMs). The resulting predictions of future potential habitat can be cast in light of planned land use changes, such as urban expansion and energy development to identify areas with potential conflict. However, SDMs rarely incorporate an understanding of dispersal capacity, and therefore assume unlimited dispersal in potential range shifts under uncertain climate futures. We use SDMs to predict future distributions of the Mojave ground squirrel, Xerospermophilus mohavensis Merriam, and incorporate partial dispersal models informed by field data on juvenile dispersal to assess projected impact of climate change and energy development on future distributions of X. mohavensis . Our models predict loss of extant habitat, but also concurrent gains of new habitat under two scenarios of future climate change. Under the B1 emissions scenario- a storyline describing a convergent world with emphasis on curbing greenhouse gas emissions- our models predicted losses of up to 64% of extant habitat by 2080, while under the increased greenhouse gas emissions of the A2 scenario, we suggest losses of 56%. New potential habitat may become available to X. mohavensis , thereby offsetting as much as 6330 km 2 (50%) of the current habitat lost. Habitat lost due to planned energy development was marginal compared to habitat lost from changing climates, but disproportionately affected current habitat. Future areas of overlap in potential habitat between the two climate change scenarios are identified and discussed in context of proposed energy development.

California

Future frequencies of extreme weather events in the National Wildlife Refuges of the conterminous U.S.

Climate change is a major challenge for managers of protected areas world-wide, and managers need information about future climate conditions within protected areas. Prior studies of climate change effects in protected areas have largely focused on average climatic conditions. However, extreme weather may have stronger effects on wildlife populations and habitats than changes in averages. Our goal was to quantify future changes in the frequency of extreme heat, drought, and false springs, during the avian breeding season, in 415 National Wildlife Refuges in the conterminous United States. We analyzed spatially detailed data on extreme weather frequencies during the historical period (1950–2005) and under different scenarios of future climate change by mid- and late-21st century. We found that all wildlife refuges will likely experience substantial changes in the frequencies of extreme weather, but the types of projected changes differed among refuges. Extreme heat is projected to increase dramatically in all wildlife refuges, whereas changes in droughts and false springs are projected to increase or decrease on a regional basis. Half of all wildlife refuges are projected to see increases in frequency (> 20% higher than the current rate) in at least two types of weather extremes by mid-century. Wildlife refuges in the Southwest and Pacific Southwest are projected to exhibit the fastest rates of change, and may deserve extra attention. Climate change adaptation strategies in protected areas, such as the U.S. wildlife refuges, may need to seriously consider future changes in extreme weather, including the considerable spatial variation of these changes.

Biological Conservation

Global biodiversity monitoring: from data sources to essential biodiversity variables

Essential Biodiversity Variables (EBVs) consolidate information from varied biodiversity observation sources. Here we demonstrate the links between data sources, EBVs and indicators and discuss how different sources of biodiversity observations can be harnessed to inform EBVs. We classify sources of primary observations into four types: extensive and intensive monitoring schemes, ecological field studies and satellite remote sensing. We characterize their geographic, taxonomic and temporal coverage. Ecological field studies and intensive monitoring schemes inform a wide range of EBVs, but the former tend to deliver short-term data, while the geographic coverage of the latter is limited. In contrast, extensive monitoring schemes mostly inform the population abundance EBV, but deliver long-term data across an extensive network of sites. Satellite remote sensing is particularly suited to providing information on ecosystem function and structure EBVs. Biases behind data sources may affect the representativeness of global biodiversity datasets. To improve them, researchers must assess data sources and then develop strategies to compensate for identified gaps. We draw on the population abundance dataset informing the Living Planet Index (LPI) to illustrate the effects of data sources on EBV representativeness. We find that long-term monitoring schemes informing the LPI are still scarce outside of Europe and North America and that ecological field studies play a key role in covering that gap. Achieving representative EBV datasets will depend both on the ability to integrate available data, through data harmonization and modeling efforts, and on the establishment of new monitoring programs to address critical data gaps.

Biological Conservation