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New Forests

, Volume 50, Issue 1, pp 89–114 | Cite as

Regeneration for resilience framework to support regeneration decisions for species with populations at risk of extirpation by white pine blister rust

  • Anna W. SchoettleEmail author
  • William R. Jacobi
  • Kristen M. Waring
  • Kelly S. Burns
Article

Abstract

Natural forests are increasingly invaded by nonnative pests and pathogens that threaten host species with population extirpation and cascading ecological impacts. The regeneration for resilience (R4R) framework provides a decision structure to prioritize limited resources and utilize artificial and natural regeneration management to offer the best likelihood of success in positioning stands and landscapes to support multi-generational self-sustaining host populations in the presence of the nonnative invader by (1) increasing host population size to offset invader-caused mortality, (2) increasing the frequency of genetic resistance traits in host populations in habitats that enable their expression and durability to retard future mortality and facilitate population sustainability and recovery, and (3) maintain host genetic diversity, adaptive capacity, and population connectivity. This application is designed for conditions where the nonnative invader is expected to be a persistent threat, the host species naturally has some genetic resistance to the invasive species, and the forest host populations are integral to support valued ecosystem processes and services. The R4R framework has been developed for application in high elevation five-needle pine ecosystems of North America impacted and threatened by the nonnative pathogen Cronartium ribicola that causes the lethal disease white pine blister rust (WPBR). Several examples using the R4R framework to integrate information on current forest condition, WPBR risk or hazard, genetic resistance to WPBR, and host population dynamics and silvics to prioritize areas and design interventions are discussed. Effective management of forest regeneration dynamics can increase forest resilience and adaptive capacity to mitigate impacts of invasive species.

Keywords

Pinus albicaulis Pinus flexilis Pinus aristata Pinus strobiformis Five-needle pine White pine blister rust Genetic resistance Natural regeneration Artificial regeneration Invasive species 

Notes

Acknowledgements

We thank Kas Dumroese and John Stanturf for the invitation to prepare this manuscript for New Forests. Previous versions of this framework were presented by AWS at the Reforestation “Matters” Symposium (Portland, OR; April 2017) and the 5th International Workshop on the Genetics of Tree-Parasite Interactions (Orléans, France, August 2015) and we thank the organizers of these conferences and the discussions and feedback received from participants. We also thank three anonymous reviewers and recognize that this work has been enriched by discussions with Mike Antolin, Stu Field, Richard Sniezko, Jeff Connor, Christy Cleaver, Angelia Kegley, Betsy Goodrich, Holly Kearns, John Schwandt, Christine Holtz, Sparkle Malone, John Guyon, Gregg DeNitto, and others. Funding was provided in part by USDA Economic Research Service Program of Research on the Economics of Invasive Species Management grant PREISM-58-7000-8-0096 (Schoettle).

References

  1. Aitken SN, Yeaman S, Holliday JA, Wang T, Curtis-McLane S (2008) Adaptation, migration or extirpation: climate change outcomes for tree populations. Evol Appl 1:95–111CrossRefGoogle Scholar
  2. Alexander HM (2010) Disease in natural plant populations, communities, and ecosystems: insights into ecological and evolutionary processes. Plant Dis 94:492–503.  https://doi.org/10.1094/PDIS-94-5-0492 CrossRefGoogle Scholar
  3. Aubry C, Goheen D, Shoal R, Ohlson T, Lorenz T, et al (2008) Whitebark pine restoration strategy for the Pacific Northwest 2009–2013, Portland, OR: U.S. Department of Agriculture, Forest Service, Pacific Northwest Region, 212 pGoogle Scholar
  4. Baho DL, Allen CR, Garmestani AS, Fried-Petersen HB, Renes SE et al (2017) A quantitative framework for assessing ecological resilience. Ecol Soc 22(3):17.  https://doi.org/10.5751/ES-09427-220317 CrossRefGoogle Scholar
  5. Bentz BJ, Régnière J, Fettig CJ, Hansen EM, Hayes JL et al (2010) Climate change and bark beetles of the western United States and Canada: direct and indirect effects. Bioscience 60:602–613.  https://doi.org/10.1525/bio.2010.60.8.6 CrossRefGoogle Scholar
  6. Bond CA, Champ P, Meldrum J, Schoettle A (2011) Investigating the optimality of proactive management of an invasive forest pest. In: Keane RE, Tomback DF, Murray MP, Smith CM (eds) The future of high-elevation, five-needle white pines in Western North America: proceedings of the high five symposium, 28–30 June 2010, Missoula, MT. Proceedings RMRS-P-63. USDA Forest Service, Fort Collins, CO, pp 295–302. https://www.fs.fed.us/rm/pubs/rmrs_p063/rmrs_p063_295_302.pdf. Accessed 26 Apr 2018
  7. Borgman EM, Schoettle AW, Angert AL (2015) Assessing the potential for maladaptation during active management of limber pine populations: a common garden study detects genetic differentiation in response to soil moisture in the Southern Rocky Mountains. Can J For Res 45: 496–505. http://www.nrcresearchpress.com/doi/pdfplus/10.1139/cjfr-2014-0399. Accessed 26 Apr 2018
  8. Bower AD, Clair JB, Erickson V (2014) Generalized provisional seed zones for native plants. Ecol Appl 24:913–919CrossRefGoogle Scholar
  9. Boyd IL, Freer-Smith PH, Gilligan CA, Godfray HCJ (2013) The consequence of tree pests and diseases for ecosystem services. Science 342:1235773.  https://doi.org/10.1126/science.1235773 CrossRefGoogle Scholar
  10. Burns K, Blodgett J, Jackson M, Howell B, Jacobi W, et al (2011) Monitoring limber pine health in the Rocky Mountains and North Dakota. In: Keane RE, Tomback DF, Murray MP, Smith CM (eds) The future of high-elevation, five-needle white pines in Western North America: proceedings of the high five symposium, 28–30 June 2010, Missoula, MT. Proceedings RMRS-P-63. USDA Forest Service, Fort Collins, CO, pp 47–50. http://www.fs.fed.us/rm/pubs/rmrs_p063/rmrs_p063_047_050.pdf. Accessed 26 Apr 2018
  11. Carlson SM, Cunningham CJ, Westley PAH (2014) Evolutionary rescue in a changing world. Trends Ecol Evol 29:521–530CrossRefGoogle Scholar
  12. Casper AMA, Jacobi WR, Schoettle AW, Burns KS (2016) Restoration planting options for limber pine (Pinus flexilis James) in the Southern Rocky Mountains. J Torrey Bot Soc 143:21–37.  https://doi.org/10.3159/TORREY-D-14-00085 CrossRefGoogle Scholar
  13. Cavers S, Cottrell JE (2014) The basis of resilience in forest tree species and its use in adaptive forest management in Britain. Forestry 88:13–26.  https://doi.org/10.1093/forestry/cpu027 CrossRefGoogle Scholar
  14. Cleaver CM, Jacobi WR, Burns KS, Means RE (2015) Limber pine in the central and southern Rocky Mountains: stand conditions and interactions with blister rust, mistletoe, and bark beetles. For Ecol Manage 358:139–153CrossRefGoogle Scholar
  15. Cleaver CM, Burns KS, Schoettle AW (2017a) Limber Pine and White Pine Blister Rust Monitoring and Assessment Guide for Rocky Mountain National Park. Final Report prepared by Rocky Mountain Research Station for Rocky Mountain National Park for Inter-Agency Agreement 15-IA-11221633-157.p 28. https://www.fs.usda.gov/treesearch/pubs/56244. Accessed 23 July 2018
  16. Cleaver CM, Jacobi WR, Burns KS, Means RE (2017b) Limber pine regeneration and white pine blister rust in the central and southern Rocky Mountains. For Sci 63:151–164.  https://doi.org/10.5849/forsci.16-052 Google Scholar
  17. Conklin DA, Fairweather ML, Ryerson DE, Geils BW, Vogler DR (2009) White pines, blister rust, and management in the Southwest. USDA Forest Service, Southwestern Region, R3-FH-09-01Google Scholar
  18. Coop JD, Schoettle AW (2009) Regeneration of Rocky Mountain bristlecone pine (Pinus aristata) and limber pine (Pinus flexilis) three decades after stand-replacing fires. For Ecol Manage 257:893–903CrossRefGoogle Scholar
  19. Dale VH, Joyce LA, McNulty S, Neilson RP, Ayres MP et al (2001) Climate change and forest disturbances. Bioscience 51(9):723–734.  https://doi.org/10.1641/0006-3568(2001)051%5b0723:CCAFD%5d2.0.CO;2 CrossRefGoogle Scholar
  20. DeRose RJ, Long JN (2014) Resistance and resilience: a conceptual framework for silviculture. For Sci 60:1205–1212Google Scholar
  21. Dumroese RK, Williams MI, Stanturf JA, Clair JB (2015) Considerations for restoring temperate forests of tomorrow: forest restoration, assisted migration, and bioengineering. New For 46:947–964CrossRefGoogle Scholar
  22. Ennos RA (2015) Resilience of forests to pathogens: an evolutionary ecology perspective. Forestry 88:41–52CrossRefGoogle Scholar
  23. Field SG, Schoettle AW, Klutsch JD, Tavener SJ, Antolin MF (2012) Demographic projection of high elevation white pines infected with white pine blister rust: a nonlinear disease model. Ecol Appl 22:166–183CrossRefGoogle Scholar
  24. Ganley RJ, Sniezko RA, Newcombe G (2008) Endophyte-mediated resistance against white pine blister rust in Pinus monticola. For Ecol Manag 255:2751–2760CrossRefGoogle Scholar
  25. Geils BW, Conklin DA, Van Arsdel EP (1999) A preliminary hazard model of white pine blister rust for the Sacramento Ranger District, Lincoln National Forest. Research Note RMRS-RN-6. USDA Forest Service, Fort Collins, CO, 6pGoogle Scholar
  26. Geils BW, Hummer KE, Hunt RS (2010) White pines, Ribes, and blister rust: a review and synthesis. For Pathol 40:147–185.  https://doi.org/10.1111/j.1439-0329.2010.00654.x CrossRefGoogle Scholar
  27. Goodrich BA, Waring KM, Kolb TE (2016) Genetic variation in Pinus strobiformis growth and drought tolerance from southwestern United States populations. Tree Physiol 36:1219–1235CrossRefGoogle Scholar
  28. Goodrich BA, Waring KM, Auty D, Sánchez Meador AJ (2018) Interactions of management and white pine blister rust on Pinus strobiformis regeneration abundance in southwestern USA. Forestry 91:492–505.  https://doi.org/10.1093/forestry/cpy009 CrossRefGoogle Scholar
  29. Government of Alberta (2014) Species assessed by Alberta’s endangered species conservation committee. Retrieved November 10, 2014. http://esrd.alberta.ca/fish-wildlife/species-at-risk/documents/SpeciesAssessed-EndangeredSpecies-Jul18-2014.pdf
  30. Government of Canada (2012) Order amending Schedule 1 to the Species at Risk Act. Canada Gazette Part II, vol 146, no 14, SOR/2012-113, June 20, 2012 [online]. Retrieved March 19, 2015. http://www.sararegistry.gc.ca/virtual_sara/files/orders/g2-14614i_e.pdf
  31. Government of Canada (2014) COSEWIC Wildlife Species Assessments (detailed version), November 2014; Limber pine. Wildlife Species Assessment. Retrieved September 29, 2017. http://www.registrelep-sararegistry.gc.ca/virtual_sara/files/cosewic/sr_Limber%20Pine_2014_e.pdf
  32. Greater Yellowstone Coordinating Committee Whitebark Pine Subcommittee (2011) Whitebark pine strategy for the Greater Yellowstone Area, 41 pGoogle Scholar
  33. Gӓrtner SM, Bokalo M, Macdonald SE, Stadt K (2014) Variation in post-wildfire regeneration of boreal mixedwood forests: underlying factors and implications for natural disturbance-based management. New For 45:215–234CrossRefGoogle Scholar
  34. Hahn B, Landres P (2017) Supplement to minimum requirements analysis/decision guide (MRA/MRDG): evaluating proposals for ecological intervention in wilderness. Unpublished report from the Aldo Leopold Wilderness Research Institute, Missoula MT. 9p. https://www.wilderness.net/toolboxes/documents/restoration/Supplement%20to%20MRA-MRDG.pdf
  35. Hebard FV (2005) The backcross breeding program of the American Chestnut Foundation. J Am Chest Found 19(2):55–77Google Scholar
  36. Holtz CT, Tull AR, Merkle SA (2017) Influence of species and hybrid status on induction of somatic embryogenesis in Castanea. Can J For Res 47:382–388.  https://doi.org/10.1139/cjfr-2016-0362 CrossRefGoogle Scholar
  37. Howell B, Burns KS, Kearns HSJ, Witcosky JJ, Cross FJ (2006) Biological evaluation of a model for predicting presence of white pine blister rust in Colorado based on climatic variable and susceptible white pine species distribution. USDA Forest Service Biol Eval R2-06-04Google Scholar
  38. Jacobi WR, Kearns HSJ, Kegley A, Savin DP, Danchok R, Sniezko RA (2018) A comparative look at rust infection and resistance in limber pine and Rocky Mountain bristlecone pine following artificial inoculation at three inoculum densities. In: Schoettle AW, Sniezko RA, Kliejunas J (eds) Genetics of five-needle pines, rusts of forest trees, and Strobusphere: proceedings of the IUFRO joint conference. 15–20 June 2014, Fort Collins, CO. Proceedings RMRS-P-76, USDA Forest Service, Fort Collins, CO, pp 151–157. https://www.fs.usda.gov/treesearch/pubs/56054
  39. Jacobi WR, Kearns HSJ, Cleaver CM, Goodrich BA, Burns KS (in press) Epidemiology of white pine blister rust on limber pine in Colorado and Wyoming. For Pathol  https://doi.org/10.1111/efp.12465
  40. Jacobs DF, Dalgleish HJ, Nelson CD (2013) A conceptual framework for restoration of threatened plants: the effective model of American chestnut (Castanea dentata) reintroduction. New Phytol 197:378–393.  https://doi.org/10.1111/nph.12020 CrossRefGoogle Scholar
  41. Jacobs DF, Oliet JA, Aronson J, Bolte A, Bullock JM et al (2015) Restoring forests: What constitutes success in the twenty-first century? New For 46:601–614CrossRefGoogle Scholar
  42. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241.  https://doi.org/10.1111/j.1461-0248.2004.00684.x CrossRefGoogle Scholar
  43. Keane RE, Parsons RA (2010) Restoring Whitebark Pine Forests of the Northern Rocky Mountains, USA. Ecol Restor 28:56–70CrossRefGoogle Scholar
  44. Keane RE, Schoettle AW (2011) Strategies, tools, and challenges for sustaining and restoring high elevation five-needle white pine forests in Western North America. In: Keane RE, Tomback DF, Murray MP, Smith CM (eds) The future of high-elevation, five-needle white pines in Western North America: proceedings of the high five symposium, 28–30 June 2010, Missoula, MT. Proceedings RMRS-P-63. USDA Forest Service, Fort Collins, CO, pp 276–294Google Scholar
  45. Keane RE, Tomback DF, Aubry CA, Bower AD, Campbell EM, et al (2012) A range-wide restoration strategy for whitebark pine (Pinus albicaulis). General technical report. RMRS-GTR-279. Fort Collins, CO: U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, 108pGoogle Scholar
  46. Kearns HSJ, Jacobi WR, Reich RM, Flynn RL, Burns KS, Geils BW (2014) Risk of white pine blister rust to limber pine in Colorado and Wyoming, USA. For Pathol 44:21–38.  https://doi.org/10.1111/efp.12065 CrossRefGoogle Scholar
  47. Kim M-S, Brunsfeld SJ, McDonald GI, Klopfenstein NB (2003) Effect of white pine blister rust (Cronartium ribicola) and rust-resistance breeding on genetic variation in western white pine (Pinus monticola). Theor Appl Genet 106:1004–1010CrossRefGoogle Scholar
  48. King JN, David A, Noshad D, Smith J (2010) A review of genetic approaches to the management of blister rust in white pines. For Pathol 40:292–313.  https://doi.org/10.1111/j.1439-0329.2010.00659.x CrossRefGoogle Scholar
  49. Kinloch BB Jr (1992) Distribution and frequency of a gene for resistance to white pine blister rust in natural populations of sugar pine. Can J Bot 70:1319–1323CrossRefGoogle Scholar
  50. Kinloch BB Jr, Sniezko RA, Dupper GE (2004) Virulence gene distribution and dynamics of the white pine blister rust pathogen in western North America. Phytopathology 94:751–758.  https://doi.org/10.1094/PHYTO.2004.94.7.751 CrossRefGoogle Scholar
  51. Laine A-L, Burdon JJ, Dodds PN, Thrall PH (2011) Spatial variation in disease resistance: from molecules to metapopulations. J Ecol 99:96–112.  https://doi.org/10.1111/j.1365-2745.2010.01738.x CrossRefGoogle Scholar
  52. Landguth EL, Holden ZA, Mahalovich MF, Cushman SA (2017) Using landscape genetics simulations for planting blister rust resistant Whitebark Pine in the US Northern Rocky Mountains. Front Genet 8:9.  https://doi.org/10.3389/fgene.2017.00009 CrossRefGoogle Scholar
  53. Lenoir J, Hattab T, Pierre G (2017) Climatic microrefugia under anthropogenic climate change: implications for species redistribution. Ecography 40(2):253–266CrossRefGoogle Scholar
  54. Liu JJ, Schoettle AW, Sniezko RA, Sturrock RN, Zamany A et al (2016) Genetic mapping of Pinus flexilis major gene (Cr4) for resistance to white pine blister rust using transcriptome-based SNP genotyping. BMC Genom 17(1):753.  https://doi.org/10.1186/s12864-016-3079-2 CrossRefGoogle Scholar
  55. Looney CE, Waring KM (2012) Patterns of forest structure, competition and regeneration in southwestern white pine (Pinus strobiformis) forests. For Ecol Manage 286:159–170CrossRefGoogle Scholar
  56. Looney CE, Waring KM, Fairweather ML (2015) Chapter 12. Monitoring the health of Pinus strobiformis: Early impacts of white pine blister rust invasion (Project INT-EM-B-10-03). In: Potter KM, Conkling BL (eds) Forest health monitoring: national status, trends, and analysis 2013. General technical report SRS-GTR- 207. USDA Forest Service, Asheville, NC, pp 167–175Google Scholar
  57. Lovett GM, Weiss M, Liebhold AM, Holmes TP, Leung B et al (2016) Nonnative forest insects and pathogens in the United States: impacts and policy options. Ecol Appl 26:1437–1455CrossRefGoogle Scholar
  58. Mahalovich MF (2006) Limber pine seed transfer guidelines. USDA Forest Service Regions 1–4, internal reportGoogle Scholar
  59. Mahalovich MF, Dickerson GA (2004) Whitebark pine genetic restoration program for the Intermountain West (United States). In: Sniezko RA, Samman S, Schlarbaum S, Kriebel HB (eds) Breeding and genetic resources of five-needle pines: growth, adaptability and pest resistance; 2001 July 23–27; Medford, OR, USA. Proceedings RMRS-P-32. USDA Forest Service, Fort Collins, CO, pp 181–187Google Scholar
  60. Maher CT, Nelson CR, Larson AJ, Sala A (2018) Ecological effects and effectiveness of silvicultural restoration treatments in whitebark pine forests. For Ecol Manage 429:534–548.  https://doi.org/10.1016/j.foreco.2018.07.040 CrossRefGoogle Scholar
  61. Malone SL, Schoettle AW, Coop JD (2018) The future of subalpine forests in the Southern Rocky Mountains: trajectories for Pinus aristata genetic lineages. PLoS ONE 13(3):e0193481.  https://doi.org/10.1371/journal.pone.0193481 CrossRefGoogle Scholar
  62. Maloney PE, Vogler DR, Jensen CE, Mix AD (2011) Ecology of whitebark pine populations in relation to white pine blister rust infection in subalpine forests of the Lake Tahoe Basin, USA: implications for restoration. For Ecol Manage 280:166–175.  https://doi.org/10.1016/j.foreco.2012.05.025 CrossRefGoogle Scholar
  63. McKenney D, Pedlar J, O’Neill G (2009) Climate change and forest seed zones: past trends, future prospects and challenges to ponder. For Chron 85(2):258–266CrossRefGoogle Scholar
  64. McKinney ST, Fiedler CE, Tomback DF (2009) Invasive pathogen threatens bird-pine mutualism: implications for sustaining a high-elevation ecosystem. Ecol Appl 19:597–607CrossRefGoogle Scholar
  65. Meentemeyer R, Rizzo D, Mark W, Lotz E (2004) Mapping the risk of establishment and spread of sudden oak death in California. For Ecol Manage 200:195–214.  https://doi.org/10.1016/j.foreco.2004.06.021 CrossRefGoogle Scholar
  66. Meldrum JR, Champ PA, Bond CA (2013) Heterogeneous nonmarket benefits of managing white pine blister rust in high-elevation pine forests. J For Econ 19:61–77Google Scholar
  67. Millar CI, Stephenson NL (2015) Temperate forest health in an era of emerging megadisturbance. Science 349:823–826CrossRefGoogle Scholar
  68. Millar CI, Stephenson NL, Stephens SL (2007) Climate change and forests of the future: managing in the face of uncertainty. Ecol Appl 17(8):2145–2151CrossRefGoogle Scholar
  69. Millar CI, Charlet DA, Westfall RD, King J, Delany DL, et al (2018) Do low-elevation ravines provide climate refugia for subalpine limber pine (Pinus flexilis) in the Great Basin, USA? Can J For Res (in press)Google Scholar
  70. Nagel LM, Palik BJ, Battaglia MA, D’Amato AW, Guldin JM et al (2017) Adaptive silviculture for climate change: a national experiment in manager-science partnerships to apply an adaptation framework. J For 115(3):167–178Google Scholar
  71. Neuenschwander LF, Byler JW, Harvey AE, McDonald GI, Ortiz DS, et al (1999) White Pine in the American West: a vanishing species—Can we save it? United States Department of Agriculture Forest Service Rocky Mountain Research Station General Technical Report RMRS-GTR-35, 22pGoogle Scholar
  72. Oliva J, Boberg JB, Hopkins AJM, Stenlid J (2013) Concepts of epidemiology of forest diseases In: Gonthier P, Nicolotti G (eds) Infectious forest diseases CAB international, pp 1–28Google Scholar
  73. Potter KM, Jetton RM, Bower A, Jacobs DF, Man G et al (2017) Banking on the future: progress, challenges and opportunities for the genetic conservation of forest trees. New For 48:153–180.  https://doi.org/10.1007/s11056-017-9582-8 CrossRefGoogle Scholar
  74. Reynolds RT, Sanchez Meador AJ, Youtz JA, Nicolet T, Matonis MS et al (2013) Restoring composition and structure in Southwestern frequent-fire forests: a science-based framework for improving ecosystem resiliency. General technical reports RMRS-GTR-310. USDA Forest Service, Fort Collins, CO, 76pGoogle Scholar
  75. Richardson BA, Ekramoddoulah AKM, Liu J-J, Kim M-S, Klopfenstein NB (2010) Current and future molecular approaches to investigate the white pine blister rust pathosystem. For Pathol 40:314–331CrossRefGoogle Scholar
  76. Schoettle AW (2004) Ecological roles of five-needle pines in Colorado: Potential consequences of their loss. In: Sniezko RA, Samman S, Schlarbaum S, Kriebel HB (eds) Breeding and genetic resources of five-needle pines: growth, adaptability and pest resistance; 2001 July 23–27; Medford, OR, USA. Proceedings RMRS-P-32. USDA Forest Service, Fort Collins, CO, pp 124–135. https://www.fs.usda.gov/treesearch/pubs/52826
  77. Schoettle AW, Coop JD (2017) Range-wide conservation of Pinus aristata: a genetic collection with ecological context for proactive management today and resources for tomorrow. New For 48(2):181–199 http://link.springer.com/article/10.1007/s11056-017-9570-z
  78. Schoettle AW, Sniezko RA (2007) Proactive intervention to sustain high-elevation pine ecosystems threatened by white pine blister rust. J For Res 12: 327–336. http://www.springerlink.com/content/9v91t44278w74430/fulltext.pdf. Accessed 26 Apr 2018
  79. Schoettle AW, Sniezko RA, Burns KS (2009) Sustaining Pinus flexilis ecosystems of the Southern Rocky Mountains (USA) in the presence of Cronartium ribicola and Dendroctonus ponderosae in a changing climate. In: Breeding and Genetic Resources of Five-Needle Pines Conference, IUFRO Working Party 2.02.15, Yangyang, Republic of Korea, 2008 September 22–26. Korea Forest Research Institute, pp 63–65. http://www.iufro.org/download/file/4989/1191/20215-yangyang08-proceedings.pdf/
  80. Schoettle AW, Goodrich BA, Klutsch JG, Burns KS, Costello S, et al. (2011a) The proactive strategy for sustaining five-needle pine populations: An example of its implementation in the southern Rocky Mountains. In: Keane RE, Tomback DF, Murray MP, Smith CM (eds) The future of high-elevation, five-needle white pines in Western North America: proceedings of the high five symposium, 28–30 June 2010, Missoula, MT. Proceedings RMRS-P-63. USDA Forest Service, Fort Collins, CO, pp 323–334. https://www.fs.usda.gov/treesearch/pubs/38244
  81. Schoettle AW, Sniezko RA, Kegley A, Burns KS (2011b) Preliminary overview of the first extensive rust resistance screening tests of Pinus flexilis and Pinus aristata. In: Keane RE, Tomback DF, Murray MP, Smith CM (eds) The future of high-elevation, five-needle white pines in Western North America: proceedings of the high five symposium, 28–30 June 2010, Missoula, MT. Proceedings RMRS-P-63. USDA Forest Service, Fort Collins, CO, pp 265–269 http://www.fs.fed.us/rm/pubs/rmrs_p063/rmrs_p063_265_269.pdf
  82. Schoettle AW, Goodrich BA, Hipkins V, Richards C, Kray J (2012a) Geographic patterns of genetic variation and population structure in Pinus aristata, Rocky Mountain bristlecone pine. Can J For Res 42:23–37CrossRefGoogle Scholar
  83. Schoettle AW, Klutsch JG, Sniezko RA (2012b) Integrating regeneration, genetic resistance, and timing of intervention for the longterm sustainability of ecosystems challenged by non-native pests—a novel proactive approach. In: Sniezko RA, Yanchuk AD, Kliejunas JT, Palmieri KM, Alexander JM, Frankel SJ (tech. coord.) Proceedings of fourth international workshop genetics host-parasite interactions in forestry: disease and insect resistance in forest Trees, 31 July–5 Aug 2011, Eugene, OR. General technical reports. PSW-GTR-240. USDA Forest Service, Albany, CA, pp 112–123. https://www.fs.fed.us/psw/publications/documents/psw_gtr240/psw_gtr240_112.pdf
  84. Schoettle AW, Connor J, Mack J, Pineda Bovin P, Beck J, Baker GM, Sniezko RA, Burns KS (2013) Establishing the science foundation to sustain high-elevation five-needle pine forests threatened by novel interacting stresses in four western National Parks. George Wright Forum 30:302–312. http://www.georgewright.org/303schoettle.pdf. Accessed 26 Apr 2018
  85. Schoettle AW, Sniezko RA, Kegley A, Burns KS (2014) White pine blister rust resistance in limber pine: evidence for a major gene. Phytopathology 104:163–173.  https://doi.org/10.1094/PHYTO-04-13-0092-R. Accessed 26 Apr 2018
  86. Schoettle AW, Burns KS, Cleaver CM, Connor JJ (2018a) Proactive limber pine conservation strategy for the Greater Rocky Mountain National Park Area. General technical report RMRS-GTR-379 (in production). Fort Collins, CO: U.S. Department of Agriculture, Forest Service, Rocky Mountain Research StationGoogle Scholar
  87. Schoettle AW, Burns KS, Jacobi W, Popp J, Alberts S, et al. (2018b) Southern Rockies rust resistance trial. In: Schoettle AW, Sniezko RA, Kliejunas J (eds) Genetics of five-needle pines, rusts of forest trees, and Strobusphere: Proceedings of the IUFRO Joint Conference, 15–20 June 2014; Fort Collins, CO. Proceedings RMRS-P-076. USDA Forest Service, Fort Collins, CO, pp 158–161 https://www.fs.fed.us/rm/pubs_series/rmrs/proc/rmrs_p076.pdf
  88. Schubert GH, Pitcher JA (1973) A provisional tree seed-zone and cone-crop rating system for Arizona and New Mexico. USDA-FS Res. Pap. RM-105, Rocky Mountain Forest and Range Exp. Stat., Fort Collins, CO, 8 pGoogle Scholar
  89. Schwandt JW, Lockman IB, Kliejunas JT, Muir JA (2010) Current health issues and management strategies for white pines in the western United States and Canada. For Pathol 40:226–250.  https://doi.org/10.1111/j.1439-0329.2010.00656.x CrossRefGoogle Scholar
  90. Seidl R (2014) The shape of ecosystem management to come: anticipating risks and fostering resilience. Bioscience 64:1159–1169CrossRefGoogle Scholar
  91. Seidl R, Spies TA, Peterson DL, Stephens SL, Hicke JA (2016) Searching for resilience: addressing the impacts of changing disturbance regimes on forest ecosystem services. J Appl Ecol 53:120–129CrossRefGoogle Scholar
  92. Smith CM, Langor DW, Myrholm C, Weber J, Gillies C, Stuart-Smith J (2013a) Changes in white pine blister rust infection and mortality in limber pine over time. Can J For Res 43:919–928.  https://doi.org/10.1139/cjfr-2013-0072 CrossRefGoogle Scholar
  93. Smith CM, Shepherd B, Gillies C, Stuart-Smith J (2013b) Changes in blister rust infection and mortality in whitebark pine over time. Can J For Res 43:90–96.  https://doi.org/10.1139/cjfr-2012-0127 CrossRefGoogle Scholar
  94. Sniezko RA (2006) Resistance breeding against nonnative pathogens in forest trees: current successes in North America. Can J Plant Pathol 28:S270–S279CrossRefGoogle Scholar
  95. Sniezko RA, Koch J (2017) Breeding trees resistant to insects and diseases: putting theory into application. Biol Invasions 19:3377.  https://doi.org/10.1007/s10530-017-1482-5 CrossRefGoogle Scholar
  96. Sniezko RA, Mahalovich MF, Schoettle AW, Vogler DR (2011) Past and current investigations of the genetic resistance to Cronartium ribicola in high-elevation five-needle pines. In: Keane RE, Tomback DF, Murray MP, Smith CM (eds) The future of high-elevation, five-needle white pines in Western North America: proceedings of the high five symposium, 28–30 June 2010, Missoula, MT. Proceedings RMRS-P-63. USDA Forest Service, Fort Collins, CO, pp 246–264. https://www.fs.usda.gov/treesearch/pubs/38234
  97. Stanturf JA (2015) Future landscapes: opportunities and challenges. New For 46:615–644CrossRefGoogle Scholar
  98. Steiner KC, Westbrook JW, Hebard FV, Georgi LL, Powell WA, Fitzsimmons SF (2017) Rescue of American chestnut with extra specific genes following its destruction by a naturalized pathogen. New For 48:317–336CrossRefGoogle Scholar
  99. Telford A, Cavers S, Ennos RA, Cottrell JE (2015) Can we protect forests by harnessing variation in resistance to pests and pathogens? For Int J For Res 88:3–12.  https://doi.org/10.1093/forestry/cpu012 Google Scholar
  100. Thrall PH, Burdon JJ, Young A (2001) Variation in resistance and virulence among demes of a plant host-pathogen metapopulation. J Ecol 89:736–748.  https://doi.org/10.1046/j.0022-0477.2001.00597.x Google Scholar
  101. Tomback DF, Achuff P (2010) Blister rust and western forest biodiversity: ecology, values and outlook for white pines. For Pathol 40:186–225CrossRefGoogle Scholar
  102. U.S. Fish and Wildlife Service (2015) Endangered and threatened wildlife and plants: review of native species that are candidates for listing as endangered or threatened, annual notice of findings on resubmitted petitions, annual description of progress on listing actions. Federal register. A notice by the fish and wildlife service on 12/24/2015. https://federalregister.gov/a/2015-32284. Accessed 1 Nov 2017
  103. Vogler DR, Delfino-Mix AD, Schoettle AW (2006) White pine blister rust in high-elevation white pines: screening for simply-inherited, hypersensitive resistance. In: Guyon JC (ed) Proceedings of the 53rd western international forest disease work conference; 2005 September 26–30; Jackson, WY. USDA Forest Service, Intermountain Region, Ogden UT, pp 73–82Google Scholar
  104. Waring KM, Goodrich BA (2012) Artificial regeneration of five-needled pines of western North America: a survey of current practices and future needs. Tree Plant Notes 55(2):55–71Google Scholar
  105. Waring KM, O’Hara KL (2005) Silvicultural strategies in forest ecosystems affected by introduced pests. For Ecol Manage 209:27–41CrossRefGoogle Scholar
  106. Whiteley AR, Fitzpatrick SW, Funk WC, Tallmon DA (2015) Genetic rescue to the rescue. Trends Ecol Evol 30:42–49CrossRefGoogle Scholar
  107. Woo K-S, Fins L, McDonald GI, Wiese MV (2001) Differences in needle morphology between blister rust resistant and susceptible western white pine stocks. Can J For Res 31:1880–1886CrossRefGoogle Scholar
  108. Woodcock P, Cottrell JE, Buggs RJA, Quine CP (2017) Mitigating pest and pathogen impacts using resistant trees: a framework and overview to inform development and deployment in Europe and North America. For Int J For Res 00:1–16.  https://doi.org/10.1093/forestry/cpx031 Google Scholar
  109. Xhaard C, Fabre B, Andrieux A, Gladieux P, Barrès B et al (2011) The genetic structure of the plant pathogenic fungus Melampsora larici-populina on its wild host is extensively impacted by host domestication. Mol Ecol 20:2739–2755CrossRefGoogle Scholar
  110. Zeglen S, Pronos J, Merler H (2010) Silvicultural management of white pines in western North America. For Pathol 40:347–368CrossRefGoogle Scholar

Copyright information

© This is a U.S. government work and its text is not subject to copyright protection in the United States; however, its text may be subject to foreign copyright protection 2018

Authors and Affiliations

  1. 1.USDA Forest ServiceRocky Mountain Research StationFort CollinsUSA
  2. 2.Department of Bioagricultural Sciences and Pest ManagementColorado State UniversityFort CollinsUSA
  3. 3.School of ForestryNorthern Arizona UniversityFlagstaffUSA
  4. 4.USDA Forest ServiceForest Health ProtectionLakewoodUSA

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