Appropriate conservation management of P. lemhiensis, holistically, has presented a challenge for land managers, especially considering the unequal management practices already applied. Big Hole National Battlefield (POP8), which supports the largest known population of P. lemhiensis has applied monitoring procedures since 2009 (Rodhouse et al. 2018; Stucki et al. 2013). Further, the area has undergone controlled burns and spotted knapweed invasion removal. To date, this population is the only area known to have recently applied an active management strategy. Outside of NPS, the species has been monitored by USFS, BLM, the Montana Natural Heritage Program, and the Idaho Native Plant Society (BLM 2016; Brown & Proctor 2018; INPS 2020). Monitoring has elevated P. lemhiensis as a species of conservation concern (SCC) within USFS, and a Type 3 species within BLM, indicating that the species is moderately endangered. Irrespective of classifications, no direct action or mitigation strategy has been applied by BLM or USFS. Further, these evaluations are less formally structured and haphazardly timed, when compared to those conducted by NPS. The extent to which actions undertaken by NPS have worked to enhance the genetic integrity and diversity of the population within the Battleground is unknown. A firm understanding of how preceding management strategies has impacted populations, negatively or positively, can guide future management in establishing priorities for population conservation and act as a foundation for conservation plan formulation.
3.1. Population genetic diversity and structure.
Genetic differentiation (FST) is an estimate that provides insight into the dynamics of population connectivity. Traditionally, FST values > 0.15 are considered to represent significant genetic differentiation (Frankham et al. 2002) but more contemporary research suggests that FST values ≥ 0.20 indicate insufficient gene flow between populations such that harmful effects of inbreeding could manifest within small populations (Lowe & Allendorf 2010). The largest degree of differentiation, valuing at FST = 0.280, elaborates on the relationship between POP1 and POP6. Given the extent of geographic separation, nearly 62 miles in lateral distance, the approximate 776 meters difference in elevation, and the Beaverhead Mountain Range between both populations, this resulting degree of differentiation is expected. Correlation between genetic differentiation and geographic distance is a well observed pattern (Bontrager & Angert 2018; Hou & Lou 2011). A Nm value of 1.266 between POP1 and POP6, however, indicates some degree of gene flow. This phenomenon was detected in equally distant populations; POP5 and POP6 (FST = 0.254) and POP6 and POP7 (FST = 0.249), as well as the relationship seen between POP1 and every other population (Table 3). While FST values were broadly consistent with the number of migrants per generation, such that populations with the largest degree of differentiation had a smaller number of migrants per generation, and vice versa, it is notable that all values of Nm remain above 1. Based on Wright (1931) and ensuing analyses, one migrant individual per local population per generation is considered sufficient to maintain gene flow and impede differentiation (Mills & Allendorf 1996). The extent to which some populations are isolated from one another despite the detected gene flow is likely an indicator of the presence of a larger ancestral population in recent geological time. This population is likely undistinguishable in our current analyses due to the recency of divergence of the section in which this species resides, and the genus more broadly (Blischak et al. 2020; Wessinger et al. 2016; Wolfe et al. 2006; Wolfe et al. 2021) This conclusion is compounded by the remarkably low inbreeding coefficient values seen across all eight populations. Five out of eight populations were found to have negative inbreeding coefficient values, indicating a departure from Hardy-Weinberg equilibrium and an excess of heterozygosity within populations (Johnson & Shaw 2015). This, together with the lack of a significant difference between HO and HS values, is suggestive of outbreeding and gene flow amongst populations. Fitness traits were not measured in this study and neither inbreeding nor outbreeding depression could be assessed. In comparison to FIS values observed in other vulnerable species of Penstemon (Table 4), the values detected in this study do not raise immediate concerns that can be applied to conservation management practices. However, given the aforementioned degree of differentiation between populations, the existence of a large, ancestral population is a plausible explanation for the high amount of connectivity detected. While the effects of habitat fragmentation, both negative and positive, are well documented (Fahrig 2003; Fahrig 2017), the strength of the response detected is dependent on several factors, one of which is time since fragmentation. This is particularly true for measures of FIS, where effects become more pronounced and identifiable as more generations elapse (Schlaepfer et al. 2018).
While we were unable to detect ancestral connectivity across all eight populations, the results of the PCA show similarity across ancestral composition between POP1, POP7, and POP8, despite geographic isolation and physical distance between populations. This connectivity is likely the result of population shifts in response to climatic changes across the landscape, a phenomenon that is common for plant species following post glaciation (Huntley & Webb 1989). Although massive ice sheets such as the Cordilleran existed significantly farther North than extant populations of P. lemhiensis, areas of Western Montana were covered by mountain glaciers throughout the late Pleistocene (Alden 1953; Locke 1990). Further, the areas where both POP1 and POP7 are currently found was once within the Missoula flood extent and within bounds of the Late Wisconsin ice sheet (Cerling et al. 1994). Thus, the possibility of post-glacial expansion into Northern territory is likely an explanation for ancestral connectivity detected by the PCA. The expansion of suitable habitat detected in the mid-Holocene stands to confirm the likelihood of ancestral connectivity (Fig. 4). Following the Last Glacial Maximum retreat, southern populations would expand north into suitable, open habitats (Hewitt, 2000), as is often seen in Penstemon, a genus notorious for expansion into niches opened by glacial retreat (Wolfe et al. 2006; Wolfe et al. 2021). Suitable habitat estimates through the Last Glacial Maximum (Fig. 4) showcase the likelihood of southern populations, which would migrant north with a shifting climate.
3.2. Stakeholder Analysis
In addition to an understanding of the genetic integrity of populations, this study aims to evaluate the stakeholders relevant to the conservation of P. lemhiensis in order to better understand the influence of different individuals and organizations in directing appropriate conservation policy in the present and future (Bryson 2018). The identified major stakeholders, as outlined in Fig. 4, have been categorized based on their respective interest and authority in conservation action. Authority is defined, in part according to Cox and Jacobson (1973) as the “aggregate of political resources available to an actor”, as well as according to Ackerman & Eden (2011) as having the “capability to influence the delivery” of policy decisions. Interest is defined as having a politically, socially, morally, or economically motivated stake in the outcome of a policy decision (Bryson et al. 2011). Stakeholders with the most authority and influence can be considered key stakeholders (Eckhard & Jankauskas 2018) and should be both considered and leveraged in any policy decision regarding P. lemhiensis. We recognize that the stakeholders identified in this paper are by no means an exhaustive list and that other groups or organizations close to the issue, particularly those within marginalized communities, may have been excluded (Reed et al. 2009). It is therefore our recommendation that moving forward, conservation efforts are cognizant of this and work to bridge any perceived information gaps.
3.2.1. Players
Any conservation intervention initiatives for P. lemhiensis must thoroughly consider standing land management policies as well as the organizations with the legal discretion to mandate those policies (Koontz & Bodine 2008). The eight populations of P. lemhiensis fall collectively across the jurisdiction of three major land management agencies - the National Park Service, the US Forest Service, and the Bureau of Land Management (Fig. 5). Each agency draws its discretion from separate mandates that, in turn, subsequently affects the prioritization of conservation initiatives.
The Bureau of Land Management (BLM) is nested within the Department of the Interior and as mandated by the Federal Land Policy and Management Act (FLPMA) of 1976 (43 U.S.C. §§ 1701 et seq.) and the National Environmental Policy Act (NEPA) of 1969 (42 U.S.C. § 4321 et seq), balances both multiple use and sustained yield in its’ land management approach. Multiple uses of BLM-managed land include recreation, grazing, timber harvesting, and watershed, wildlife, and fish habitat management, and other conservation practices. Additionally, BLM facilitates federal mineral resource management and energy resource leasing and management. The US Forest Service, under the Department of Agriculture, is similar to BLM in its multiple use approach to land management. Following the discretion of FLPMA, NEPA, and the National Forest Management Act (P.L. 94–588; 16 U.S.C. §§ 1600–1614), the Multiple Use Sustained Yield Act of 1960 (16 U.S.C. §§ 528–531), and adjacent legislation, follows a land management style analogous to BLM. The Forest Service similarly facilitates a mission in managing land under principles of sustained yield and multiple use. Mandated to preserve the delegated land, water, and wildlife, the Forest Service also administers recreational activities, livestock grazing, timber extraction, and the management of renewable resources. Under the guise of multiple-use land management priorities, conservation priorities are difficult to equitably coincide with factors such as commodity production (Robbins 2013).
The National Park Service (NPS), while also maintaining a dual-purpose mission, focuses on preservation and recreation, as mandated by the National Park Service Organic Act of 1916 (16 U.S.C. § 1), the Wilderness Act of 1964 (16 U.S.C. ch. 23 § 1131 et seq), and the Historic Preservation Act (54 U.S.C. 300101 et seq.). Land and resources managed by the NPS are offered a greater degree of protection than those by the Forest Service or BLM due to differences in management priorities (Congressional Research Service 2019).
While the aforementioned legislations guide land management planning and prioritization, agency authority affords a wide degree of discretion towards actual implementation (Stern & Mortimer 2009). Both BLM and the USFS are often faced with competing interests in consideration of a singular land management approach. NPS faces this issue as well in balancing between recreation and conservation, albeit to a lesser degree. Statutes authorizing agency action will influence the priority placed on P. lemhiensis conservation efforts by each respective agency.
Consolidated conservation efforts across different federal and state agencies will be reliant upon cooperation across these agencies. The Council on Environmental Quality, for instance, mandates such cooperation under NEPA in instances of shared projects or interests. However, agencies have reported challenges in executing interagency projects; notably issues regarding timely communication, variation across agency standards, and a lack of memoranda of understanding defining agency roles (Stern & Mortimer 2009). Concentrated efforts across the BLM, USFS, and NPS to collectively manage and conserve populations of P. lemhiensis must first acknowledge historic roadblocks to cooperation and actively seek to mitigate them.
3.2.2. Subjects
Subjects in this analysis are classified as individuals or organizations that hold high interest in conservation initiatives but have little to no authority in the matter (Fig. 5). In this case, non-governmental organizations (NGOs), the academic community, and private industry represent a few of the most significant subjects in the context of P. lemhiensis conservation.
The academic community plays a critical role in contributing to the policy decisions of state and federal agencies actively approaching various issues (Clancy & Glied 2012), especially issues directly relevant to species conservation (Posner et al. 2016; Rose et al. 2019). This can be accomplished through academic-led research focusing on the genetic diversity of species in question, peer-reviewed publications, and public dissemination of objective information as it impacts species conservation (Fisher et al. 2020; Taft et al. 2020; Walsh et al. 2014). Academics also have a high interest, for a variety of reasons, in the formulation of conservation protocols (Evans & Cvitanovic 2018). Assuring that scientific research is interpreted appropriately and offering feedback on written policy in the form of public comments throughout the Administrative Procedure Act rulemaking process. The academic community does not, however, maintain the legal authority or power to influence decision-making directly, unless through litigation.
Non-governmental organizations (NGOs), specifically those focused on species conservation and environmental integrity, hold a high degree of interest in conservation initiatives broadly (Boiral & Heras-Saizarbitoria 2017), but also more specifically for P. lemhiensis. NGOs, such as the Montana Native Plant Society and the Idaho Native Plant Society, work to educate the public on environmental and conservation issues, as well ecological values, and provide the resources to tackle issues firsthand. Similar to the academic community, NGOs lack the legal authority to mandate state or federal conservation management of P. lemhiensis. NGOs, as well as the academic community, hold the ability to litigate on behalf of conservation issues or in response to the absence of agency action. Norton v. Southern Utah Wilderness Alliance (542 U.S. 55, 2004), as well as the preceding lower court cases stand as notable examples of the litigative capacity of NGOs in affecting agency actions.
In addition to organizations with a commitment to conservation initiatives, others carry contradictory interest as it can interfere with their own organizational goals. Most prominently, the agriculture industry in both Idaho and Montana, among other private industries, is highly interested in any potential conservation measures applied towards P. lemhiensis populations. Private organizations retain significant political influence and are themselves subject to governmental regulation (Rainey 1997). Conservation mandates enacted by either BLM, USFS, or NPS can directly affect the interests of private industries in the area, which in this case, is predominantly private landowners and the agricultural industry within these two states. Both Idaho P. lemhiensis populations occur on land allotted by BLM for grazing - POP7 occurs on the Perreau Creek allotment while POP6 occurs on the Muleshoe allotment (Bureau of Land Management, 2020). While the Montana populations do not occur on land allotted for grazing directly, POP3 occurs within approximately 130 meters of the Vipond-Glendale grazing allotment and within a reasonable distance such conservation management of the population could impact the neighboring allotment. Grazing allotment places individuals at risk of herbivory and trampling, as well as habitat alteration more broadly (Elzinga 1997).
3.2.3. Crowd
In this analysis, the crowd is designated as individuals or organizations that hold little authority and interest in the proceedings of conservation initiatives for P. lemhiensis (Fig. 5). The general civilian population of both Idaho and Montana have little power over the actions of BLM, USFS, and NPS and broadly low interest in their day-to-day priorities. This standing is conditional, and thus is subject to change across individuals based on their unique interests (Boiral & Heras-Saizarbitoria 2017). The citizenry has the capability of reaching out to representatives and public organizations when they feel the agency is not doing their due diligence regarding land management practices and obligations. This is most evident through citizen engagement during the public comment period of the Administrative Procedure Act.
3.2.4. Context Setters
Context setters are individuals or organizations that are within the scope of power to significantly affect conservation management for P. lemhiensis but have little interest in the process (Fig. 5). The prerogative of organizations to impact action is often derived from monetary allocation. In this case, the US Department of the Interior and US Department of Agriculture set agency priorities based on the annual budget and specified project appropriations. For example, the US Department of the Interior’s 2021 budget authorizes $244.1 million for the purpose of conserving, protecting, and enhancing both listed and at-risk fish, wildlife, plants, and their habitats, a 1.71% increase compared to their Fiscal Year 2020 budget (US Department of the Interior 2020). Further, the US Department of the Interior increased their Fiscal Year 2021 budget for listed species recovery by 13.5% when compared to Fiscal Year 2020. The US Department of Agriculture, which allocates annual funding to the US Forest Service, increased their budget for the National Forest System by 2.4% from Fiscal Year 2020 to Fiscal Year 2021 (US Department of Agriculture 2020). This prioritizes the implementation of programs that work to increase the health and resilience of Forest Service land while simultaneously meeting multiple-use land mandates. While both the Department of Interior and Department of Agriculture have generally increased their annual budgets for each agency, is it notable that only the Department of Interior specifically addressed the conservation and protection of at-risk or listed plant species within its budget summary. This detail, while incidental, denotes the priority placed by each department unto conservation initiatives. Organizations within the ‘Crowd’ designation are not considered key stakeholders but should be monitored regardless because of the impact they may have on policy decisions (Reed et al. 2009).
3.3. Conservation Management
The long-term persistence of a species is dependent upon its genetic diversity, a factor responsible for species resilience to deterministic and stochastic events as well as overall fitness (Bouzat 2010; Frankham 2005). Based on the genetic statistics and population structure, it is not immediately evident that P. lemhiensis is threatened or lacking in genetic diversity (Table 2). However, the high degree of physical separation, and the relatively small-estimated population sizes, despite detection of gene flow, is indicative of ancestral connectivity via a larger population. As a case in point, POP1 and POP4, two of the smallest estimated populations and physically distant, are still observed to maintain gene flow between each other. The relative recency of fragmentation makes aspects such as differentiation, inbreeding, and restricted gene flow more difficult to observe in our analyses. The small population sizes seen in a majority of the populations included in this study can contribute to the aforementioned effects and, eventually, to extinction (Markert et al. 2010). It is therefore recommended that, in the future, particular populations be monitored for ecological and demographic threats, along with measurements of fitness assessed within each population such that deleterious effects of inbreeding may be better detected (Reed & Frankham, 2003).
The high degree of differentiation observed between certain populations supports the conservation of as many populations as possible (Gaudeul et al. 2000). Priority should be placed upon populations with the most diversity; POP7 and POP8, in this case, albeit small in comparison. Future suitable habitat range, estimated based on climate change projections under a high-carbon emission scenario, severely reduce suitable habitat for P. lemhiensis (Fig. 4) such that only POP8 will likely persist (Fig. 4). While we advocate for the broadscale preservation of all P. lemhiensis populations, priority could be placed on populations with a high likelihood of survival under a rapidly changing planet.
Following the framework established by Ottewell et al. (2015), populations that are less differentiated from one another and show a high degree of gene flow, that is corroborated by close geographic proximity, should be monitored and managed to reduce threats to the populations – POP2, POP3, and POP4 fall into this category. Given that inbreeding within populations may be more serious than currently detectable, seed migration between close populations may also be more feasible. Seed germination practices should be cognizant of cold treatment and growth hormone requirements (Ramstetter 1983; Shelly 1990).
Populations that are highly differentiated from one another should be approached more cautiously. Analogously, these populations should be monitored, and ecological threats reduced. However, translocation of individuals, seeds, or pollen should be avoided due to risks associated with outbreeding depression (Frankham et al. 2011; Ottewell et al. 2015). Rather, focus should be placed on germplasm conservation. This includes methodology such as in situ and ex situ seed and pollen conservation, in vitro cultures, and cryptopreservation (Oseni et al. 2018; Paunescu 2009).
As indicated by the stakeholder analysis, the organizations with the most authority and interest in conservation management of P. lemhiensis are BLM, NPS, and USFS. Shifts in climate and subsequent suitable habitat for P. lemhiensis will likely result in only NPS-managed populations, but nevertheless, inter-agency relationships should be developed and fostered. Given the benefits of inter-agency collaboration in conservation, it is thus paramount that all three agencies work collectively to conserve the species uniformly (Maier & Wirth 2018). A cooperation tactic that may be utilized across agencies is the Landscape Conservation Cooperatives (LCC). Established in 2009, LCCs are intended to streamline interagency cooperation through a formal collaborative framework (NASEM 2016). Conservation management strategies founded on shared priorities across formal jurisdictions would, theoretically, lead to more effective and successful management. However, despite well intentions, it has become clear that conservation management is still approached independently by agencies. The complex web of federal, state, and local statutes and jurisdiction curtails cooperation and presents institutional challenges, even through programs such as LCCs (NASEM 2016). It is our recommendation that LCCs not be abandoned but utilized and built upon to ensure interagency cooperation in developing management strategies for P. lemhiensis conservation. Notably, collaborative organizational capacity must be developed in order to succeed (Foster-Fishman et al. 2001). Through the use of gap analysis, disparity in infrastructure and individual agency needs can be identified and remedied through various policy tools. Further, a formal participatory process should be developed and fostered. Expanding beyond the eight populations included within this study, all known, historic, observations of P. lemhiensis broaden the scope of agency involvement from three agencies to twelve, as well as privately managed land. This, together with the stakeholders identified in this study, constructs a need for a strong participatory process. Collaboration between public and private entities is a powerful tool (Ansell & Gash 2008) that should be explored.
An interagency communication strategy that allows for engagement of federal, state, tribal, private, and non-governmental stakeholders can be beneficial (Kark et al. 2015) and ensure the longevity of conservation management initiatives. While isolated to the issue of P. lemhiensis conservation, successful cooperative conservation strategies hold the potential to advance the dynamics of how issues of conservation are approached and valued in this country.