Sagebrush Framework References

1. Cropland expansion in the United States produces marginal yields at high costs to wildlife

Recent expansion of croplands in the United States has caused widespread conversion of grasslands and other ecosystems with largely unknown consequences for agricultural production and the environment. Here we assess annual land use change 2008–16 and its impacts on crop yields and wildlife habitat. We find that croplands have expanded at a rate of over one million acres per year, and that 69.5% of new cropland areas produced yields below the national average, with a mean yield deficit of 6.5%. Observed conversion infringed upon high-quality habitat that, relative to unconverted land, had provided over three times higher milkweed stem densities in the Monarch butterfly Midwest summer breeding range and 37% more nesting opportunities per acre for waterfowl in the Prairie Pothole Region of the Northern Great Plains. Our findings demonstrate a pervasive pattern of encroachment into areas that are increasingly marginal for production, but highly significant for wildlife, and suggest that such tradeoffs may be further amplified by future cropland expansion.

Lark, T.J., S.A. Spawn, M. Bougie, and H.K. Gibbs. 2020. Cropland expansion in the United States produces marginal yields at high costs to wildlife. Nature Communications 11:4295. https://doi.org/10.1038/s41467-020-18045-z


2. Cattle, conservation, and carbon in the western Great Plains

Sanderson, J.S., C. Beutler, J.R. Brown, I. Burke, T. Chapman, R.T. Conant, J.D. Derner, M. Easter, S.D. Fuhlendorf, G. Grissom, J.E. Herrick, D. Liptzin, J.A. Morgan, R. Murph, C. Pague, I. Rangwala, D. Ray, R. Rondeau, T. Schulz, and T. Sullivan. 2020. Cattle, conservation, and carbon in the western Great Plains. Journal of Soil and Water Conservation 75:5-12. https://doi.org/10.2489/jswc.75.1.5A


3. Coproducing science to inform working lands: the next frontier in nature conservation

Conservationists are increasingly convinced that coproduction of science enhances its utility in policy, decision-making, and practice. Concomitant is a renewed reliance on privately owned working lands to sustain nature and people. We propose a coupling of these emerging trends as a better recipe for conservation. To illustrate this, we present five elements of coproduction, contrast how they differ from traditional approaches, and describe the role of scientists in successful partnerships. Readers will find coproduction more demanding than the loading dock approach to science delivery but will also find greater rewards, relevance, and impact. Because coproduction is novel and examples of it are rare, we draw on our roles as scientists within the US Department of Agriculture–led Sage Grouse Initiative, North America’s largest effort to conserve the sagebrush ecosystem. As coproduction and working lands evolve, traditional approaches will be replaced in order to more holistically meet the needs of nature and people.

Naugle, D.E., B.W. Allred, M.O. Jones, D. Twidwell, and J.D. Maestas. 2020. Coproducing science to inform working lands: the next frontier in nature conservation. BioScience 70:90-96. https://doi.org/10.1093/biosci/biz144


4. Outcomes in conservation Sage Grouse Initiative

Natural Resources Conservation Service. 2015. Outcomes in conservation Sage Grouse Initiative. U.S. Department of Agriculture. https://www.sagegrouseinitiative.com/wp-content/uploads/2015/08/SGI2.0_Final_Report.pdf


5. Endangered and threatened wildlife and plants; 12-month finding on a petition to list Greater Sage-Grouse (Centrocercus urophasianus) as an endangered or threatened species

US Fish and Wildlife Service (USFWS). 2015. Endangered and threatened wildlife and plants; 12-month finding on a petition to list Greater Sage-Grouse (Centrocercus urophasianus) as an endangered or threatened species. Federal Register 80, 59857–59942. https://www.federalregister.gov/d/2015-24292


6. Cheatgrass (Bromus tectorum) distribution in the intermountain Western United States and its relationship to fire frequency, seasonality, and ignitions

Cheatgrass (Bromus tectorum) is an invasive grass pervasive across the Intermountain Western US and linked to major increases in fire frequency. Despite widespread ecological impacts associated with cheatgrass, we lack a spatially extensive model of cheatgrass invasion in the Intermountain West. Here, we leverage satellite phenology predictors and thousands of field surveys of cheatgrass abundance to create regional models of cheatgrass distribution and percent cover. We compare cheatgrass presence to fire probability, fire seasonality and ignition source. Regional models of percent cover had low predictive power (34% of variance explained), but distribution models based on a threshold of 15% cover to differentiate high abundance from low abundance had an overall accuracy of 74%. Cheatgrass achieves ≥ 15% cover over 210,000 km2 (31%) of the Intermountain West. These lands were twice as likely to burn as those with low abundance, and four times more likely to burn multiple times between 2000 and 2015. Fire probability increased rapidly at low cheatgrass cover (1–5%) but remained similar at higher cover, suggesting that even small amounts of cheatgrass in an ecosystem can increase fire risk. Abundant cheatgrass was also associated with a 10 days earlier fire seasonality and interacted strongly with anthropogenic ignitions. Fire in cheatgrass was particularly associated with human activity, suggesting that increased awareness of fire danger in invaded areas could reduce risk. This study suggests that cheatgrass is much more spatially extensive and abundant than previously documented and that invasion greatly increases fire frequency, even at low percent cover.

Bradley, B.A., C.A. Curtis, E.J. Fusco, et al. 2018. Cheatgrass (Bromus tectorum) distribution in the intermountain Western United States and its relationship to fire frequency, seasonality, and ignitions. Biological Invasions 20:1493-1506. https://doi.org/10.1007/s10530-017-1641-8


7. Annual Herbaceous Cover across Rangelands of the Sagebrush Biome: U.S. Geological Survey data release

Maestas, J.D., M.O. Jones, N.J. Pastick, M. Rigge, B.K. Wylie, L. Garner, M. Crist, C. Homer, S.P. Poyte, and B. Whitacre. 2020. Annual Herbaceous Cover across Rangelands of the Sagebrush Biome: U.S. Geological Survey data release, https://doi.org/10.5066/P9VL3LD5


8. A synthesis of the effects of cheatgrass invasion on US Great Basin carbon storage

  1. Non‐native, invasive Bromus tectorum (cheatgrass) is pervasive in sagebrush ecosystems in the Great Basin ecoregion of the western United States, competing with native plants and promoting more frequent fires. As a result, cheatgrass invasion likely alters carbon (C) storage in the region. Many studies have measured C pools in one or more common vegetation types: native sagebrush, invaded sagebrush and cheatgrass‐dominated (often burned) sites, but these results have yet to be synthesized.
  2. We performed a literature review to identify studies assessing the consequences of invasion on C storage in above‐ground biomass (AGB), below‐ground biomass (BGB), litter, organic soil and total soil. We identified 41 articles containing 386 unique studies and estimated C storage across pools and vegetation types. We used linear mixed models to identify the main predictors of C storage.
  3. We found consistent declines in biomass C with invasion: AGB C was 55% lower in cheatgrass (40 ± 4 g C/m2) than native sagebrush (89 ± 27 g C/m2) and BGB C was 62% lower in cheatgrass (90 ± 17 g C/m2) than native sagebrush (238 ± 60 g C/m2). In contrast, litter C was >4× higher in cheatgrass (154 ± 12 g C/m2) than native sagebrush (32 ± 12 g C/m2). Soil organic C (SOC) in the top 10 cm was significantly higher in cheatgrass than in native or invaded sagebrush. SOC below 20 cm was significantly related to the time since most recent fire and losses were observed in deep SOC in cheatgrass >5 years after a fire. There were no significant changes in total soil C across vegetation types.
  4. Synthesis and applications. Cheatgrass invasion decreases biodiversity and rangeland productivity and alters fire regimes. Our findings indicate cheatgrass invasion also results in persistent biomass carbon (C) losses that occur with sagebrush replacement. We estimate that conversion from native sagebrush to cheatgrass leads to a net reduction of C storage in biomass and litter of 76 g C/m2, or 16 Tg C across the Great Basin without management practices like native sagebrush restoration or cheatgrass removal.

Nagy, R.C., E.J. Fusco, J.K. Balch, J.T. Finn, A. Mahood, J.M. Allen, B.A. Bradley. 2020. A synthesis of the effects of cheatgrass invasion on US Great Basin carbon storage. Journal of Applied Ecology. https://doi.org/10.1111/1365-2664.13770


9. Tackling Idaho’s cheatgrass challenge

Natural Resources Conservation Service (NRCS). 2020. Tackling Idaho’s cheatgrass challenge. Idaho. https://www.nrcs.usda.gov/wps/PA_NRCSConsumption/download?cid=nrcseprd1560032&ext=pdf


10. A toolkit for invasive annual grass management in the West

Western Governors Association (WGA). 2020. A toolkit for invasive annual grass management in the West. https://westgov.org/images/editor/FINAL_Cheatgrass_Toolkit_July_2020.pdf


11. Resilience to stress and disturbance, and resistance to Bromus tectorum L. invasion in the cold desert shrublands of western North America

Alien grass invasions in arid and semi-arid ecosystems are resulting in grass–fire cycles and ecosystem-level transformations that severely diminish ecosystem services. Our capacity to address the rapid and complex changes occurring in these ecosystems can be enhanced by developing an understanding of the environmental factors and ecosystem attributes that determine resilience of native ecosystems to stress and disturbance, and resistance to invasion. Cold desert shrublands occur over strong environmental gradients and exhibit significant differences in resilience and resistance. They provide an excellent opportunity to increase our understanding of these concepts. Herein, we examine a series of linked questions about (a) ecosystem attributes that determine resilience and resistance along environmental gradients, (b) effects of disturbances like livestock grazing and altered fire regimes and of stressors like rapid climate change, rising CO2, and N deposition on resilience and resistance, and (c) interacting effects of resilience and resistance on ecosystems with different environmental conditions. We conclude by providing strategies for the use of resilience and resistance concepts in a management context. At ecological site scales, state and transition models are used to illustrate how differences in resilience and resistance influence potential alternative vegetation states, transitions among states, and thresholds. At landscape scales management strategies based on resilience and resistance—protection, prevention, restoration, and monitoring and adaptive management—are used to determine priority management areas and appropriate actions.

Chambers, J.C., Bradley, B.A., Brown, C.A., D’Antonio, C., Germino, M.J., Hardegree, S.P., Grace, J.B., Miller, R.F., Pyke, D.A., 2014. Resilience to stress and disturbance, and resistance to Bromus tectorum L. invasion in the cold desert shrublands of western North America. Ecosystems 17, 360–375. https://doi.org/10.1007/s10021-013-9725-5


12. Spatial imaging and screening for regime shifts

Screening is a strategy for detecting undesirable change prior to manifestation of symptoms or adverse effects. Although the well-recognized utility of screening makes it commonplace in medicine, it has yet to be implemented in ecosystem management. Ecosystem management is in an era of diagnosis and treatment of undesirable change, and as a result, remains more reactive than proactive and unable to effectively deal with today’s plethora of non-stationary conditions. In this paper, we introduce spatial imaging-based screening to ecology. We link advancements in spatial resilience theory, data, and technological and computational capabilities and power to detect regime shifts (i.e., vegetation state transitions) that are known to be detrimental to human well-being and ecosystem service delivery. With a state-of-the-art landcover dataset and freely available, cloud-based, geospatial computing platform, we screen for spatial signals of the three most iconic vegetation transitions studied in western USA rangelands: (1) erosion and desertification; (2) woody encroachment; and (3) annual exotic grass invasion. For a series of locations that differ in ecological complexity and geographic extent, we answer the following questions: (1) Which regime shift is expected or of greatest concern? (2) Can we detect a signal associated with the expected regime shift? (3) If detected, is the signal transient or persistent over time? (4) If detected and persistent, is the transition signal stationary or non-stationary over time? (5) What other signals do we detect? Our approach reveals a powerful and flexible methodology, whereby professionals can use spatial imaging to verify the occurrence of alternative vegetation regimes, image the spatial boundaries separating regimes, track the magnitude and direction of regime shift signals, differentiate persistent and stationary transition signals that warrant continued screening from more concerning persistent and non-stationary transition signals, and leverage disciplinary strength and resources for more targeted diagnostic testing (e.g., inventory and monitoring) and treatment (e.g., management) of regime shifts. While the rapid screening approach used here can continue to be implemented and refined for rangelands, it has broader implications and can be adapted to other ecological systems to revolutionize the information space needed to better manage critical transitions in nature.

Uden, D., D. Twidwell, C. Allen, M. Jones, D. Naugle, J. Maestas, B. Allred. 2019. Spatial imaging and screening for regime shifts. Frontiers in Ecology and Evolution, 7, p. 407 https://doi.org/10.3389/fevo.2019.00407


13. Reducing cultivation risk for at-risk species: predicting outcomes of conservation easements for sage-grouse

Conversion of native habitats to cropland is a leading cause of biodiversity loss. The northeastern extent of the sagebrush (Artemisia L.) ecosystem of western North America has experienced accelerated rates of cropland conversion resulting in many declining shrubland species including greater sage-grouse (Centrocercus urophasianus). Here we present point-process models to elucidate the magnitude and spatial scale of cropland effects on sage-grouse lek occurrence in eastern Montana, northeastern Wyoming, North Dakota and South Dakota. We also use a non-parametric, probabilistic crop suitability model to simulate future cropland expansion and estimate impacts to sage-grouse. We found cropland effects manifest at a spatial scale of 32.2 km2 and a 10 percentage point increase in cropland is associated with a 51% reduction in lek density. Our crop suitability model and stochastic cropland build-outs indicate 5–7% of the remaining population in the US portion of sage-grouse Management Zone I is vulnerable to future cropland conversion under a severe scenario where cropland area expands by 50%. Using metrics of biological value, risk of conversion, and acquisition cost to rank parcels, we found that a US $100 M investment in easements could reduce potential losses by about 80%, leaving just over 1% of the population in the study are vulnerable to cropland expansion. Clustering conservation easements into high-risk landscapes by incorporating landscape-scale vulnerability to conversion into the targeting scheme substantially improved conservation outcomes.

Smith, J.T., J.S. Evans, B.H. Martin, S. Baruch-Mordo, J.M. Kiesecker, and D.E. Naugle. 2016. Reducing cultivation risk for at-risk species: predicting outcomes of conservation easements for sage-grouse. Biological Conservation 201:10-19. https://doi.org/10.1016/j.biocon.2016.06.006


14. Mule deer and pronghorn migration in western Wyoming

Migratory mule deer (Odocoileus hemionus) and pronghorn (Antilocapra americana) populations rely on seasonal ranges to meet their annual nutritional and energetic requirements. Because seasonal ranges often occur great distances apart and across a mix of vegetation types and land ownership, maintaining migration corridors to and from these ranges can be difficult, especially if managers do not have detailed information on mule deer and pronghorn seasonal movements. We captured, radiomarked, and monitored mule deer (n = 171) and pronghorn (n = 34) in western Wyoming to document seasonal distribution patterns and migration routes. Mule deer and pronghorn migrated 20–158 km and 116–258 km, respectively, between seasonal ranges. These distances represented the longest recorded migrations for either species. We identified a number of bottlenecks along the migration routes of mule deer and pronghorn, but the most critical appeared to be the 1.6‐km‐wide Trapper’s Point bottleneck, which was used by both mule deer and pronghorn during their spring and autumn migrations. Housing developments and roadways apparently have reduced the effective width of this bottleneck to < 0.8 km. We estimate 2,500‐3,500 mule deer and 1,500‐2,000 pronghorn move through the bottleneck twice a year during spring and autumn migrations. Identification and protection of migration corridors and bottlenecks will be necessary to maintain mule deer and pronghorn populations throughout their range.

Sawyer, H., F. Lindzey, and D. McWhirter. 2005. Mule deer and pronghorn migration in western Wyoming. Wildlife Society Bulletin 33:1266-1273. https://doi.org/10.2193/0091-7648(2005)33[1266:MDAPMI]2.0.CO;2


15. Measuring the effectiveness of conservation: a novel framework to quantify the benefits of sage-grouse conservation policy and easements in Wyoming

Increasing energy and housing demands are impacting wildlife populations throughout western North America. Greater sage-grouse (Centrocercus urophasianus), a species known for its sensitivity to landscape-scale disturbance, inhabits the same low elevation sage-steppe in which much of this development is occurring. Wyoming has committed to maintain sage-grouse populations through conservation easements and policy changes that conserves high bird abundance “core” habitat and encourages development in less sensitive landscapes. In this study, we built new predictive models of oil and gas, wind, and residential development and applied build-out scenarios to simulate future development and measure the efficacy of conservation actions for maintaining sage-grouse populations. Our approach predicts sage-grouse population losses averted through conservation action and quantifies return on investment for different conservation strategies. We estimate that without conservation, sage-grouse populations in Wyoming will decrease under our long-term scenario by 14-29% (95% CI: 4-46%). However, a conservation strategy that includes the “core area” policy and $250 million in targeted easements could reduce these losses to 9-15% (95% CI: 3-32%), cutting anticipated losses by roughly half statewide and nearly two-thirds within sage-grouse core breeding areas. Core area policy is the single most important component, and targeted easements are complementary to the overall strategy. There is considerable uncertainty around the magnitude of our estimates; however, the relative benefit of different conservation scenarios remains comparable because potential biases and assumptions are consistently applied regardless of the strategy. There is early evidence based on a 40% reduction in leased hectares inside core areas that Wyoming policy is reducing potential for future fragmentation inside core areas. Our framework using build-out scenarios to anticipate species declines provides estimates that could be used by decision makers to determine if expected population losses warrant ESA listing.

Copeland, H., A. Pocewicz, D.E. Naugle, T. Griffiths, D. Keinath, J. Evans, and J. Platt. 2013. Measuring the effectiveness of conservation: a novel framework to quantify the benefits of sage-grouse conservation policy and easements in Wyoming. PLoS One 8:e67261. https://doi.org/10.1371/journal.pone.0067261


16. Conserving migratory mule deer through the umbrella of sage-grouse

Conserving migratory ungulates in increasingly human‐dominated landscapes presents a difficult challenge to land managers and conservation practitioners. Nevertheless, ungulates may receive ancillary benefits from conservation actions designed to protect species of greater conservation priority where their ranges are sympatric. Greater Sage‐Grouse (Centrocerus urophasianus), for example, have been proposed as an umbrella species for other sagebrush (Artemesia spp.)‐dependent fauna. We examined a landscape where conservation efforts for sage‐grouse overlap spatially with mule deer (Odocoileus hemionus) to determine whether sage‐grouse conservation measures also might protect important mule deer migration routes and seasonal ranges. We conducted a spatial analysis to determine what proportion of migration routes, stopover areas, and winter ranges used by mule deer were located in areas managed for sage‐grouse conservation. Conservation measures overlapped with 66–70% of migration corridors, 74–75% of stopovers, and 52–91% of wintering areas for two mule deer populations in the upper Green River Basin of Wyoming. Of those proportions, conservation actions targeted towards sage‐grouse accounted for approximately half of the overlap in corridors and stopover areas, and nearly all overlap on winter ranges, indicating that sage‐grouse conservation efforts represent an important step in conserving migratory mule deer. Conservation of migratory species presents unique challenges because although overlap with conserved lands may be high, connectivity of the entire route must be maintained as barriers to movement anywhere within the migration corridor could render it unviable. Where mule deer habitats overlap with sage‐grouse core areas, our results indicate that increased protection is afforded to winter ranges and migration routes within the umbrella of sage‐grouse conservation, but this protection is contingent on concentrated developments within core areas not intersecting with high‐priority stopovers or corridors, and that the policy in turn does not encourage development on deer ranges outside of core areas. With the goal of protecting entire migration routes, our analysis highlights areas of potential conservation focus for mule deer, which are characterized by high exposure to residential development and use by a large proportion of migrating deer.

Copeland, H., H. Sawyer, K.L. Monteith, D.E. Naugle, A. Pocewicz, N. Graf, and M.J. Kauffman. 2014. Conserving migratory mule deer through the umbrella of sage-grouse. Ecosphere 5:art117. https://doi.org/10.1890/ES14-00186.1


17. Thinking like a grassland: challenges and opportunities for biodiversity conservation in the Great Plains of North America

Fauna of North America’s Great Plains evolved strategies to contend with the region’s extreme spatiotemporal variability in weather and low annual primary productivity. The capacity for large-scale movement (migration and/or nomadism) enables many species, from bison to lark buntings, to track pulses of productivity at broad spatial scales (> 1 000 km2). Furthermore, even sedentary species often rely on metapopulation dynamics over extensive landscapes for long-term population viability. The current complex pattern of land ownership and use of Great Plains grasslands challenges native species conservation. Approaches to managing both public and private grasslands, frequently focused at the scale of individual pastures or ranches, limit opportunities to conserve landscape-scale processes such as fire, animal movement, and metapopulation dynamics. Using the US National Land Cover Database and Cropland Data Layers for 2011−2017, we analyzed land cover patterns for 12 historical grassland and savanna communities (regions) within the US Great Plains. On the basis of the results of these analyses, we highlight the critical contribution of restored grasslands to the future conservation of Great Plains biodiversity, such as those enrolled in the Conservation Reserve Program. Managing disturbance regimes at larger spatial scales will require acknowledging that, where native large herbivores are absent, domestic livestock grazing can function as a central component of Great Plains disturbance regimes if they are able move at large spatial scales and coexist with a diverse array of native flora and fauna. Opportunities to increase the scale of grassland management include 1) spatial prioritization of grassland restoration and reintroduction of grazing and fire, 2) finding creative approaches to increase the spatial scale at which fire and grazing can be applied to address watershed to landscape-scale objectives, and 3) developing partnerships among government agencies, landowners, businesses, and conservation organizations that enhance cross-jurisdiction management and address biodiversity conservation in grassland landscapes, rather than pastures.

Augustine, D., A. Davidson, K. Dickinson, and B. Van Pelt. In Press. Thinking like a grassland: challenges and opportunities for biodiversity conservation in the Great Plains of North America. Rangeland Ecology and Management. https://doi.org/10.1016/j.rama.2019.09.001


18. Land use decisions after the Conservation Reserve Program: re-enrollment, reversion, and persistence in the southern Great Plains

The temperate grasslands of North America remain one of the most modified and threatened ecosystems on the planet. In the United States, the conservation of grassland‐dependent wildlife continues to be challenged by the widespread conversion of privately owned grasslands to cropland. Recent analyses indicate that land exiting the Conservation Reserve Program (CRP), the country’s largest private lands conservation program, is a primary source of grassland conversion. In this mixed‐methods study, we employed focus groups and mail surveys to understand the decisions made by landowners in the southern Great Plains as their CRP contracts near expiration and up to 7 years following expiration. We explored both the post‐contract intentions of landowners with fields currently enrolled in CRP and the self‐reported, post‐contract decisions of landowners whose CRP contracts expired between 2011 and 2017. Interest in re‐enrolling in CRP upon contract expiration was high among landowners with current fields; however, over half of landowners with former CRP fields reported being unable to re‐enroll when they tried. We found higher rates of grassland persistence than have been previously reported, but also detected temporal patterns that suggest that cropland reversion is increasingly likely as the time since contract expiration increases. This study highlights the need for increased attention to the barriers that preclude transition into other conservation programs following CRP and more detailed understanding of what drives landowner decision‐making about re‐enrollment and post‐CRP land use. These insights will be critical for increasing the effectiveness of programs for enduring grassland conservation on private lands.

Barnes, J.C., M. Sketch, A.R. Gramza, M.G. Sorice, R. Iovanna, and A.A. Dayer. 2020. Land use decisions after the Conservation Reserve Program: re-enrollment, reversion, and persistence in the southern Great Plains. Conservation Science and Practice 2:e254. https://doi.org/10.1111/csp2.254


19. Landowners and the Conservation Reserve Program: understanding needs and motivations to cultivate participation, retention, and ongoing stewardship behavior

Barnes, J.C., A.A. Dayer, M. Sketch, A. Gramza, T. Nocera, A. Steinmetz, and M.G. Sorice. 2019. Landowners and the Conservation Reserve Program: understanding needs and motivations to cultivate participation, retention, and ongoing stewardship behavior. Virginia Tech Department of Fish and Wildlife Conservation. http://hdl.handle.net/10919/88444


20. Beyond protected areas: private lands and public policy anchor intact pathways for multi-species wildlife migration

Migration is a critical strategy in maintaining populations, and pathways used by individuals lend insight into habitat quality and connectivity. Yet sustaining migration among large-ranging wildlife poses a challenge for conservation, particularly among landscapes that include a diverse matrix of land tenure. Such is the case in the Northern Great Plains (NGP), a sagebrush (Artemisia spp.) steppe and grassland ecosystem that is home to the longest-ever recorded migrations by both pronghorn (Antilocapra americana) and greater sage-grouse (Centrocercus urophasianus). Here, we identify migratory pathways for both species, and measure the ability of current conservation and policy to maintain cross-taxa migration in the face of continued cultivation. Migratory behavior was similar between species in their timing and duration of migration, and in their use of stopovers along the way. Large and intact private and public working lands largely underpinned migratory pathways, whereas protected areas provided another 5% of habitats. Most pathways for sage-grouse were within state- and federally-designated sage-grouse Core Areas, which contain regulatory caps on anthropogenic disturbance on public lands and help guide conservation efforts; these benefits extended to over half of pathways used by pronghorn. Among private lands, both species largely migrated through intact grazing lands, including many that were already perpetually protected from cultivation with conservation easements. Optimization of remaining private parcels provides managers with a spatial tool to prioritize private-lands conservation, and suggests that comprehensive conservation of shared migratory pathways for pronghorn and sage-grouse in the NGP is within reach of completion given the ongoing pace of conservation.

Tack, J.D., A.F. Jakes, P.F. Jones, J.T. Smith, R.E. Newton, B.H. Martin, M. Hebblewhite, and D.E. Naugle. 2019. Beyond protected areas: private lands and public policy anchor intact pathways for multi-species wildlife migration. Biological Conservation 234:18-27. https://doi.org/10.1016/j.biocon.2019.03.017


21. The nebulous ecology of native invasions

For much of the 21st century, and before, scientists from around the world have reported the occurrence of populations of native plant species establishing and spreading outside historical plant communities. In general, native plant invasions were considered small scale and driven by local land use. However, on review of the subject literature it becomes evident that native plant invasions are in fact very widespread, often very large, and often independent of local land-use changes, driven rather by global climate. Currently, policy for and management of ecological systems focuses on alien invasive plant species, in part because of the widespread awareness of the impacts of alien plant species. Considerably less attention has been given to invasive native plant species, even when the impacts are structurally and functionally similar to those of invasive alien plant species. In the Anthropocene, alien species are no longer the only category of biological organism establishing and rapidly spreading beyond historical boundaries. We review evidence showing that invasions by native species are a global phenomenon and present case studies from Southern Africa, and elsewhere, that reveal how climate-mediated expansions of native plants into adjacent communities can emulate the functional and structural changes associated with invasions by alien plant species. We conclude that integrating native invasions into ecological practice and theory will improve mechanistic models and better inform policy and adaptive ecological management in the 21st century.

Nackley, L.L., A.G. West, A.L. Skowno, and W.J. Bond. 2017. The nebulous ecology of native invasions. Trends in Ecology and Evolution 32:814-824. https://doi.org/10.1016/j.tree.2017.08.003


22. Characteristics of sagebrush habitats and limitations to long-term conservation

Miller, R.F., S.T. Knick, D.A. Pyke, C.W. Meinke, S.E. Hanser, M.J. Wisdom, A.L. Hild. 2011. Characteristics of sagebrush habitats and limitations to long-term conservation. In: Knick ST, Connelly JW, Eds. Greater sage-grouse: ecology and conservation of a landscape species and its habitats. Studies in Avian Biology, Vol. 38. Berkeley, CA: University of California Press. p. 145–185. https://www.jstor.org/stable/10.1525/j.ctt1ppq0j


23. Conifer expansion. Chapter 12 in Sagebrush Ecosystem Conservation Strategy

Maestas, J.D., D.E. Naugle, J.C. Chambers, J.D. Tack, C.S. Boyd, J.M. Tague. 2020. Conifer expansion. Chapter 12 in Sagebrush Ecosystem Conservation Strategy. Western Association of Fish and Wildlife Agencies.


24. Quantifying pinyon-juniper reduction within North America’s sagebrush ecosystem

One of the primary conservation threats surrounding sagebrush (Artemisia spp.) ecosystems in the Intermountain West of the United States is the expansion and infilling of pinyon pine (Pinus edulis, P. monophylla) and juniper (Juniperus spp.) woodlands. Woodland expansion into sagebrush ecosystems has demonstrated impacts on sagebrush-associated flora and fauna, particularly the greater sage-grouse (Centrocercus urophasianus). These impacts have prompted government agencies, land managers, and landowners to ramp up pinyon-juniper removal efforts to maintain and restore sagebrush ecosystems. Accurately quantifying and analyzing management activities over time across broad spatial extents still poses a major challenge. Such information is vital to broad-scale planning and coordination of management efforts. To address this problem and aid future management planning, we applied a remote sensing change detection approach to map reductions in pinyon-juniper cover across the sage-grouse range and developed a method for rapidly updating maps of canopy cover. We found total conifer reduction over the past several yr (2011−2013 to 2015−2017) amounted to 1.6% of the area supporting tree cover within our study area, which is likely just keeping pace with estimates of expansion. Two-thirds of conifer reduction was attributed to active management (1.04% of the treed area) while wildfire accounted for one-third of all estimated conifer reduction in the region (0.56% of the treed area). Our results also illustrate the breadth of this management effort—crossing ownership, agency, and state boundaries. We conclude by identifying some key priorities that should be considered in future conifer management efforts based on our comprehensive assessment.

Reinhardt, J.R., S. Filippelli, M. Falkowski, B. Allred, J.D. Maestas, J.C. Carlson, and D.E. Naugle. 2020. Quantifying pinyon-juniper reduction within North America’s sagebrush ecosystem. Rangeland Ecology and Management 73:420-432. https://doi.org/10.1016/j.rama.2020.01.002


25. Saving sage-grouse from the trees: a proactive solution to reducing a key threat to a candidate species

Conservation investment in management of at-risk species can be less costly than a delay-and-repair approach implemented after species receive legal protection. The United States Endangered Species Act candidate species designation represents an opportunity to implement proactive management to avoid future listing. Such efforts require substantial investments, and the challenge becomes one of optimization of limited conservation funds to maximize return. Focusing on conifer encroachment threats to greater sage-grouse (Centrocercus urophasianus), we demonstrated an approach that links species demographics with attributes of conservation threats to inform targeting of investments. We mapped conifer stand characteristics using spatial wavelet analysis, and modeled lek activity as a function of conifer-related and additional lek site covariates using random forests. We applied modeling results to identify leks of high management potential and to estimate management costs. Results suggest sage-grouse incur population-level impacts at very low levels of encroachment, and leks were less likely to be active where smaller trees were dispersed. We estimated costs of prevention (treating active leks in jeopardy) and restoration (treating inactive leks with recolonization potential) management across the study area (2.5 million ha) at a total of US$17.5 million, which is within the scope of landscape-level conservation already implemented. An annual investment of US$8.75 million can potentially address encroachment issues near all known Oregon leks within the next decade. Investments in proactive conservation with public and private landowners can increase ecosystem health to benefit species conservation and sustainable land uses, replace top-down regulatory approaches, and prevent conservation reliance of at-risk species.

Baruch-Mordo, S., J.S. Evans, J.P. Severson, D.E. Naugle, J.D. Maestas, J.M. Kiesecker, M.J. Falkowski, C.A. Hagen, and K.P. Reese. 2013. Saving sage-grouse from the trees: a proactive solution to reducing a key threat to a candidate species. Biological Conservation 167:233-241. https://doi.org/10.1016/j.biocon.2013.08.017


26. Pinyon and juniper encroachment into sagebrush ecosystems impacts distribution and survival of greater sage-grouse

In sagebrush (Artemisia spp.) ecosystems, encroachment of pinyon (Pinus spp.) and juniper (Juniperus spp.; hereafter, “pinyon-juniper”) trees has increased dramatically since European settlement. Understanding the impacts of this encroachment on behavioral decisions, distributions, and population dynamics of greater sage-grouse (Centrocercus urophasianus) and other sagebrush obligate species could help benefit sagebrush ecosystem management actions. We employed a novel two-stage Bayesian model that linked avoidance across different levels of pinyon-juniper cover to sage-grouse survival. Our analysis relied on extensive telemetry data collected across 6 yr and seven subpopulations within the Bi-State Distinct Population Segment (DPS), on the border of Nevada and California. The first model stage indicated avoidance behavior for all canopy cover classes on average, but individual grouse exhibited a high degree of heterogeneity in avoidance behavior of the lowest cover class (e.g., scattered isolated trees). The second stage modeled survival as a function of estimated avoidance parameters and indicated increased survival rates for individuals that exhibited avoidance of the lowest cover class. A post hoc frailty analysis revealed the greatest increase in hazard (i.e., mortality risk) occurred in areas with scattered isolated trees consisting of relatively high primary plant productivity. Collectively, these results provide clear evidence that local sage-grouse distributions and demographic rates are influenced by pinyon-juniper, especially in habitats with higher primary productivity but relatively low and seemingly benign tree cover. Such areas may function as ecological traps that convey attractive resources but adversely affect population vital rates. To increase sage-grouse survival, our model predictions support reducing actual pinyon-juniper cover as low as 1.5%, which is lower than the published target of 4.0%. These results may represent effects of pinyon-juniper cover in areas with similar ecological conditions to those of the Bi-State DPS, where populations occur at relatively high elevations and pinyon-juniper is abundant and widespread.

Coates, P.S., B.G. Prochazka, M.A. Ricca, K.B. Gustafson, P. Ziegler, and M.L. Casazza. 2017. Pinyon and juniper encroachment into sagebrush ecosystems impacts distribution and survival of greater sage-grouse. Rangeland Ecology and Management 70:25-38. https://doi.org/10.1016/j.rama.2016.09.001


27. Understory cover responses to pinon–juniper treatments across tree dominance gradients in the Great Basin

Piñon (Pinus spp.) and juniper (Juniperus spp.) trees are reduced to restore native vegetation and avoid severe fires where they have expanded into sagebrush (Artemisia tridentata Nutt.) communities. However, what phase of tree infilling should treatments target to retain desirable understory cover and avoid weed dominance? Prescribed fire and tree felling were applied to 8–20-ha treatment plots at 11 sites across the Great Basin with a tree-shredding treatment also applied to four Utah sites. Treatments were applied across a tree infilling gradient as quantified by a covariate tree dominance index (TDI = tree cover/&lsqb;tree + shrub + tall perennial grass cover]). Mixed model analysis of covariance indicated that treatment × covariate interactions were significant (P &spilt; 0.05) for most vegetation functional groups 3 yr after treatment. Shrub cover was most reduced with fire at any TDI or by mechanical treatment after infilling resulted in over 50% shrub cover loss (TDI &spigt; 0.4). Fire increased cheatgrass (Bromus tectorum L.) cover by an average of 4.2% for all values of TDI. Cutting or shredding trees generally produced similar responses and increased total perennial herbaceous and cheatgrass cover by an average of 10.2% and 3.8%, at TDIs ≥ 0.35 and ≥ 0.45. Cheatgrass cover estimated across the region was &spilt; 6% after treatment, but two warmer sites had high cheatgrass cover before (19.2% and 27.2%) and after tree reduction (26.6% and 50.4%). Fuel control treatments are viable management options for increasing understory cover across a range of sites and tree cover gradients, but should be accompanied by revegetation on warmer sites with depleted understories where cheatgrass is highly adapted. Shrub and perennial herbaceous cover can be maintained by mechanically treating at lower TDI. Perennial herbaceous cover is key for avoiding biotic and abiotic thresholds in this system through resisting weed dominance and erosion.

Roundy, B. A., R. F. Miller, R. J. Tausch, K. Young, A. Hulet, B. Rau, B. Jessop, J. C. Chambers, and D. Egget. 2014. Understory cover responses to pinon–juniper treatments across tree dominance gradients in the Great Basin. Rangeland Ecology and Management 67:482–494. https://doi.org/10.2111/REM-D-13-00018.1


28. Herbaceous response to cattle grazing following juniper cutting in Oregon

The rapid expansion of western juniper (Juniperus occidentalis spp. occidentalis Hook.) across the northern Great Basin has diminished shrub and understory plant composition and reduced forage production. Juniper removal has accelerated during the past decade in Oregon and California to restore shrub–steppe plant communities. Livestock grazing can affect posttreatment successional dynamics, but these impacts have not received adequate study. This study evaluated herbaceous plant recovery in a cut western juniper woodland subjected to grazed and ungrazed prescriptions over 4 growing seasons. The study consisted of 4 treatments: ungrazed cut, grazed cut, ungrazed woodland, and grazed woodland. Stocking rates were 0.78 cow–calf pairs per ha for 5 days in the first year following treatment and 0.94 cow–calf pairs per ha for 4 days in the second year after treatment. The grazing portion of the study lacked true replication because grazed plots were not independent of each other (cattle had access to all plots simultaneously). This limits the strength and interpretation of the grazing results. Juniper cutting removed overstory interference and resulted in significant increases in herbaceous cover, biomass, and seed production when compared to adjacent woodlands. Herbaceous cover, standing crop, perennial grass density, and seed production all increased in the ungrazed cut treatment compared to ungrazed woodland. A similar level of response was measured in the grazed pasture where herbaceous responses were greater in the grazed cut vs. the grazed woodland. Grazing in the cut treatment did not limit herbaceous recovery except that perennial grass seed production was lower in the grazed cut than in the ungrazed cut. Rest or deferment is required the first several growing seasons after juniper cutting to provide plants the opportunity to maximize seed crops. These results imply that juniper cutting had a greater effect on herbaceous dynamics than did the grazing application.

Bates, J. D. 2005. Herbaceous response to cattle grazing following juniper cutting in Oregon. Rangeland Ecology and Management 58:225-233. https://doi.org/10.2111/1551-5028(2005)58[225:HRTCGF]2.0.CO;2


29. Reversing tree expansion in sagebrush steppe yields population level benefit for imperiled grouse

Olsen, A.C., J.P. Severson, J.D. Maestas, D.E. Naugle, J.T. Smith, J.D. Tack, K.H. Yates, and C.A. Hagen. 2021. Reversing tree expansion in sagebrush steppe yields population level benefit for imperiled grouse. Ecosphere: In Press.


30. Bird responses to removal of western juniper in sagebrush-steppe

We investigated bird abundance in response to western juniper (Juniperus occidentalis) removal using a short-term chronosequence approach and generated estimates of density and responses to management for the most abundant species. Stands targeted for tree removal were primarily in the middle stages of juniper encroachment (Phase II, 7 851 ha). Trees were removed using hand felling combined with either lop and scatter, single tree burning, or jackpot burning, which were carried out to minimize loss of shrub cover. Brewer’s sparrow (Spizella breweri) density was greater at treated versus untreated portions of the study area. At sites in the third year following tree removal, Brewer’s sparrow density was 23.6 (95% confidence interval [CI]: 19.4–27.8) territories per km2 higher than locations that had not yet been treated. This equates to a net increase of 1 212 − 1 737 nesting pairs within the project area. Green-tailed towhee increased by 4.6 (95% CI: 3.1–6.1) territories per km2 for an estimated project-wide increase of 194–381 nesting pairs, and vesper sparrow (Poocetes gramineus) increased by 6.5 (95% CI: 4.6–8.4) territories per km2 corresponding to an estimated increase of 460–559 nesting pairs within the project area. Density of gray flycatcher (Empidonax wrighti) was lower in cut areas, and over the entire project area we estimate a net loss of 183–486 nesting pairs as a result of juniper tree removal. This study demonstrates that conifer removal projects designed to retain shrub cover and structure can have benefits to multiple species of ground and shrub nesting birds, including several species of conservation concern.

Holmes, A.L., J.D. Maestas, and D.E. Naugle. 2017. Bird responses to removal of western juniper in sagebrush-steppe. Rangeland ecology and management 70:87-94. https://doi.org/10.1016/j.rama.2016.10.006


31. Habitat management influences overwinter survival of mule deer fawns in Colorado

In the absence of natural or anthropogenic disturbance, many pinyon pine (Pinus edulis)–Utah juniper (Juniperus osteosperma) woodland habitats reach late seral stages that encroach into forest openings. This encroachment typically occurs at the expense of browse species that are preferred by mule deer (Odocoileus hemionus). Wildlife managers often treat habitat management as a tool to bolster mule deer populations, but documented changes in deer vital rates in response to habitat manipulations are lacking. We evaluated the effects of different levels of habitat improvement on pinyon pine–Utah juniper winter ranges in Colorado on mule deer overwinter survival. Mule deer fawns that overwintered on areas that received both a traditional mechanical treatment as well as follow‐up chemical treatments experienced increased survival (urn:x-wiley:0022541X:media:jwmg683:jwmg683-math-0001 = 0.768, SE = 0.0851) over fawns on winter range that had only received traditional mechanical treatments or no habitat treatments (urn:x-wiley:0022541X:media:jwmg683:jwmg683-math-0002 = 0.675, SE = 0.112). When treatment intensity was partitioned into 3 levels: no treatment, traditional mechanical treatments, and advanced treatments comprised of both mechanical and chemical treatments, mule deer fawns inhabiting winter range subjected to advanced treatments experienced higher survival (urn:x-wiley:0022541X:media:jwmg683:jwmg683-math-0003 = 0.768, SE = 0.0849) than fawns on units that experienced only traditional mechanical treatments (urn:x-wiley:0022541X:media:jwmg683:jwmg683-math-0004 = 0.687, SE = 0.108), which in turn experienced higher survival than fawns in areas that had received no habitat treatments (urn:x-wiley:0022541X:media:jwmg683:jwmg683-math-0005 = 0.669, SE = 0.113). Our study provides evidence that habitat management on winter ranges can positively influence a key vital rate for mule deer in pinyon pine–Utah juniper ecosystems. We recommend that as habitat treatments are planned for benefit of mule deer, those plans include follow‐up reseeding and weed control efforts.

Bergman, E.J., C.J. Bishop, D.J. Freddy, G.C. White, and P.F. Doherty, Jr. 2014. Habitat management influences overwinter survival of mule deer fawns in Colorado. Journal of Wildlife Management 78:448-455. https://doi.org/10.1002/jwmg.683


32. Wildlife habitats in managed rangelands - the Great Basin of southeastern Oregon

Management practices and options to provide habitat for wildlife in the Great Basin of southeastern Oregon deal with both vegetation treatment and protection, livestock management, maintenance or distribution of water developments, protection of wildlife areas through road closures or fencing, and direct manipulation of wildlife through hunting, trapping, or other means. This chapter deals primarily with livestock management in relationship to wildlife and wildlife habitat. Included are discussions of ecological status (range condition), livestock management, multiple-use options for each species featured in previous chapters (trout, sage grouse, pronghorn, mule deer, and bighorn sheep), and diversity.

Thomas, J.W., C. Maser, J.E. Rodiek. 1979. Wildlife habitats in managed rangelands - the Great Basin of southeastern Oregon. Riparian Zones. USDA Forest Serv. Gen. Tech. Rep. PNW-80. https://www.srs.fs.usda.gov/pubs/gtr/gtr_pnw080.pdf


33. Public lands and private waters: scarce mesic resources structure land tenure and sage-grouse distributions

Water scarcity in semiarid environments provides a model system to evaluate the role of mesic resources in structuring the distribution and abundance of wildlife. We used remote sensing and point process analyses to evaluate spatio–temporal variability in limited mesic resources in relation to greater sage‐grouse (Centrocercus urophasianus) distributions in Oregon, California, and northwest Nevada, USA, 1984–2011. We then link population distribution to changes in resource availability over time, space, and land tenure. Despite encompassing only 2.4% of landscape area, mesic sites influenced sage‐grouse breeding distributions as evidenced by significantly shorter lek to mesic resource distances in observed (5.3 km) vs. predicted (8.2 km) values. Population abundance increased with proximity to mesic sites. Lag effects evident in abundance and proximity trends of mesic resources suggest a level of drought tolerance that moderated climatic variability. Mesic abundance and proximity remained relatively stable during the study period in comparison to more dynamic climatic patterns. Drought effects were most pronounced during multiyear events as evidenced by the 1987–1992 period that decreased mesic abundance >25% and approximately doubled mean lek to mesic resource distances (4.8–8.3 km). In our study area, 75% of all mesic resources were in private ownership, where the predominant land use is livestock ranching. Results suggest a holistic conservation strategy inclusive of private and public lands is needed to ensure sage‐grouse habitat requisites are met throughout the life cycle of this landscape species.

Donnelly, J.P., D.E. Naugle, C.A. Hagen, and J.D. Maestas. 2016. Public lands and private waters: scarce mesic resources structure land tenure and sage-grouse distributions. Ecosphere e01208. https://doi.org/10.1002/ecs2.1208


34. Mesic habitat conservation planning guide

Natural Resources Conservation Service (NRCS). 2017. Mesic habitat conservation planning guide. https://www.sagegrouseinitiative.com/wp-content/uploads/2017/04/Mesic_Habitat_Conservation_Planning_Guide1.pdf


35. Let the water do the work: induced meandering, an evolving method for restoring incised channels

Zeedyk B., V. Clothier. 2009. Let the water do the work: induced meandering, an evolving method for restoring incised channels. Chelsea Green Publishing, White River Junction, VT https://www.chelseagreen.com/product/let-the-water-do-the-work/


36. Smokey the beaver: Beaver-dammed riparian corridors stay green during wildfire throughout the western USA

Beaver dams are gaining popularity as a low‐tech, low‐cost strategy to build climate resiliency at the landscape scale. They slow and store water that can be accessed by riparian vegetation during dry periods, effectively protecting riparian ecosystems from droughts. Whether or not this protection extends to wildfire has been discussed anecdotally but has not been examined in a scientific context. We used remotely sensed Normalized Difference Vegetation Index (NDVI) data to compare riparian vegetation greenness in areas with and without beaver damming during wildfire. We include data from five large wildfires of varying burn severity and dominant landcover settings in the western United States in our analysis. We found that beaver‐dammed riparian corridors are relatively unaffected by wildfire when compared to similar riparian corridors without beaver damming. On average, the decrease in NDVI during fire in areas without beaver is 3.05 times as large as it is in areas with beaver. However, plant greenness rebounded in the year after wildfire regardless of beaver activity. Thus, we conclude that, while beaver activity does not necessarily play a role in riparian vegetation post‐fire resilience, it does play a significant role in riparian vegetation fire resistance and refugia creation.

Fairfax E., A. Whittle. 2020. Smokey the beaver: Beaver-dammed riparian corridors stay green during wildfire throughout the western USA. Ecol Appl. https://doi.org/10.1002/eap.2225


37. Low‐tech riparian and wet meadow restoration increases vegetation productivity and resilience across semi‐arid rangelands

Restoration of riparian and wet meadow ecosystems in semiarid rangelands of the western United States is a high priority given their ecological and hydrological importance in the region. However, traditional restoration approaches are often intensive and costly, limiting the extent over which they can be applied. Practitioners are increasingly trying new restoration techniques that are more cost‐effective, less intensive, and can more practically scale up to the scope of degradation. Unfortunately, practitioners typically lack resources to undertake outcome‐based evaluations necessary to judge the efficacy of these techniques. In this study, we use freely available, satellite remote sensing to explore changes in vegetation productivity (normalized difference vegetation index) of three distinct, low‐tech, riparian and wet meadow restoration projects. Case studies are presented that range in geographic location (Colorado, Oregon, and Nevada), restoration practice (Zeedyk structures, beaver dam analogs, and grazing management), and time since implementation. Restoration practices resulted in increased vegetation productivity of up to 25% and increased annual persistence of productive vegetation. Improvements in productivity with time since restoration suggest that elevated resilience may further enhance wildlife habitat and increase forage production. Long‐term, documented outcomes of conservation are rare; we hope our findings empower practitioners to further monitor and explore the use of low‐tech methods for restoration of ecohydrologic processes at meaningful spatial scales.

Silverman N.L., B.W. Allred, J.P. Donnelly, T.B. Chapman, J.D. Maestas, J.M. Wheaton, J. White, D.E. Naugle. 2018. Low‐tech riparian and wet meadow restoration increases vegetation productivity and resilience across semi‐arid rangelands. Rest Ecol 27(2):269-278. https://doi.org/10.1111/rec.12869


38. Low-tech process-based restoration of riverscapes: design manual

The purpose of this design manual is to provide restoration practitioners with guidelines for implementing a subset of low-tech tools —namely beaver dam analogues (BDAs) and post-assisted log structures (PALS)—for initiating process-based restoration in structurally-starved riverscapes. While the concept of process-based restoration in riverscapes has been advocated for at least two decades, details and specific examples on how to implement it remain sparse. Here, we describe ‘low-tech process-based restoration’ (LT-PBR) as a practice of using simple, low unit-cost, structural additions (e.g. wood and beaver dams) to riverscapes to mimic functions and initiate specific processes. Hallmarks of this approach include: - An explicit focus on the processes that a low-tech restoration intervention is meant to promote - A conscious effort to use cost-effective, low-tech treatments (e.g. hand-built, natural materials, non-engineered, short-term design life-spans) because of the need to efficiently scale-up application. - ‘Letting the system do the work’ which defers critical decision making to riverscapes and nature’s ecosystem engineers. Other resources available at: http://lowtechpbr.restoration.usu.edu

Wheaton J.M., S.N. Bennett, N. Bouwes, J.D. Maestas, S.M. Shahverdian (eds). 2019. Low-tech process-based restoration of riverscapes: design manual. Version 1.0. Utah State University Restoration Consortium. Logan, UT. http://dx.doi.org/10.13140/RG.2.2.19590.63049/2