On the Cutting Edge of Research to Conserve At-Risk Species: Maximizing Impact through Partnerships

On the Cutting Edge of Research to Conserve At-Risk Species: Maximizing Impact through Partnerships Abstract Today’s conservation challenges are complex. Solving these challenges often requires scientific collaborations that extend beyond the scope, expertise, and capacity of any single agency, organization, or institution. Conservation efforts can benefit from interdisciplinary collaboration, scientific and technological innovations, and the leveraging of capacity and resources among partners. Here we explore a series of case studies demonstrating how collaborative scientific partnerships are furthering the mission of the US Fish and Wildlife Service (USFWS), including: (1) contaminants of emerging concern in the Great Lakes Basin, (2) Poweshiek skipperling conservation, (3) using technology to improve population survey methods for bats and monarch butterfly, and (4) Big River restoration in the Southeast Missouri lead mining district. These case studies illustrate how strategic and effective scientific collaboration is a multi-stage process that requires investment of time and resources by all participants. Early coordination and communication is crucial to aligning planned work with scientific and decision-making needs. Collaborations between USFWS and external scientists can be mutually beneficial by supporting the agency mission while also providing an avenue for innovative research to be directly applied in conservation decisions and management actions. Introduction The US Fish and Wildlife Service (USFWS) manages National Wildlife Refuges, protects and recovers endangered species, manages migratory birds, conserves nationally significant fisheries, and enforces federal wildlife laws. Many of the conservation challenges faced by the USFWS necessitate active engagement of stakeholders and scientific experts to achieve the agency mission. Notably, the agency mission of the USFWS—working with others to conserve, protect, and enhance fish, wildlife, and plants and their habitats for the continuing benefit of the American people—emphasizes the involvement of partners in the conservation of the nation’s natural resources. All USFWS programs have a role in accomplishing the agency mission. Programs such as Ecological Services, Migratory Birds, and Fish and Aquatic Conservation do so through implementation of policy, development of conservation and restoration strategies, restoration and protection of habitats and species, and evaluation of the success of conservation actions and strategies. There is a scientific basis to all of these activities. Whereas the USFWS workforce maintains a wide breadth of scientific expertise, the agency does not house experts in all necessary fields to address all possible complex and emerging conservation issues and thus often relies on external scientists to serve as technical experts (USFWS 1994). Furthermore, conservation and recovery efforts often benefit from input from diverse perspectives and skill sets offered by a combination of agency and external scientists (Asquith 2001; Boersma et al. 2001; Gerber and Schultz 2001; Stinchcombe et al. 2002). The responsibility of the USFWS to inform policy, conservation strategy, and management decisions with sound science makes collaboration with external scientists instrumental to accomplishing effective conservation. Additionally, many opportunities exist for external scientists to proactively engage the USFWS as a means to move their work from theory to practice. A more complete understanding by academic scientists and students of the breadth of opportunities to interface with agency scientists and subsequent adoption of an effective approach for developing collaborative science partnerships can lead to increased visibility and relevancy of their work to the public. Engagement with external scientists The USFWS interfaces in multiple ways with scientists from numerous sectors of the conservation field, including academic institutions, non-governmental organizations, state agencies, tribes, and other federal agencies. Modes of engagement with external scientists can vary from relatively brief collaborations, which can include data collection exercises, information sharing through meetings, and participation in webinars on topics of mutual interest, to more formalized and complex partnerships focused on developing conservation strategies or original research. In this discussion we distinguish formal or informal collaborative science partnerships from general collaborative activities with external scientists based on a longer duration, shared objectives, and higher level of resource investment by all parties. Collaboration for data collection refers to compiling existing empirical and anecdotal data as well as eliciting and incorporating knowledge and opinion from subject matter experts. Data collection is accomplished through participatory exercises such as working groups and structured expert elicitation. Working groups are formed to address specific conservation issues or prioritization needs through interactive discussions, strategy development, and product creation. The membership of working groups typically includes individuals who are experts in species biology, specialists in applicable laboratory or field methodologies, members of diverse stakeholder groups, and specialists that bring to the effort interdisciplinary and technical skills that are value-added for addressing the issue at hand. Expert elicitation is a data collection process that enables the inclusion of expert opinion and professional judgment while reducing bias, quantifying uncertainty, and allowing for peer review through structured processes (Burgman et al. 2011; Martin et al. 2012; Drescher et al. 2013). Use of expert knowledge is advantageous, or even essential, when empirical data are lacking either because complex conservation issues have not been thoroughly studied or there is an imminent need to understand and act on emerging conservation issues. The latter is often the case when addressing threats to imperiled species. For example, structured expert elicitation has been used in the conservation of at-risk species to rank threats (Donlan et al. 2010), evaluate impacts from specific threats (Frick et al. 2017), and provide parameters to inform demographic population models (Oberhauser et al. 2016). Collaborative science partnerships between the USFWS and external scientists differ from data collection exercises in that they result in generation of data, techniques, and relevant knowledge to further the conservation of federally protected species, at-risk species, or their habitats, as well as to inform restoration and management efforts. Projects can be undertaken to address priority information needs identified by working groups or during expert elicitation, or they can be developed independently by agency biologists and collaborators. Agency scientists and collaborators work together to understand conservation issues, define project goals and objectives, identify useful products and science delivery tools, convene teams of scientists with the expertise to achieve project goals, and secure sufficient financial and logistical support for project implementation. The USFWS invests in priority science initiatives through allocation of funding and in-house scientific expertise. For example, the USFWS has allocated $40 million since 2008 to fund bat and white-nose syndrome (WNS) related surveillance and monitoring, research, and management activities. This includes $30 million in grants to other federal, state, provincial, and non-governmental agencies (https://www.whitenosesyndrome.org/research-monitoring). Additionally, since 2010, the USFWS has managed more than $256 million in funds from the Great Lakes Restoration Initiative (GLRI), both to directly implement conservation as well as to collaborate with partners to address data gaps and evaluate environmental conditions. In addition to funding provided by the agency to support collaborative science initiatives, USFWS scientists actively engage with partners in studies and data analyses to understand species biology, evaluate threats, and develop new techniques and tools. Recent collaborative projects completed in the Midwest Region of the USFWS involving agency scientists include work on: identification and assessment of threats to federally listed and at-risk species and their habitats (ThogMartin et al. 2012a, 2012b, 2013, 2017b; Erickson et al. 2016; Daniel et al. 2017; Strobel and Giorgi 2017); habitat conservation actions (Thogmartin et al. 2017a); adaptive management strategies for federally listed species (Moore et al. 2011); species ecology and distribution (Russell et al. 2014; Clymer and Blanchong 2016); impacts of environmental contaminants on wildlife and natural systems (Simon and Morris 2009; Weber et al. 2015; Simon et al. 2013; Eidels et al. 2016); and large-scale prioritization of conservation actions (Januchowski-Hartley et al. 2013; Daniel et al. 2017). Considerations for developing partnerships Establishing strategic science partnerships requires an investment of time and resources by all partners and a clear understanding of expectations, goals, resources, and modes of delivery. The early stages of partnership development can be conceptualized as a stepwise process, although the progression is rarely truly linear or the steps strictly sequential. Viewing the process as steps (Fig. 1) ensures that consideration is given to all stages and allows emphasis to be placed on pivotal components as appropriate, such as early communication with resource managers. Fig. 1 View largeDownload slide Partnership development is a cyclical, adaptive process, but the early stages can be viewed in a stepwise manner to facilitate thorough consideration of foundational elements. Communication and engagement between collaborators and USFWS scientists at each stage, from project conceptualization to acquisition of resources, serves to maximize mutual benefits and likelihood of successful implementation. Fig. 1 View largeDownload slide Partnership development is a cyclical, adaptive process, but the early stages can be viewed in a stepwise manner to facilitate thorough consideration of foundational elements. Communication and engagement between collaborators and USFWS scientists at each stage, from project conceptualization to acquisition of resources, serves to maximize mutual benefits and likelihood of successful implementation. The early stages of development, while vital to the overall success of the partnership, can be undervalued and overlooked. For example, it is during the stage of Initial Coordination that agency scientists and external collaborators can engage in active dialog to ensure that future work is relevant to current conservation issues and useful to conservation practitioners. Such early communication facilitates well-aligned research that minimizes the research-implementation gap (Knight et al. 2008) and maximizes the likelihood that research will have an instrumental impact directly influencing policy development, regulatory decisions, or deployment of conservation resources (Rudd et al. 2011; Rudd 2011). Case studies of collaborative science partnerships To illustrate the USFWS’s engagement in interdisciplinary science partnerships that facilitate achievement of the agency mission, we present case studies from the Midwest Region of the USFWS. The case studies highlight some of the contemporary conservation issues faced by the USFWS giving insight into the breadth of the agency’s science needs and providing examples of various ways that external scientists have interfaced with agency scientists. Additionally, the case studies demonstrate how effective, mutually beneficial partnerships directly inform resource management because of deliberative and strategic approaches to development. Contaminants of emerging concern in the Great Lakes Basin The GLRI, launched in 2010, provides guidance and support for actions to help restore and sustain the health of the Great Lakes ecosystem in the Upper Midwest of the United States (https://www.glri.us/). One focus of GLRI is to identify potential impacts to fish and wildlife from contaminants of emerging concern (CECs), including pharmaceuticals, personal care products, and new agricultural and industrial chemicals, and their byproducts. CECs are ubiquitous throughout the Great Lakes, yet in 2010 little was known about their extent and impacts (Choy et al. 2013; Elliott et al. 2017). Biologists from USFWS partnered with other federal and state agencies, academia, and independent specialists to understand the extent of CEC contamination (Phase I 2010–2015) and impacts to natural resources (Phase II 2015–2020) in order to manage and sustain natural resources for current and future generations. Collaborations among federal agencies (e.g., USFWS, US Environmental Protection Agency [EPA], US Geological Survey [USGS], US Army Corps of Engine ers, and National Oceanic and Atmospheric Administration) have created an opportunity to leverage limited resources, harness individual expertise, and address each agency’s mandates while achieving mutual goals. In addition to contributing to the integrated work among federal agencies, USFWS is specifically assessing population-level impacts of CECs to USFWS trust resources including fish, migratory birds, and threatened and endangered (T/E) species. Collaborative work includes ongoing field and laboratory studies to assess how CECs affect reproduction and fitness of various taxa (Thomas et al. 2017; Jorgenson et al. 2018): fish with St. Cloud State University, St. Thomas University, Michigan Department of Natural Resources, and Wisconsin Department of Natural Resources; freshwater mussels with Central Michigan University; and birds with Dr. James Ludwig. Initial studies focused on common species, but new techniques are being developed to allow non-lethal sampling and modeling to assess T/E species. USFWS and partners are using empirical data from laboratory and field studies to evaluate CEC sensitivity, including chemical characterization with Southern Illinois University and cell receptor sensitivity with St. Cloud State University. Modeling exercises are being conducted by the University of Minnesota and Ball State University to validate CEC population impacts, and by USGS to validate watershed hazard assessments by evaluating the presence and occurrence of CECs throughout the Great Lakes Basin. USFWS will use results from the suite of studies to inform resource management decisions by providing sublethal population-level assessments of CEC risks to trust resources, including T/E species. Preliminary results suggest that CECs are contributing to sublethal effects on fish and may lead to population-level declines (Thomas et al. 2017; Jorgenson et al. 2018). Results will be disseminated through outreach to federal, state, tribal, and local natural resource managers and the public. In addition, federal agencies will produce an Integrated Report assessing CEC impacts that provide management recommendations in 2020. Further, USFWS and collaborators are producing peer-reviewed articles for technical audiences. With limited resources, it is more important than ever for resource managers to understand the stressors which may impact vulnerable species populations to help prioritize areas best suited for restoration and conservation efforts. These studies will provide information regarding potential population-level impacts of CECs enabling managers to select optimal conservation and management practices in order to avoid further population declines, future listing of imperiled species, and loss of trust resources for the continued benefit of current and future generations. Lessons learned—GLRI exemplifies how a large, well-coordinated partnership can address complex, large scale conservation issues to achieve the missions of multiple agencies. Implementation of a restoration project with a broad scope requires scientific expertise of equivalent breadth that is harnessed through continuous coordination and clearly defined goals, objectives, and actions. The initiative has been successful through assembly and engagement of numerous, appropriate agencies, and organizations while still capitalizing on the expertise of individual scientific experts. Whereas coordination can present challenges, engagement of an extensive suite of collaborators has maximized the cumulative financial and logistical capacity that has been brought to bear. The success of GLRI has hinged on mutual investment of time, human capital, and tangible resources. Poweshiek skipperling conservation strategy Until recently, the Poweshiek skipperling (Oarisma poweshiek), a small butterfly that occurred historically in tallgrass prairie and prairie fens, was regarded as “the most frequently and reliably encountered of the prairie-obligate skippers” in the Upper Midwest, but now faces a high risk of extinction (Dana 2008). This species is now known only from approximately 1% of the sites where it previously occurred in Wisconsin and Michigan, USA, and Manitoba, Canada. The USFWS listed the Poweshiek skipperling as endangered under the Endangered Species Act (16 U.S.C. 1531 et seq.) (ESA) in 2014 (USFWS 2014). A multi-agency partnership was created in 2015 to develop a conservation strategy for the Poweshiek skipperling, the basis of which would be development of protocols to facilitate captive rearing, augmentation of existing populations, and, eventually, reintroduction of the species to sites within its historical range (Smith et al. 2016; USFWS 2016, 2017). The USFWS convened a workshop with partnering agencies and researchers in October, 2015, at the Minnesota Zoo, Apple Valley, Minnesota, USA, to assess ex situ rearing as a conservation tool for Poweshiek skipperling. Scientists with the International Union for the Conservation of Nature (IUCN) Species Status Commission (SSC) Conservation Breeding Specialist Group (CBSG) facilitated the workshop in which the group of scientists provided data, professional opinion, and biological expertise on potential recovery tools. Experts recommended a strategy that incorporated both short-term and long-term measures, including a head-start program, surrogate research using the closely related Garita skipper (O. garita), and an insurance population program (Delphey et al. 2016; Smith et al. 2016). A suite of collaborators are conducting complementary research on breeding and husbandry techniques, larval host preferences, and pesticide tolerance using closely related species to support ex situ management. Additional research projects on habitat restoration and pesticide risk assessments are occurring at extant and potential reintroduction sites to determine suitability for reintroductions. Development of complex conservation and recovery strategies requires cooperation between the USFWS, State of Michigan, Michigan Natural Features Inventory, Springfield Township in Michigan, Minnesota Zoo, The Nature Conservancy (TNC) of Canada, Assiniboine Park Zoo, Central Michigan University, University of Winnipeg, Minnesota Department of Natural Resources, Minot University, Milwaukee Public Museum, Wisconsin Department of Natural Resources, New College of Florida, independent researchers, and private landowners. The Poweshiek Skipperling Conservation Strategy project is in its second year (Smith et al. 2016). After 5 years, USFWS biologists will evaluate captive rearing and reinforcement actions by comparing population trends post-release to trends observed from 2011 to 2016. They also will evaluate survival from egg to release while in captivity to determine whether it is likely to exceed an estimated 3% survival rate in the wild, based on that of another rare butterfly (Lambert 2011). The USFWS and partners will take immediate action to prevent the extinction of the Poweshiek skipperling by augmenting populations at two to three sites using head-started, captive-reared individuals (Smith et al. 2016). This action is intended to stabilize declining population trends and increase growth rates of current populations through reinforcement and protection of populations and will be supported with appropriate habitat management (Smith et al. 2016; USFWS 2016, 2017). The ultimate goal of the Poweshiek Skipperling Conservation Strategy project is recovery of the species according to measureable criteria defined in the reintroduction and propagation plan (Smith et al. 2016), the conservation strategy (USFWS 2016), focal species action plan (USFWS 2017), and in the future recovery plan (in development). Lessons learned—The effort for Poweshiek skipperling recovery demonstrates how input from external scientists is included in multiple stages of imperiled species recovery programs, from workshops with experts to identify conservation actions to targeted research on key aspects of biology and threats. Because agency and external scientists worked together during the initial coordination stage of project development, the scope of research being undertaken is well-defined and highly relevant to implementation of the overall conservation strategy. The effort involves the agency scientists responsible for coordinating the program as well as experts from academia and conservation organizations who are intimately familiar with the species’ biology. Success of the partnership is further demonstrated through the development of innovative techniques and approaches that are being applied to the Poweshiek skipperling as well as other imperiled grass skippers (Delphey et al. 2017; Runquist and Nordmeyer 2018). Counting bats and butterflies using LiDAR Bats and butterflies may seem to have relatively little in common. Yet scientists who need to quantify their numbers face similar challenges. The USFWS uses data on status and trends for populations of imperiled species to evaluate threats, make listing decisions, and develop recovery plans and recovery criteria. Traditional approaches to quantify populations tended to rely on census measures, sampling, and statistical techniques to infer an estimate of population size. However, some species are particularly difficult to count due to unique behaviors, detection challenges, environmental conditions, and sheer numbers. Gregarious hibernating bats and monarch butterflies (Danaus plexippus) overwinter in large numbers in highly dense, three-dimensional clusters presenting the opportunity to measure populations when they congregate during their overwintering seasons. The gray myotis (Myotis grisescens) and Indiana myotis (M. sodalis) are two of the seven federally listed bat species in the United States. Many decisions about conservation efforts and recovery status of these species are based on winter survey data acquired while bats are hibernating in caves and mines (e.g., USFWS 1982, 2007). Traditional survey methods of hibernating populations, which can number in the thousands or hundreds of thousands, are plagued with biases because of irregularities in substrate, roosting behavior, and low repeatability among survey years, and have the potential to cause excessive disturbance (Thomas and LaVal 1988). The level of disturbance caused to hibernating bats coupled with the high uncertainty of traditionally acquired estimates necessitates a reevaluation of methodologies and modern technological tools have shown promise as an alternative (Azmy et al. 2012; McFarlane et al. 2015; Shazali et al. 2017). Similarly, overwintering sites for monarch butterflies in high-elevation forests of central Mexico hold upward of 10 million or more monarchs clustered over the surface of a few trees (Urquhart and Urquhart 1976; Brower 1977). Since the early 1990s, efforts to estimate populations have been led by World Wildlife Fund-Mexico, in collaboration with the Mexican Secretariat of Environment and Natural Resources (Secretaría de Medio Ambiente y Recursos Naturales), the National Commission for Protected Areas (Comisión Nacional de Áreas Naturales Protegidas), and the Monarch Butterfly Biosphere Reserve. Biologists have used the occupied surface area of the colonies, a hectare-based estimate, as an index of population size (Rendón-Salinas and Tavera-Alonso 2014). Various methods have been attempted to count individual overwintering monarchs, including capture–mark–recapture techniques (Calvert 2004), netting and removal of occupied branches from trees (Calvert 2004), and drawing inferences from storm mortality events (Brower et al. 2004). Still, a 95% credible interval ranging between 2.4 and 80.7 million monarchs per hectare indicates that much uncertainty remains regarding absolute numbers (Thogmartin et al. 2017c). Recognizing the potential benefits from a parallel, collaborative approach, USFWS scientists initiated a unique, interdisciplinary partnership to leverage resources and expertise, and explore technological solutions to address a common problem between bats and butterflies. Currently, efforts are underway to use Light Detection and Ranging (LiDAR)—laser-based tools for measuring three-dimensional structures—and other technological approaches to estimate population sizes. In partnership with the Center for Design Innovation, Winston-Salem State University, TERC, and the USGS, a team of biologists, quantitative ecologists, engineers, and outreach specialists are drawing from tools typically used in the fields of architecture or historical preservation to explore new methods to quantify the volume occupied by overwintering bats and monarchs, which can then be used to estimate abundance. Results will directly inform the conservation and management of imperiled bats and monarch butterflies and will be communicated to the public through traditional scientific channels as well as through outreach tools and programs targeted to a broader audience. Lessons learned—The foundational relationships that have facilitated the notably swift and innovative work of this partnership were developed during initial coordination. Early coordination and transparent communication between agency and external scientists served to clearly define expectations of all partners and identify desired outcomes and products. The progression of development of the bats and butterflies LIDAR project also illustrates the non-linear, often cyclical process of project development, with the scope evolving as more diverse expertise and creative lines of thought are introduced to the team. In this case, the original project that focused on hibernating bats was expanded to include monarch and effectively maximized the efficient use of resources, breadth of scientific capacity, and overall conservation impact. Big river restoration in the southeast Missouri lead mining district In the Big River and Meramec River watersheds of the southeast Missouri Ozarks, the largest historic lead mining district in the United States intersects with one of the most diverse aquatic riverine ecosystems in the Upper Mississippi Basin with some unfortunate results. Researchers through the decades have documented impacts to aquatic biota, including mussels, associated with heavy metal contaminated sediments. The Old Lead Belt, which drains into the Big River in southeast Missouri, produced several millions of tons of mine and mill waste that have eroded into the Big River and its tributaries since the mid-1800s. Of specific concern to the USFWS are four federally listed mussel species that contribute to the diversity of the area. This unfortunate circumstance for benthic biota has been a rich setting for the USFWS, other agencies, and researchers have collaborated on research to understand the extent of impacts and restore habitats necessary to support aquatic organisms. Modern scientific investigations of lead impacts began in the Big River in the late 1970s after a storm event caused a large scale release of lead mill waste (approximately 50,000 cubic meters) into the river. Early research by the Missouri Department of Conservation (MDC) and USFWS investigated distribution of freshwater mussels and uptake of heavy metals in mussels and other benthic biota following this event (Buchanan 1980; Schmitt and Finger 1982; Czarnezki 1985). Based on threats to human health identified through the investigation, the Missouri Department of Health and Senior Services (MDHSS) issued an advisory against consuming certain benthic fish species for over 170 km of the Big River. Furthermore, researchers documented toxic levels of lead-contaminated sediment in the Big River that extend over 170 km to its confluence with the Meramec River (Schmitt and Finger 1982; Roberts et al. 2010; Pavlowsky et al. 2017). Identification of the severity and extent of impairment to the river were a springboard for developing a partnership between federal and state agencies, academic institutions, contractors for the mining companies, and TNC. A suite of collaborative research projects contributing to the Big River restoration effort were undertaken as part of a Natural Resource Damage Assessment of the area. A major focus of the assessment was to determine which benthic organisms were adversely affected by metal toxicity versus adverse effects from other habitat factors such as excessive sediment load, point source discharge, and agricultural or urban land use. From 2008 to 2017 scientists from USFWS, USGS, MDC, Missouri Department of Natural Resources, Missouri State University, and University of Missouri designed and implemented cohesive and complementary studies to identify impacts to mussels, crayfish, riffle-dwelling fish; document the extent of contamination in sediment and the floodplain; and identify drivers of mussel distribution. One such series of consecutive studies included a quantitative evaluation by USFWS of mussel populations and correlations with sediment contamination, a USGS evaluation of toxicity to juvenile mussels and amphipods from sediments collected from the same locations as a field evaluation conducted by USFWS (Besser et al. 2009; Roberts et al. 2010); an evaluation by USGS and MDC of impacts to crayfish density and in situ toxicity (Allert et al. 2009; McKee et al. 2010); an evaluation by USGS and USFWS of habitat factors that dictate freshwater mussel distribution (Albers et al. 2016; Roberts et al. 2016); and documentation of the longitudinal and vertical extent of sediment contamination in stream and floodplains by researchers at Missouri State University (Pavlowsky et al. 2017). Ultimately, the purpose of all investigations is to inform clean-up decisions and restoration methods beneficial to mussels and other aquatic life in the Big River and Meramec River basins. Lessons learned—Partnership development for the Big River Restoration Project followed an ideal progression through the stages of collaborative definition of the project scope, assembling the necessary team of scientists, and pooling resources to ensure that research goals and objectives were met. Because of the extensive scope of work to be completed, once collaborators identified and prioritized research needs, individual projects, or activities within a project, were completed by agency or academic scientists with the appropriate expertise and resources. The approach maintains a focus on injury assessment and restoration for the purposes of the Natural Resource Damage Assessment, yet provides information that will inform clean-up decisions for EPA, and provides sufficient flexibility for external scientists to engage in aspects of the effort that meet their academic interests. Conclusions Effective, science-driven conservation is accomplished through strategic partnerships and continuously evolving collaborations. Case studies from the Midwest Region of the USFWS are a small representation of the wide breadth of investigations and analyses occurring across the agency that would not be possible without engagement of diverse external scientists. These case studies also illustrate how attention to key stages of partnership development can result in relevant, well-aligned research. Partnerships between USFWS and external scientists can be viewed as mutually beneficial in that they facilitate accomplishment of the agency mission while providing an avenue for innovative research to have a direct influence on conservation decisions. Acknowledgments We thank L. Williams, A. Trowbridge, M. Merson, and L. Morgan for review and feedback on the manuscript. 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Phosphate treatment of lead-contaminated soil: effects on water quality, plant uptake, and lead speciation . J Environ Qual 44 : 1127 – 36 . Google Scholar CrossRef Search ADS PubMed Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology 2018. This work is written by US Government employees and is in the public domain in the US. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Integrative and Comparative Biology Oxford University Press

On the Cutting Edge of Research to Conserve At-Risk Species: Maximizing Impact through Partnerships

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Oxford University Press
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Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology 2018. This work is written by US Government employees and is in the public domain in the US.
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1540-7063
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1557-7023
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Abstract

Abstract Today’s conservation challenges are complex. Solving these challenges often requires scientific collaborations that extend beyond the scope, expertise, and capacity of any single agency, organization, or institution. Conservation efforts can benefit from interdisciplinary collaboration, scientific and technological innovations, and the leveraging of capacity and resources among partners. Here we explore a series of case studies demonstrating how collaborative scientific partnerships are furthering the mission of the US Fish and Wildlife Service (USFWS), including: (1) contaminants of emerging concern in the Great Lakes Basin, (2) Poweshiek skipperling conservation, (3) using technology to improve population survey methods for bats and monarch butterfly, and (4) Big River restoration in the Southeast Missouri lead mining district. These case studies illustrate how strategic and effective scientific collaboration is a multi-stage process that requires investment of time and resources by all participants. Early coordination and communication is crucial to aligning planned work with scientific and decision-making needs. Collaborations between USFWS and external scientists can be mutually beneficial by supporting the agency mission while also providing an avenue for innovative research to be directly applied in conservation decisions and management actions. Introduction The US Fish and Wildlife Service (USFWS) manages National Wildlife Refuges, protects and recovers endangered species, manages migratory birds, conserves nationally significant fisheries, and enforces federal wildlife laws. Many of the conservation challenges faced by the USFWS necessitate active engagement of stakeholders and scientific experts to achieve the agency mission. Notably, the agency mission of the USFWS—working with others to conserve, protect, and enhance fish, wildlife, and plants and their habitats for the continuing benefit of the American people—emphasizes the involvement of partners in the conservation of the nation’s natural resources. All USFWS programs have a role in accomplishing the agency mission. Programs such as Ecological Services, Migratory Birds, and Fish and Aquatic Conservation do so through implementation of policy, development of conservation and restoration strategies, restoration and protection of habitats and species, and evaluation of the success of conservation actions and strategies. There is a scientific basis to all of these activities. Whereas the USFWS workforce maintains a wide breadth of scientific expertise, the agency does not house experts in all necessary fields to address all possible complex and emerging conservation issues and thus often relies on external scientists to serve as technical experts (USFWS 1994). Furthermore, conservation and recovery efforts often benefit from input from diverse perspectives and skill sets offered by a combination of agency and external scientists (Asquith 2001; Boersma et al. 2001; Gerber and Schultz 2001; Stinchcombe et al. 2002). The responsibility of the USFWS to inform policy, conservation strategy, and management decisions with sound science makes collaboration with external scientists instrumental to accomplishing effective conservation. Additionally, many opportunities exist for external scientists to proactively engage the USFWS as a means to move their work from theory to practice. A more complete understanding by academic scientists and students of the breadth of opportunities to interface with agency scientists and subsequent adoption of an effective approach for developing collaborative science partnerships can lead to increased visibility and relevancy of their work to the public. Engagement with external scientists The USFWS interfaces in multiple ways with scientists from numerous sectors of the conservation field, including academic institutions, non-governmental organizations, state agencies, tribes, and other federal agencies. Modes of engagement with external scientists can vary from relatively brief collaborations, which can include data collection exercises, information sharing through meetings, and participation in webinars on topics of mutual interest, to more formalized and complex partnerships focused on developing conservation strategies or original research. In this discussion we distinguish formal or informal collaborative science partnerships from general collaborative activities with external scientists based on a longer duration, shared objectives, and higher level of resource investment by all parties. Collaboration for data collection refers to compiling existing empirical and anecdotal data as well as eliciting and incorporating knowledge and opinion from subject matter experts. Data collection is accomplished through participatory exercises such as working groups and structured expert elicitation. Working groups are formed to address specific conservation issues or prioritization needs through interactive discussions, strategy development, and product creation. The membership of working groups typically includes individuals who are experts in species biology, specialists in applicable laboratory or field methodologies, members of diverse stakeholder groups, and specialists that bring to the effort interdisciplinary and technical skills that are value-added for addressing the issue at hand. Expert elicitation is a data collection process that enables the inclusion of expert opinion and professional judgment while reducing bias, quantifying uncertainty, and allowing for peer review through structured processes (Burgman et al. 2011; Martin et al. 2012; Drescher et al. 2013). Use of expert knowledge is advantageous, or even essential, when empirical data are lacking either because complex conservation issues have not been thoroughly studied or there is an imminent need to understand and act on emerging conservation issues. The latter is often the case when addressing threats to imperiled species. For example, structured expert elicitation has been used in the conservation of at-risk species to rank threats (Donlan et al. 2010), evaluate impacts from specific threats (Frick et al. 2017), and provide parameters to inform demographic population models (Oberhauser et al. 2016). Collaborative science partnerships between the USFWS and external scientists differ from data collection exercises in that they result in generation of data, techniques, and relevant knowledge to further the conservation of federally protected species, at-risk species, or their habitats, as well as to inform restoration and management efforts. Projects can be undertaken to address priority information needs identified by working groups or during expert elicitation, or they can be developed independently by agency biologists and collaborators. Agency scientists and collaborators work together to understand conservation issues, define project goals and objectives, identify useful products and science delivery tools, convene teams of scientists with the expertise to achieve project goals, and secure sufficient financial and logistical support for project implementation. The USFWS invests in priority science initiatives through allocation of funding and in-house scientific expertise. For example, the USFWS has allocated $40 million since 2008 to fund bat and white-nose syndrome (WNS) related surveillance and monitoring, research, and management activities. This includes $30 million in grants to other federal, state, provincial, and non-governmental agencies (https://www.whitenosesyndrome.org/research-monitoring). Additionally, since 2010, the USFWS has managed more than $256 million in funds from the Great Lakes Restoration Initiative (GLRI), both to directly implement conservation as well as to collaborate with partners to address data gaps and evaluate environmental conditions. In addition to funding provided by the agency to support collaborative science initiatives, USFWS scientists actively engage with partners in studies and data analyses to understand species biology, evaluate threats, and develop new techniques and tools. Recent collaborative projects completed in the Midwest Region of the USFWS involving agency scientists include work on: identification and assessment of threats to federally listed and at-risk species and their habitats (ThogMartin et al. 2012a, 2012b, 2013, 2017b; Erickson et al. 2016; Daniel et al. 2017; Strobel and Giorgi 2017); habitat conservation actions (Thogmartin et al. 2017a); adaptive management strategies for federally listed species (Moore et al. 2011); species ecology and distribution (Russell et al. 2014; Clymer and Blanchong 2016); impacts of environmental contaminants on wildlife and natural systems (Simon and Morris 2009; Weber et al. 2015; Simon et al. 2013; Eidels et al. 2016); and large-scale prioritization of conservation actions (Januchowski-Hartley et al. 2013; Daniel et al. 2017). Considerations for developing partnerships Establishing strategic science partnerships requires an investment of time and resources by all partners and a clear understanding of expectations, goals, resources, and modes of delivery. The early stages of partnership development can be conceptualized as a stepwise process, although the progression is rarely truly linear or the steps strictly sequential. Viewing the process as steps (Fig. 1) ensures that consideration is given to all stages and allows emphasis to be placed on pivotal components as appropriate, such as early communication with resource managers. Fig. 1 View largeDownload slide Partnership development is a cyclical, adaptive process, but the early stages can be viewed in a stepwise manner to facilitate thorough consideration of foundational elements. Communication and engagement between collaborators and USFWS scientists at each stage, from project conceptualization to acquisition of resources, serves to maximize mutual benefits and likelihood of successful implementation. Fig. 1 View largeDownload slide Partnership development is a cyclical, adaptive process, but the early stages can be viewed in a stepwise manner to facilitate thorough consideration of foundational elements. Communication and engagement between collaborators and USFWS scientists at each stage, from project conceptualization to acquisition of resources, serves to maximize mutual benefits and likelihood of successful implementation. The early stages of development, while vital to the overall success of the partnership, can be undervalued and overlooked. For example, it is during the stage of Initial Coordination that agency scientists and external collaborators can engage in active dialog to ensure that future work is relevant to current conservation issues and useful to conservation practitioners. Such early communication facilitates well-aligned research that minimizes the research-implementation gap (Knight et al. 2008) and maximizes the likelihood that research will have an instrumental impact directly influencing policy development, regulatory decisions, or deployment of conservation resources (Rudd et al. 2011; Rudd 2011). Case studies of collaborative science partnerships To illustrate the USFWS’s engagement in interdisciplinary science partnerships that facilitate achievement of the agency mission, we present case studies from the Midwest Region of the USFWS. The case studies highlight some of the contemporary conservation issues faced by the USFWS giving insight into the breadth of the agency’s science needs and providing examples of various ways that external scientists have interfaced with agency scientists. Additionally, the case studies demonstrate how effective, mutually beneficial partnerships directly inform resource management because of deliberative and strategic approaches to development. Contaminants of emerging concern in the Great Lakes Basin The GLRI, launched in 2010, provides guidance and support for actions to help restore and sustain the health of the Great Lakes ecosystem in the Upper Midwest of the United States (https://www.glri.us/). One focus of GLRI is to identify potential impacts to fish and wildlife from contaminants of emerging concern (CECs), including pharmaceuticals, personal care products, and new agricultural and industrial chemicals, and their byproducts. CECs are ubiquitous throughout the Great Lakes, yet in 2010 little was known about their extent and impacts (Choy et al. 2013; Elliott et al. 2017). Biologists from USFWS partnered with other federal and state agencies, academia, and independent specialists to understand the extent of CEC contamination (Phase I 2010–2015) and impacts to natural resources (Phase II 2015–2020) in order to manage and sustain natural resources for current and future generations. Collaborations among federal agencies (e.g., USFWS, US Environmental Protection Agency [EPA], US Geological Survey [USGS], US Army Corps of Engine ers, and National Oceanic and Atmospheric Administration) have created an opportunity to leverage limited resources, harness individual expertise, and address each agency’s mandates while achieving mutual goals. In addition to contributing to the integrated work among federal agencies, USFWS is specifically assessing population-level impacts of CECs to USFWS trust resources including fish, migratory birds, and threatened and endangered (T/E) species. Collaborative work includes ongoing field and laboratory studies to assess how CECs affect reproduction and fitness of various taxa (Thomas et al. 2017; Jorgenson et al. 2018): fish with St. Cloud State University, St. Thomas University, Michigan Department of Natural Resources, and Wisconsin Department of Natural Resources; freshwater mussels with Central Michigan University; and birds with Dr. James Ludwig. Initial studies focused on common species, but new techniques are being developed to allow non-lethal sampling and modeling to assess T/E species. USFWS and partners are using empirical data from laboratory and field studies to evaluate CEC sensitivity, including chemical characterization with Southern Illinois University and cell receptor sensitivity with St. Cloud State University. Modeling exercises are being conducted by the University of Minnesota and Ball State University to validate CEC population impacts, and by USGS to validate watershed hazard assessments by evaluating the presence and occurrence of CECs throughout the Great Lakes Basin. USFWS will use results from the suite of studies to inform resource management decisions by providing sublethal population-level assessments of CEC risks to trust resources, including T/E species. Preliminary results suggest that CECs are contributing to sublethal effects on fish and may lead to population-level declines (Thomas et al. 2017; Jorgenson et al. 2018). Results will be disseminated through outreach to federal, state, tribal, and local natural resource managers and the public. In addition, federal agencies will produce an Integrated Report assessing CEC impacts that provide management recommendations in 2020. Further, USFWS and collaborators are producing peer-reviewed articles for technical audiences. With limited resources, it is more important than ever for resource managers to understand the stressors which may impact vulnerable species populations to help prioritize areas best suited for restoration and conservation efforts. These studies will provide information regarding potential population-level impacts of CECs enabling managers to select optimal conservation and management practices in order to avoid further population declines, future listing of imperiled species, and loss of trust resources for the continued benefit of current and future generations. Lessons learned—GLRI exemplifies how a large, well-coordinated partnership can address complex, large scale conservation issues to achieve the missions of multiple agencies. Implementation of a restoration project with a broad scope requires scientific expertise of equivalent breadth that is harnessed through continuous coordination and clearly defined goals, objectives, and actions. The initiative has been successful through assembly and engagement of numerous, appropriate agencies, and organizations while still capitalizing on the expertise of individual scientific experts. Whereas coordination can present challenges, engagement of an extensive suite of collaborators has maximized the cumulative financial and logistical capacity that has been brought to bear. The success of GLRI has hinged on mutual investment of time, human capital, and tangible resources. Poweshiek skipperling conservation strategy Until recently, the Poweshiek skipperling (Oarisma poweshiek), a small butterfly that occurred historically in tallgrass prairie and prairie fens, was regarded as “the most frequently and reliably encountered of the prairie-obligate skippers” in the Upper Midwest, but now faces a high risk of extinction (Dana 2008). This species is now known only from approximately 1% of the sites where it previously occurred in Wisconsin and Michigan, USA, and Manitoba, Canada. The USFWS listed the Poweshiek skipperling as endangered under the Endangered Species Act (16 U.S.C. 1531 et seq.) (ESA) in 2014 (USFWS 2014). A multi-agency partnership was created in 2015 to develop a conservation strategy for the Poweshiek skipperling, the basis of which would be development of protocols to facilitate captive rearing, augmentation of existing populations, and, eventually, reintroduction of the species to sites within its historical range (Smith et al. 2016; USFWS 2016, 2017). The USFWS convened a workshop with partnering agencies and researchers in October, 2015, at the Minnesota Zoo, Apple Valley, Minnesota, USA, to assess ex situ rearing as a conservation tool for Poweshiek skipperling. Scientists with the International Union for the Conservation of Nature (IUCN) Species Status Commission (SSC) Conservation Breeding Specialist Group (CBSG) facilitated the workshop in which the group of scientists provided data, professional opinion, and biological expertise on potential recovery tools. Experts recommended a strategy that incorporated both short-term and long-term measures, including a head-start program, surrogate research using the closely related Garita skipper (O. garita), and an insurance population program (Delphey et al. 2016; Smith et al. 2016). A suite of collaborators are conducting complementary research on breeding and husbandry techniques, larval host preferences, and pesticide tolerance using closely related species to support ex situ management. Additional research projects on habitat restoration and pesticide risk assessments are occurring at extant and potential reintroduction sites to determine suitability for reintroductions. Development of complex conservation and recovery strategies requires cooperation between the USFWS, State of Michigan, Michigan Natural Features Inventory, Springfield Township in Michigan, Minnesota Zoo, The Nature Conservancy (TNC) of Canada, Assiniboine Park Zoo, Central Michigan University, University of Winnipeg, Minnesota Department of Natural Resources, Minot University, Milwaukee Public Museum, Wisconsin Department of Natural Resources, New College of Florida, independent researchers, and private landowners. The Poweshiek Skipperling Conservation Strategy project is in its second year (Smith et al. 2016). After 5 years, USFWS biologists will evaluate captive rearing and reinforcement actions by comparing population trends post-release to trends observed from 2011 to 2016. They also will evaluate survival from egg to release while in captivity to determine whether it is likely to exceed an estimated 3% survival rate in the wild, based on that of another rare butterfly (Lambert 2011). The USFWS and partners will take immediate action to prevent the extinction of the Poweshiek skipperling by augmenting populations at two to three sites using head-started, captive-reared individuals (Smith et al. 2016). This action is intended to stabilize declining population trends and increase growth rates of current populations through reinforcement and protection of populations and will be supported with appropriate habitat management (Smith et al. 2016; USFWS 2016, 2017). The ultimate goal of the Poweshiek Skipperling Conservation Strategy project is recovery of the species according to measureable criteria defined in the reintroduction and propagation plan (Smith et al. 2016), the conservation strategy (USFWS 2016), focal species action plan (USFWS 2017), and in the future recovery plan (in development). Lessons learned—The effort for Poweshiek skipperling recovery demonstrates how input from external scientists is included in multiple stages of imperiled species recovery programs, from workshops with experts to identify conservation actions to targeted research on key aspects of biology and threats. Because agency and external scientists worked together during the initial coordination stage of project development, the scope of research being undertaken is well-defined and highly relevant to implementation of the overall conservation strategy. The effort involves the agency scientists responsible for coordinating the program as well as experts from academia and conservation organizations who are intimately familiar with the species’ biology. Success of the partnership is further demonstrated through the development of innovative techniques and approaches that are being applied to the Poweshiek skipperling as well as other imperiled grass skippers (Delphey et al. 2017; Runquist and Nordmeyer 2018). Counting bats and butterflies using LiDAR Bats and butterflies may seem to have relatively little in common. Yet scientists who need to quantify their numbers face similar challenges. The USFWS uses data on status and trends for populations of imperiled species to evaluate threats, make listing decisions, and develop recovery plans and recovery criteria. Traditional approaches to quantify populations tended to rely on census measures, sampling, and statistical techniques to infer an estimate of population size. However, some species are particularly difficult to count due to unique behaviors, detection challenges, environmental conditions, and sheer numbers. Gregarious hibernating bats and monarch butterflies (Danaus plexippus) overwinter in large numbers in highly dense, three-dimensional clusters presenting the opportunity to measure populations when they congregate during their overwintering seasons. The gray myotis (Myotis grisescens) and Indiana myotis (M. sodalis) are two of the seven federally listed bat species in the United States. Many decisions about conservation efforts and recovery status of these species are based on winter survey data acquired while bats are hibernating in caves and mines (e.g., USFWS 1982, 2007). Traditional survey methods of hibernating populations, which can number in the thousands or hundreds of thousands, are plagued with biases because of irregularities in substrate, roosting behavior, and low repeatability among survey years, and have the potential to cause excessive disturbance (Thomas and LaVal 1988). The level of disturbance caused to hibernating bats coupled with the high uncertainty of traditionally acquired estimates necessitates a reevaluation of methodologies and modern technological tools have shown promise as an alternative (Azmy et al. 2012; McFarlane et al. 2015; Shazali et al. 2017). Similarly, overwintering sites for monarch butterflies in high-elevation forests of central Mexico hold upward of 10 million or more monarchs clustered over the surface of a few trees (Urquhart and Urquhart 1976; Brower 1977). Since the early 1990s, efforts to estimate populations have been led by World Wildlife Fund-Mexico, in collaboration with the Mexican Secretariat of Environment and Natural Resources (Secretaría de Medio Ambiente y Recursos Naturales), the National Commission for Protected Areas (Comisión Nacional de Áreas Naturales Protegidas), and the Monarch Butterfly Biosphere Reserve. Biologists have used the occupied surface area of the colonies, a hectare-based estimate, as an index of population size (Rendón-Salinas and Tavera-Alonso 2014). Various methods have been attempted to count individual overwintering monarchs, including capture–mark–recapture techniques (Calvert 2004), netting and removal of occupied branches from trees (Calvert 2004), and drawing inferences from storm mortality events (Brower et al. 2004). Still, a 95% credible interval ranging between 2.4 and 80.7 million monarchs per hectare indicates that much uncertainty remains regarding absolute numbers (Thogmartin et al. 2017c). Recognizing the potential benefits from a parallel, collaborative approach, USFWS scientists initiated a unique, interdisciplinary partnership to leverage resources and expertise, and explore technological solutions to address a common problem between bats and butterflies. Currently, efforts are underway to use Light Detection and Ranging (LiDAR)—laser-based tools for measuring three-dimensional structures—and other technological approaches to estimate population sizes. In partnership with the Center for Design Innovation, Winston-Salem State University, TERC, and the USGS, a team of biologists, quantitative ecologists, engineers, and outreach specialists are drawing from tools typically used in the fields of architecture or historical preservation to explore new methods to quantify the volume occupied by overwintering bats and monarchs, which can then be used to estimate abundance. Results will directly inform the conservation and management of imperiled bats and monarch butterflies and will be communicated to the public through traditional scientific channels as well as through outreach tools and programs targeted to a broader audience. Lessons learned—The foundational relationships that have facilitated the notably swift and innovative work of this partnership were developed during initial coordination. Early coordination and transparent communication between agency and external scientists served to clearly define expectations of all partners and identify desired outcomes and products. The progression of development of the bats and butterflies LIDAR project also illustrates the non-linear, often cyclical process of project development, with the scope evolving as more diverse expertise and creative lines of thought are introduced to the team. In this case, the original project that focused on hibernating bats was expanded to include monarch and effectively maximized the efficient use of resources, breadth of scientific capacity, and overall conservation impact. Big river restoration in the southeast Missouri lead mining district In the Big River and Meramec River watersheds of the southeast Missouri Ozarks, the largest historic lead mining district in the United States intersects with one of the most diverse aquatic riverine ecosystems in the Upper Mississippi Basin with some unfortunate results. Researchers through the decades have documented impacts to aquatic biota, including mussels, associated with heavy metal contaminated sediments. The Old Lead Belt, which drains into the Big River in southeast Missouri, produced several millions of tons of mine and mill waste that have eroded into the Big River and its tributaries since the mid-1800s. Of specific concern to the USFWS are four federally listed mussel species that contribute to the diversity of the area. This unfortunate circumstance for benthic biota has been a rich setting for the USFWS, other agencies, and researchers have collaborated on research to understand the extent of impacts and restore habitats necessary to support aquatic organisms. Modern scientific investigations of lead impacts began in the Big River in the late 1970s after a storm event caused a large scale release of lead mill waste (approximately 50,000 cubic meters) into the river. Early research by the Missouri Department of Conservation (MDC) and USFWS investigated distribution of freshwater mussels and uptake of heavy metals in mussels and other benthic biota following this event (Buchanan 1980; Schmitt and Finger 1982; Czarnezki 1985). Based on threats to human health identified through the investigation, the Missouri Department of Health and Senior Services (MDHSS) issued an advisory against consuming certain benthic fish species for over 170 km of the Big River. Furthermore, researchers documented toxic levels of lead-contaminated sediment in the Big River that extend over 170 km to its confluence with the Meramec River (Schmitt and Finger 1982; Roberts et al. 2010; Pavlowsky et al. 2017). Identification of the severity and extent of impairment to the river were a springboard for developing a partnership between federal and state agencies, academic institutions, contractors for the mining companies, and TNC. A suite of collaborative research projects contributing to the Big River restoration effort were undertaken as part of a Natural Resource Damage Assessment of the area. A major focus of the assessment was to determine which benthic organisms were adversely affected by metal toxicity versus adverse effects from other habitat factors such as excessive sediment load, point source discharge, and agricultural or urban land use. From 2008 to 2017 scientists from USFWS, USGS, MDC, Missouri Department of Natural Resources, Missouri State University, and University of Missouri designed and implemented cohesive and complementary studies to identify impacts to mussels, crayfish, riffle-dwelling fish; document the extent of contamination in sediment and the floodplain; and identify drivers of mussel distribution. One such series of consecutive studies included a quantitative evaluation by USFWS of mussel populations and correlations with sediment contamination, a USGS evaluation of toxicity to juvenile mussels and amphipods from sediments collected from the same locations as a field evaluation conducted by USFWS (Besser et al. 2009; Roberts et al. 2010); an evaluation by USGS and MDC of impacts to crayfish density and in situ toxicity (Allert et al. 2009; McKee et al. 2010); an evaluation by USGS and USFWS of habitat factors that dictate freshwater mussel distribution (Albers et al. 2016; Roberts et al. 2016); and documentation of the longitudinal and vertical extent of sediment contamination in stream and floodplains by researchers at Missouri State University (Pavlowsky et al. 2017). Ultimately, the purpose of all investigations is to inform clean-up decisions and restoration methods beneficial to mussels and other aquatic life in the Big River and Meramec River basins. Lessons learned—Partnership development for the Big River Restoration Project followed an ideal progression through the stages of collaborative definition of the project scope, assembling the necessary team of scientists, and pooling resources to ensure that research goals and objectives were met. Because of the extensive scope of work to be completed, once collaborators identified and prioritized research needs, individual projects, or activities within a project, were completed by agency or academic scientists with the appropriate expertise and resources. The approach maintains a focus on injury assessment and restoration for the purposes of the Natural Resource Damage Assessment, yet provides information that will inform clean-up decisions for EPA, and provides sufficient flexibility for external scientists to engage in aspects of the effort that meet their academic interests. Conclusions Effective, science-driven conservation is accomplished through strategic partnerships and continuously evolving collaborations. Case studies from the Midwest Region of the USFWS are a small representation of the wide breadth of investigations and analyses occurring across the agency that would not be possible without engagement of diverse external scientists. These case studies also illustrate how attention to key stages of partnership development can result in relevant, well-aligned research. Partnerships between USFWS and external scientists can be viewed as mutually beneficial in that they facilitate accomplishment of the agency mission while providing an avenue for innovative research to have a direct influence on conservation decisions. Acknowledgments We thank L. Williams, A. Trowbridge, M. Merson, and L. Morgan for review and feedback on the manuscript. 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Integrative and Comparative BiologyOxford University Press

Published: Jul 1, 2018

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