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Drought-Mediated Changes in Tree Physiological Processes Weaken Tree Defenses to Bark Beetle Attack

  • Thomas KolbEmail author
  • Ken Keefover-Ring
  • Stephen J. Burr
  • Richard Hofstetter
  • Monica Gaylord
  • Kenneth F. Raffa
Article
  • 68 Downloads

Abstract

Interactions between water stress and induced defenses and their role in tree mortality due to bark beetles are poorly understood. We performed a factorial experiment on 48 mature ponderosa pines (Pinus ponderosa) in northern Arizona over three years that manipulated a) tree water stress by cutting roots and removing snow; b) bark beetle attacks by using pheromone lures; and c) phloem exposure to biota vectored by bark beetles by inoculating with dead beetles. Tree responses included resin flow from stem wounds, phloem composition of mono- and sesqui-terpenes, xylem water potential, leaf gas exchange, and survival. Phloem contained 21 mono- and sesqui-terpenes, which were dominated by (+)-α-pinene, (−)-limonene, and δ-3-carene. Bark beetle attacks (mostly Dendroctonus brevicomis) and biota carried by beetles induced a general increase in concentration of phloem mono- and sesqui-terpenes, whereas water stress did not. Bark beetle attacks induced an increase in resin flow for unstressed trees but not water-stressed trees. Mortality was highest for beetle-attacked water-stressed trees. Death of beetle-attacked trees was preceded by low resin flow, symptoms of water stress (low xylem water potential, leaf gas exchange), and an ephemeral increase in concentrations of mono- and sesqui-terpenes compared to surviving trees. These results show a) that ponderosa pine can undergo induction of both resin flow and phloem terpenes in response to bark beetle attack, and that the former is more constrained by water stress; b) experimental evidence that water stress predisposes ponderosa pines to mortality from bark beetles.

Keywords

Dendroctonus Drought Pinus ponderosa Terpenes Tree chemical defense Induced defenses Tree mortality 

Notes

Acknowledgements

This work was supported by McIntire-Stennis Program project accession no. 230732 from the USDA National Institute of Food and Agriculture. John Kaplan, Ansley Roberts, Teresa Reyes, and Patrick Dunn provided valuable help in the field and laboratory; Roberts and Reyes were supported by the Hooper Undergraduate Research Program at Northern Arizona University and the National Science Foundation Research Experience for Undergraduates Program, respectively. The Northern Arizona University Centennial Forest provided the study site.

Supplementary material

10886_2019_1105_MOESM1_ESM.docx (643 kb)
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References

  1. Adams AS, Aylward FO, Adams SM, Erbilgin N, Aukema BH, Currie CR, Suen G, Raffa KF (2013) Mountain pine beetles colonizing historical and naive host trees are associated with a bacterial community highly enriched in genes contributing to terpene metabolism. Appl Environ Microbiol 79:3468–3475CrossRefGoogle Scholar
  2. Adams AS, Six DL, Adams SL, Holben WE (2008) In vitro interactions between yeasts and bacteria and the fungal symbionts of the mountain pine beetle (Dendroctonus ponderosae). Microb Ecol 56:460–466CrossRefGoogle Scholar
  3. Arango-Velez A, Chakraborty S, Blascyk K, Phan MT, Barsky J, El Kayal W (2018) Anatomical and chemical responses of eastern white pine (Pinus strobus) to blue-stain (Ophiostoma minus) inoculation. Forests 9:690.  https://doi.org/10.3390/f9110690 CrossRefGoogle Scholar
  4. Arango-Velez A, El Kayal W, Copeland CCJ, Zaharia LI, Lusebrink I, Cooke JEK (2016) Differences in defence responses of Pinus contorta and Pinus banksiana to the mountain pine beetle fungal associate Grosmannia clavigera are affected by water deficit. Plant, Cell Env 39:726–744CrossRefGoogle Scholar
  5. Bentz BJ, Régnière J, Fettig CJ, Hansen EM, Hayes JL, Hicke JA, Kelsey RG, Negron JF, Seybold SJ (2010) Climate change and bark beetles of the western United States and Canada: direct and indirect effects. Bioscience 60:602–613CrossRefGoogle Scholar
  6. Boone C, Aukema B, Bohlmann J, Carroll A, Raffa RF (2011) Efficacy of tree defense physiology varies with herbivore population density: a basis for positive feedback in eruptive species. Can J For Res 41:1174–1188CrossRefGoogle Scholar
  7. Boone CK, Keefover-Ring K, Mapes AC, Adams AS, Bohlmann J, Raffa KF (2013) Bacteria associated with a tree-killing insect reduce concentrations of plant defense compounds. J Chem Ecol 39:1003–1006CrossRefGoogle Scholar
  8. Burr S (2016) Where the maxilla meets the meristem: an examination of how bark beetles kill ponderosa pine in northern Arizona. Northern Arizona University, PhD Dissertation, 110 ppGoogle Scholar
  9. Davis TS (2015) The ecology of yeasts in the bark beetle holobiont: a century of research revisited. Microb Ecol 69:723–732CrossRefGoogle Scholar
  10. Davis TS, Hofstetter RW (2011) Reciprocal interactions between the bark beetle-associated yeast Ogataea pini and host plant phytochemistry. Mycologia 103:1201–1207CrossRefGoogle Scholar
  11. Davis TS, Hofstetter RW (2012) Plant secondary chemistry mediates the performance of a nutritional symbiont associated with a tree-killing herbivore. Ecology 93:421–429CrossRefGoogle Scholar
  12. Davis TS, Hofstetter RW (2013) Allometry of phloem thickness and resin flow and their relation to tree chemotype in a southwestern ponderosa pine forest. For Sci 60:270–274Google Scholar
  13. DeGomez TE, Hayes CJ, Anhold JA, McMillin JD, Clancy KM, Bosu PP (2006) Evaluation of insecticides for protecting southwestern ponderosa pines from attack by engraver beetles (Coleoptera: Curculionidae: Scolytinae). J Econ Entomol 99:393–400CrossRefGoogle Scholar
  14. Delalibera I, Handelsman J, Raffa KF (2005) Contrasts in cellulolytic activities of gut microorganisms between the wood borer, Saperda vestita (Coleoptera: Cerambycidae), and the bark beetles, Ips pini and Dendroctonus frontalis (Coleoptera: Curculionidae). Environ Entomol 34:541–547CrossRefGoogle Scholar
  15. Devine WD, Harrington TB (2008) Belowground competition influences growth of natural regeneration in thinned Douglas-fir stands. Can J For Res 38:3085–3097CrossRefGoogle Scholar
  16. Dobbertin M, Wermelinger B, Bigler C, Bürgi M, Carron M, Forster B, Gimmi U (2007) Rigling A. Linking increasing drought stress to Scots pine mortality and bark beetle infestations Sci World J 7:231–239Google Scholar
  17. Dunn JP, Lorio PL (1993) Modified water regimes affect photosynthesis, xylem water potential, cambial growth, and resistance of juvenile Pinus taeda L. to Dendroctonus frontalis (Coleoptera: Scolytidae). Environ Entomol 22:948–957CrossRefGoogle Scholar
  18. Erbilgin N (2019) Phytochemicals as mediators for host range expansion of a native invasive forest insect herbivore. New Phytol 221:1268–1278CrossRefGoogle Scholar
  19. Erbilgin N, Cale JA, Lusebrink I, Najar A, Klutsch JG, Sherwood P, Bonello PE, Evenden ML (2017) Water-deficit and fungal infection can differentially affect the production of different classes of defense compounds in two host pines of mountain pine beetle. Tree Physiol 37:338–350CrossRefGoogle Scholar
  20. Erbilgin N, Colgan LJ (2012) Differential effects of plant ontogeny and damage type on phloem and foliage monoterpenes in jack pine (Pinus banksiana). Tree Physiol 32:946–957CrossRefGoogle Scholar
  21. Erbilgin N, Powell JS, Raffa KF (2003) Effect of varying monoterpene concentrations on the response of Ips pini (Coleoptera: Scolytidae) to its aggregation pheromone: implications for pest management and ecology of bark beetles. Agric For Entomol 5:269–274CrossRefGoogle Scholar
  22. Feeney SR, Kolb TE, Wagner MR, Covington WW (1998) Influence of thinning and burning restoration treatments on presettlement ponderosa pines at the Gus Pearson natural area. Can J For Res 28:1295–1306CrossRefGoogle Scholar
  23. Fettig CJ, Reid ML, Bentz BJ, Sevanto S, Spittlehouse DL, Wang T (2013) Changing climates, changing forests: a western north American perspective. J For 111:214–228Google Scholar
  24. Franceschi VR, Krokene P, Christiansen E, Krekling T (2005) Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol 167:353–376CrossRefGoogle Scholar
  25. Fredericksen TS, Steiner KC, Skelly JM, Joyce BJ, Kolb TE, Kouterick KB, Ferdinand J|E (1996) Diel and seasonal patterns of leaf gas exchange and xylem water potentials in different-sized Prunus serotina Ehrh. Trees. For Sci 42:359–365Google Scholar
  26. Gaylord ML, Hofstetter RW, Kolb TE, Wagner MR (2011) Limited response of ponderosa pine bole defenses to wounding and fungi. Tree Physiol 31:428–437CrossRefGoogle Scholar
  27. Gaylord ML, Kolb TE, Pockman WT, Plaut JA, Yepez EA, Macalady AK, Pangle RE, McDowell NG (2013) Drought predisposes piñon-juniper woodlands to insect attacks and mortality. New Phytol 198:567–578CrossRefGoogle Scholar
  28. Gaylord ML, Kolb TE, Wallin KF, Wagner MR (2007) Seasonal dynamics of tree growth, physiology, and resin defenses in a northern Arizona ponderosa pine forest. Can J For Res 37:1173–1183CrossRefGoogle Scholar
  29. Gilmore AR (1977) Effects of soil moisture stress on monoterpenes in loblolly pine. J Chem Ecol 3:667–676CrossRefGoogle Scholar
  30. Herms D, Mattson W (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335CrossRefGoogle Scholar
  31. Hicke JA, Meddens AJH, Kolden CA (2016) Recent tree mortality in the western United States from bark beetles and forest fires. For Sci 62:141–153Google Scholar
  32. Hodges JD, Lorio PL (1975) Moisture stress and composition of xylem oleoresin in loblolly pine. For Sci 21:283–290Google Scholar
  33. Hofstetter RW (2004) Dynamics of the southern pine beetle. PhD Dissertation, Dartmouth College, New Hampshire, USAGoogle Scholar
  34. Hofstetter RW, Dempsey TD, Mahfouz JB, Klepzig KD (2007) Temperature-dependent effects on mutualistic, antagonistic and commensalistic interactions among insects, fungi and mites. Community Ecology 8:47–56CrossRefGoogle Scholar
  35. Hofstetter RW, Dinkins-Bookwalter J, Davis TS, Klepzig KD (2015) Symbiotic associations of bark beetles. In: Vega FE, Hofstetter RH (eds) Bark beetles: biology and ecology of native and invasive species. Academic Press, Elsevier Inc, San Diego, CA, pp 209–245CrossRefGoogle Scholar
  36. Hofstetter RW, Mahfouz JB, Klepzig KD, Ayres MP (2005) Effects of tree phytochemistry on the interactions among endophloedic fungi associated with the southern pine beetle. J Chem Ecol 31:551–572CrossRefGoogle Scholar
  37. Hood S, Sala A (2015) Ponderosa pine resin defenses and growth: metrics matter. Tree Physiol 35:1223–1235Google Scholar
  38. Hubbard RM, Rhoades CC, Elder K, Negron J (2013) Changes in transpiration and foliage growth in lodgepole pine trees following mountain pine beetle attack and mechanical girdling. For Ecol Manag 289:312–317CrossRefGoogle Scholar
  39. Kane JM, Kolb TE (2010) Importance of resin ducts in reducing ponderosa pine mortality following bark beetle attack. Oecologia 164:601–609CrossRefGoogle Scholar
  40. Kaufmann MR, Thor GL (1982) Measurement of water stress in subalpine trees: effects of temporary tissue storage methods and needle age. Can J For Res 12:969–972CrossRefGoogle Scholar
  41. Keefover-Ring K, Linhart YB (2010) Variable chemsitry and herbivory of ponderosa pine cones. Int J Plant Sci 171:293–302CrossRefGoogle Scholar
  42. Keefover-Ring K, Trowbridge A, Mason CJ, Raffa KF (2016) Rapid induction of multiple terpenoid groups by ponderosa pine in response to bark beetle-associated fungi. J Chem Ecol 42:1–12CrossRefGoogle Scholar
  43. Kerhoulas LP, Kolb TE, Koch GW (2013) Tree size, stand density, and the source of water used across seasons by ponderosa pine in northern Arizona. For Ecol Manag 289:425–433CrossRefGoogle Scholar
  44. Klepzig KD, Kruger EL, Smalley EB, Raffa KF (1995) Effects of biotic and abiotic stress on induced accumulation of terpenes and phenolics in red pines inoculated with bark beetle-vectored fungus. J Chem Ecol 21:601–626CrossRefGoogle Scholar
  45. Klepzig KD, Robison DJ, Fowler G, Minchin PR, Hain FP, Allen HL (2005) Effects of mass inoculation on induced oleoresin response in intensively managed loblolly pine. Tree Physiol 25:681–688CrossRefGoogle Scholar
  46. Koepke DF, Kolb TE (2013) Species variation in water relations and xylem vulnerability to cavitation at a forest-woodland ecotone. For Sci 59:524–535Google Scholar
  47. Kolb TE, Fettig CJ, Ayers MP, Bentz BB, Hicke JA, Mathiasen R, Stewart JE, Weed AS (2016) Observed and anticipated impacts of drought on forest insects and diseases in the United States. For Ecol Manag 380:321–334CrossRefGoogle Scholar
  48. Kolb TE, Holmberg KM, Wagner MR, Stone JE (1998) Regulation of ponderosa pine foliar physiology and insect resistance mechanisms by basal area treatments. Tree Physiol 18:375–381CrossRefGoogle Scholar
  49. Kolb T, Stone J (2000) Differences in leaf gas exchange and water relations among species and tree sizes in an Arizona pine–oak forest. Tree Physiol 20:1–12CrossRefGoogle Scholar
  50. Krokene P (2015) Conifer defense and resistance to bark beetles. In: Vega FE, Hofstetter RW (eds) Bark beetles. Academic Press, Elsevier Inc, San Diego, CA, Biology and Ecology of Native and Invasive Species, pp 177–207CrossRefGoogle Scholar
  51. Latta RG, Linhart YB (1997) Path analysis of natural selection on plant chemistry: the xylem resin of ponderosa pine. Oecologia 109:251–258CrossRefGoogle Scholar
  52. Latta RG, Linhart YB, Snyder MA, Lundquist L (2003) Patterns of variation and correlation in the monoterpene composition of xylem oleoresin within populations of ponderosa pine. Biochem Syst Ecol 31:451–465CrossRefGoogle Scholar
  53. Lieutier F (2004) Mechanisms of resistance in conifers and bark beetle attack. In: Wagner MR, Clancy KM, Lieutier F, Paine TD (eds) Mechanisms and deployment of resistance in trees to insects. Kluwer Academic, Boston, Massachusetts, pp 31–78Google Scholar
  54. Lorio PL Jr (1993) Environmental stress and whole-tree physiology. In: Schowalter TD, Filip GW (eds) Beetle-pathogen interactions in conifer forests. Academic Press, London, England, pp 81–101Google Scholar
  55. Lorio PL Jr, Stephen FM, Paine TD (1995) Environment and ontogeny modify loblolly pine response to induced acute water deficits and bark beetle attack. For Ecol Manag 73:97–110CrossRefGoogle Scholar
  56. Lombardero M, Ayres MP, Lorio PL, Ruel J (2000) Environmental effects on constitutive and inducible resin defences of Pinus taeda. Ecol Lett 3:329–339CrossRefGoogle Scholar
  57. Lusebrink I, Evenden ML, Guillaume Blanchet F, Cooke JEK, Erbilgrin N (2011) Effect of water stress and fungal inoculation on monoterpene emission from an historical and a new pine host of the mountain pine beetle. J Chem Ecol 37:1013–1026CrossRefGoogle Scholar
  58. Mason CJ, Keefover-Ring K, Villari C, Klutsch JG, Cook S, Bonello P, Erbilgin N, Raffa KF, Townsend PA (2018) Anatomical defenses against bark beetles relate to degree of historical exposure between species and are allocated independently of chemical defenses within trees. Plant Cell Env: DOI 42:633–646.  https://doi.org/10.1111/pce.13449 CrossRefGoogle Scholar
  59. Matthews B, Netherer S, Katzensteiner K, Pennerstorfer J, Blackwell E, Henschke P, Hietz P, Rosner S, Jannsson P-E, Schume H, Schopf A (2018) Transpiration deficits increase host susceptibility to bark beetle attack: experimental observations and practical outcomes for Ips typographus hazard assessment. Agr For Meteor 263:69–89CrossRefGoogle Scholar
  60. Mattson WJ, Haack RA (1987) The role of drought in outbreaks of plant-eating insects. Bioscience 37:110–118CrossRefGoogle Scholar
  61. McCullough DG, Wagner MR (1987a) Evaluation of four techniques to assess vigor of water-stressed ponderosa pine. Can J For Res 17:138–145CrossRefGoogle Scholar
  62. McCullough DG, Wagner MR (1987b) Influence of watering and trenching ponderosa pine on a pine sawfly. Oecologia 71:382–387CrossRefGoogle Scholar
  63. McDowell NG, Adams HD, Bailey JD, Kolb TE (2007) The role of stand density on growth efficiency, leaf area index and resin flow in southwestern ponderosa pine forests. Can J For Res 37:343–355CrossRefGoogle Scholar
  64. Miller G, Ambos N, Boness P, Reyher D, Robertson G, Scalzone K, Steinke R, Subirge T (1995) Terrestrial ecosystems survey of the Coconino National Forest. USDA Forest Service, Southwestern RegionGoogle Scholar
  65. Nebeker TE, Hodges JD, Blanche CA, Honea CR, Tisdale RA (1992) Variation in the constitutive defensive system of loblolly pine in relation to bark beetle attack. For Sci 38:457–466Google Scholar
  66. Netherer S, Matthews B, Katzensteiner K, Blackwell E, Henschke P, Hietz P, Pennerstorfer J, Rosner S, Kikuta S, Schume H, Schopt A (2015) Do water-limiting conditions predispose Norway spruce to bark beetle attack? New Phytol 205:1128–1141CrossRefGoogle Scholar
  67. Powell EN, Townsend PA, Raffa KF (2012) Wildfire provides refuge from local extinction but is an unlikely driver of outbreaks by mountain pine beetle. Ecol Monogr 82:69–84CrossRefGoogle Scholar
  68. Raffa KF, Aukema BH, Bentz BJ, Carroll AL, Hicke JA, Kolb TE (2015) Responses of tree-killing bark beetles to a changing climate. In: Niemela P (ed) Bjorkman C. CABI International Press, Climate Change and Insect Pests, pp 173–201Google Scholar
  69. Raffa KF, Aukema BH, Bentz BJ, Carroll AL, Hicke JA, Turner MG, Romme WH (2008) Cross-scale drivers of natural disturbances prone to anthropogenic amplification: dynamics of biome-wide bark beetle eruptions. Bioscience 58:501–518CrossRefGoogle Scholar
  70. Raffa KF, Berryman AA (1982) Physiological differences between lodgepole pines resistant and susceptible to the mountain pine beetle and associated microorganisms. Env Entomol 11:486–492CrossRefGoogle Scholar
  71. Raffa KF, Berryman AA (1983) The role of host plant resistance in the colonization behavior and ecology of bark beetles (Coleoptera: Scolytidae). Ecol Monogr 53:27–49CrossRefGoogle Scholar
  72. Raffa KF, Mason CJ, Bonello P, Cook S, Erbilgrin N, Keefover-Ring K, Klutsch JG, Villari C, Townsend PA (2017) Defence syndromes in lodgepole – whitebark pine ecosystems relate to degree of historical exposure to mountain pine beetles. Plant, Cell Env 40:1791–1806CrossRefGoogle Scholar
  73. Reeve JD, Ayres MP, Lorio PL Jr (1995) Host suitability, predation, and bark beetle population dynamics. In: Cappuccino N, Price PW (eds) Population dynamics: new approaches and synthesis. Academic Press, San Diego, California, pp 339–357CrossRefGoogle Scholar
  74. Reid RW, Whitney HS, Watson JA (1967) Reactions of lodgepole pine to attack by Dendroctonus ponderosae Hopkins and blue stain fungi. Can J Bot 45:1115–1126CrossRefGoogle Scholar
  75. Roth M, Hussain A, Cale JA, Erbilgin N (2018) Successful colonization of lodgepole pine trees by mountain pine beetle increased monoterpene production and exhausted carbohydrate reserves. J Chem Ecol: doi.org/10.1007/s10886-017-0922-0
  76. SAS Institute (2013) SAS version 9.4. SAS Institute, CaryGoogle Scholar
  77. Schoettle AW (1994) Influence of tree size on shoot structure and physiology of Pinus contorta and Pinus aristata. Tree Physiol 14:1055–1068CrossRefGoogle Scholar
  78. Seager R, Vecchi GA (2010) Greenhouse warming and the 21st century hydroclimate of southwestern North America. Proceedings of the National Academy of Sciences USA 107:21277–21282CrossRefGoogle Scholar
  79. Shea PJ, McGregor M (1987) A new formulation and reduced rates of carbaryl for protecting lodgepole pine from mountain pine beetle attack. W J Appl For 2:114–116Google Scholar
  80. Sheppard PR, Comrie AC, Packin GD, Angerbach K, Hughes MK (2002) The climate of the US southwest. Clim Res 21:219–238CrossRefGoogle Scholar
  81. Six D, Bracewell R (2015) Dendroctonus. In: Vega FE, Hofstetter RH (eds) Bark beetles: biology and ecology of native and invasive species: academic press. Elsevier Inc, San Diego, CA, pp 305–350Google Scholar
  82. Skov KR, Kolb TE, Wallin KF (2004) Tree size and drought affect ponderosa pine physiological response to thinning and burning treatments. For Sci 50:81–91Google Scholar
  83. Smith RH (2000) Xylem monoterpenes of pines, distribution, variation, genetics, function. General technical report PSW-GTR-177:U.S.D.a. Forest ServiceGoogle Scholar
  84. Squillace AE (1971) Inheritance of monoterpene composition in cortical oleoresin of slash pine. For Sci 17:381–387Google Scholar
  85. Strom BL, Goyer RA, Ingram LL Jr, Boyd GDL, Lott LH (2002) Oleoresin characteristics of progeny of loblolly pines that escaped attack by the southern pine beetle. For Ecol Manag 158:169–178CrossRefGoogle Scholar
  86. Turtola S, Manninen AM, Rikala R, Kainulainen P (2003) Drought stress alters the concentration of wood terpenoids in scots pine and Norway spruce seedlings. J Chem Ecol 29:1981–1995CrossRefGoogle Scholar
  87. Waalberg ME (2015) Fungi associated with three common bark beetle species in Norwegian scots pine forest. Norwegian University of Life Sciences, Ås, Master's thesisGoogle Scholar
  88. Wallin KF, Raffa KF (1999) Altered constitutive and inducible phloem monoterpenes following natural defoliation of jack pine: implications to host mediated interguild interactions and plant defense theories. J Chem Ecol 25:861–880CrossRefGoogle Scholar
  89. Wallin KF, Kolb TE, Skov K, Wagner MR (2003) Effects of crown scorch on ponderosa pine resistance to bark beetles in northern Arizona. Env Entomol 32:652–661CrossRefGoogle Scholar
  90. Wallin KF, Kolb TE, Skov K, Wagner MR (2008) Forest management treatments, tree resistance, and bark beetle resource utilization in ponderosa pine forests of northern Arizona. For Ecol Manag 255:3263–3269CrossRefGoogle Scholar
  91. Wright LC, Berryman AA, Gurusiddaiad S (1979) Host resistance to the fir engraver beetle, Scolytus ventralis (Coleoptera: Scolytidae). 4. Effect of defoliation on wound monoterpene and inner bark carbohydrate concentrations. Can Entomol 111:1255–1262CrossRefGoogle Scholar
  92. Vite JP (1961) The influence of water supply on oleoresin exudation pressure and resistance to bark beetle attack in Pinus ponderosa. Contr Boyce Thompson Inst 21:37–66Google Scholar
  93. Vite JP, Wood DL (1961) A study on the applicability of the measurement of oleoresin exudation pressure in determining susceptibility of second-growth ponderosa pine to bark beetle infestation. Contrib Boyce Thomps Inst 21:67–78Google Scholar
  94. Willyard A, Gernandt DS, Potter K, Hipkins V, Marguardt P, Mahalovich MF, Langer SK, Telewski FW, Cooper B, Douglas C, Finch K, Karemera HH, Lefler J, Lea P, Wofford A (2017) Pinus ponderosa: a checked past obscured four species. Am J Bot 104:1–21CrossRefGoogle Scholar
  95. Wood SL (1982) The bark and ambrosia beetles of north and Central America (Coleoptera: Scolytidae), a taxonomic monograph. Great Basin naturalist memoirs 6:1359 ppGoogle Scholar
  96. Yoder BJ, Ryan MG, Waring RH, Schoettle AW, Kaufmann MR (1994) Evidence of reduced photosynthetic rates in old trees. For Sci 40:513–527Google Scholar
  97. Zausen GL, Kolb TE, Bailey JD, Wagner MR (2005) Long-term impacts of thinning and prescribed burning on ponderosa pine physiology and bark beetle abundance in northern Arizona: a replicated landscape study. For Ecol Manag 218:291–305CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.School of ForestryNorthern Arizona UniversityFlagstaffUSA
  2. 2.Departments of Botany and GeographyUniversity of Wisconsin-MadisonMadisonUSA
  3. 3.Forest Health ProtectionUSDA Forest ServiceFairbanksUSA
  4. 4.Forest Health ProtectionUSDA Forest ServiceFlagstaffUSA
  5. 5.Department of EntomologyUniversity of Wisconsin-MadisonMadisonUSA

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