Abstract Conservation scientists emphasize the importance of maintaining a connected network of protected areas to prevent ecosystems and populations from becoming isolated, reduce the risk of extinction, and ultimately sustain biodiversity. Keeping protected areas connected in a network is increasingly recognized as a conservation priority in the current era of rapid climate change. Models that identify suitable linkages between core areas have been used to prioritize potentially important corridors for maintaining functional connectivity. Here, we identify the most “natural” (i.e., least human-modified) corridors between large protected areas in the contiguous Unites States. We aggregated results from multiple connectivity models to develop a composite map of corridors reflecting agreement of models run under different assumptions about how human modification of land may influence connectivity. To identify which land units are most important for sustaining structural connectivity, we used the composite map of corridors to evaluate connectivity priorities in two ways: (1) among land units outside of our pool of large core protected areas and (2) among units administratively protected as Inventoried Roadless (IRAs) or Wilderness Study Areas (WSAs). Corridor values varied substantially among classes of “unprotected” non-core land units, and land units of high connectivity value and priority represent diverse ownerships and existing levels of protections. We provide a ranking of IRAs and WSAs that should be prioritized for additional protection to maintain minimal human modification. Our results provide a coarse-scale assessment of connectivity priorities for maintaining a connected network of protected areas.

Citation: Belote RT, Dietz MS, McRae BH, Theobald DM, McClure ML, Irwin GH, et al. (2016) Identifying Corridors among Large Protected Areas in the United States. PLoS ONE 11(4): e0154223. https://doi.org/10.1371/journal.pone.0154223 Editor: Robert F. Baldwin, Clemson University, UNITED STATES Received: January 22, 2016; Accepted: April 11, 2016; Published: April 22, 2016 Copyright: © 2016 Belote et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability: All relevant data are within the paper and its Supporting Information files. Funding: The Wilderness Society funded this work. The funder provided support in the form of salaries for author JAG, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section. Competing interests: Author Gage is employed by Gage Cartographics. This does not alter the authors' adherence to PLOS ONE policies on sharing data and materials.

Introduction Protected areas or ecological reserves (e.g., wilderness areas, national parks) form the foundation of conservation strategies to sustain biological diversity [1]. Established to reduce human impacts, protected areas are intended to maintain populations of species and ecological functions [2, 3]. Isolated protected areas, however, may not provide for species migration and dispersal or ecological flows of materials required to sustain genetic and species diversity, population recovery, and ecosystem processes [4]. Protected areas unconnected to a network may serve only as temporary insular ecosystems, vulnerable to population isolation or environmental change [5, 6] and may be at greater risk of experiencing local species extirpations. A long history of ecological and conservation science has addressed questions of reserve design, extinction risks from isolation, and the value of connectivity [7]. Moreover, creating, restoring, and maintaining large, connected networks of protected areas has emerged as one of the highest priorities for conservation in the age of climate change [8–11]. Providing organisms opportunities to move long distances, possibly over many generations, is a necessary conservation strategy to ensure that species can shift their distributions to track expected climate change [12]. Maintaining relatively natural and undeveloped connections between protected areas in a network of ecological reserves may be the best means for conserving biodiversity now and in the future [13]. In response to a growing number of theoretical frameworks [14–16] and empirical demonstrations of the importance of connectivity for maintaining biodiversity [17–19], a suite of analytical tools has been developed to identify linkages or potential corridors between protected areas, known populations, or potential habitat [20,21]. Two primary approaches to assess connectivity have been used [22]: those based on species-specific habitat requirements and those focused on identifying corridors using landscape “naturalness” as a proxy for the needs of multiple species [23,24]. Most connectivity models assume that organisms moving across a landscape or region will incur costs of movement (or resistance to travel) corresponding to energetic expense or risk of mortality [25]. Many connectivity models thus identify corridors where cost of, or resistance to, movement is minimized [26,27]. Connectivity models based on a landscape’s “naturalness” (i.e., degree of human modification) likely represent well the potential costs of movement, especially for species that are sensitive to human disturbance [24]. In fact, many species-specific connectivity models assume animal avoidance of human-altered areas [25]. As climate change forces shifts in the distribution of species and habitats [12,28], identifying large, continental-scale corridors of high naturalness (sensu [23]) may also be a critical conservation strategy to sustain biodiversity [3]. Many federally-owned and -managed lands of the United States (e.g., lands managed by the U.S. Forest Service and Bureau of Land Management) are currently undergoing land-use planning. Identifying regionally important corridors that may provide ecological connections between protected areas, as well as federal land units that fall along these corridors, can inform decisions regarding additional land protection or mitigating impacts of land use, including resource extraction, motorized recreation, and other activities. In some cases, land units are being considered as candidates for elevated levels of protection. For example, Inventoried Roadless and Wilderness Study Areas could be recommended for permanent protection, or alternatively for “release” to increased recreational or commercial use. Quantifying the contribution of these candidate land units for maintaining a connected network of large protected areas may help the public and land managers prioritize which units should receive elevated levels of protection. Here, we develop a national-scale connectivity model with the aim of identifying potential priorities for maintaining connectivity among existing, large protected areas of the contiguous United States of America (hereafter, U.S.). This differs from a previous national analysis of connectivity developed by Theobald et al. [23] that identified pathways through lands with low human modification, but without an explicit aim to model potential connections between protected areas. Here, we identify the least human-modified corridors between large protected areas based on two different indices of human modification (or inversely, naturalness) to create a composite map of corridors that highlights agreement among models run with various assumptions about how connectivity potential may be influenced by the degree of human modification of lands. We used the composite corridor map to ask two questions about connectivity between existing protected areas. First, we asked which conservation lands not within our pool of identified large protected core areas contribute to the identified corridors. Second, we asked which Inventoried Roadless Areas and Wilderness Study Areas on U.S. federal lands would contribute most to connectivity if added to the protected area system in the future.

Discussion Corridors identified here represent the “wildest” or most “natural” lands that may provide broad-scale ecological linkages between large protected core areas. Maintaining or enhancing the relatively high degree of naturalness and low degree of human impact along these corridors may be an important strategy to ensure that the large protected areas in the U.S. do not become isolated and are maintained in a connected network [3]. Such continental-scale connectivity is a critical component to conserving ecosystems and biodiversity under a changing climate and accelerated land use change [35,41]. Maintaining relatively natural corridors between protected areas should allow mobile organisms short-term opportunities for movement, while providing more sessile organisms opportunities to move over generations. Our connectivity assessment could be used in regional conservation strategies, administrative planning, or legislative or executive efforts (such as wilderness bills or national monument proclamations) that support important linkages between protected areas. Corridors identified here may be among the most important areas on which to focus conservation efforts, including the elevation of their protective status through conservation designations (e.g., permanently limit human impacts of an area by increasing the level of land protection from an inventoried roadless area to recommended or legislated wilderness). We demonstrate one relatively easy way to evaluate connectivity priorities by calculating the mean composite corridor value of different ecoregions and land management units. Here, we focused on lands ≥ 3,000 ha within the PAD, IRAs, and WSAs, but similar methods could be used to evaluate individual national forests or BLM jurisdictions to help prioritize areas to maintain connectivity (e.g., [42]). Prioritizing lands to maintain connectivity could result in management objectives that maintain natural land cover and limit development along the best corridors. It can also help inform designation to higher levels of protection on high priority lands (e.g., Basin and Range National Monument). By far the greatest number of PAD units outside of core protected areas are managed by the U.S. Forest Service and Bureau of Land Management, and many of these units (IRAs and WSAs) are eligible to receive a higher level of protection through administrative or legislative means. Our results demonstrate that some PAD lands outside of existing cores, even those with low levels of protection (Gap 3 and 4 lands), possess high value as corridors and should be considered for inclusion in a national network of large protected areas. Although federal agencies dominated the total land area evaluated in this analysis, many non-federal agency and private lands possessed high connectivity importance. Maintaining connectivity and functioning corridors will require that conservation strategies be developed across all lands, even when their management objectives may be less protective or lack explicit goals to maintain biodiversity. For example, S1 Table shows that lands administered by universities, the NRCS, Regional Agencies, and private landowners all can make important contributions. This assessment could also inform land trust efforts to prioritize acquisition of conservation easements on lands that contribute to broad-scale connectivity. Cross-ownership efforts to create or sustain a connected network of protected areas will be challenging and require further study, including economic cost-benefit analyses coupled with further ecological research (sensu [43]). Although our study focused on identifying linkages among large and highly protected core areas, similar models could be run to investigate corridors between much smaller—but ecologically important—core areas with varying levels of maximum distance thresholds between cores. These analyses may be important supplements to the national-scale analysis presented here for identifying local connectivity priorities. Given the expanse of our study (the U.S.), we chose to focus on identifying corridors between the largest and most-well-protected core areas with maximum distances between cores of 300 km, reflecting maximum dispersal of large wide-ranging mammals [39, and see 24]. However, we acknowledge that different core areas and maximum distances will yield different outcomes. While we developed our corridor maps based on assumption of the widest-ranging species, we did not explicitly consider any species-specific habitat requirements. We assume if the wild or natural character of lands are maintained or restored between protected areas that animals with shorter dispersal distances would be also benefit (see discussion of “umbrella” species in [44]). At more regional scales, other smaller core areas could be used in similar analyses with varying assumptions (see S5 Fig). Corridor values may change depending on choices in number and location of cores and the maximum distance between cores. In situations where core areas are few and maximum distances used to connect cores is relatively low, corridors may be absent between protected areas. Direct connections between cores can be made by increasing the number of core areas (e.g., by reducing the minimum size threshold or changing assumptions about what is considered a core protected area) so that they fall between large cores and serve as “stepping stones” [45] or by increasing the maximum distances between cores. Users of our national model outputs should be aware of these sensitivities. Our final maps removed the 10% most costly corridors. We pruned the connections in this way to ensure that the “worst” corridors were not reflected in the final map of connectivity priorities. These relatively developed and human modified corridors may be too far modified to actually function as high value linkages, though our 10% cutoff was arbitrary and the functionality of corridors both above and below this threshold is expected to depend on many factors. S4 Fig shows where these pruned corridors occurred, which was mostly in the agricultural and highly developed Mid-west and eastern U.S. However, we also recognize that these relatively costly linkages may actually be critical regions on which to focus connectivity efforts. For example, corridors passing through the highly altered Tennessee Valley between protected areas on the Cumberland Plateau and the Great Smoky Mountains National Park were removed based on our 10% highest cost pruning but could actually represent important connectivity potential for organisms such as black bears (Ursa Americana [46]). While our final maps presented here focus on the best corridors, we believe that even costly linkages could represent important priorities for maintaining or restoring connectivity. Models that identify landscape permeability irrespective of existing, designated protected cores are an important—and complementary—means of identifying national connectivity priorities (sensu [23]). In fact, many corridors our model identified were similar to flowpaths identified by Theobald et al. [23]. Other efforts have emphasized the importance of riparian areas for the value as functional or potential corridors [13,47]. We did not explicitly incorporate riparian features in our models, but our results could be combined with efforts focused on riparian corridors (e.g., [48]). We view the model outputs presented here and other similar efforts [23] as presenting a reasonable first-approximation for identifying lands that should receive a higher degree of protection through management policy, legislation, or executive action that establish and sustain a connected network of large protected areas in the U.S. Such efforts are ongoing through land management planning of federal agencies, investment decisions by land trusts, and legislative actions by policy makers. Our models could be supplemented or modified based on any available data on individual organisms’ dispersal needs or habitat models generated by more in-depth study [24].

Conclusions Our results provide an initial identification of priorities to create a national connected network of large protected areas. As federal land agencies begin assessments of connectivity, the models presented here could serve as a coarse-filter assessment for evaluating regional connectivity priorities. They could also serve in the evaluation of individual land units and their potential role in maintaining connectivity among large core protected areas. Land units with high connectivity value could be prioritized for future protection to maintain potential large-scale connectivity. Maintaining such large-scale corridors between protected areas may ensure that protected cores are connected via a system of relatively natural lands. These lands may allow individual wide-ranging animals to disperse via corridors in the short-term [24], with potential for long-term migration and dispersal to take place by organisms with more limited dispersal abilities.

Acknowledgments We thank Paul Beier, Kathy Zeller, Rob Baldwin, and one anonymous reviewer for comments and suggestions that significantly improved the paper. Thanks to Anne Rockhold for help with copy-editing.

Author Contributions Conceived and designed the experiments: RTB MSD GHI PSM GHA JAG BHM. Performed the experiments: RTB JAG. Analyzed the data: RTB. Contributed reagents/materials/analysis tools: RTB BHM DMT MLM JAG. Wrote the paper: RTB MSD GHA BHM DMT MLM GHI PSM.