ASSOCIATIONS OF SECONDARY BARK BEETLES WITH DYING AND LIVE LODGEPOLE PINE IN THE POST-OUTBREAK PHASE OF MOUNTAIN PINE BEETLE, DENDROCTONUS PONDEROSAE (HOPKINS), IN THE CENTRAL INTERIOR OF BRITISH COLUMBIA, CANADA by EwingTeen1 B.S. University of Wisconsin-Madison, 2003 Under the supervision of Dr. Brian H. Aukema1,3 Committee members: Dr. Allan L. Carroll2, Dr. Lisa M. Poirier1 External examiner: Dr. Richard W. Hofstetter4 THESIS IS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE IN BIOLOGY University of Northern British Columbia, Canada 2University of British Columbia, Canada 3University of Minnesota, United States of America "Northern Arizona University, United States of America April 2012 © EwingTeen, 2012 1+1 Library and Archives Canada Bibliotheque et Archives Canada Published Heritage Branch Direction du Patrimoine de I'edition 395 Wellington Street Ottawa ON K1A0N4 Canada 395, rue Wellington Ottawa ON K1A 0N4 Canada Your file Votre reference ISBN: 978-0-494-87520-9 Our file Notre reference ISBN: 978-0-494-87520-9 NOTICE: AVIS: The author has granted a non­ exclusive license allowing Library and Archives Canada to reproduce, publish, archive, preserve, conserve, communicate to the public by telecommunication or on the Internet, loan, distrbute and sell theses worldwide, for commercial or non­ commercial purposes, in microform, paper, electronic and/or any other formats. L'auteur a accorde une licence non exclusive permettant a la Bibliotheque et Archives Canada de reproduire, publier, archiver, sauvegarder, conserver, transmettre au public par telecommunication ou par I'lnternet, preter, distribuer et vendre des theses partout dans le monde, a des fins commerciales ou autres, sur support microforme, papier, electronique et/ou autres formats. The author retains copyright ownership and moral rights in this thesis. Neither the thesis nor substantial extracts from it may be printed or otherwise reproduced without the author's permission. L'auteur conserve la propriete du droit d'auteur et des droits moraux qui protege cette these. Ni la these ni des extraits substantiels de celle-ci ne doivent etre imprimes ou autrement reproduits sans son autorisation. In compliance with the Canadian Privacy Act some supporting forms may have been removed from this thesis. Conformement a la loi canadienne sur la protection de la vie privee, quelques formulaires secondaires ont ete enleves de cette these. While these forms may be included in the document page count, their removal does not represent any loss of content from the thesis. Bien que ces formulaires aient inclus dans la pagination, il n'y aura aucun contenu manquant. Canada Dendroctonus ponderosae (Hopkins) or mountain pine beetle is a native bark beetle (Coleoptera: Curculionidae: Scolytinae) that feeds on more than 20 species of pine in western North America. In British Columbia, its principal host is lodgepole pine (Pinus contorta var. latifolia Engelmann). As a "primary" bark beetle, D. ponderosae kills its host at epidemic stages, exerting profound landscape-level mortality. As of 2012, D. ponderosae has caused the loss of 726 million cubic meters of timber, covering an area of 17.5 million hectares of mature pine forest in British Columbia and Alberta. Small diameter hosts are not suitable for D. ponderosae, however, creating a niche for the "secondary" bark beetles, including Ips pini (Say), Pseudips mexicanus (Hopkins), and Orthotomicus latidens (LeConte). At the post-epidemic stage of D. ponderosae, we found the rate of new mortality was approximately 4%, which 1% of the mortality was associated with a complex of secondary bark beetles, and not D. ponderosae, as the principal mortality agent in those stands. This finding suggests that at high population densities, secondary bark beetles are potential mortality agents of residual pines, sustaining the apparent outbreak of D. ponderosae by killing smaller diameter trees, with the highest rate of mortality among younger stands. Table of Contents ABSTRACT II TABLE OF CONTENTS Ill LIST OF TABLES V LIST OF FIGURES XXVII ACKNOWLEDGEMENTS XU INTRODUCTION 1 THE OUTBREAK OF DENDROCTONUS PONDEROSAE IN BRITISH COLUMBIA AND SUBSEQUENT LODGEPOLE PINE MORTALITY THE BARK BEETLES OF LODGEPOLE PINE IN BRITISH COLUMBIA DENDROCTONUS PONDEROSAE (HOPKINS), MOUNTAIN PINE BEETLE IPS PINI (SAY), PINE ENGRAVER 4 4 4 5 HYLURGOPS SPP. (LECONTE), SOUR SAP BARK BEETLES 6 ORTHOTOMICUS LATIDENS (LECONTE), SMALLER WESTERN PINE ENGRAVER PSEUDIPS MEXICANUS (HOPKINS), MONTEREY PINE ENGRAVER 7 7 DENDROCTONUS MURRAYANAE (HOPKINS), LODGEPOLE PINE BEETLE 8 PLTYOGENES SPP. (BEDEL), TWIG BEETLES PITYOPHTHORUS SPP. (EICHHOFF), TWIG BEETLES AMBROSIA BEETLES (TRYPODENDRON LINEATUM [OLIVER], GNATHOTRICHUS [LECONTE]) 8 9 9 EPIDEMIOLOGY OF BARK BEETLE POPULATIONS 10 IMPORTANCE OF THE OUTBREAK OF DENDROCTONUS PONDEROSAE AND ITS EFFECT ON THE ECONOMY AND ENVIRONMENT 12 OBJECTIVES 15 AUTHORSHIP 15 MATERIALS AND METHODS 16 SECTION 1: WHAT DO STANDS LOOK LIKE IN THE POST-OUTBREAK PHASE OF AN EPIDEMIC OF DENDROCTONUS PONDEROSAE? . 16 PART I. STAND SELECTION PART II. STAND ESTABLISHMENT PART III. STAND CLASSIFICATIONS (DENSITY AND MATURITY) SECTION 2: WHICH INSECTS AND/OR PATHOGENS ARE MOST CLOSELY ASSOCIATED WITH NEW TREE MORTALITY? RESULTS 16 17 18 19 23 SECTION 1: WHAT DO STANDS LOOK LIKE IN THE POST-OUTBREAK PHASE OF AN EPIDEMIC OF DENDROCTONUS PONDEROSAE? . 23 COMPARISONS BETWEEN DIAMETERS AND HEIGHTS OF LIVE VS. DEAD LODGEPOLE PINE 24 SECTION 2: WHICH INSECTS AND/OR PATHOGENS ARE MOST CLOSELY ASSOCIATED WITH NEW TREE MORTALITY? 25 DISCUSSION 31 iii CONCLUSION: SYNTHESIS AND IMPLICATIONS FOR CONTROL AND MANAGEMENT 37 MECHANICAL INTERVENTION: STAND HYGIENE AND HEALTHY SANITATION PRACTICES 38 PARTI. PREVENTION: CULTURAL CONTROLS 38 PART II. TREATMENT: DIRECT CONTROLS 39 BIOLOGICAL MANIPULATION: SEMIOCHEMICALS 40 PART I. MONITORING THE POPULATIONS OF BARK BEETLES 41 PART II. AGGREGATION AND ANTI-AGGREGATION MECHANISMS 42 PART III. INDUCED COMPETITION AND PREDATORY RESPONSE 42 CHEMICAL CONTROL 43 BEST CONTROL METHODS OF BARK BEETLES AT DIFFERENT POPULATION DENSITIES 44 PUBLIC PARTICIPATION, EDUCATION, AWARENESS AND REGULATION 46 IMPORTANCE AND CONSEQUENCES OF BARK BEETLE OUTBREAKS 47 REFERENCES 48 APPENDICES 73 APPENDIX A. NICHE PARTITIONING BY CHEMICAL PROFILES BY VARIOUS BARK BEETLES 77 APPENDIX B. PHOTOGRAPHIC GUIDE TO THE ATTACK STAGES OF LODGEPOLE PINE IN THE CENTRAL INTERIOR OF BRITISH COLUMBIA 83 APPENDIX C. MAP OF THE SEVEN STUDY SITES AND SNAPSHOT OF DENDROCTONUS PONDEROSAE OUTBREAKS IN THE CENTRAL INTERIOR OF BRITISH COLUMBIA IN THE YEAR 1999,2004, AND 2008 84 APPENDIX D. PHOTOGRAPHS OF THE SEVEN SITES IN THE CENTRAL INTERIOR OF BRITISH COLUMBIA 86 APPENDIX E. SURVEY METHODOLOGY TO EXAMINE AND MONITOR MORTALITY OF LODGEPOLE PINE IN THE CENTRAL INTERIOR OF BRITISH COLUMBIA 93 APPENDIX F. PHOTOGRAPHIC GUIDE AND DESCRIPTIONS OF THE VARIOUS INSECTS (I.E. ADULT BARK BEETLES AND THEIR GALLERIES) AND OTHER AGENTS OF LODGEPOLE PINE MORTALITY IN SITES IN THE CENTRAL INTERIOR OF BRITISH COLUMBIA 95 APPENDIX 6. REFERENCES OF THE AGENT OF LODGEPOLE PINE MORTALITY APPENDIX GL: IDENTIFICATION OF ADULT BARK BEETLES ASSOCIATED UNDER THE BARK APPENDIX G2. IDENTIFICATION OF BARK BEETLE GALLERIES UNDER THE BARK APPENDIX H: SIZE RELATIONSHIPS OF TREES WITH VARIOUS SIGNS OF BARK BEETLE ACTIVITY 116 116 118 123 INDIVIDUAL SECONDARY BARK BEETLES 124 OTHER BIOTIC DISTURBANCES: ROOT COLLAR DAMAGE BY INSECTS, WOOD BORERS AND WESTERN GALL RUST INTERACTIONS AMONG THE BARK BEETLES AND WITH OTHER BIOTIC DISTURBANCES 126 127 APPENDIX I: CASE STUDY OF MAC3-C: THE PERFECT MORTALITY-STORM FROM A COMBINED EFFECT OF STAND DENSITY AND MATURITY FROM SECONDARIES 130 RATIOS AMONG STANDS, AS COMPARABLE INDICATORS OF MORTALITY ASSOCIATED-AGENTS EXCEPTION THAN THE RULE: HIGHER ASSOCIATIONS OF SECONDARY BARK BEETLES IN MAC3-C 133 138 SUMMARY OF CASE STUDY OF MAC3-C, IN COMPARISON TO SIMILAR TYPE OF STANDS 140 APPENDIX J: CROSS INTERACTIONS BETWEEN BARK BEETLES IN TREES WITH FRASS 143 APPENDIX K: SIZE RELATIONSHIPS OF TREES WITH FRASS WITH BARK BEETLE ACTIVITY 151 APPENDIX L: JUSTIFICATION FOR GROUPING HYLURGOPS SPP. AND DENDROCTONUS MURRAYANAE IN THE SAME CATEGORY 155 iv List of Tables Table 1. Spatial niche partitioning by various bark beetles: Dendroctonus ponderosae, Ips pini, Hylurgops spp., Orthotomicus latidens, Pseudips mexicanus, Dendroctonus murrayanae, Pityogenes spp., Pityophthorus spp., and ambrosia beetles, in lodgepole pine in British Columbia Table 2. Temporal niche partitioning by various bark beetles: Dendroctonus ponderosae, Ips pini, Hylurgops spp., Orthotomicus latidens, Pseudips mexicanus, Dendroctonus murrayanae, Pityogenes spp., Pityophthorus spp., and ambrosia beetles, in lodgepole pine in British Columbia Table 3. Summary of coniferous and deciduous tree species surveyed in 10 x 10 m plots across seven sites in the central interior of British Columbia, Canada, 2009-2010 Table 4. Stand density and maturity categorizations based on lodgepole pine surveyed for this study in seven plots, comprising 15 plots in the central interior of British Columbia, Canada, 2009-2010 Table 5. Differences in diameter-at-breast-height (dbh) and height as a function of current lodgepole pine condition in 2010 (category: dead or alive) in the postoutbreak stage of a Dendroctonus ponderosae outbreak in British Columbia, Canada Table 6. Summary of diameter-at-breast-heights (in cm) measured on live lodgepole pine surveyed in the central interior regions of British Columbia, Canada, 2009 and 2010 v Table 7. Summary of tree height measurements (in m) of the live lodgepole pines surveyed in the central interior regions of British Columbia, Canada, 2009 and 2010 Table 8. Summary of the 373 dead lodgepole pine associated with the individual species of secondary bark beetle: Ips pini (IP), Hylurgops spp. and/or Dendroctonus murrayanae (H-LPB), Orthotomicus latidens (OL), Pseudips mexicanus (PM), Pityogenes spp. and/or Pityophthorus spp. (PT), and ambrosia beetles (AMB) in the northern interior region of British Columbia at the post-outbreak stage of Dendroctonus ponderosae in the seven sites (Table 8A) and the 15 plots (Table 8B) Table 9. Summary of all the surveyed lodgepole pines, the presence of Dendroctonus ponderosae (2009, 2010), the presence of root collar damage by insects (2010) and the assemblage of secondary bark beetles (2010) in the northern interior region of British Columbia at the post-outbreak stage of D. ponderosae in the seven sites (Table 9A) and the 15 plots (Table 9B). Table 10. Likelihood of tree mortality as a function of presence/absence of signs of various insects and root collar damage by insects in 624 lodgepole pine across the overall seven sites (Table 10A) and the individual study sites (Table 10B) in British Columbia, Canada in 2010, with the best models ranked by decreasing AIC value Table 11. A detailed summary of 21 lodgepole pines with frass and their interactions with various insects, broken tops, or the other agents of tree mortality recorded in 2010 at the post-outbreak stage of Dendroctonus ponderosae in central British Columbia, Canada Table 12. A detailed summary of 25 lodgepole pines with new mortality recorded in the five sites near Mackenzie in 2010 at the post-outbreak stage of D. ponderosae, exhibiting the multiple interactions of bark beetles in the trees in the stands vi Table 1. Spatial niche partitioning in lodgepole pine by various bark beetles: Dendroctonus ponderosae, Ips pini, Hylurgops spp., Orthotomicus latidens, Pseudips mexicanus, Dendroctonus murrayanae, Pityogenes spp., Pityophthorus spp., and ambrosia beetles, in lodgepole pine in British Columbia Bark beetles Number of host species Characteristics (SPATIAL partition) Predominant regions on tree (Location) Gallery shape, and length (Appendices F and G) Beetle morphological features Unique characteristics for identification Dendroctonus ponderosae (Hopkins) >30 hosts of pines, 8 non-pine hosts, 11exotics Main bole, below 5 m on healthy trees (at outbreaks) Hook-(J)shaped, gallery 30 cm long, monogamous, female-initiated Dark brown to black, 3.7-7.5 mm No spines, broader than Hylurgops Ips pini (Say) >10 hosts of pines, 7 non-pine hosts, all pine hosts overlapped with D. ponderosae Top larger branches, and spreading downward or main bole in absence of competitors Star-(X,Y)shaped, each arm 13-25 cm long polygamous (up to 8 females), male-initiated Dark reddish brown to nearly black, 3.5-4.2 mm 4 declivity spines, with third spine elongated (male) Antenna club is subcapitated, bi-sinuate Hylurgops spp. (LeConte), sour sap bark beetles Most conifers: pines, spruces, firs, Douglas fir, western hemlock Large roots, and root collar regions Aggregated feeding by larvae without a pattern, black stain on gallery to separate from D. murrayanae Reddish brown to black, 3.1-5.7 mm (depending on species Hylurgops porosus: known vector of Leptographium wageneri (W.B. Kendr.) M.J.Wingf. that stain the gallery black Orthotomicus latidens (LeConte) >10 hosts of pines, 6 non-pine hosts, most pine hosts overlapped with D. ponderosae Thinner bark of smaller trees, upper canopy of larger trees Horizontal-(L,Y)shaped, each arm 3-5 cm long, monogamous, male-initiated Dark reddish brown, 2.3-3.6 mm 3 declivity spines Antenna club is broadly sinuate to nearly straight Pseudips mexicanus (Hopkins) >15 hosts of pines, which 8 is exotics, 10 overlapped pine hosts with D. ponderosae Root collar regions, below 1m Curved-(C,S)shaped, each arm 5-6 cm long, polygamous (up to 3 females), maleinitiated Dark reddish brown, 3.6-5.0 mm 3 declivity spines Antenna club is strongly arcuate - continued next page vii - continuation - Characteristics (SPATIAL partition) of host species Predominant regions on tree (Location) Gallery shape, and length (Appendices F and G) Beetle morphological features Unique characteristics for identification Dendroctonus murrayanae (Hopkins) 5 hosts of pines: lodgepole, jack. red, whitebark. and eastern white 3 spruces Large roots, and root collar regions. below 0.6 m Aggregated feeding chambers by larvae, 13-23 cm long, monogamous, female-initiated Dark brown to black body with reddish brown elytra. 5.0-7.3 mm Aggregated feeding chamber with red frass (if fresh). median longitunidal subcarinate line above the epistomal process Pityogenes spp. (Bedel), i.e. primarily P. knechteli (Swaine) found in lodgepole pine Most pines, and some spruce (species dependent) Mostly on smaller trees, or on the smaller branches, larger twigs. thinner barks of larger trees Star-(*)shaped, polygamous (up to 10 females), male-initiated Dark reddish brown to nearly black, 1.8-3.7 mm (depending on species) Pityophthorus spp. (Eichhoff), >10 species of this genus attacks lodgepole pine Most conifers, and some deciduous, (species dependent) Mostly on smaller trees, or on the smaller branches, twigs, thinner barks of larger tree Star-(* (shaped, mainly polygamous (up to 5 or more females, initiated by male), but some monogamous Yellowish brown to almost black. 0.8-3.2 mm (depending on species) 2,3 large teeth spines on male declivity, deeply excavated frons on female, among the smallest of beetle. Antenna club is compressed with two sutures Chitinized septa on antennal clubs (refer Bright, 1981), among the smallest of beetle based on size Ambrosia beetles, i.e. primarily Trypodendron lineatum, and Gnathotrichus spp. Most conifers, and some deciduous (species dependent) Primarily in sapwood. between the outermost phloem and hardwood in the center Pinsized-hole of tunnels (into the wood), 3-dimensional galleries within sapwood Dark reddish brown to black. 2.0-3.7 mm (depending on species) Bark beetles viii 'Hole' tunnels, with black stain fungus surrounding the 'hole' T. lineatum: unmarked suture in antenna club, pronotum is flattened and subquadrate (if male) or subcircular (if female) Table 2. Temporal niche partitioning in lodgepole pine by various bark beetles: Dendroctonus ponderosae, Ips pini, Hylurgops spp., Orthotomicus latidens, Pseudips mexicanus, Dendroctonus murrayanae, Pityogenes spp., Pityophthorus spp., and ambrosia beetles, in lodgepole pine in British Columbia Characteristics (TEMPORAL partition) Bark beetles Peak flight period(s) Mean generation time Number of generation(s) per year Dendroctonus ponderosae (Hopkins) End-July to mid-August Lodgepole pine: more than 28 days at constant 24°C Univoltine, up to 2 broods per year Ips pini (Say) Mid-May (last season adults), end-July (re-emergent or brood 1), end-Aug to early-Sept (re-emergents) Lodgepole pine: about 34 days at 25-35°C, or about 60 days (in field, Alberta) Bivoltine, up to 3 broods per year (in BC) Hylurgops spp. (LeConte) sour sap bark beetles All summer throughout the growing period Unknown, possibly more than one year per generation, common to other root-feeders Semivoltine, one generation every 1.5-2.5 years Orthotomicus latidens (LeConte) End-May to early-June, end-July (re-emergent or brood 1) Lodgepole pine: 64-124 (mean: 77) days at 25-35°C Univoltine, up to 2 broods per year Pseudips mexicanus (Hopkins) End-May to early-June, early to mid-Aug (re-emergent or brood 1) Lodgepole pine: 49 days at constant 26.5°C Univoltine, up to 2 broods per year - continued next page - ix continuation Characteristics (TEMPORAL partition) Bark beetles Peak flight period(s) Mean generation time Number of generation(s) per year Dendroctonus murrayanae (Hopkins) Mid-June to mid-July Lodgepole pine: >26 days (in the field) Univoltine Pityogenes spp. (Bedel), i.e. primarily P. knechteli (Swaine) found in lodgepole pine P. knechteli: end-May, early-July to early-August (re-emergent or brood 1) P. knechteli in lodgepole pine: about 6-8 weeks in field, Alberta (estimate from Reid 1955) P. knechteli: Univoltine, up to 2 broods per year Pityophthorus spp. (Eichhoff), >10 species of this genus attacks lodgepole pine Unknown, possibly highly variable, depending on species Unknown, possibly highly dependent on the latitude, elevation and host Univoltine (in general), but can vary by latitude and elevation (Bright 1981) Ambrosia beetles, i.e. primarily Trypodendron lineatum, and Gnathotrichus spp. T. lineatum: end-April to May, & mid-summer Gnathotrichus spp.: May-June, & throughout summer Ambrosia beetles (in general): 6-10 weeks in the field 7. lineatum: 9-10 weeks Univoltine, up to 2 broods per year x Table 3. Summary of coniferous and deciduous tree species surveyed in 10 x 10 m plots across seven sites in the central interior of British Columbia, Canada, 2009-2010 Conifers Site Plot Total trees n Macl Macl Mac2 Mac2 Mac3 Mac3 Mac3 Mac4 Mac4 Mac5 Mac5 CCk CCk CLk CLk Total A B A B A B C A B A B A B A B % 76 9 150 18 21 3 72 9 11 1 77 9 67 8 55 7 82 10 33 4 57 7 51 6 28 3 24 3 23 3 827 100 Lodgepole pine (PI) Interior spruce (Sx) % n 52 68 126 84 57 12 71 99 11 100 61 79 67 100 37 67 63 77 30 91 35 20 35 69 17 61 14 58 35 8 75 624 0 4 6 1 0 14 0 16 15 1 25 n Black spruce (Sb) 0 3 29 1 0 18 0 29 18 3 44 3 6 1 4 7 29 3 13 96 12 xi Subalpine fir (Bl) Douglas fir (Fd) Trembling aspen (At) Paper birch (Ep) % n % n % n % n 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 8 14 0 0 0 0 3 13 11 48 22 3 0 0 0 0 0 0 0 1 4 0 0 13 10 0 0 28 0 0 0 0 0 0 0 2 5 0 0 25 36 0 0 3 0 0 0 0 0 2 0 0 0 2 4 0 0 0 0 0 3 0 0 0 6 7 0 0 0 0 1 24 17 3 0 0 0 0 0 0 0 0 0 0 0 1 45 32 11 14 0 0 0 0 0 0 0 0 0 0 3 2 0 0 0 0 0 0 0 0 0 0 1 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 4 1 n % Deciduous 0 0 0 0 8 0 0 0 4 5 % Table 4. Stand density and maturity categorizations based on lodgepole pine surveyed for this study in seven plots, comprising 15 plots in the central interior of British Columbia, Canada, 2009-2010. Each plot was unique, with a variety of alive and dead lodgepole pine, mean diameters, and mean heights. Refer to text (M1.3) for further details in the methods of categorization Stand density of lodgepole pine Site Macl Macl Mac2 Mac2 Mac3 Mac3 Mac3 Mac4 Mac4 Mac5 Mac5 CCk CCk CLk CLk Total Plot A B A B A B C A B A B A B A B n 52 126 12 71 11 61 67 37 63 30 20 35 17 14 8 624 2009 2010 Alive DeadRatio Alive DeadRatio 37 15 58 68 8 4 34 37 7 4 23 38 0 0 6 31 21 42 10 20 10 10 10 25 8 9 2 12 2 6 236 321 0.4 1.2 0.5 1.1 0.6 1.7 - 5.2 2.0 2.0 1.0 2.5 1.1 6.0 3.0 1.4 37 54 6 24 15 72 6 47 6 5 20 41 40 27 4 33 21 42 9 21 8 12 10 25 8 9 2 12 2 6 251 373 Stand maturity of lodgepole pine Classt 0.4 1.3 1.0 2.0 0.8 2.1 0.7 8.3 2.0 2.3 1.5 2.5 1.1 6.0 3.0 1.5 Diameter (cm) Height (m) Class* Min Max Mean Min Max Mean M H L H 0.7 0.9 1.1 0.4 3.5 1.6 2.1 3.8 3.1 1.5 1.7 1.8 8.5 5.9 3.6 0.4 5.1 5.8 7.6 6.5 10.3 6.9 7.3 12.0 9.9 10.9 10.6 11.8 17.3 16.6 13.8 8.4 1.5 2.0 1.7 1.5 3.2 2.4 3.9 4.0 2.0 2.4 2.1 2.2 10.6 10.1 5.4 1.5 10.6 14.0 L H H M H M L M L L L M 14.5 17.0 18.4 15.5 21.2 14.2 13.6 23.9 20.7 19.9 20.2 22.2 26.9 26.5 20.4 26.9 5.3 7.8 5.6 8.2 9.8 9.0 9.6 15.0 13.4 12.4 10.7 12.6 17.5 18.8 15.2 10.1 9.3 14.7 16.0 13.4 16.5 24.8 21.2 16.8 15.8 20.3 22.0 25.6 20.4 25.6 Y Y Y Y YO Y Y O O YO YO O O O O YO * L (low density, 0-25 pine/plot), M (medium density, 26-59 pine/plot), H (high density, 260 pine/plot) * O (old or 'mature', average diameter i10cm, max. diam. 2 20cm, average height a 10m, max. height 2 20m), YO (young-old, meet more than 2 but less than 4 of the old (O) requirements, 2 £ YO < 4), Y (young, average diameter < 10cm, max. diam. < 20cm, average height < 10m, max. height < 20m) Table 5. Differences in diameter-at-breast-height (dbh) and height as a function of current Iodgepole pine condition in 2010 (category: dead or alive) in the post-outbreak stage of a Dendroctonus ponderosae outbreak in British Columbia, Canada. The results with a significance difference are in bold Sample size Lodgepole Plots pine Mean diameter-at-breast-height Alive(cm) Dead(cm) df t (±SE) (±SE) p-value Alive(m) (±SE) Mean height Dead(m) t (+SE) Mad 178/177* 2 6.4(±1.0) 4.4(±1.1) 3.86 175 <0.001 7.9(±1.8) 4.7(±1.9) Mac2 83 2 4.9(±1.4) 8.1(±1.6) 4.16 80 <0.001 6.0(±1.7) Mac3 72 2 8.1(±2.2) 8.7(±2.4) 0.68 69 0.50 Mac4 100 2 9.0(±1.7) 11.4(±2.0) 2.27 97 Mac5 50 2 9.4(±2.5) 11.4(±3.0) 1.19 CCk 52 2 15.9(±3.5) 13.5{±3.9) CLk 22 2 15.8(±4.7) Total 624 15 9.9(±1.4) Site df p-value 6.94 174 <0.001 7.9(±1.9) 2.12 80 <0.05 9.4(±1.3) 9.0(±1.5) 0.46 69 0.64 <0.05 14.0(±1.9) 14.1(±2.2) 0.08 97 0.93 47 0.24 12.3(±2.2) 11.3(+2.6) 0.71 47 0.48 1.42 49 0.16 17.9(±2.9) 13.3(±3.3) 3.13 49 <0.01 15.6{±5.8) 0.06 19 0.95 18.8(±4.3) 16.8(±5.2) 0.66 19 0.52 10.4(±1.5) 1.40 608 0.16 12.1(±1.6) 11.2(±1.6) 2.54 607 <0.05 The difference in sample size between the diameter and height was due to one iodgepole pine height determined to be non-measurable (on ground, with missing top) xiii Table 6. Summary of diameter-at-breast-heights (in cm) measured on live lodgepole pine surveyed in the central interior regions of British Columbia, Canada, 2009 and 2010. The table shows the total number of residual live lodgepole pine within the site, the measurements (in cm) of the smallest, largest and mean diameter size of the residuals, the changes in the number of dead trees within year 2009 and 2010, and as a result, the changes in mean diameter-atbreast-height of the residuals within each site 2009 Site Alive (n) Macl 2010 Plot A 37 Min Max Mean Alive (n) Min Max Mean 1.4 12.5 5.6 1.4 12.5 5.6 37 New mortality (2009 to 2010) Changes in mean diameter (cm) = Macl B 58 1.6 11.3 7.0 54 1.6 11.3 7.1 0 +4 Mac2 A 8 1.1 11.6 5.0 6 1.1 5.0 3.0 +2 4, 2.0 Mac2 B 34 1.1 9.6 5.4 24 1.1 9.6 5.0 + 10 4, 0.4 Mac3 A 7 3.5 14.6 9.4 6 3.5 14.6 9.4 +1 = Mac3 B 23 2.6 10.7 6.8 20 2.6 10.7 6.6 +3 4/ 0.2 Mac3 C - 40 2.1 10.3 6.1 N.A. +2 N.A. - - -f 0.1 Mac4 A 6 6.3 13.2 9.2 4 6.3 11.3 8.9 Mac4 B 21 5.0 12.5 8.6 21 5.0 12.5 8.6 Mac5 A 10 2.5 12.9 8.9 9 2.5 12.9 9.1 0 +1 Mac5 B 10 2.9 14.4 9.9 8 2.9 14.4 9.9 +2 = CCk A 10 10.6 22.2 14.6 10 10.6 22.2 14.6 0 = CCk B 8 12.0 22.0 17.0 8 12.0 22.0 17.0 0 = CLk A 2 14.9 15.2 15.1 2 14.9 15.2 15.1 0 = CLk B 2 16.1 16.8 16.5 2 16.1 16.8 251 1.1 22.2 16.5 0 + 25 = Total 236 1.1 22.2 7.7 xiv 7.5 4,0.3 = t 0.1 4* 0.2 Table 7. Summary of tree height measurements (in m) of the live lodgepole pines surveyed in the central interior regions of British Columbia, Canada, 2009 and 2010. The table shows the total number of residual live lodgepole pine within the site, the measurements (in m) of the smallest, largest and mean height of the residuals, the changes in the number of dead trees within year 2009 and 2010, and, as a result, the changes in mean height of the residuals within each site 2009 Site 2010 Plot Alive (n) Min Max Mean Alive (n) Min Max Mean 2.0 10.6 6.0 37 2.0 10.6 6.0 Macl A 37 Macl B 58 3.0 13.5 9.6 54 3.0 13.5 Mac2 A 8 1.7 8.6 4.5 1.7 4.9 Mac2 B 34 2.4 13.8 7.6 6 24 2.4 13.1 New mortality (2009 to 2010) 9.7 1-0.1 3.3 +2 4, 1.2 7.3 + 10 4^0.3 >1,0.5 Mac3 A 7 3.2 12.3 8.9 6 3.2 12.3 8.4 Mac3 B 23 5.0 13.3 9.9 20 5.0 13.3 9.6 +3 Mac3 C - - 40 4.0 14.2 8.4 Mac4 A 6 11.8 17.4 14.7 4 13.2 16.2 14.7 N.A. +2 Mac4 B 21 3.1 19.0 13.5 21 3.1 19.0 13.5 Mac5 A 10 5.0 15.7 12.4 9 5.0 - 15.7 = 0 +4 +1 - Changes in mean height (m) 4, 0.3 N.A. = = 12.7 0 +1 t0.3 t 0.1 MacS B 10 6.3 14.2 11.8 8 11.9 CCk A 10 14.0 19.7 17.0 10 14.0 14.2 19.7 +2 17.0 0 = CCk B 8 14.1 21.6 18.5 18.5 0 = CLk A 2 14.0 19.7 17.0 8 14.1 21.6 2 14.0 19.7 17.0 0 = 0 + 25 = CLk Total B 2 236 14.1 21.6 18.5 1.7 21.6 10.0 6.3 2 14.1 21.6 251 xv 1.7 21.6 18.5 9.8 4,0.2 Table 8A. Site Summary of the presence of various bark beetles associated with lodgepole pine mortality in 2010 in the seven plots surveyed in the central interior region of British Columbia. The frequency (n) represents the total number of lodgepole pine and the percentage composition (%) of the explanatory variables over the dead lodgepole pine surveyed within each plot Stand aensiiy and maturity* Lodgepole pine Bark beetles associated with dead lodgepole pine in 2010 Dead B. Top MPB n n n % % 2°BB 2°BB (D) n % n % n % n IP H-LPB % PM PT n n % OL n % % AMB n % Macl H-Y 85 10 11 21 25 20 23 4 5 12 14 16 18 3 3 4 5 5 6 2 2 Mac2 M-Y 53 3 6 29 55 34 64 4 8 14 26 29 55 9 17 8 15 9 17 8 15 Mac3 M-Y 46 6 13 29 63 24 52 4 9 11 24 22 48 7 15 2 4 6 13 9 20 Mac4 M-0 75 6 36 48 42 56 1 1 7 9 40 53 7 9 6 8 0 0 21 28 MacS L-YO 33 2 66 25 76 23 70 1 3 5 15 22 67 3 9 0 0 1 3 18 55 CCk M-0 34 3 22 65 19 56 0 0 1 3 16 47 10 29 3 9 0 0 14 41 CLk L-0 18 3 17 10 56 14 78 0 0 1 6 5 28 7 39 1 6 0 0 5 28 Total M-YO 373 41 11 195 200 54 23 6 70 19 171 46 48 13 27 7 25 7 77 21 8 9 52 Abbreviations: B.Top=Broken top trees, MPB=mountain pine beetle or Dendroctonus ponderosae, 2°BB=secondary bark beetles, 2°BB (D)=Trees killed by the presence of predominantly secondary bark beetles (some trees had other agents of mortality weakening the trees, but is of minor significance), IP=lps pini, Ol=Orthotomicus latidens, PM=Pseudips mexicanus, H-LPB=Hylurgops spp. and/or Dendroctonus murrayanae (lodgepole pine beetle), PT=Pityogenes spp. and/or Pityophthorus spp., AMB=ambrosia beetles f Density (L=low, 0-25 pine/plot; M=medium, 26-59 pine/plot; H=high, 2:60 pine/plot) and maturity (Y=young, YO=young-old, 0=old) (refer Table 2 for more details of classifications) xvi Table 8B. Site Plot A more detailed view of Table 8A with each site broken into their respective plots of various bark beetles associated with the total lodgepole pine mortality in 2010. The frequency (n) represents the total number of lodgepole pine and the percentage composition (%) of the explanatory variables over all the lodgepole pine surveyed within each plot Stand density and maturity' Lodgepole pine Bark beetles associated with dead lodgepole pine in 2010 Dead B. Top MPB n n % n % n % n 5 33 5 67 4 27 2°BB 2°BB (D) IP H-LPB OL PM PT AMB % n % n % n % n % n % n % 0 0 2 13 2 13 0 0 2 13 4 27 0 0 Macl A M-Y 15 Macl B H-Y 72 5 7 16 22 16 22 4 6 10 14 14 19 3 4 2 3 1 1 2 3 Mac2 A L-Y 6 0 0 4 67 5 83 0 0 2 33 2 33 2 33 2 33 1 17 0 0 Mac2 B H-Y 47 3 6 25 53 29 62 4 9 12 26 26 55 7 15 6 13 8 17 8 17 Mac3 A L-YO 5 3 60 2 40 1 20 0 0 1 20 1 20 0 0 0 0 1 20 0 0 Mac3 B H-Y 41 3 7 27 66 23 56 4 10 10 24 21 51 7 17 2 5 5 12 9 22 Mac3 C H-Y 27 8 30 23 85 24 89 9 33 19 70 21 78 2 7 3 11 4 15 0 0 Mac4 A M-0 33 4 12 16 48 22 67 1 3 1 3 22 67 2 6 1 3 0 0 9 27 Mac4 B H-0 42 2 5 20 48 20 48 0 0 6 14 18 43 5 12 5 12 0 0 12 29 MacS A M-YO 21 1 5 16 76 16 76 1 5 3 14 16 76 3 14 0 0 1 5 13 62 Mac5 B L-YO 12 1 8 9 75 7 58 0 0 2 17 6 50 0 0 0 0 0 0 5 42 CCk A M-0 25 0 0 14 56 11 44 0 0 0 0 9 36 5 20 1 4 0 0 8 32 CCk B L-0 9 3 33 8 11 8 89 0 0 1 11 7 78 5 56 2 22 0 0 6 67 CLk A L-0 12 1 7 58 11 92 0 0 1 4 33 4 33 1 8 0 0 4 33 CLk B L-0 6 2 33 3 50 3 50 0 0 0 0 1 17 3 50 0 0 0 0 1 17 M-YO 373 41 11 195 52 200 54 23 6 70 19 171 46 48 13 27 7 25 7 77 Total 8 Abbreviations: 8 21 B.Top=Broken top trees, MPB=mountain pine beetle or Dendroctonus ponderosae, 2°BB=secondary bark beetles, 2°BB (D)=Trees killed by the presence of predominantly secondary bark beetles (some trees had other agents of mortality weakening the trees, but is of minor significance), IP=/ps pini, OL=Orthotomicus latidens, PM-Pseudips mexicanus, H-LPB=Hylurgops spp. and/or Dendroctonus murrayanae (lodgepole pine beetle), PT=Pityogenes spp. and/or Pityophthorus spp., AMB=ambrosia beetles f Density (L=low, 0-25 pine/plot; M=medium, 26-59 pine/plot; H=high, 260 pine/plot) and maturity (Y=young, YO=young-old, 0=old) (refer Table 2 for more details of classifications) xvii Table 9A. Summary of the live and dead lodgepole pines, the presence of Dendroctonus ponderosae in 2009 and 2010, and other weakening agents affecting the tree mortality (i.e. root collar damage by insects (RC), wood borers (WB), and western gall rusts (WGR) in 2010) in the seven plots surveyed in the central interior region of British Columbia. The frequency (n) represents the total number of live and dead lodgepole pine or the variable of interest with the percentage composition (%) of the explanatory variables over all the lodgepole pines surveyed within each site Stand maturity* _ „ lodgepole pine 2009 2010 Others (2010) Alive Dead MPB Alive Dead MPB n n n % n n n % % % % % RC n WB % n WGR % n % 117 66 Macl M-Y 178 95 53 83 47 20 11 91 51 87 49 21 13 61 34 8 4 Mac2 H-Y 83 42 51 41 49 28 34 30 36 53 64 29 35 30 36 23 28 30 36 Mac3 L-Y 72 30 42 42 28 39 26 36 46 64 29 40 30 42 22 31 47 65 27 27 25 75 32 23 23 3 3 24 22 44 Mac4 H-Y 100 73 58 73 36 36 25 75 36 36 32 Mac5 L-YO 50 20 40 30 60 24 48 17 34 33 66 25 50 33 66 12 CCk H-Y 52 18 35 34 65 22 42 18 35 34 65 22 42 17 33 12 23 1 2 CLk H-Y 22 4 18 18 82 10 45 4 18 18 82 10 45 13 59 13 59 1 5 Total M-YO 624 - - - - 168 27 251 40 373 60 195 31 238 38 113 18 221 35 Abbreviations: MPB=mountain pine beetle or Dendroctonus ponderosae, RC=root collar damage by insects, WB=wood borers, WGR=western gall rusts f Density (L=low, 0-25 pine/plot; M=medium, 26-59 pine/plot; H=high, 260 pine/plot) and maturity (Y=young, YO=young-old, 0=old) (refer Table 2 for more details of classifications) xviii Table 9B. Site A more detailed view of Table 9A with each site broken into its respective plots of live and dead lodgepole pine in 2009 and 2010, indicating the presence of Dendroctonus ponderosae and other potentially weakening agents of lodgepole pine Plot Stand density and maturity* Total lodgepole pine Others (2010) 2010 2009 Alive Dead MPB Alive Dead MPB RC n % n n % n % n n % n % % % WB WGR n % n % Mad A M-Y 52 37 71 15 29 5 10 37 71 15 29 5 10 7 13 2 4 36 69 Mad B H-Y 126 58 46 68 54 15 12 54 43 72 57 16 13 54 43 6 5 81 64 Mac2 A L-Y 33 11 92 Mac2 B Mac3 A Mac3 12 8 67 4 33 3 25 6 50 6 H-Y 71 L-YO 11 B H-Y 61 50 4 33 4 33 4 34 48 37 52 25 35 24 34 7 64 4 36 2 18 6 55 47 66 25 35 26 37 19 27 19 27 5 45 2 18 2 18 2 18 3 23 38 38 62 26 43 20 33 27 41 67 27 44 28 46 14 23 12 20 32 48 5 Mac3 C H-Y 67 - - - - - 40 60 27 40 23 34 22 33 6 9 Mac4 A M-0 37 6 16 31 84 16 43 4 11 33 89 16 43 15 41 8 22 2 Mac4 B H-0 63 21 33 42 67 20 32 21 33 42 67 20 32 17 27 15 24 1 2 Mac5 A M-YO 30 10 33 20 67 16 53 9 30 21 70 16 53 19 63 10 33 13 53 Mac5 B L-YO 20 10 50 10 50 8 40 8 40 12 60 9 45 14 70 2 10 9 45 CCk A M-0 35 10 29 25 71 14 40 10 29 25 71 14 40 6 17 6 17 1 3 CCk B L-0 17 8 47 9 53 8 47 8 47 9 53 8 47 11 65 6 35 0 0 CLk A L-0 14 2 14 12 86 7 50 2 14 12 86 7 50 11 79 10 71 0 0 CLk B L-0 8 2 25 6 75 3 38 2 25 6 75 3 38 2 25 3 38 1 13 M-YO 624 - - - - 168 27 251 40 373 60 195 31 238 38 113 18 221 35 Total Abbreviations: f Density (L=low, 0- - MPB=mountain pine beetle or Dendroctonus ponderosae, RC=root collar damage by insects, WB=wood borers, WGR=western gall rusts 25 pine/plot; M=medium, 26-59 pine/plot; H=high, 260 pine/plot) and maturity (Y=young, YO=young-old, 0=old) (refer Table 2 for more details of classifications) xix Table 10A. Likelihood of tree mortality as a function of presence/absence of signs of various insects and root collar damage by insects in 624 lodgepole pine across 15 plots in British Columbia, Canada in 2010, with the best models ranked by decreasing AIC value. p(tree death) = exp80*6'"'* -*B|,X|' , where xK are covariates listed below and coefficients are estimates (± SE) 1+ exp®°+ ®iXi+ "•+ ®kXk Model rank J. O 4 D D 8 y 10 Explanatory variables of agent of mortality of lodgepole pine* Intercept DBH 0.963*** (±0.205) -0.102 NS (±0.109) -0.234* (±0.102) -0.324** (±0.098) 0.357** (±0.174) -0.142 NS (±0.099) -0.289 NS (±0.171) 0.424* (±0.173) -0.092 NS (±0.098) -0.085 NS (±0.098) MPB RC 2BB -1.219*** (±0.279) -1.368 * (±0.456) -0.064** (±0.024) -0.087** (±0.025) OL 2.269*** (±0.615) 2.247*** (±0.610) 2.294*** (±0.610) 1.957*** (±0.323) 1.203*** (±0.225) 1.896*** (±0.311) 2.179*** (±0.308) 1.330*** (±0.221) 1.463*** (±0.218) d.f. AIC 621 571 621 607 621 618 622 628 619 726 620 737 620 746 620 747 621 752 621 758 PM 6.111*** (±0.624) 4.787*** (±0.511) 5.105*** (±0.618) 3.987*** (±0.464) -0.221*** (±0.032) -0.087*** (±0.025) IP 2.636*** (±0.759) 2.289** (±0.743) 2.650*** (±0.751) 2.314*** (±0.607) 2.373** (±0.737) f Abbreviations: DBH=diameter at breast height in centimeters, MPB=mountain pine beetle or Dendroctonus ponderosae, RC=root collar damage by insects, Significance: 2BB=Secondary bark beetles, IP=lps pini (Say), OL=Orthotomicus latidens (LeConte), PM=Pseudips mexicanus (Hopkins) * (p<0.05), ** (p<0.01), *** (p<0.001), N.S. (not significant, p>0.05) - continued next page- xx continuation Model rank 11 12 13 14 15 16 17 18 19 20 Explanatory variables of agent of mortality of lodgepole pine* Intercept 0.381* (±0.171) 0.115 NS (±0.088) 0.380* (±0.170) -0.048 NS (±0.097) -0.033 NS (±0.097) 0.210* (±0.085) 0.273** (±0.084) 0.328*** (±0.083) 0.166 NS (±0.102) -0.072 NS (±0.157) OBH MPB -0.072** (±0.024) 2.096*** (±0.300) RC 2BB IP 2.629*** (±0.734) 2.182*** (±0.295) 1.508*** (±0.217) 1.624*** (±0.214) d.f. AIC 620 762 621 766 621 769 621 770 622 776 622 791 622 809 622 824 622 832 622 833 PM 2.298* (±1.046) 2.742*** (±0.600) -0.069** (±0.024) OL 2.193* (±1.037) 2.896*** (±0.596) 2.863*** (±0.727) 2.930** (±1.022) 0.630*** (±0.173) 0.057** (±0.017) f Abbreviations: DBH = diameter at breast height in centimeters, MPB=mountain pine beetle or Dendroctonus ponderosae, RC=root collar damage by insects, Significance: 2BB = Secondary bark beetles, IP=lps pini (Say), Ol=Orthotomicus latidens (LeConte), PM=Pseudips mexicanus (Hopkins) * (p<0.05), ** (p<0.01), *** (p<0.001), N.S. (not significant, p>0.05) xxi Table 10B. Likelihood of tree mortality as a function of lodgepole pine mortality across pine diameter sizes (in cm), the presence/absence of various bark beetles, and root collar damage by insects in each individual sites in British Columbia, Canada in 2010, with the best models ranked by decreasing AIC value. p(tree death) = expB,tB'X|t--tBkXt , where xK are covariates listed below and coefficients are estimates (± SE) 1+ expBo+B»Xi++ BkXl Model rank Site 1 Macl JL Macl 3 Macl 9 Macl 10 Macl 11 Macl 1 Mac2 2 Mac2 3 Mac2 4 Mac2 5 Mac2 'Abbreviations: Significance: Sites (n): Intercept (i SE) 2.747*** (±0.486) 2.508*** (±0.454) 2.181*** (±0.417) -0.788** (±0.295) -0.169 NS (±0.156) -0.166 NS (±0.160) -0.372 NS (±0.291) -0.148 NS (±0.273) -1.208* (±0.530) 0.113 NS (±0.275) 0.322 NS (±0.244) Explanatory variables of agent of mortality of lodgepole pine* DBH MPB -0.712*** (±0.116) -0.640*** (±0.105) -0.546*** (±0.092) -0.151** (±0.046) 3.025* (±1.361) RC 2BB IP 6.816*** (±1.587) 8.911*** (±1.593) 3.570** (±1.194) 4.465*** (±0.957) 2.567* (±1.056) 1.082* (±0.509) 3.868*** (±1.056) 3.481*** (±1.054) 0.295*** (±0.085) 1.496** (±0.562) 2.243* (±1.066) d.f. AIC 174 160 175 161 174 189 176 239 176 240 176 246 81 79 81 87 81 97 81 104 81 105 OL DBH = diameter at breast height in centimeters, MPB=mountain pine beetle or Dendroctonus ponderosae, RC=root collar damage by insects, 2BB = Secondary bark beetles, IP=/ps pini (Say), OL=Orthotomicus latidens (LeConte) * (p<0.05), ** (p<0.01), *** (p<0.001), N.S. (not significant, p>0.05) Mad = Mackenzie 1 (n=178,2 plots), Mac2 = Mackenzie 2 (n=83,2 plots) - continued next page xxii continuation Model rank Site 1 Mac3 z Mac3 3 Mac3 4 Mac3 5 Mac3 6 Mac3 1 Mac3-C 2 Mac3-C 3 Mac3-C 4 Mac3-C 5 Mac3-C Intercept (±SE) -0.916*** (±0.232) 0.704** (±0.236) -0.390* (±0.195) -0.493* (±0.221) -0.301 NS (±0.217) -0.911* (±0.433) -2.277*** (±0.525) -1.466*** (±0.370) -3.984*** (±1.025) -1.224*** (±0.360) -0.901** (±0.329) Explanatory variables of agent of mortality of lodgepole pine* DBH RC MPB 2BB IP 4.766*** (±1.037) 3.329** (±1.049) 3.758*** (±1.036) 1.128** (±0.438) 1.696*** (±0.396) 1.112** (±0.371) 0.139* (±0.055) 5.413*** (±1.148) 4.357*** (±1.092) 0.476*** (±0.128) 2.265*** (±0.596) 1.460** (±0.552) * Abbreviations: d.f. AIC 137 123 136 155 137 160 137 176 137 187 137 189 65 39 65 58 65 75 65 78 65 87 OL DBH = diameter at breast height in centimeters, MPB=mountain pine beetle or Dendroctonus ponderosae, RC=root collar damage by insects, 2BB = Secondary bark beetles, IP=/ps pini (Say), Ol=Orthotomicus latidens (LeConte) Significance: * (p<0.05), ** (p<0.01), *** (p<0.001), N.S. (not significant, p>0.05) Sites (n): Mac3 = Mackenzie 3 (n=139,3 plots), Mac3-C = Mackenzie 3-Plot C (n=67) - continued next page - xxiii continuation Model rank Site 1 Mac4 2 Mac4 1 Mac5 2 Mac5 1 CCk* 2 CCk* 3 CCk* 4 CCk 5 CCk Intercept (±SE) -0.578* (±0.261) -0.296 NS (±0.588) Explanatory variables of agent of mortality of lodgepole pine* DBH RC 2BB IP 0.141* (±0.058) 4.041*** (±1.222) 2.234** (±0.736) -0.176** (±0.067) -0.255** (±0.089) -0.116* (±0.055) -0.145* (±0.061) -0.192* (±0.076) 1.885* (±0.943) -2.605* (±1.176) 1.726* (±0.879) 1.691* (±0.853) 2.35000503 (±1.201) 2.242* (±1.136) 1.622* (±0.802) 1.807* (±0.889) 'Abbreviations: d.f. AlC 98 103 98 110 47 52 48 57 48 62 48 63 49 64 49 65 49 65 OL 2.255** (±0.773) 0.514 NS (±0.516) -0.241NS (±0.403) 2.267* (±0.888) 2.920** (±1.009) 1.941* (±0.828) 2.185* (±0.865) 2.567** (±0.925) MPB DBH = diameter at breast height in centimeters, MPB=mountain pine beetle or Dendroctonus ponderosae, RC=root collar damage by insects, 2BB = Secondary bark beetles, IP-Ips pini (Say), Oi=Orthotomicus latidens (LeConte) ' AlC values were significant (or close to it) when tested using generalized linear model, and close to significant (p<0.063) when tested using generalized linear mixed effect models, compared to the other models that remained significant when scrutinized from either tests Significance: * (p<0.05), ** (p<0.01), *** (pcO.OOl), N.S. (not significant, p>0.05) Sites (n): Mac4 = Mackenzie 4 (n=100, 2 plots), Mac5 = Mackenzie 5 (n=50, 2 plots), CCk = Crassier Creek (n=52, 2 plots) xxiv Table 11. Site Ml Ml M2 M2 M2 M2 M2 M2 M2 M2 M3 M3 M3 M3 M3 M3 M3 M3 M3 M5 CCk Plot B B B B B B B B B B A B B B B C C C C B A A detailed summary of 21 lodgepole pines with frass and their interactions with various insects, broken tops, or the other agents of tree mortality recorded in 2010 at the post-outbreak stage of Dendroctonus ponderosae in central British Columbia, Canada DBH (cm) 9.2 8.7 9.5 5.7 9.0 7.3 8.2 6.5 10.2 8.1 9.0 10.9 7.4 7.3 8.1 10.7 5.7 8.2 8.4 13.6 14.6 Abbreviations: Hgt (m) 9.7 10.2 13.8 9.5 13.1 8.4 13.2 7.2 12.9 11.1 11.6 13.1 11.0 10.5 9.4 13.5 9.0 8.5 11.3 12.9 17.1 Dead/Alive 2009 A A A A A A D A D A A D A A A - _ _ A A 2010 A D D D A D D D D D D D D D A D D A D D A Secondary bark beetles (2BB) (final in 2010) MPB 2009 • 2010 • • • • • • • • • • • • • • • • • • • • 2BB IP • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • H-LPB • OL • • PM PT AMB • • • • • • • • • • • • • • • • • • • • • RC • • • • • • • • • Others • • • WGR WB • • • • • • • • • • • • • • • • • V • • • • • • • ? • • • DBH=diameter at breast height (in cm), Hgt=height (in m), MPB=mountain pine beetle or Dendroctonus ponderosae, 2BB=Secondary bark beetles, IP=/ps pini (Say), H-LPB=Hylurgops spp. and/or Dendroctonus murrayanae (Hopkins), OL=Orthotomicus latidens (LeConte), PM=Pseudips mexicanus (Hopkins), PT=Pityogenes spp. and/or Pityophthorus spp., AMB=ambrosia beetles, RC=root collar damage by insects, WGR=western gall rust, WB=wood borers, BT=Broken top trees XXV BT ? • • • ? • • •/ • • • Kill • ? Table 12. Tree 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 Site A detailed summary of 25 lodgepole pines with new mortality recorded in the five sites near Mackenzie in 2010 at the post-outbreak stage of Dendroctonus ponderosae, exhibiting the multiple interactions of bark beetles in the trees in the stands Plot Ml Ml Ml Ml M2 M2 M2 M2 M2 M2 M2 M2 M2 M2 M2 M2 M3 M3 M3 M3 M4 M4 M5 M5 M5 Abbreviations: B B B B A A B B B B B B B B B B A B B B A A A B B DBH (cm) 3.0 3.5 8.7 5.6 11.6 10.0 9.5 5.7 7.3 3.7 8.3 6.5 5.6 4.0 8.1 5.1 9.0 10.5 7.4 7.3 13.2 6.6 7.0 6.7 13.6 Hgt (m) 5.9 8.0 10.2 8.6 8.6 7.2 13.8 9.5 8.4 5.5 11.7 7.2 7.6 3.4 11.1 4.1 11.6 12.7 11.0 10.5 17.4 11.8 9.7 9.8 12.9 MPB 2009 2010 Secondary bark beetles (2BB) (final in 2010) H-LPB PM PT AMB 2BB IP OL • • • • • • • • • • • • • • • • • • RC • • • • • • • V S • • • • • • • • • • • • • • • • • • • • • WB • • • • • • •/ Frass • • • • • • • • • • • • • • • • • • • • • • • • • • • • V • • • • • • • S • • • • • • • • • • • • • • • • • • • • DBH=diameter at breast height (in cm), Hgt=height (in m), MPB=mountain pine beetle or Dendroctonus ponderosae, 2BB=Secondary bark beetles, IP=/ps pini (Say), H-LPB=Hylurgops spp. and/or Dendroctonus murrayanae (Hopkins), Ol=Orthotomicus latidens (LeConte), PM=Pseudips mexicanus (Hopkins), PT=Pityogenes spp. and/or Pityophthorus spp., AMB=ambrosia beetles, RC=root collar damage by insects, WGR=western gall rust, WB=wood borers, BT=Broken top trees xxvi BT • • • • • Others WGR • • List of Figures Figure 1. The epidemiology of Dendroctonus ponderosae (black line/shade), and their four phases of population cycles (endemic, incipient, epidemic, and postepidemic) (Figure 1A), in relation to secondary bark beetle populations (red line/shade), and the potential extension of the outbreak by bark beetles associated with additional tree mortality (Figure IB), in the post-outbreak stage of D. ponderosae. This new mortality may arise from the secondary species that are consuming smaller-diameter residual pine Figure 2. Tree abundance in seven study sites in the central interior of British Columbia, Canada, 2009-2010 A. Total trees surveyed by species B. Total lodgepole pine surveyed by site Figure 3. Status of lodgepole pine (alive/dead) in seven study sites in the central interior of British Columbia, Canada, 2009-2010 Figure 4. Number (Figure 4A) and percentage (Figure 4B) of lodgepole pine in three vigour classes surveyed in each of 14 plots in the central interior of British Columbia, Canada, 2009-2010 Figure 5. Density distribution of live (Figure 5A) and dead (Figure 5B) lodgepole pines by site in seven sites in the central interior of British Columbia, Canada, 2010 Figure 6. Distribution of dbh of live residuals (Figure 6A) and dead lodgepole pines (Figure 6B) in the central interior of British Columbia, Canada, 2009 and 2010 xxvii Figure 7. Relationship between mean tree diameter and mean stand density per site among seven sites in the central interior of British Columbia, Canada Figure 8. Spatial niche partitioning in same lodgepole pine host by bark beetles in the central interior of British Columbia, Canada Figure 9. Temporal niche partitioning of flight dispersal periods by bark beetles in central British Columbia, Canada Figure 10. Semiochemical attraction and repellence by bark beetles in central interior of British Columbia, Canada xxviii Figure 1. The epidemiology of Dendroctonus ponderosae (black line/shade), and their four phases of population cycles (endemic, incipient, epidemic, and post-epidemic), in relation to secondary bark beetle populations (red line/shade), and the potential extension of the outbreak by bark beetles associated with additional tree mortality, in the post-outbreak stage of Dendroctonus ponderosae. This new mortality may arise from the secondary species that are consuming smaller-diameter residual pines (black line/shaded area) Dendroctonus ponderosae Secondary bark beetles: (red line/shaded area) Ips pini Hylurgops spp. O. latidens P. mexicanus — D. murrayanae Pityogenes spp. Pityophtorus spp. Population stages: xxix Figure 2. Tree abundance in seven study sites in the central interior of British Columbia, Canada, 2009-2010 A. Total trees surveyed by species (n=827] .Interior spruce, n=96(12%) Trembling aspen, n=45(5%) Subalpine fir, n=28(3%) .Black spruce, n=22(3%) .Douglas fir, n=8(l%) B. Total lodgepole pine surveyed by sites (n=624) •Macl (Mackenzie), n=178(29%) • Mac2 (Mackenzie), n=83(13%) • Mac3 (Mackenzie), n= 139(22%) • Mac4 (Mackenzie), n= 100(16%) • MacS (Mackenzie), n=50(8%) • CCk (Peace River), n=52(8%) • CLk (Prince George), n=22(4%) • xxx Figure 3. Status of lodgepole pine (alive/dead) in seven study sites in the central interior of British Columbia, Canada, 2009-2010 Lodgepole pine surveyed in all seven sites* • Dead-2009 • Newly dead-2010 • Alive 100 200 300 400 500 * Total excludes a 15th plot (Mac3-C) established in 2010 (27 dead trees of 67 trees total) because no baseline measurement was taken in 2009 to permit reference of time of death xxxi Figure 4A. Vigour of lodgepole pine surveyed in each of 14 plots in the central interior of British Columbia, Canada, 2009-2010 alive/dead lodgepole pine surveyed by site-plot i Dead-2009 0 • Dead-2010 20 40 60 • Alive 80 100 120 Macl-A 2009 Macl-A 2010 Macl-B 2009 Macl-B 2010 Mac2-A 2009 Mac2-A 2010 Mac2-B 2009 Mac2-B 2010 Mac3-A 2009 Mac3-A 2010 Mac3-B 2009 Mac3-B 2010 Mac4-A 2009 Mac4-A 2010 Mac4-B 2009 Mac4-B 2010 Mac5-A 2009 Mac5-A 2010 Mac5-B 2009 Mac5-B 2010 CCk-A 2009 CCk-A 2010 CCk-B 2009 CCk-B 2010 CLk-A 2009 CLk-A 2010 CLk-B 2009 CLk-B 2010 Total: 557 XXXII Figure 4B. Percentages of lodgepole pine of different vigours surveyed in each of 14 plots in the central interior of British Columbia, Canada, 2009-2010 Percentage{%) of alive/dead lodgepole pine surveyed by site-plot 0% • Dead-2009 2096 • Dead-2010 40% 60% • Alive 80% 100% n Mad-A (2009 52 Macl-A (2010 Macl-B (2009 126 Macl-B (2010 Mac2-A (2009 12 Mac2-A (2010 Mac2-B (2009 71 Mac2-B (2010 Mac3-A (2009 11 Mac3-A (2010 Mac3-B (2009 61 Mac3-B (2010 Mac4^A (2009 37 Mac4-A (2010 Mac4-B (2009 63 Mac4-B (2010 Mac5-A (2009 30 Mac5-A (2010 Mac5-B (2009 20 Mac5-B (2010 CCk-A (2009 35 CCk-A (2010 CCk-B (2009 17 CCk-B (2010 CLk-A (2009 14 CLk-A (2010 CLk-B (2009 CLk-B (2010 Total: 557 XXXIII Figure 5A. Density distribution of live Mad n=91 lodgepole pines by site in seven sites in the central interior of British Columbia, Canada, 2010 Mac2 n=30 Mac3 n=26(+40) Mac4 n=25 Mac5 n=17 Crassier Creek ,n=18 Mackenzie 1 Chief Lake n=4 Mackenzie 2 Mackenzie 3 Mackenzie 4 Mackenzie 5 Crassier Creek Chief Lake All 7 sites 5 20" Overall 7 sites n=211(+40) 5 10 15 20 Diameter (cm) of lodgepole pine xxxiv Figure 5B. Density distribution of dead lodgepole pines by site in seven sites in the central interior of British Columbia, Canada, 2010 20 Macl n=87 15 10 5 Of 20- Mac2 n=53 15 10 5 0' 20 is­ le­ s' or 20 Mac3 n=46(+27) Mac4 n=75 15 10- Mac5 n=33 Grassier Creek n=34 Mackenzie 1 Mackenzie 2 Mackenzie 3 Mackenzie 4 Chief Lake n=18 Mackenzie 5 Crassier Creek Chief Lake All 7 sites Overall 7 sites n=346(+27) 5 10 15 20 Diameter (cm) of lodgepole pine xxxv Figure 6. Distribution of dbh of live residuals (Figure 6A) and dead lodgepole pines (Figure 6B) in the central interior of British Columbia, Canada, 2009 and 2010 28.0 24.0 O 2009 20.0 t 1= u a) c a. _a> Diameter distribution of lodgepole pine A. Live pines J,... • 2010 16.0 O • <> 12.0 <> 8.0 4.0 0.0 o a 28.0 1 1 1 r i i i 1 1 1 1 1 1 1 1 r ~i i i r B. Dead pines a> (to O 2009 • 2010 TJ o 24.0 % 20.0 £ 16.0 0 • <• 0 t t1I _r ~r ~r T T ~r T ~r i f ~r ~r _r ~r CT> O o > o o ^ o o > o o i o c n o c n o c r i o c n o o > o a > o o ^ o o > o a > o O H Q H O H O H O H Q H O H O H O H O H O H O H O H § 3 o o o o o o o o o o o o o o o o o o o o o o o o o o CM (N N f M N M M f M M N N N N r M f M N f M N N f M M f M f M N N N N M T < < C D C D U O u m > P. knechteli Trypodendron lineatum Gnathotrichus spp. ^ ^ < > < <> Dendroctonus ponderosae Dendroctonus murrayanae Ips pini Pityogenes spp. Hylurgops spp. ' Ambrosia beetle Orthotomicus latidens Pseudips mexicanus <—^ <—> xxxix First flight Second flight Third flight (potentially) Nov I Dec I Figure 10. Semiochemical attraction and repellence by bark beetles in central British Columbia, Canada ^-^Response Presence\ ** — — mm mm mm mm * 1 • 1 Ml Dendroctonus ponderosae Ips pini Hylurgops porosus Orthotomicus latidens Pseudips mexicanus Dendroctonus murrayanae Pityogenes knechteli Pheromones: Stronger attraction Positive attraction Stronger repellence Negative repellence Neutral Unknown xl 1 trans-verbenol 2 (+)-exo-brevicomin verbenone 4 ipsdienol 5 ipsenol 3 Acknowledgements This study was only made possible with the support and dedication of Dr. Brian Aukema and the Aukema lab, Dr. Allan Carroll, Dr. Staffan Lindgren, Dr. Lisa Poirier, Dr. Dezene Huber, the FIRG team of UNBC, and many more. I would not have gotten very far in the process if not for their enthusiastic guidance and stimulating discussions on the population dynamics of Dendroctonus ponderosae. First and foremost, my heartfelt gratitude to my mentor, Dr. Brian Aukema, for trusting me, when others (or myself) were in doubt (or indecisive), and for the countless supervision in all aspects of life ranging from his insights on Ips pini and statistics to his directions for me (who was in a panic) to navigate through the United States Immigration and Customs. Nothing short of amazing, the journey with the Aukema entourage has been awesome; Dr. Fraser McKee, in the making, has been a (big brother) role model, exemplified from his endless streams of ideas for this study, or even random facts on life, and redefining the boundary of excellence from his tireless fortitude; big sister, Honey-Marie de la Giroday, for her help in the field, as well as introducing PG localities and research technician extraordinaire; Laura Machial as the lab's social ambassador and exquisite baker; the highly gifted Jordan Koopmans (could have been the next MLB superstar) for co-piloting the UNBC's Masters program together and introducing the Canadian culture, lifestyle and the way how things are done (thank you especially for not abandoning me at the mercy of the U.S. borders); thank you also to research assistants Rurik Muenter, Kathryn Berry, Gareth Hopkins, and especially Sarah (Genny) Michiel for being so liberal with her time and unwavering commitment; and to the new crew in University of Minnesota (Tahoe-Sam and St.Paulian-Andrea), thank you for energizing the lab in tip-top condition to keep on ballin'. Finally, I would like to take this opportunity to thank all my friends and colleagues, and at the same time apologize if I have slighted any of you in any form of speech, writing or demeanour. Though I'm short on words (in person or physical stature), I am truly blessed to have been able to be part of the Aukema entourage (and their families), and truly grateful to know and work with such extraordinary people, developing such pleasant memories, as well as those with more challenging personalities. This remarkable period is definitely a well-spent three years in UNBC, Canada and the University of Minnesota. xli Introduction British Columbia has a richer diversity of ecosystems than any other Canadian province. The province possesses 16 biogeoclimatic zones; a complex of geological terrains and varying climatic regions, ranging from continental to alpine tundra to maritime. This westernmost province of Canada supports a wide variety of biota from the depths of the Pacific Ocean to the peaks of the Rocky Mountains, with its multitude of ecosystems of kelp beds, estuaries, wetlands, mountain slopes, alpine meadows and desert-like steppes. The province is larger than any European country, except Russia, with a total land area of 95 million hectares. Almost 60% of the land is forested: approximately 55 million hectares or roughly 11 billion cubic meters of timber (BCMOE 2007, BCMoFML 2010). Coniferous forests make up 83% of the forested land, with lodgepole pine constituting more than two billion cubic meters of growing stock. Mature lodgepole pine, as the leading tree species, comprises almost a third of the annual provincial timber harvest: approximately 1.35 billion cubic meters of timber or 14 million hectares of mature pine (BCMoFR 2007, 2008, BCMoFML 2010). This natural resource, a natural treasure of the province, generates substantial revenues to support the local economy in the form of a wide variety of forest products and sustains innumerable ecological functions, such as supporting plants and wildlife biodiversity and other provisions of invaluable non-timber forest products and services (Hamre 1975, Fahey and Knight 1986, Campbell et al. 2009). In terms of human economics, the accrued benefits of ecosystem services worldwide have an average value of 33 trillion U.S. dollars. 1 Proportionally for the size of British Columbia, the estimated value of ecosystem services is valued at more than 200 billion U.S. dollars (Costanza et al. 1997). Pinus contorta var. latifolia Engelmann, the dominant inland form of lodgepole pine among the four major geographical varieties (Lotan and Perry 1983), exhibits one of the most widespread geographical ranges among the pines in North America, ranging from central Yukon to the Rocky Mountains in British Columbia, and from Colorado to the Black Hills in South Dakota in the United States (Lowery 1984). Lodgepole pine is a ubiquitous species that has a wide range of environmental tolerance, occurring at elevations from 500 to 3600 meters, with a preference for cool and dry habitats over warm and moist sites, but persisting even on poor soils in British Columbia and Alberta (Smithers 1961). Lodgepole pine is a serotinous subclimax species. As a fire-maintained species, it is highly adapted to regenerate quickly to overcome competition from other species, as the seedlings are intolerant to shade and are poor competitors (Fowells 1965). This species has multiple uses, aesthetic and recreational functions, and ecological roles, acting as a carbon sink, foraging material, and/or wildlife habitat. Given its timber and non-timber yields, lodgepole pine is important to the province of British Columbia (McDougal 1973, Pfister and Daubenmire 1975, Lotan and Perry 1983, Lotan and Critchfield 1990). Lodgepole pine is associated with a variety of insect groups such as terminal, shoot and twig insects, sap-sucking insects, folivores, seed and cone feeders, lower stem and root insects, bark beetles, ambrosia beetles, and wood borers (Keen 1952, Smithers 1961, Coulson and Witter 1984). Among these groups of insects, which are classified according to the type and part of tree on which they feed and reproduce, bark beetles cause more 2 mortality to lodgepole pine than any other abiotic factor, forest fires or annual harvests of anthropogenic origin, and any biotic disturbance agents, combined (Amman 1975, BCMoFML 2010). The name bark beetle is derived from the beetle's habit of breeding under the bark, or in the subcortical tissue region of trees, primarily conifers (Wood 1982b). There are more than 50 species of scolytid bark beetles associated with lodgepole pine in Canada (Bright 1976). The colonization behaviour of bark beetles can vary from "primary" to "secondary" users of lodgepole pine as host. "Primary" refers to the more aggressive beetles that can attack and kill healthy trees (Rudinsky 1962). In contrast, "secondary" bark beetles reproduce in unthrifty trees, such as those stricken by diseases or drought, and in recently-killed trees, such as in windfalls, freshly cut logs, and logging slash (Swaine 1918, Wood 1982b, Safranyik et al. 1999b, 2000,2004). If a live tree is colonized, the secondary species are often found at a distance away from the main bole, in the lower bole or upper limbs of decadent trees. Under normal circumstances, secondary bark beetles might further weaken the tree, or only on occasion cause mortality. Secondary bark beetles are not usually a significant source of tree mortality, however (Keen 1952, Furniss and Carolin 1977). The majority of bark beetles are secondary, and only a few species are primary (Rudinsky 1962). Bark beetles play an important role in promoting a heterogenous forest community, supporting a multitude of wildlife, biodiversity, and ecological functions (ChanMcLeod 2006, Burton 2008). Bark beetles may promote higher growth and vigor by removing stagnated and weakened trees, accelerating the deterioration of dead or dying trees, and by recycling nutrients (Wood 1982b, Romme et al. 1986, Brown et al. 2010). 3 The outbreak of Dendroctonus ponderosae in British Columbia and subsequent Iodgepole pine mortality In the following section, the biology and ecology of Dendroctonus ponderosae and each of the secondary bark beetles in the north-central region of British Columbia are briefly described. All of these insects may colonize Iodgepole pine, but reduce competition by partitioning the resource spatially and temporally, often via complex chemical cues. A description of the spatial and temporal partitioning can be found in Tables 1and 2, respectively, while the known chemical ecology of these species is provided in Appendix A. The bark beetles of Iodgepole pine in British Columbia "Primary" bark beetle Dendroctonus ponderosae (Hopkins), mountain pine beetle Dendroctonus ponderosae (Hopkins) is a primary phloeophagous generalist on more than BO species of pines (Furniss and Schenk 1969, Smith et al. 1981). In British Columbia, its primary host is Iodgepole pine. Among all the mortality agents of pines, D. ponderosae inflicts the highest rate of tree mortality in the western hemisphere of North America, ranging from the provinces of British Columbia and Alberta in Canada to the 12 western states of United States (Furniss and Carolin 1977, Wood 1982b, Amman and Cole 1983). The insect prefers the largest-diameter mature pines during outbreaks (Amman 1975, Raffa 1988, Boone et al. 2011). Dendroctonus ponderosae is the principal mortality agent in this study, infesting the main bole, below 5 m, of apparently healthy Iodgepole pine of at least 10 cm in diameter at epidemic phases (Hopkins 1909, Linger 1993, Safranyik and Carroll 2006, Gibson et al. 2009) (Table 1). It is considered a primary bark beetle. Dendroctonus ponderosae has four larval instars. Each instar takes, on average, 28-30 days to develop at constant 24°C (in phloem of 4 high quality, as in epidemic conditions). Maturation feeding ranges from days to months as the adults emerged synchronously (Safranyik and Whitney 1985, Bentz et al. 1991). Dendroctonus ponderosae has one generation per year in British Columbia, with peak emergence usually occurring at the end of July to mid-August, and lasting between 7-10 days. Occassionally, parent adults may re-emerge to establish a second brood (Reid 1962a, Safranyik and Carroll 2006). "Secondary" bark beetles Ips pini (Say), pine engraver Ips pini is the most common sympatric with D. ponderosae, and is one of the most aggressive species of secondary bark beetles, with the capacity to cause mortality of sapling or pole-sized lodgepole pine with a diameter of 5 cm and greater (Roe and Amman 1970, Furniss and Carolin 1977). Ips pini may also kill larger trees with weakened defenses, such as trees with concurrent attacks from other species of bark beetles (Weaver 1934, Rudinsky 1962, Ayres et al. 2001), or any other disturbance agents in the forest (Kennedy 1969, Klepzig et al. 1991, Santoro et al. 2001, Lombardero et al. 2006, Fettig et al. 2010). Ips pini has a transcontinental distribution in most pine species, and is most commonly found in downed materials such as windfalls, freshly cut logs, and thin-barked portions of slash. Suitable breeding material includes the tops and branches of trees recently killed or weakened by D. ponderosae (Reid 1957a, Bright 1976, Kegley et al. 1997), as in this study (Table 1). Ips pini has three larval instars, with a life cycle of between 34-60 days in lodgepole pine (Reid 1955, Miller and Borden 1985), between 31-48 days in white pine (Prebble 1933), between 40-55 days in ponderosa pine (Kegley et al. 1997), approximately 15 days at constant 25°C to 65 days under normal seasonal temperatures in red pine (Ayres et al. 2001) or 33-35 5 days in jack pine, in addition to 6-11 days for maturation feeding under the bark (Thomas 1961, Schenk and Benjamin 1969). Ips pini overwinter near their brood trees in the duff as adults, which provides close proximity to available host materials upon emerging from hibernation early the next spring (Schmitz 1980, Safranyik et al. 1999a). Normally a bivoltine species in Ontario, Canada, I. pini can have up to three broods, with peak flights starting in mid-May, the second in end of July, and, in warmer summers, a smaller peak of reemerging parents or brood adults flying in late August to early September (Thomas 1961, Bright 1976, Safranyik et al. 1996, 2000, Ayres et al. 2001) (Table 2). Hylurgops spp. (LeConte), sour sap bark beetles Hylurgops spp. commonly infest the phloem at the lower bole of recently cut lodgepole pine stumps, or at the root collar region of the larger main roots of dead or severely weakened conifers (Keen 1952, Wood 1982b, Safranyik et al. 1999a, 2000,2004) (Table 1). Similar to other root inhabiting insects, this genus exhibits a semivoltine life cycle. For example, Hylurgops rugipennis (Mann.) has approximately one generation every 1.5-2.5 years due to the varying rate of development from temperature differences within the subcortical tissues of the roots (Reid 1957a, 1957b). The most abundant Hylurgops spp. is Hylurgops porosus (LeConte) (Safranyik et al. 2000, 2004, Schweigkofler et al. 2005). This species is likely responsible for dark staining in the phloem where it occurs. Hylurgops porosus and Hylurgops rugipennis have a flight period throughout the growing season, based on the extended period of emergence from the stumps. These insects breed in the base of trees killed by D. ponderosae without competing directly with the more aggressive species in the upper bole (Safranyik et al. 1999a, 2000,2004) (Table 2). 6 Orthotomicus latidens (LeConte), smaller western pine engraver Orthotomicus latidens is a ubiquitous species, breeding in ephemeral, patchy habitats, such as in wind-downed or diseased trees, and in tops and branches of trees recently killed by D. ponderosae (Keen 1952, Bright 1976, Miller and Borden 1985, Miller et al. 1986, Reid 1999) (Table 1). Orthotomicus latidens has three larval instars, with an estimated mean generation time of 64-124 days in lodgepole pine. Maturation feeding can last from weeks to months to synchronize adult emergence, as most O. latidens overwinter under the bark (Miller and Borden 1985). Orthotomicus latidens is univoltine in south-central British Columbia, and can produce up to two broods per year. The main flight period occurs in spring, around late May to early June, with a second flight peak in late July from re-emerging adults (Miller and Borden 1985) (Table 2). Pseudips mexicanus (Hopkins), Monterey pine engraver Pseudips mexicanus often occur together with endemic D. ponderosae (Smith et al. 2011), preferring the lower boles of suppressed trees below a height of 1.0 m (Smith et al. 2009) (Table 1). Pseudips mexicanus has four larval instars, and can complete its life cycle in approximately 50 days at 26.5°C. The insect may emerge in less than four days of maturation feeding (Smith et al. 2009). Pseudips mexicanus primarily overwinter as larvae and adults (Struble 1970), based on the finding of amorphous galleries in lodgepole pine (Smith et al. 2009). Pseudips mexicanus is univoltine in lodgepole pine in British Columbia and California, with the ability to produce up to two broods per year, with two peak flights. The first flight peaks around late May to early June. A subsequent flight from re-emerging adults peaks in early to mid-August (Bright and Stark 1973, Smith et al. 2009). 7 In California, P. mexicanus may have up to three generations per year in Monterey pine (Struble 1970) (Table 2). Dendroctonus murrayanae (Hopkins), lodgepole pine beetle Dendroctonus murrayanae is most commonly associated with lodgepole pine, but is also found in four other species of pines and three species of spruce. Lodgepole pine beetle prefers the lower boles near the roots on overmature or weakened standing pines or the stump areas of windfallen trees. This insect is seldom found more than 60 cm above ground level (Keen 1952, Bright 1976, Wood 1982b) (Table 1). Dendroctonus murrayanae has four larval instars, with larval offspring aggregating and feeding gregariously side-by-side in communal chambers, and taking more than 26 days to mature into adults from second-instar larvae (Furniss and Kegley 2008). Dendroctonus murrayanae is univoltine, overwintering as larvae . Flight to attack new hosts occurs in mid-June to mid-July, with eggs hatching into larvae in August before winter (Safranyik et al. 2004, Furniss and Kegley 2008) (Table 2). Pityogenes spp. (Bedel), twig beetles Pityogenes spp. are predominantly found among the smaller-diameter slash and stems in most species of pines and in several species of spruces, with each species having their preferred host (Bright and Stark 1973) (Table 1). The most common and important species of Pityogenes associated with lodgepole pine in the western hemisphere of North America is Pityogenes knechteli (Swaine) (Reid 1955, Bright 1976, Safranyik et al. 2004), which can increase to outbreak levels and kill up to 16% of live trees after a D. ponderosae epidemic (Evenden and Gibson 1940). Pityogenes spp. have four or five larval instars, with varying rates of development, depending on tree species. Pityogenes knechteli has a mean 8 generation time of about 6-8 weeks to complete its life cycle from egg to adults (Reid 1955), and is univoltine, with the capacity to have up to two broods per year. The main dispersal period peaks at the end of May. Re-emergent adults establishing a second brood may produce a second lower peak from early June to August (Reid 1955, Safranyik et al. 2004) (Table 2). Pityophthorus spp. (Eichhoff), twig beetles Multiple species of Pityophthorus may occur in almost all of the commercially important conifers and on some deciduous trees. There are more than ten species of Pityophthorus that regularly occur in lodgepole pine, but the species within this genus are difficult to distinguish (Bright 1976) (Table 1). Pityophthorus spp. are more common on smaller trees, and only found in twigs or the thinner-barked sections of larger trees. Pityophthorus spp. have two or three larval instars, and are presumably univoltine in general, depending on latitude and elevation (Bright 1981) (Table 2). This genus might be widespread, but its impact on tree mortality is likely minimal, including on lodgepole pine. Thus, research on their biology and population dynamics is limited. Literature on life tables, population structure, host selection behaviour or dispersal patterns for this genus is almost nonexistent. Ambrosia beetles (Trypodendron lineatum [Oliver], Gnathotrichus [LeConte]) The three native species of ambrosia beetles most commonly found in the western hemisphere of North America are the striped ambrosia beetle, Trypodendron lineatum (Oliver), Gnathotrichus sulcatus (LeConte) and Gnathotrichus retusus (LeConte) (Daterman and Overhulser 2002). Ambrosia beetles are found in a broad range of coniferous and broadleaved trees of at least 10 cm in diameter (Wood 1957) (Table 1). Lodgepole pine is not always their 9 most preferred host, in comparison to most of the other species or genera of bark beetles above. Ambrosia beetles are often univoltine, laying up to two broods per year, with an estimated mean generation time of 6-10 weeks from egg to emergence (Daterman and Overhulser 2002). Trypodendron lineatum begins its flight as early as March, peaking in late April to May. The main flight of Gnathotrichus species is around May to June with flight throughout summer, depending on the warmth of days (Daterman et al. 1965, Daterman and Overhulser 2002) (Table 2). Trypodendron lineatum begins flight earlier in the spring than Gnathotrichus spp. because T. lineatum prefer aged timber of at least 3-5 months old, or trees that have died the previous autumn or winter (Borden 1988). Ambrosia beetles are appropriately grouped together because all species of this tribe bore into the inner sapwood to feed on their cultivated 'garden' of mycelial growth of ambrosial fungi that they vector, instead of consuming the phloem or woody tissue of the trees. Epidemiology of bark beetle populations There are four phases in the population dynamics of Dendroctonus ponderosae: endemic, incipient-epidemic, epidemic or outbreak, and post-epidemic (Safranyik and Carroll 2006). At endemic phases, D. ponderosae exhibits similar colonization behavior to that of a "secondary" bark beetle, reproducing in weakened, dying or dead trees. There are insufficient numbers of beetles to overcome even a single large-diameter live tree within the stand; thus, the insects are restricted to subsistence on low-quality hosts (Evenden et al. 1943). The population reaches incipient-epidemic levels under favorable conditions, such as declining tree resistance from a series of stress events like fire or drought. This allows the population to reach an epidemic threshold to successfully attack and overcome the tree defenses and begin to kill live large-diameter trees within the stand (Berryman 1982a, Raffa and Berryman 1983). This critical turning point reflects a threshold upon which a population may decline to endemic stages or to continue to build up to a full-scale outbreak if ideal conditions for beetle survival, development and establishment persist. Such conditions may include, but are not limited to, stressed trees, forest disturbance events, and the insects' interactions or associations with other secondary bark beetles that facilitate an epidemicity (Weaver 1934, Roe and Amman 1970, Carroll et al. 2006a, Safranyik and Carroll 2006, Fettig et al. 2010, Koopmans 2011, Smith et al. 2011). Once populations enter epidemic stages, D. ponderosae acts as a "primary" bark beetle to exert stand-replacing mortality at a landscape-level. This stage of the population is highly resilient to large losses. The outbreak is sustained as long as an abundance of preferable hosts is available, such as mature pines. The insects also require favourable weather conditions, such as mild winters or warm summers or prolonged stress events like droughts and diseases. When there are insufficient supply of large-diameter host trees to sustain the outbreak or when the population suffers huge losses from lethal low temperatures, the population enters the post-epidemice phase (Safranyik and Carroll 2006). Secondary bark beetles may exhibit similar population phases, but with less steep population growth and peaks at lower population sizes. Secondary bark beetles may be facultative mortality agents of lodgepole pine for two to three years following an outbreak of D. ponderosae. High numbers may build due to increased host abundance from the weakened, dying, or dead host pines from a D. ponderosae outbreak or simply under favourable climatic conditions, owing to an extended period of growth and development 11 while minimizing mortality rates (Keen 1952, Linger 1993, Kegley et al. 1997). The secondary bark beetles potentially causing new lodgepole pine mortality among live residuals in British Columbia following an outbreak of Dendroctonus ponderosae include sympatric species such as Ips pini (Say), Hylurgops spp., Orthotomicus latidens (LeConte), Pseudips mexicanus (Hopkins), Dendroctonus murrayanae (Hopkins), Pityogenes spp. (Bedel), Pityophthorus spp. (Eichoff), as well as ambrosia beetles. Importance of the outbreak of Dendroctonus ponderosae and its effect on the economy and environment The present outbreak of D. ponderosae in western Canada is the most destructive outbreak by a forest insect in recorded history (Kurz et al. 2008). The latest reports, as of 2012, indicate that D. ponderosae had caused a mortality of mature lodgepole pine over an estimated cumulative area of 17.5 million hectares in British Columbia and Alberta, or a total of 726 million cubic meters of timber, since the outbreak began around 1997 (Walton 2010, BCMoFLNRO 2011). The mortality to date is larger than the combined total of all other bark beetles' mortality in the western coniferous forests of the United States recorded since 1997 to the present day (16.8 million hectares; USDAFS 2011), and the scale of mortality is at least six times larger than the combined total of all recorded outbreaks in the province from 1910 to 1995 (Unger and Fiddick 1979, Wood and Linger 1996). At present, more than 250 thousand trees, or a total of more than 3.6 million cubic meters of pine forests (jack pine, Pinus banksiana Lamb, and the lodgepole-jack pine hybrid) at risk in Alberta have been removed, as preventive measures (ABSRD 2010, 2011) to reduce the beetles' spread eastwards into the boreal forests of North America (Safranyik et al. 2010, Cullingham et al. 2011, Giroday et al. 2011). Currently, the insect has spread as far east as the Alberta- 12 Saskatchewan border (Brian H. Aukema 2012, personal communication). Currently, the D. ponderosae population in British Columbia is experiencing a decline as its preferred host, larger diameter, mature lodgepole pine, has been killed since the outbreak peaked in 2005-2007 (Westfall and Ebata 2010, Sambaraju et al. 2012). The scale of this outbreak is so extensive and unprecedented that beetle populations with exhausted host supplies have begun to attack small tree in dense stands or mixed-species stands around the peripheries of the outbreak. For instance, pine stands as young as 18 years of age or as small as 8 cm in average diameter around the Prince George Forest District (Westfall 2004) have been attacked, and non-pine trees (such as interior hybrid spruce, Picea engelmanni Parry x Picea glauca (Moench) Voss) have signs of colonization by the beetles, though these events are rare occurrences (Evenden et al. 1943, Furniss and Schenk 1969, Huber et al. 2009, Safranyik et al. 2010). Concomitant with the decline of numbers of D. ponderosae in the central interior of British Columbia, there has been an increase in secondary bark beetle populations breeding in an abundance of unoccupied phloem, such as the limbs, branches and twigs of the crowns, and root collar regions of pines whose stems have been colonized by D. ponderosae (Evenden and Gibson 1940, Rudinsky 1962, Furniss and Carolin 1977, Safranyik et al. 1996,1999a, 2000). Those areas may be considered poor quality substrate for D. ponderosae, or outright unsuitable, but may be excellent host material for secondary bark beetles (Reid and Robb 1999, Safranyik et al. 1999a, 1999b, 1999c, 2000,2004). At the same time as D. ponderosae may deplete hosts, so too secondary bark beetles may reproduce by attacking almost any surrounding trees as resources become scarcer. The trees at risk are primarily residuals, 13 comprising the smaller diameter classes or next generations of trees as the future mid-term timber supply for the province (Roe and Amman 1970). The outcome may be extension of the bark beetle outbreak from the additional mortality of the pole-sized trees, for up to three years, depending on the abundance and years of accumulation from the populations built up, after the collapse of populations of D. ponderosae (Evenden and Gibson 1940, Kennedy 1969, Roe and Amman 1970, Kegley et al. 1997, Safranyik and Carroll 2006, Westfall 2006). Westfall (2006) noted that I. pini accounted for 20% of young lodgepole pine mortality in plantations. In recent years, annual surveys of the forest health conditions in British Columbia by Westfall (2005) and Westfall and Ebata (2007, 2008,2009,2010) have reported that young pine mortality has been on the rise, totaling almost 800 thousand hectares out of the approximately two million hectares of available young, lodgepole pine leading stands between the ages of 20-55 years in the province. Such losses are depicted schematically in Figure 1. These estimates represent increasing mortality within the mid-term supply in the province, or an additional 5% mortality following the current outbreak (0.8 million hectares/17.5 million hectares). While the causative agents of mortality are unknown, outbreaks of secondary bark beetles should not be treated as an event of limited or nonsignificance. These estimates came from calculations from aerial surveys for D. ponderosae at the landscape level. At present, no detailed assessments of stand characteristics have been analysed on an annual basis that would allow (I) estimates of the rate of residual mortality in the post-outbreak stands and (II) identification of bark beetles (primary and secondary) that may be associated with such mortality. 14 Objectives There were two main objectives in this study: (I) to assess a variety of stands in the declining phase of an outbreak of Dendroctonus ponderosae over a two-year period to determine the extent and rate of lodgepole pine mortality, and (II) to examine the relationship between the rate of mortality and associations with Dendroctonus ponderosae, secondary bark beetles, and root collar damage by insects or other agents of mortality. Authorship While the work in this thesis is my own, I use the first person plural pronoun throughout. This work is being prepared for submission to a peer-reviewed journal with co-authors Allan Carroll and Brian Aukema. As such, I retain 'we' and 'our7 throughout the thesis to signify joint authorship. 15 Materials and Methods Section 1: What do stands look like in the post-outbreak phase of an epidemic of Dendroctonus ponderosae? Forest profiles may be altered as D. ponderosae activity shifts the balance of dead and live lodgepole pine composition in stands throughout the course of an outbreak. Thus, the first goal was to survey the patterns of mortality over two years in several stands along a gradient of activity of D. ponderosae in central British Columbia, focusing primarily on stands where populations of D. ponderosae were declining, or in a "post-outbreak" mode (Safranyik and Carroll 2006). Parti. Stand selection Stands were selected where lodgepole pine was the dominant species and there was evidence of recent tree-killing activity by 0. ponderosae. The latter criterion was judged by an abundance of trees in the "green, red, and grey-attack" categories (referencing the colour of the crown in years prior to, during, and following tree death (Safranyik et al. 1974, Aukema et al. 2006). "Green-attack" represents live trees, subsequently examined in following years for new tree mortality associated with D. ponderosae and/or secondary bark beetles. "Red-attack" denotes recent colonization by D. ponderosae and tree death within the past year or two, as foliage fades to a chlorotic yellow, then red, within one year. "Grey-attack" represents lodgepole pine killed by D. ponderosae in previous years (i.e. often more than two years old). A photographic reference guide of the crown conditions are provided in Appendix B. The presence or absence of D. ponderosae and/or secondary bark beetles was evaluated based on visual observation of pitch tubes, boring dust at the base of the tree, and galleries under the bark. 16 In total, seven study sites were selected as representative samples of lodgepole pine distributions in the central interior region of British Columbia were selected: five near Mackenzie (Mackenzie Forest District at 55° 29' N, 123° 26' W, elevation: ~800m), one near Crassier Creek (Peace River Forest District at 55° 39' N, 122° 17' W, elevation: ~1050m), and one near Chief Lake (Prince George Forest District at 54° 13' N, 123° 04' W, elevation: ~750m). The Mackenzie Forest District is located between the Peace River Forest District and the Prince George Forest District, in the center of British Columbia. All seven sites were located at least one kilometer apart from each other. A map of the study sites, their locations relative to tree-killing activity by D. ponderosae recorded by aerial surveys and photographs of the study sites are provided in Appendix C and Appendix D. Part II. Stand establishment In each of the seven sites, two plots measuring 10 x 10 meter (0.01 hectares) were placed at random in the spring of 2009. At one site in Mackenzie, a third plot of similar size was also established in the second year of the study. Within each plot, a census of each tree was recorded over two years: species of tree, diameter at breast height (DBH, 1.3m), height, and condition (alive or dead) (Avery and Burkhart 2002). The diameter of trees were measured using a DBH tape, or a caliper for smaller trees, and the tree height was recorded using a Haglof vertex IV hypsometer, or a tape measurer for smaller trees. The first survey to establish the stand profiles was conducted in mid-summer 2009, the second survey in early summer of 2010, before the primary flight of D. ponderosae, and the third survey latesummer of 2010 to detect any trees that had died in 2010. 17 Part III. Stand classifications (density and maturity) Forest stands can be measured both qualitatively and quantitatively. Forest productivity can be evaluated using qualitative measures such as climate, soil and vegetation characteristics, or quantitatively using an economical value in wood productivity (Ford-Robertson and Winters 1983). Quantitative methods are often favored because measurements of stand density can be made if the topographic or climatic conditions permit classification of certain qualitative biogeoclimatic zones. These measurements facilitate comparison among sites' potential productivity relative to one another, which is a useful tool for forest managers. Stand density is important because density is directly proportionate to growth rate and the stand's consequential future merchantable yield. For example, in an ideal pure lodgepole pine stand, the optimum density of 1,980 trees/hectare might yield 280 m3/hectare of merchantable timber, compared to 4,450 trees/hectare yielding only 21 m3/hectare (Lotan and Critchfield 1990). The four most common measurements of stand density use diameter, height, form, and number of trees per unit area (Bickford 1957). This study used two quantitative measures of stand density as direct and indirect measures of the current and potential productivity of the forest. The first method of stand density estimation used the number of lodgepole pine stems per hectare. The stand density per hectare for each site was estimated by multiplying the quantity of trees within the 10 x 10 meter plots by 100, since all plots were standardized to a fixed area of 0.01 hectare (1 hectare = 100 plots of 0.01 hectare /10 x 10 meter). Based on the survey data, the sites and plots were grouped into three categories: (I) low density at 0-25 lodgepole pine per 10 x 10 meter plot (0-2500 stems/hectare), (II) medium density at 26-60 pines per plot (2600-6000 stems/hectare), and (III) high density with more than 60 pines per plot (>6000 stems/hectare). The second method of stand density estimation evaluated the height and diameter of the trees (Briegleb 1952). Stands were classified as 'old' if the trees exhibited an average diameter of at least 10 cm, including more than one large diameter pine of at least 20 cm in circumference, and mean height of at least 10 m, with more than one pine at least 20 m tall. In contrast, a stand was classified as 'young' if the mean diameter of lodgepole pine was less than 10 cm and the average height was less than 10 m, with no lodgepole pine larger than 20 cm DBH or taller than 20 m. If all of the criteria for an 'old' stand were not met, the plot or site was considered a 'young' stand with high annual growth potential. If the surveyed pines met at least two, but less than four, of the criteria, the site or plot was considered a 'young-old stand'; a stand with a moderate rate of growth that will gradually diminish as the stand matures. The effect of diameter and height of lodgepole pine on pine condition (dead or alive) was examined using a logistic regression in a mixed effect model. Fixed effects included diameter at breast height and tree height, fitted as continuous variables. Sites and plots were modeled as random effects. Section 2: Which insects and/or pathogens are most closely associated with new tree mortality? For reference, a flow chart of the methodology is provided in Appendix E. An initial survey for all plots, except for the fifteenth plot in Mackenzie, was performed at the beginning of the summer in June or July of 2009. The survey involved visual examination of all trees for any signs of bark beetle infestation. If a lodgepole pine was dead or showing signs of dying, such as yellowing or reddish foliage or drying phloem, the putative source of tree mortality was sought by peeling back a small section of the bark, approximately 30 cm x 30 cm, to look for any signs of D. ponderosae and/or any secondary bark beetles. The presence or absence of bark beetles or their galleries was noted and photographed. This inspection was performed at the roots, at breast height (1.3 m), and at approximately three meters high. In each plot, the lodgepole pines were also checked for the presence or absence of root collar damage by insects at the bases of the trunks by scraping away leaf litter and the tree bark, digging down up to 50 cm below root collar of the main trunk. Western gall rusts (Endocronartium harknessii) were noted as well, when found on the upper branches of the lodgepole pines, or the main bole of smaller trees. A photographic reference for each gallery type by species of the insect, and the descriptions of the insects themselves, occasionally encountered, are included in Appendix F. The plots were established and surveyed once in 2009. In 2010, a mortality survey was performed twice in all 15 plots, once before August 15, and another after August 15 (i.e. before and after the peak flight period of D. ponderosae and secondary species, determined from unpublished data of pheromone traps in the locality). In the second and third surveys, the live lodgepole pine in the 10 x 10 m plots were re-examined for any new mortality. Trees that were dying or dead were checked for corresponding bark beetle activity. If the survey before August 2010 detected the presence of D. ponderosae, the beetles were concluded to have arrived in the 2009 flight season. If a tree remained alive and vigorous, the conclusion was that there was no beetle colonization (or an unsuccessful one). For data quality purposes, all dead trees were revisited and measured a second time (third survey) in 2010, using similar methods of examination as in 2009 (Appendix E); i.e. diagnosis of the galleries by removing sections of the bark, with the inference that detection of D. ponderosae at this stage reflected a recent arrival within the 2010 flight period. Though all seven sites were surveyed in 2009, three of the Mackenzie sites were surveyed before the peak flight period of D. ponderosae in 2009 (before 13 August, determined from unpublished data of pheromone traps in the locality), which meant that the records of 2009 from those three sites might not reflect the arrivals of all the D. ponderosae of the same year; the remaining sites were surveyed after D. ponderosae flight, accounting for their arrival by 2009. Overall, the survey of 2010 that was performed twice (second and third surveys) served the dual purpose of monitoring for bark beetle activity before and after their main flight seasons in 2010, and this standardized those three sites with the rest, while ensuring consistency in the records from the 2009 survey. An additional plot in one of the high-insect activity sites near Mackenzie, site 3-plot C (Mac3-C) was surveyed in 2010 and added into the overall survey of tree mortality associated with various insects and pathogens. Mac3-C was randomly selected and surveyed for meeting the profile criteria as a high risk stand for mortality of secondary bark beetles. Since this plot was not surveyed in 2009, analysis of the rates of mortality was excluded, but studies of the associations of various insects, including bark beetles, with the overall tree mortality was included in the analysis. This stand, on its own, is treated in depth in Appendix I. 21 The effects of tree diameter, D. ponderosae, root collar damage by insects (such as Warren root collar weevil, Hylobius warreni Wood), and the presence/absence of secondary bark beetles or individual secondary bark beetles such as I. pini (Say), 0. latidens (LeConte), and P. mexicanus (Hopkins), on associated pine mortality (i.e. live/dead) were examined using generalized linear mixed effect models for binary response data. Fixed effects included diameter at breast height and tree height, fitted as continuous variables, and the presence or absence of D. ponderosae, root collar damage by insects, and the presence of any secondary bark beetles or individual species of secondary bark beetles, fitted as categorical variables. Terms for the stand variations within the seven sites, or the 15 plots within the sites, were modeled as random effects. The most parsimonious models were selected based on Akaike Information Criteria (AIC), a measure of relative goodness of fit (Akaike 1974), with the lowest AIC score for a given response variable representing the best fit. All data analysis was conducted using R (Dalgaard 2008, R Development Core Team 2010). 22 Results Section 1: What do stands look like in the post-outbreak phase of an epidemic of Dendroctonus ponderosae? Within the 15 plots, 827 trees were surveyed, consisting of 624 lodgepole pines, 96 interior hybrid spruces [Picea engelmanni Parry x Picea glauca (Moench) Voss], 45 trembling aspens [Populus tremuloides Michx.], 22 black spruces [Picea mariana (Mill) BSP], 28 subalpine firs [Abies lasiocarpa (Hook) Nutt], eight Douglas-firs [Pseudotsuga menziesii (Mirb.) Franco], and four paper birches [Betula papyrifera Marsh.] (Figure 2, Table 3). Eighty eight percent (550/624) of the lodgepole pines were located in the sites near Mackenzie. All plots located near Mackenzie had 50% -100% lodgepole pine composition, except for one, which had only 35% lodgepole pine (Table 3). The remaining 12% (74/624) of the lodgepole pines occurred in plots near Chief Lake and Crassier Creek (Figure 4). In these latter plots, lodgepole pines were more mature and found in mixed-species compositions, characteristic of lodgepole pine as a subclimax species. Even so, the lowest composition of lodgepole pine was 35% in the CLk site, plot B (Table 3). The density of lodgepole pine varied among sites, from eight to 126 stems per 10 x 10 m plot (or 800-12,600 stems per hectare) (Table 4). Based on the stand 'maturity' criterion, six of the 15 plots were young, six could be considered old, and the remaining three plots were transitioning young-old plots. These categorizations were derived from the diameter and height of the trees in the plots (BCMoFLNRO 2011; Briegleb 1952) (Table 4). Of the 557 lodgepole pines surveyed in 2009,42% (236/557) were alive and 58% (321/557) were dead. If lodgepole pine in Mac3-C was included, the final tallied results were 40% live (251/624) and 60% dead (373/624) lodgepole pine. Only 557 lodgepole pines 23 from the 14 plots were used in the determination of the annual rate of tree mortality, since the remaining 67 (Mac3-C) of total 624 lodgepole pines were only surveyed in 2010, precluding calculations of the changes in mortality from 2009. Surveys in 2010 revealed that an additional 25 lodgepole pines had died, decreasing the percentage of live lodgepole pines to 38% (211/557), and increasing the percentage of dead pines to 62% (346/557) (Figure 3). The 25 dead trees in 2010 yielded, then, an annual rate of pine mortality of approximately 4% (25/557 trees). The rate of mortality was highly variable between sites, ranging between zero and 15% depending on the lodgepole pine density and its maturity class. Among the sites near Mackenzie, site two (Mac2) exhibited the highest rate of mortality at 14% (12/83) in 2010, supplying almost half of the new mortality (12/25) (Figure 4). This was a relatively young stand (Table 4); plot A within that site (Mac2-A) exhibited a low stocking density, and displayed a mortality rate of 17% (2/12), while plot B within that site (Mac2-B), exhibited a high density of trees and a mortality rate of 14% (10/71). The plot with the highest cumulative lodgepole pine mortality, 89% (33/37 trees), occurred within the fourth site of Mackenzie (Mac4-A; a medium density 'old' stand). Comparisons between diameters and heights of live vs. dead lodgepole pine On average, the 624 lodgepole pines had mean measurements of 8.4 cm in diameter and 10.1 m in height. Overall, the dead lodgepole pines exhibited slightly larger diameters than the live residuals (9.9 ± 1.4cm vs. 10.4 ± 1.5cm), although this difference was not statistically significant (t6os = 1-40, p = 0.16) (Table 5). In contrast, live trees were taller than dead trees (12.1 ± 1.6m vs. 11.2 ± 1.6 m) (tSi7 = 2.54, p<0.05) (Table 5). There was, however, considerable plot to plot variation and year-to-year differences could alter a 24 stand's profile with only minor mortality. For example, plots Mac2-A and Mac4-A sustained the deaths of only two trees within each plot from 2009 to 2010. Although Mac2-A was a 'young' stand with a low density (n=12, live=8 in 2009), the death of two of its largest live lodgepole pines (tree #1: 11.6 cm and 8.6 m, tree #2:10.0 cm and 7.2 m) decreased the plot's average diameter from 5.0 cm to 3.0 cm and average height from 4.5 m to 3.3 m. In the moderately dense stand of Mac4-A, the death of the largest tree (13.2 cm and 17.4 m) was sufficient to shrink the stand's mean diameter range from 6.3-13.2 cm to 6.3-11.3 cm, and the height range from 11.8-17.4m to 13.2-16.2m. These results are illustrated graphically in Figures 5 and 6, with numerical summaries presented in Tables 6 and 7. Section 2: Which insects and/or pathogens are most closely associated with new tree mortality? Overall, 60% of the lodgepole pines surveyed (373/624) within the 15 plots in 2010 were dead. The 373 dead lodgepole pines comprised a combination of 321dead pines from the 14 plots surveyed in 2009,25 new dead trees near Mackenzie in 2010, and 27 dead trees from the new plot of Mac3-C in 2010 (Figure 3). Among the 373 dead trees, 191had signs of D. ponderosae in 2009. Surveys detected an additional four pines with D. ponderosae in 2010 (Table 8A). By the end of summer in 2010, two out of those four attacked trees had died. More than 80% (163/193) of the trees with galleries of O. ponderosae were associated with plots near Mackenzie. This figure was consistent with the majority of the lodgepole pines being found near Mackenzie (550/624 lodgepole pines surveyed, or 88%) (Figure 2). Among the seven sites in Mackenzie Forest District in 2010, D. ponderosae were most frequent in a low density 25 'young-old' stand (Mac5) at 76% (25/33) and least frequent in a high density 'young' stand (Macl) at 23% (21/87) (Table 9). Secondary bark beetles were found in 54% of the dead trees (200/373) (Table 8). Among the 200 trees with secondary bark beetles, the frequency of each species detected in the survey were 35% I. pini (70/200), 86% Hylurgops spp. and/or D. murrayanae (171/200), 24% O. latidens (48/200), 14% P. mexicanus (27/200), 13% Pityogenes spp. and/or Pityophthorus spp. (25/200), and 39% ambrosia beetles (77/200). Most of the time, when galleries of Hylurgops spp. and/or D. murrayanae overlapped, Hylurgops spp. appeared to be the more likely agent associated with the dead trees rather than D. murrayanae, based on the type and location of the galleries (extending below the root collar) and/or on the presence of the black stain fungus (Appendix F and photos in Appendix G). The presence of O. latidens with P. mexicanus were associated with the larger trees (n: 13/27, d: 13.3 cm, fi: 14.9 m) in comparison to the presence of P. mexicanus in the absence of O. latidens (n: 14/27, d: 11.8 cm, ft: 13.6 m). The presence of ambrosia beetles was highly variable. These insects appeared to prefer older, more mature stands. The highest occurrence of trees with these xylophagous insects was in Mac5, 55% of the time (18/33), followed by Crassier Creek, 41% of the time (14/34) (Table 8). The survey found 30% or more (113/373) of the dead trees to contain wood borers, evidenced by the wood shavings of the larval galleries by the wood borers that often intermingled with those of the secondary bark beetles (Table 8). 26 The presence of feeding damage around the root collar by insects from plot to plot was also highly variable, from a low 13% of the time (7/52) in Macl-A to a high 79% of the time (11/14) in CLk-A. Most of the more mature sites had higher occurrences of root collar damage compared to the younger sites. On average, the presence of root collar damage on most plots (11/15) encompassed about one third or more of the plots' area, where four of those plots had root collar damage presences of more than 50% of the plot area (Table 8). Western gall rust occurred on approximately one third of all lodgepoie pines surveyed (221/624) and occurred on 30% (113/373) of the dead trees (Table 8). One site was responsible for more than half of these occurrences, Macl at 66% (117/178). Western gall rust was most frequently noted on the smaller trees. In general, galleries of D. ponderosae and secondary bark beetles were found in almost equal abundance in trees of similar diameter and height. For example, galleries of D. ponderosae were found in trees with mean diameter of 13.6 cm (6.0-26.9 cm) and mean height of 14.8 m (5.9-25.6 m), and galleries of secondary bark beetles were found in trees with mean diameter of 13.0 cm (4.5-26.9 cm) and mean height of 14.2 m (4.0-25.6 m). Trees with secondary bark beetles, but without indication of D. ponderosae, were much smaller (d: 6.6-10.8 cm, fi: 7.8-11.9 m). These relationships of the tree size measurements with individual bark beetles and/or their interactions are further explored in Appendix H. When all 624 trees were examined, the best model explaining the likelihood of lodgepoie pine mortality indicated that the probability of tree death was associated with the presence of any of the assemblage of secondary bark beetles, and decreased with increasing diameter of the lodgepoie pines (AIC: 571) (Table 10A). No term for the presence of 27 D. ponderosae occurred in that model. The best model that demonstrated tree death increased with presence of D. ponderosae in the post-outbreak stands showed that the probability of tree death increased simultaneously with the presence of /. pini and/or O. latidens in the same trees, and was only the 5th best model overall (AIC: 726, Table 10A). Examining the effect of D. ponderosae in the tree on its own was only the 15th best model in predicting tree death (AIC: 775). Other secondary insects or damage on their own were similarly unsuitable: I. pini reflected the 16th best model (AIC: 791); O. latidens reflected the 17th best model (AIC: 809); P. mexicanus the 18th best model (AIC: 824); root collar damage by insects the 19th best model (AIC: 832). Physical attributes such as diameter produced only the 20th best model(AIC: 833). In contrast, a model containing the complex of secondary bark beetles was the 4th best model overall (AIC: 628) (Table 10A). These results were highly variable across sites. The top models for each of the sites are shown in Table 10B. Among the seven sites, almost half had secondary bark beetles associated as the primary indicator of tree death (3/7), two had D. ponderosae as the most significantly associated mortality agent (2/7), and the remaining sites showed no relationships with bark beetles as agents of mortality (2/7). A detailed study of one of those stands, Mac3-C, is provided in Appendix I. Secondary bark beetles may be attacking or colonizing many more trees than just those killed. In 2010,21 of the lodgepole pine contained frass from new activity by bark beetles in 2010 (mean diameter, d: 8.9 cm, mean height, ft: 11.3m; Appendix J). All of these trees originated from the plots near Mackenzie (20/21) and Crassier Creek (1/21). Among the 21 lodgepole pines, 57% had D. ponderosae (12/21), 95% had an assemblage of 28 secondary bark beetles (20/21), 86% had I. pini (18/21), 52% had Hylurgops spp. and D. murrayanae (11/21), 33% had 0. latidens (7/21), 33% had P. mexicanus (7/21), 38% had Pityogenes spp. and/or Pityophthorus spp. (8/21), 5% had ambrosia beetles (1/21), 62% had root collar damage by insects (13/21), 14% had wood borers (3/21), and 38% had western gall rust (8/21) (Table 11). A full accounting of tree sizes and interactions among the insects in trees with frass, and the respective sizes of those trees is provided in Appendix K. Among the 21 trees with frass, half had died (10/21) by 2010. Some trees had been dead since the first survey in 2009 (3/21). Others looked alive, having predominantly green needles (4/21). The last four trees (three dead, one alive) occurred in Mac3-C and were surveyed in 2010 (Table 11). Among the 10 trees that died in 2010 with frass, some of the trees displayed a high likelihood that the mortality was the work of bark beetles (6/10), without evidence of other critical mortality agents. The other four trees with frass had some form of mechanical injury, such as broken tops (4/10). All 10 trees harboring bark beetles had at least part of the complex of secondary bark beetles (d: 8.3 cm, h: 10.6 m). Ips pini was the most commonly associated individual secondary species found 90% of the time (9/10) (d: 8.4 cm, fi: 10.6 m) (Table 11). Although these models indicate that secondary bark beetles may be as, or more, associated with dead trees than D. ponderosae in the post-outbreak period, correlation is not causation. The trees could have been heavily infested with secondary bark beetles well in advance of (or after) colonization by D. ponderosae. Hence, the associations of bark beetles with trees that died in 2010 was also studied. The rate of new mortality in the stands was approximately 4% (25/624) in 2010. These trees are displayed in Table 12. 29 Eight of these trees had D. ponderosae; six trees in 2009, and two new dying trees in 2010 (total of 8/25). Six of the 25 trees appeared to have no colonization by D. ponderosae or any structural defects, displaying only colonization by secondary bark beetles (Table 12). Thus, annual new mortality for 2010 associated with activity by secondary bark beetles appeared to be only 1% overall (6/624). Of the eight trees that had evidence of attack by D. ponderosae, only one did not have heavy amounts of colonization by secondary bark beetles such as I. pini or structural defects such as a broken top (Table 12). In total, sixteen of the 25 trees had an assemblage of secondary bark beetles, and ten of them contained frass (10/25), an indicator of fresh attack by secondary bark beetles. Among the 16 trees with secondary bark beetles, the individual species included I. pini (11/16), Hylurgops spp. and/or D. murrayanae (9/16), O. latidens (9/16), P. mexicanus (5/16), and Pityogenes spp. and/or Pityophthorus spp. (7/16) and one tree with ambrosia beetles (1/16) (Table 12). Just over half of these trees, 52%, had root collar damage by insects (13/25) as well. Among the 25 trees, 28% (7/25) had broken tops. Four of the seven trees with broken tops had been attacked by various species of bark beetles other than D. ponderosae. 30 The findings are consistent with evidence that species of secondary bark beetles can kill trees in the post-outbreak phase of a landscape-level eruption of a primary bark beetle. To date, much information on colonization activity by secondary bark beetles such as pine engravers has focused on their reproduction in habitats disturbed by fires or storms (Kennedy 1969, Miller et al. 1986, Amman and Ryan 1991, Rasmussem et al. 1996, McCullough et al. 1998, Reid and Robb 1999, Lombardero et al. 2006, Ryall et al. 2006, Gandhi et al. 2007, Aukema et al. 2010, Fettig et al. 2010). Studies on tree-killing activity by these insects have been restricted primarily to instances where trees have been heavily stressed by drought (Raffa et al. 2008) or competition, where pine engravers have been known to kill small groups of trees of 5-8 inches DBH (Kegley et al. 1997). Studies of activity by secondary bark beetles in concert with other biotic disturbance agents such as rootboring insects (Aukema et al. 2010) or D. ponderosae (Safranyik et al. 1999a, 1999b, 2004) have been less abundant. To our knowledge, this is the first study to quantify the frequency of association of the members of the bole-infesting assemblage of bark beetles colonizing lodgepole pine during the post-outbreak phase of D. ponderosae epidemic over a large spatial area. Results from this study indicated that that year-over-year mortality was associated with pines of decreasing diameter, or likely those stressed by interspecific competition prior to D. ponderosae removing the largest and most dominant pines in the stands. Females of D. ponderosae, attacking vigorous trees, produce vertical J-shaped galleries that overcome host defenses by increasing the rate of depletion and cumulative resins produced by blocking water conduction in the xylem. In contrast, females of many species of secondary bark beetles simply lay eggs in north-south or randomly-oriented galleries as larval galleries radiate laterally across the grain of the wood. In this study, although galleries of secondary bark beetles may have been highly abundant, without exhaustive sampling of a whole tree, it is impossible to prove that trees putatively killed by secondary bark beetles did not have D. ponderosae. For example, even a failed attack by a few D. ponderosae, undetected in our sampling scheme, may have introducted pathogenic blue stain fungi that contributed to the demise of a tree (Kim et al. 2005, Six and Wingfield 2011). Likewise, other potential mortality factors in the stands cannot be excluded (Smithers 1961, Amman 1975, Unger and Fiddick 1979, Westfall and Ebata 2010), including pathogens like western gall rust (Peterson I960), Comandra blister rust (Johnson 1986), Atropellis canker (Lightle and Thompson 1973), Armillaria root disease (Baranyay and Stevenson 1964, Tkacz and Schmitz 1986, Williams et al. 1986), Dothistroma needle blight (Peterson 1982, Bradshaw 2004, Welsh et al. 2009), or parasitic plants like lodgepole pine dwarf mistletoe (Hawksworth and Dooling 1984). The amount and surface area covered by galleries of secondary bark beetles (results not shown) provide reasonable evidence that secondary bark beetles were associated with up to 25% of the direct mortality seen in the post-outbreak phase of this D. ponderosae epidemic. Secondary bark beetles are excellent competitors with D. ponderosae in outbreak or post-outbreak phases. For example, the more aggressive species of secondary bark beetles, such as I. pini or Pityogenes knechteli, have been recorded to have higher attack densities than D. ponderosae (optimal attack densityof /. pini is potentially higher than 32 100 attacks/m2 vs. D. ponderosae around 60-70 attacks/m2, and higher still for P. knechteli) (Raffa and Berryman 1983, Berryman et al. 1985, Rankin and Borden 1991, Borden et al. 1992, Poland and Borden 1994b, Raffa 2001). The fungal associate of /. pini is highly adapted to colonize and develop in highly stressed and dying trees compared to D. ponderosae fungi that grow best in healthy vigorous phloem (Six and Paine 1998, Solheim and Krokene 1998, Kopper et al. 2004, Kim et al. 2005). Many species of secondary bark beetles are usually bivoltine, with parents often emerging to establish second, or sometimes third, broods in a longer than usual growing season (Safranyik et al. 1996,2000). To reduce competition, the insects partition hosts in space and time, often through sophisticated communication signals that may repel competing species (Figure 8, Table 1). For example, many scolytids exhibit spatial partitioning within a tree (Reid 1955, Safranyik et al. 2000, Ayres et al. 2001, Aukema et al. 2004,2010, Wermelinger et al. 2007). In this system, the more aggressive bark beetles such as D. ponderosae often occupy the main bole of the tree, between the root collar and regions up to 5 m high. Smaller secondary bark beetles, such as I. pini and O. latidens, occupy the upper bole and larger branches, and Pityogenes spp. and/or Pityophthorus spp. occupy the thinner and higher phloem sections of the smaller branches and twigs (Poland and Borden 1994a, 1994b, Safranyik et al. 2000). Below the lower bole, the larger secondary bark beetles, such as P. mexicanus, Hylurgops spp. and/or D. murrayanae are primarily found in the root collar regions and on the larger roots (Furniss and Carolin 1977, Wood 1982b, Safranyik et al. 2000). The niche partitioning strategy exhibited was consistent with the location of attacks by the bark beetles sampled in this study (Figure 8, Table 1). 33 Differences in peak flight time between species also minimize competition with sympatrics. For example, Safranyik et al. (2000) captured the earliest flights of Hylurgops porosus and Trypodendron lineatum before flights of /. pini, P. knechteli, and D. ponderosae in British Columbia. Temporal partitioning may also avoid predation, synchronize growth capacity with symbiotes, and promote colonization during a period when the hosts are most stressed or most abundant (Reid 1955,1962a, Amman and Cole 1983, Safranyik et al. 1999b, 2000, 2004, Safranyik and Carroll 2006). Benefits of earlier or later flights are often balanced against the risk of mortality, such as arriving too late at a host, with competitors depleting most of the available common resources (Hardin 1960, Stephens and Krebs 1986, Bell 1990). A summary of the temporal partitioning between the bark beetles in this system is depicted in Figure 9, with more descriptions provided in Table 2. Bark beetles procure and partition hosts by responding to a host of chemical signals, including host monoterpenes and pheromones synthesized by their symbiote microbes, produced de novo from the insects' hindguts, and/or oxidized products from the metabolized precursors ingested in the host phloem (Byers 1987,1989,1995, Seybold et al. 2000, Raffa 2001). The combination of pheromones/allomones and host monoterpenes benefit the bark beetles by inducing a suite of behavioral responses in conspecifics or sympatrics from an aggregation or a deterence response. These results to maintain an optimal colonization density, which influenced the insects' behaviour to locate, accept, or feed upon the host trees. Such signals can also adversely affect the population by serving as kairomones to predators, parasites and competitors of bark beetles (Borden 1982, Wood 34 1982a). Discussion of the pheromone systems of the bark beetles infesting lodgepole pine in this study can be found in Figure 10 and Appendix A. Our findings extend the current understanding of the bole-infesting assemblage of bark beetles in lodgepole pine in central British Columbia, Canada. In its endemic phase, D. ponderosae acts almost as a secondary bark beetle, persisting in unthrifty trees with secondary bark beetles such as P. mexicanus and I. pini (Smith 2008, Smith et al. 2009). When conditions permit an increase in numbers, D. ponderosae may recruit enough conspecifics to be able to strip-attack a lodgepole pine (Carroll et al. 2006a, Safranyik and Carroll 2006, Koopmans 2011). Secondary bark beetles may aid in this transition by increasing the nutritional quality of the host or promoting more favourable growth conditions for the beetles, perhaps by prior fungal inoculations (Reid 1963,1969, Ayres et al. 2000, Bleiker and Six 2007), diluting the rate of predation (Aukema et al. 2004, Aukema and Raffa 2004, Boone et al. 2008), and reducing or exhausting their common host defenses (Christiansen et al. 1987, Boone et al. 2011). As D. ponderosae gains the ability to kill trees, secondary bark beetle populations build in the spatially-partitioned resource, relegated to unused phloem in tree tops or branch tips. As D. ponderosae exhausts its host supply over a period of approximately a decade (Evenden and Gibson 1940, Kennedy 1969, Roe and Amman 1970, Alfaro et al. 2004, Taylor and Carroll 2004), a delayed-density dependent response in the populations of secondary bark beetles gradually introduces a negative feedback in the declining populations of the D. ponderosae e entering the post-outbreak stage, by accelerating the collapse of D. ponderosae populations due to strong interspecific competition and increasing host exhaustion (Safranyik and Carroll 35 2006). Secondary bark beetles, however, may continue to infest and kill smaller diameter pines for one to three years after the collapse of an outbreak, especially if stand vigour is reduced (Kennedy 1969, Kegley et al. 1997). In our study, year-to-year mortality was as high as 15% of the trees surveyed, depending on the locale. 36 Conclusion: Synthesis and implications for control and management The potential mortality from secondary bark beetles after an epidemic of D. ponderosae can vary spatially and temporally. Since D. ponderosae in the central interior region of British Columbia is at the northern edge of its distribution, the associated composition and sympatric species of D. ponderosae should not be generalized to be the same in all regions of the beetle's range. The breadth of complexity in the host, insect, predators and environmental interactions are highly variable. Dendroctonus ponderosae may exhibit developmental differences in the northern boreal compared to its southern regions, for example. These differences can affect the distribution and possibly the rate of mortality at the northern edges of the outbreak. Our numbers were possibly more conservative in estimating the rate of mortality, in comparison to the growth seasons in the southern regions, which are potentially warmer and longer, with more interactions between the secondary bark beetles within the bole-infesting assemblage. This section focuses on the potential applications of the information collected in this study and/or previous studies to provide practical suggestions for forest managers to mitigate lodgepole pine mortality from bark beetles, with special reference to the incipient and post-epidemic stages, in an ongoing effort to monitor, control, manage, minimize and prevent outbreak occurrences by bark beetles in the future. 37 Mechanical intervention: Stand hygiene and healthy sanitation practices There are several direct control tactics that can be implemented to minimize the risk of mortality from epidemic bark beetles. Since D. ponderosae and secondary bark beetles are sympatrics using the same hosts, and their population dynamics are intricately connected to one another (Carroll et al. 2006a, Koopmans 2011, Smith et al. 2011), the interventions with the highest impacts will be implemented during non-epidemic periods. Parti. Prevention: Cultural controls Cultural practices are excellent preventive tools to manage bark beetles or other agents of mortality of lodgepole pine because such practices may increase the defensive threshold of the trees (Shore et al. 2006, Whitehead et al. 2006). A primary consideration is to have a well-thought plan to maintain stand hygiene, by carefully selecting sites suitable for lodgepole pines and/or harvesting species preferred by bark beetles before they become susceptible (McGregor and Cole 1985). Techniques may include silvicultural tactics such as monitoring the stocking density or spacing treatments, applying regular thinnings to dense stands and/or pruning of individual trees (Mitchell et al. 1983), fertilizing and irrigating during dry summer months (Brockley 2001, Brockley and Sanborn 2009), and reducing the competition for space, light, moisture and nutrients. Stands may also be mixed with other softwood or hardwood species (site permitting), which may decrease mortality originating from one dominant agent of mortality, providing refuges and resources for wildlife and decreased susceptibility to disturbances (McGregor and Cole 1985, Burton 2008). However, potential benefits in planting mixed stands need to be balanced against the trade-off between competition and facilitation in the growth of 38 lodgepole pine in mixed plantations, since different species can offset any potential benefits by retarding the growth of the principal harvest, for example. Part II. Treatment: Direct controls When infestations by bark beetles are detected, prompt removal may be recommended using proper salvaging methods. Some direct control methods may include treating the slash immediately, using methods such as 'lop and scatter', 'pile and burn', chipping, and debarking (Klein 1978, Six et al. 2002). Any harvesting practices, including salvage logging, are only as effective as their proper execution, especially critical during the beetles' flight season. Among the precautions to take during harvesting is prevention of injury to trees, or to roots from soil compaction, which can stress trees, making the remaining trees more susceptible to attack by bark beetles. Solar radiation can be applied on smaller piles of wood, or by homeowners planning to use recently cut firewood that may or may not contain bark beetles, by wrapping and sealing the wood in thick, clear plastic sheets placed in a sunny location to increase the heat treatment, rendering them unsuitable for bark beetles and killing the beetles within by increasing the desiccation rate of the logs. Such methods can be labor-intensive, and their effectiveness is unpredictable as this process is dependent on solar gain. Therefore, the practice is probably more suitable in southern or warmer regions (Graham 1924, Patterson 1930, Buffam and Lucht 1968, Mitchell and Schmid 1973, Sanborn 1996, Negron et al. 2001). Alternatively, the logs can be misted if an abundant water is nearby, making them unsuitable for bark beetle development and emergence (McMullen and Betts 1982, Safranyik and 39 Linton 1982). This idea is likely impractical in areas where lodgepole pine normally grows in inland areas, however. Prescribed burning is another viable option in more rural areas, where an area is less accessible or sanitation logging is not practical (Munger and Westveld 1931, Klein 1978, Swain and Remion 1981, McMullen et al. 1986). The fire must be of sufficient intensity to cause significant mortality (Stock and Gorley 1989, Safranyik et al. 2001), and needs to be balanced against the difficulty and dangers of controlling such treatments (Hirsch et al. 1998). Moreover, ecological tradeoffs of scarring the soil, causing infections and/or scorching the trees may occur, making the trees more attractive to attacks by bark beetles instead. At epidemic levels, the best direct mechanical control may be to quickly remove, burn, or chip the trees on site to prevent beetles from emerging to kill other susceptible hosts nearby, which may slow the spread but may not stop expansion (Hopping and Mathers 1945, Klein 1978). Biological manipulation: Semiochemicals Tremendous progress has been made over the years to elucidate the attraction and repellence by semiochemicals produced by the beetles and/or hosts, with hopes to exploit and manipulate the responses by insects (Appendix A). The semiochemicals can be used in a variety of ways, as a direct method to monitor and control the species of interest or, indirectly, by employing the assistance of sympatrics to increase the level of competition, or to attract the common enemies of bark beetles utilizing those semiochemicals as kairomones (Birch 1978, Borden 1982, Wood 1982a, Byers 1989,1995, Raffa 2001, Boone et al. 2008). 40 Part I. Monitoring the populations of bark beetles A survey of bark beetle populations is recommended as one of the first tools for forest managers to monitor and track population densities over time, as population dynamics of the bark beetles are reciprocally dependent and linked to one another (Berryman 1982b). There are several ways to detect and estimate the populations: by the physical appearance of symptoms and signs of bark beetle activity on the host trees, such as the number of resinous pitch tubes or streaming pitch and frass presence, by 'chopping and checking' for eggs, larvae, pupae and adults under the bark, and from the number of trees with fading foliage, woodpecker activity (or their ratios of infestation to host or area for relative comparison), all of which can be both labor- and budget-intensive for management purposes. Another, more convenient, way is to utilize semiochemicals to estimate the population in the vicinity. Monitoring using bark beetle pheromones is highly espoused because it discloses the population density of bark beetles over time. Continuous screening on an annual basis can allow intervention actions to be taken to prevent or minimize potential future mortality by detecting increases in local populations, before they exceed epidemic thresholds. Care need to be taken in evaluation of trap catch data, however, as numbers of insects in pheromone traps may not correlate well with actual numbers emerging from host trees (Bentz 2006). 41 Part II. Aggregation and anti-aggregation mechanisms The goal of a 'push-and-pull' strategy is essentially to push bark beetles away from susceptible resources using a repellent mechanism (i.e. anti-aggregant), and pull populations towards an alluring stimulus (i.e. baited lures or trapped logs) (Lindgren and Borden 1993, Miller et al. 1995, 2005, Miller and Borden 2000, Cook et al. 2007, Gillette and Munson 2009). Although the use of bark beetle pheromones or host volatiles are advocated, forest managers are recommended to consult specially-trained professionals in bark beetle management or rely heavily upon data from prior monitoring. Some pheromones may have multifunctional responses, individually or when mixed in different blends, and may unintentionally attract more bark beetles to surrounding live trees from migration events. This may potentially initiate incipient to epidemic conditions for bark beetles from events of 'spill-over', sudden stressful disturbances or untimely treatments due to human errors or budget restrictions. Part III. Induced competition and predatory response In addition to interrupting the regular communication signals of bark beetles with their conspecifics, the properties of the pheromones that attract bark beetles can be similarly manipulated to induce a kairomonal attraction by predators, parasitoids, and/or competitors. Amplified levels of interspecific and intraspecific competition between the sympatrics of secondary bark beetles with each other and/or D. ponderosae may result in drastic reduction of brood fecundity, brood production and per capita survival for both species (Rankin and Borden 1991, Poland and Borden 1994a, 1994b, Devlin and Borden 1994, Safranyik et al. 1996,1998,1999c). Multiple studies have demonstrated attraction of invertebrate 42 predators such as the clerid beetles or other generalist predators and parasitoids to pheromones of secondary bark beetles, sometimes synergistically with host volatiles (Reid 1957b, Miller et al. 1987,1991, Raffa 1991, 2001, Erbilgin and Raffa 2001, Aukema and Raffa 2002, Miller and Borden 2003, Erbilgin et al. 2003, Aukema et al. 2004, Boone et al. 2008). Though this study did not examine the interactions between bark beetles and their natural enemies, this aspect of controlling bark beetles by semiochemical manipulation may have great potential, especially in a holistic IPM (integrated pest management) approach in conjunction with the other control methods. Furthermore, if semiochemicals can induce higher competition and predatory responses, another option that holds potential to cause significant mortality of bark beetle populations at epidemic stages is application of epizootic fungal pathogens (Klepzig and Six 2004, Six and Klepzig 2004, Aanen et al. 2009, Six and Wingfield 2011); there is much to learn about these mutualistic or antagonistic interactions. Chemical control Broadcast insecticides are often ineffective and impractical in the control of bark beetles, which are naturally protected under the bark. Although there exist several topical insecticides such as lindane or monosodium methanearsonate, some which have only recently been banned in Canada and the United States, some registered ones, such as chlorpyrifos (more effective for defoliators) are expensive treatments that need to be applied regularly, sometimes twice in a season, to maintain effectiveness for the short-term (Berisford et al. 1980, Brady et al. 1980, Maclauchlan et al. 1988). Broadcast insecticides pose dangers of dermal and oral toxicity to the applicators, increased risk of groundwater 43 runoff and soil sediment contamination, and potential non-target effects to beneficial insects (Buckner 1974, CPPA1985, Morrissey et al. 2007, Morrissey and Elliott 2011). The use of pesticides can be termed a 'wicked problem' (Rittel and Webber 1973), where pesticides are a superficial treatment on the surface of a larger and more insidious issue of poor forest management (Burton 2006, Wallenius et al. 2011). Best control methods of bark beetles at different population densities Under non-epidemic conditions, recent mortality from disturbance events or stressed trees (fire-injured, girdled, drought, etc.) may be attractive to D. ponderosae and/or secondary bark beetles (Waring and Pitman 1983, Geiszler et al. 1984, Miller et al. 1986, Amman and Ryan 1991, Rasmussem et al. 1996, Santoro et al. 2001, Gandhi et al. 2007, Fettig et al. 2010). Such susceptible trees should be removed, if infested, before beetles emerge. Sanitation may be augmented by the use of trap trees and/or baited semiochemical traps to increase the effectiveness of such operations. For example in western Canada, several tried-and-true logging sanitation practices use "post-logging mopup" (Borden et al. 1983a) or trapping strategies using "containment and concentration" (Borden et al. 1983b) and can effectively reduce the residual populations over several years and slow the spread of the infestations of bark beetles, compared to a do-nothing strategy (Cole and Amman 1980, Borden and Lacey 1985). However, if populations manage to attain epidemic stages, treatment is rarely successful, as a suppression rate of 90% in the treated trees is required to compensate for the rate of increase at outbreak levels (Carroll et al. 2006b). 44 In post-epidemic phases, depending on the extensiveness of the outbreak and feasibility, future mortality could be minimized by using the strategies of "containment and concentration" with trap logs. The tactic of using logs as trapping materials for the insects referred to reduce the population levels of secondary bark beetles, and has limited feasibility in effectiveness for 'primary' bark beetles, such as D. ponderosae that primary attack live trees. Such logs would need to be promptly salvaged before the beetles emerge, hastening the collapse of the population to endemic levels. Follow-up treatments may be repeated every season until local populations return to endemic levels. Early detection of outbreak status may be achieved by aerial surveys and digital remote sensing techniques from aircraft- or satellite-borne sensors (Wulder et al. 2006). Aerial survey techniques can provide the valuable information on forest health conditions, locate the focal point(s) of potential infestations, and delineate the scale and direction of advance of outbreaks. Subsequent follow-up by systematic ground surveys is required to confirm the agent(s) of mortality to be bark beetles and, if so, to further ascertain and identify the extent of the epidemic and/or other potential weakening agents, and the associated risk to the surrounding live residuals susceptible to those populations (Carroll 2007). Early detection and continuous monitoring are important to maximize and buy time for forest managers to act promptly for the following reasons: (I) to forecast the potential outbreak and determine the magnitude of the problem, (II) to gather and assemble previous spatial and temporal information about past, or similar, successful management treatments on stands, and (III) to formulate integrated management strategies to contain the expanding populations, with an action plan that prioritizes and balances the ecological and economical 45 benefits in the application of containment treatments as well as the response (Vite 1976, McGregor and Cole 1985, Hall 2004). Prevention is the only long-term solution that provides more benefits than the active direct control methods of the short term (Shore et al. 2006, Whitehead et al. 2006). Management budgets are normally a limiting factor in effectively implementing preventative tactics. These factors are balanced against the fact, however, that bark beetles are normal, native, agents of disturbance and, as such, will always have some activity in a thriving forest. Public participation, education, awareness and regulation In all of the preceding management options, it is important to communicate with stakeholders and/or those individuals who are affected as a consequence of the management actions. This may involve providing public access to information, or providing more education on forest management in resource-based communities. This may take forms such as curricula for high school students, introducing forestry-related topics in the syllabus of science classes, including forest health with special reference to the population dynamics of insects, or bark beetles, since they are the most important mortality agent in the forests. In the age of information technology, having a dedicated website and/or online discussion forums by the province and/or federal forest service may serve as an outlet to inform the general public of action plans by the government, providing a participation forum for concerned individuals, and provide a forum of discussions engaging the parties responsible for timber supply management within respective communities. Consultative processes can increase the levels of satisfaction and provide a platform of communication for all the parties, to articulate their 46 concerns, exchange ideas, and update each other with pertinent information for a diplomatic compromise between all parties where conflicting management objectives may exist. Importance and consequences of bark beetle outbreaks Although the previous sections focus on outbreak management, this is not to suggest that all outbreaks of bark beetles are bad. Indeed, D. ponderosae is a natural disturbance agent, performing the same ecological function as an abiotic disturbance agent, such as a stand-replacing fire (Lotan et al. 1985, Taylor et al. 2006, Alfaro et al. 2008). The role and importance of bark beetles needs to be recognized as part of a valuable forest community: economic progress must be balanced with ecological function and the social and aesthetic values for individuals and communities alike. Bark beetles can encourage a higher level of productivity with higher growth yields by increasing resource availability, such as space and growth for plant succession or enhancing the service of nutrients recycling (Rudinsky 1962, Wood 1982b, Romme et al. 1986, Brown et al. 2010). 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White spotted sawyer. Forest Pest Leaflet 74(revised), U.S. Department of Agriculture Forest Service, Washington, D.C. Wood, C. S., and L. S. Unger. 1996. Mountain pine beetle: a history of outbreaks in pine forests in British Columbia, 1910 to 1995. Canadian Forest Service, Pacific Forestry Centre, Victoria, BC. Wood, D. L. 1982a. The role of pheromones, kairomones, and allomones in the host selection and colonization behavior of bark beetles. Annual Review of Entomology 27:411-446. Wood, S. L. 1957. Ambrosia beetles of the tribe Xyloterini (Coleoptera: Scolytidae) in North America. The Canadian Entomologist 89:337-354. Wood, S. L. 1982b. The bark and ambrosia beetles of North and Central America (Coleoptera: Scolytidae), a taxonomic monograph. Great Basin Naturalist Memoirs 6, Brigham Young University, Provo, UT. Wulder, M. A., C. C. Dymond, J. C. White, and B. Erickson. 2006. Chapter 5. Detection, mapping, and monitoring of the mountain pine beetle. Pages 123-154 in L. Safranyik and W. R. Wilson, editors. The mountain pine beetle: A synthesis of biology, management, and impacts on lodgepole pine. Canadian Forest Service, Pacific Forestry Centre, Victoria, BC. 72 Appendices Appendix A. Niche partitioning by chemical profiles by various bark beetles: Dendroctonus ponderosae, Ips pini, Hylurgops spp., Orthotomicus latidens, Pseudips mexicanus, Dendroctonus murrayanae, Pityogenes spp., Pityophthorus spp., and ambrosia beetles, in lodgepole pine in British Columbia Appendix B. Photographic guide to green-, red-, and grey-attack stages of lodgepole pine in sites in the central interior of British Columbia Appendix C. Map of the seven study site locations (Appendix CI), in relation to the three forest district regions in British Columbia (five in Mackenzie Forest District, one in Peace River Forest District, one in Prince George Forest District), and relative to the distribution of lodgepole pine (green) and Dendroctonus ponderosae outbreak (red) from 1999 to 2009 in the provinces of British Columbia and part of Alberta, with snapshot of the outbreak in the year 1999, 2004, and 2008 (Appendix C2) Appendix D. Photographs of each of the seven sites in this study of the central interior of British Columbia were exemplified for each site, [Appendix Dl] Mackenzie Site # 1(Macl) [Appendix D2] Mackenzie Site # 2 (Mac2) [Appendix D3] Mackenzie Site # 3 (Mac3) [Appendix D4] Mackenzie Site # 4 (Mac4) [Appendix D5] Mackenzie Site # 5 (Mac5) [Appendix D6] Crassier Creek (CCk) [Appendix D7] Chief Lake (CLk) 73 Appendix E. Survey methodology to examine and monitor the mortality of lodgepole pine, with the figures illustrating: [Appendix El] A flow chart detailing site establishment, and tree examination for presence of bark beetles or their galleries in the first year of survey in 2009 and for new mortality in 2010 [Appendix E2] Signs of bark beetles activity included the presence of pitch tubes and frass Appendix F. Photographic guide and descriptions of the various insects (i.e. adult bark beetles and their galleries) and other agents of lodgepole pine mortality in sites in central interior of British Columbia [Appendix Fl] Dendroctonus ponderosae (Hopkins), mountain pine beetle, with examples of their prevalence and desperation, including on the surrounding residuals, which were non-suitable host (smaller diameter lodgepole pines of 8 cm or less), resulting in the bark cracking (Appendix F1.2) [Appendix F2] Ips pini (Say), pine engraver [Appendix F3] Hylurgops spp. (LeConte), sour sap bark beetles [Appendix F4] Orthotomicus latidens (LeConte), smaller western pine engraver [Appendix F5] Pseudips mexicanus (Hopkins), Monterey pine engraver [Appendix F6] Dendroctonus murrayanae (Hopkins), lodgepole pine beetle [Appendix F7] Pityogenes spp. and/or Pityophthorus spp. [Appendix F8] Ambrosia beetles (with 'pin-holes') [Appendix F9] Overlapping galleries of Hylurgops spp. - D. murrayanae [Appendix F10] Root collar damage by insects [Appendix Fll] Wood borers [Appendix F12] Western gall rust [Appendix F13] Interactions of Dendroctonus ponderosae - Ips pini [Appendix F14] Interactions of Dendroctonus ponderosae - O. latidens 74 [Appendix F15] Interactions of Dendroctonus ponderosae - Ips pini - 0. latidens [Appendix F16] Interactions of Ips pini - Hylurgops spp. and/or D. murrayanae - Orthotomicus latidens - Pseudips mexicanus [Appendix F17] Interactions of Pseudips mexicanus - Orthotomicus latidens [Appendix F18] Interactions of Ips pini - Hylurgops spp. and/or D. murrayanae and/or Hylastes spp. - ambrosia 'pin-holes' [Appendix F19] Miscellaneous observation: some of the difficulties in diagnosing the 'true' mortality source, due to other (old) damages, such as rotting heartwood, decaying fungus, woods hollowed out by carpenter ants or termites, and wood-peckering damage holes [Appendix F20] Miscellaneous observation of Orthotomicus latidens tunneling randomly and intermixing with/into Dendroctonus ponderosae gallery in the older stands (perhaps due to their overwintering behaviors or maturation feeding of tenerals/adults from the previous season, since no egg galleries were present?) Appendix G. Detailed descriptions of each agent of lodgepole pine mortality (supplements to the photographic guide of Appendix F) of the adult bark beetles associated under the bark (Appendix Gl) and their characteristic galleries (Appendix G2) in sites in central interior of British Columbia Appendix H. The relationships between the physical attributes of tree sizes with various signs of bark beetle activity, other biotic disturbances, and their interactions in sites in central interior of British Columbia Appendix I. 'The perfect mortality-storm' of lodgepole pine, a combined effect of stand density and stand maturity interacting with high secondary bark beetles activity in the case study of Mackenzie site 3, plot C (Mac3-C) 75 Appendix J. Twenty one lodgepole pine with frass were found near Mackenzie and Crassier Creek at the post-outbreak stage of Dendroctonus ponderosae. The frasses were indicators of newly attacked trees in 2010, while, exhibiting the multiple interactions of the trees in the stands with the bark beetles, broken tops, and the other agents of tree mortality. [Appendix Jl] Summary of the cross-interactions between the bark beetles, as potential mortality agents, and the differences in the distribution of diameter-at-breast-height (in cm) in trees with their presence versus their absence [Appendix J2] Summary of the cross-interactions between the bark beetles, as potential mortality agents, and the differences in the distribution of height {in m) in trees with their presence versus their absence [Appendix J3] Summary of the cross-interactions between bark beetles with non-bark beetles elements, and their abundance among the dead or alive trees in the stand, and the differences in the distribution of diameter-at-breast-height (in cm) in trees with their presence versus their absence [Appendix J4] Summary of the cross-interactions between bark beetles with non-bark beetles elements, and their abundance among the dead or alive trees in the stand, and the differences in the distribution of height (in m) in trees with their presence versus their absence Appendix K. The relationships between the physical attributes of tree sizes with various new signs of bark beetle activity in trees (frass trees of 2010) in sites in central interior of British Columbia Appendix L. Justification for grouping Hylurgops spp. and Dendroctonus murrayanae in the same category 76 Appendix A. Niche partitioning by chemical profiles by various bark beetles Dendroctonus ponderosae is attracted to trans-verbenol and cis-verbenol by females, (+)-exo-brevicomin produced by males and the host monoterpenes of myrcene as a synergist attractant, and to alpha-pinene and beta-phellandrene emitted as tree volatiles indicating susceptibility or as potential hosts (Vite and Pitman 1968, Pitman and Vite 1969, Renwick and Vite 1970, Hughes 1973a, 1973b, 1974, Billings et al. 1976, Borden et al. 1983c, Lindgren and Borden 1989, Miller and Lafontaine 1991, Miller and Borden 2003). In British Columbia, I. pini is attracted to the racemic blend of (+)-ipsdienol, produced by males and had a higher response by females, and to lanierone as a synergistic compound. Ips pini is also attracted to the host monoterpene of beta-phellandrene, but their pheromone ipsdienol is repellent to D. ponderosae, O. latidens, and P. mexicanus (Angst and Lanier 1979, Lanier et al. 1980, Miller et al. 1989,1996,1997, 2005, Miller and Borden 1990a, Safranyik et al. 1996, Savoie et al. 1998) (Figure 10). The opposite is true for O. latidens attraction to the pheromone ipsenol or D. ponderosae pheromones of trans-verbenol and exo-brevicomin, which are attractive to the producing species, but repellent to I. pini (Angst and Lanier 1979, Hunt and Borden 1988, Miller and Borden 1990b, 2000, Miller et al. 1991, Borden et al. 1992, Miller 2000, Pureswaran et al. 2000) (Figure 10). Verbenone is an anti-aggregation pheromone by D. ponderosae that is repellent to its own kind, I. pini and O. latidens demonstrated the effectiveness of these pheromones to minimize competition by indicating the full occupancy within that individual-host (Renwick and Vite 1970, Ryker and Yandell 1983, Lindgren and 77 Borden 1989, Amman et al. 1991, Shore et al. 1992, Miller et al. 1995, Lindgren and Miller 2002). Cross-attractions within the secondary bark beetle circles are common, for example, Pityogenes knechteli, a sympatric of I. pini, uses similar pheromones of ipsdienol as attractants, but the differences are most likely in the enantiomeric ratios of ipsdienol or the presence of some synergist from host volatiles or either species, and both were equally repelled by the pheromone ipsenol (Miller and Borden 1992,2003, Devlin and Borden 1994, Savoie et al. 1998); similarly, P. mexicanus is attracted to the synonomes pheromone of O. latidens, attracted by ipsenol and repelled by ipsdienol (Savoie et al. 1998). Thus, the biosynthesis of the oxidized monoterpenes of ipsdienol, ipsenol, and verbenone can act as an effective synomones for those five species, including D. ponderosae, to coexist within the vicinity of each other to maximize the use of the same host-individual trees, by avoiding the competition within and among species from the potential overlapping niches otherwise without using chemical signals (Miller and Borden 1992, Poland and Borden 1994a, 1994b, Devlin and Borden 1994, Savoie et al. 1998, Miller 2000, Safranyik et al. 2000) (Figure 10); these beetles have been observed to occur together, including in this study, normally in several assortments of two or three species predominating, but it is less common for all of them to coexist together because when they do, the high levels of competitions (exploitation, exclusion, interference) severely restricts any potential growth for all species involved. Limited is known about the semiochemical attractions and anti-aggregations mechanisms of Hylurgops spp. and/or D. murrayanae, but other studies had shown 78 association of these beetles at endemic levels with D. ponderosae and other secondary bark beetles, following tree mortality events by an outbreaking population or stand thinning; showing some cross attractions between these species with the other secondary bark beetles pheromones, in addition to the potential synergistic effects from host volatiles (Reid 1955, Safranyik et al. 1999a, 1999b, 2000, 2004, Furniss and Kegley 2008); consistent with the studies by Miller et al. (1991) and Miller and Borden (2003) that found ipsenol and ipsdienol to be attractive to Hylurgops porosus. Beta-phellandrene in lodgepole pine is most attractive to D. ponderosae and some of the secondary bark beetles because it is the most abundant monoterpene in the pine (Shrimpton 1972, Miller and Borden 1990a, 1990b, 2003), therefore, potentially used for host species recognition to locate suitable host. In addition, Wallin and Raffa (2000) found that I. pini exhibited differences in post-landing behavioral responses - in host-entry, orientation within host and gallery construction - to the different concentrations of host monoterpenes, perhaps using absolute concentrations of various monoterpenes as predictors of host defensive capacity than solely on one particular monoterpene or its concentration in their decision to either colonize the host found, or perhaps, to locate another more suitable ones. Ethanol, probably released by microorganisms in decaying woody tissue (Moeck 1970, Montgomery and Wargo 1983) and other stress-chemicals produced by stressed plants (Kimmerer and Kozlowski 1982), is also a known attractant to a wide variety of species of secondary bark beetles (Visser 1986, Byers 1995, Hobson 1995). A summary of the various other host monoterpenes or pheromones that are attractive and repellant to the bark 79 beetles or towards their enemies, using those compounds as kairomones (Borden 1982, Wood 1982a, Byers 1995) are provided in the following table (below). 80 Appendix A. Niche partitioning by chemical profiles in lodgepole pine by various bark beetles: Dendroctonus ponderosae, Ips pini, Hylurgops spp., Orthotomicus latidens, Pseudips mexicanus, Dendroctonus murrayanae, Pityogenes spp., Pityophthorus spp., and ambrosia beetles Characteristics (CHEMICAL profile partition) Bark beetles Aggregation, or attractant (by host volatile/as kairomone) Anti-aggregation, or repellent (by another species) Dendroctonus ponderosae (Hopkins) trans-verbenol (female) +exo-brevicomin (male) myrcene (host volatile) alpha-pinene (host volatile) beta-phellandrene (host volatile) verbenone (0. ponderosae) ipsdienol {Ips pini) Ips pini (Say) racemic ipsdienol (male) in BC, but enantiomer ratios vary by region to 'escape' predation lanierone (male) as synergist beta-phellandrene (host volatile) 3-carene (host volatile)( some response) trans-verbenol (0. ponderosae) (±)-exo-brevicomin (0. pond.) verbenone (0. ponderosae) ipsenol (O. latidens) myrcene (host volatile) conopthorin (green leaf volatile) Hylurgops spp. (LeConte) i.e. primarily H. porosus ipsdienol (kairomone) 3-carene (host volatile)(some response) beta-phellandrene (host volatile)(some response) terpinolene (host volatile)(some response) unknown, probably conopthorin (green leaf volatile) Orthotomicus latidens (LeConte) ipsenol (male) beta-phellandrene (host volatile) ipsdienol (Ips pini) verbenone (0. ponderosae) Pseudips mexicanus (Hopkins) ipsenol (male), most likely with differences in enantiomeric ratios than 0. latidens 3-carene (host volatile)(some response) beta-phellandrene (host volatile)(some response) ipsdienol (Ips pini) - continue next page - 81 Other mechanisms of communications beta-pinene (host volatile): elicit host entry, but inhibit gallery construction alpha-pinene (host volatile): elicit within-host orientation, gallery construction, but inhibit host entry continuation - Characteristics (CHEMICAL profile partition) Bark beetles Aggregation, or attractant (by host volatile/as kairomone) Anti-aggregation, or repellent (by another species) Pityogenes spp. (Bedel), i.e. primarily P. knechteli (Swaine) found in lodgepole pine ipsdienol (male), most likely with differences in enantiomeric ratios than I. pini hexanol (male)(at low concentration) beta-pinene (host volatile)(some response) 3-carene (inhibit attractant) alpha-pinene (inhibit attractant) hexanol (male) (at high concentration) 4,6,6-lineatin (female) unknown, probably conopthorin (green leaf volatile) Other mechanisms of communications Ambrosia beetles, i.e. primarily Trypodendron lineatum, and Gnathotrichus sulcatus Gnathotrichus retusus sulcatol (male) sulcatol (male) Non-bark beetles I. Wood borers, Monochamus spp. (Coleoptera: Cerambycidae) (kairomonal responder) Ethanol and/or host volatiles and/or turpentines (in general, but response to individual monoterpene is dependent on species, i.e. beta-phellandrene/alpha-pinene/ beta-pinene/3-carene) Bark beetle pheromones (primarily from Ips DeGeer spp., i.e. ipsdienol/ipsenol) Synergism between bark beetle pheromones and monoterpenes had mixed results than the individual attractant (higher synergistic response in eastern Ontario, but not synergistic in west coast British Columbia, requiring further study) Smoke volatiles (post-fire, as indicator of damage or weaken host) 82 conopthorin (green leaf volatile) similar to the wood borers responses, bark beetle pheromones or/with host volatiles increases the attractions of predators (e.g. clerid beetles) woodpeckers and parasitoids use acoustic vibration to detect the beetle, versus chemical cues, while, mites and nematodes, or epizootics microorganisms and fungi require the beetles for phoretic transport and/or as host, non- to less-dependent on manipulation using the chemical signals Appendix B. Photographic guide to green-, red-, and grey-attack stages of lodgepole pine in sites in the central interior of British Columbia. Stands were selected based on colour of crown as a proxy for time since attack by Dendroctonus ponderosae. New mortality of trees originated from outbreaks of bark beetles, either from an ongoing epidemic of Dendroctonus ponderosae or additional activity by secondary bark beetles, or their interactions thereof, potentially with other disturbance agents Gradient of lodgepole pine attack in stand in Mackenzie <== "green-attack" to "chlorotic-yellow" to "bright-red" to "maroon-red" to "gray-attack" ==> 83 Appendix CI. Map of the seven study site locations, in relation to the three forest district regions in British Columbia (five in Mackenzie Forest District, one in Peace River Forest District, one in Prince George Forest District) • Research sites * Prince George Scale-1:10000.000 0 50100 200 300 400 500 Kilometers 84 Appendix C2. Map of the seven study site locations, relative to the distribution of lodgepole pine (green) and Dendroctonus ponderosae outbreak (red) from 1999 to 2009 in the provinces of British Columbia and part of Alberta, with snapshot of the outbreak in the year 1999, 2004, and 2008 Appendix Dl. Photographs of Mackenzie site 1(Macl) in Mackenzie Forest District 86 Appendix D2. Photographs of Mackenzie site 2 (Mac2) in Mackenzie Forest District 87 Appendix D3. Photographs of Mackenzie site 3 (Mac3) in Mackenzie Forest District "V 88 89 Appendix D5. Photographs of Mackenzie site 5 (Mac5) in Mackenzie Forest District I 90 Appendix D6. Photographs of Crassier Creek (CCk) in Peace River Forest District 91 Appendix D7. Photographs of Chief Lake (CLk) in Prince George Forest District Appendix El. Flow chart of survey methodology to diagnose and monitor of insects associations with old and new lodgepole pine mortality Selected and surveyed seven stands, based on the presence of Dendroctonus ponderosae at the post-epidemic stage \7 Recorded: I) Species, height, diameter-at-breast-height [1.3m] II) Tree condition [dead or alive] III) Root collar damage by insects [presence/absence] ilil IF dead V/ i "t August 2009 IF dead Recorded putative agent(s) of mortality [galleries diagnosis of primary bark beetle IF alive \ V i| t Resurvey of trees in 2010 /y (before peak flight of t// Dendroctonus ponderosae) IF alive and/or \7 secondary bark beetles by peeling the bark] Second survey in 2010 (after main flight of \/ IF dead Dendroctonus ponderosae) 93 Appendix E2. Pictures of frass and pitch tubes (refer to Appendixes E and F for more detailed examination of insects by species and/or by their distinctive galleries) tree with frass and attack-holes 94 Appendix Fl.l. Photographs of galleries of Dendroctonus ponderosae (Hopkins) (refer to Appendix G2 for further details of gallery) 95 Appendix F1.2. Miscellaneous observations of Dendroctonus ponderosae galleries in non-suitable hosts (< 8 cm lodgpole pines) Appendix F2. Photographs of galleries of Ips pirii (Say) (refer to Appendix G2 for further details of gallery) Appendix F3. Photographs of galleries of Hylurgops spp. (LeConte) (refer to Appendix G2 for further details of gallery) Appendix F4. Photographs of galleries of Orthotomicus latidens (LeConte) (refer to Appendix G2 for further details of gallery) 99 Appendix F5. Photographs of galleries of Pseudips mexicanus (Hopkins) (refer to Appendix G2 for further details of gallery) 100 Appendix F6. Photographs of galleries of Dendroctonus murrayanae (Hopkins) (refer to Appendix G2 for further details of gallery) 101 Appendix F7. Photographs of galleries of Pityogenes spp. and/or Pityophthorus spp. (refer to Appendix G2 for further details of gallery) 102 Appendix F8. Photographs of galleries of ambrosia beetles (refer to Appendix 62 for further details of gallery) Black/ blue fungal 'stain' discolouring the entrance 103 Photographs of galleries of Hylurgops spp. and/or Dendroctonus murrayanae (refer to Appendix G2 for further details of gallery) % 104 Appendix FIO. Photographs of root collar damage by insects (refer to Appendix 62 for further details and descriptions) Appendix Fll. Photographs of wood borers (refer to Appendix 62 for further details and descriptions) adults foraging/ovipositing wooden-shaving galleries, (larvae) emergent adults 'under the bark' 106 Appendix F12. Photographs of western gall rust (refer to Appendix G2 for further details and descriptions) 107 Appendix F13. Photographs of interactions between the galleries of Dendroctonus ponderosae and Ips pini Appendix F14. Photographs of interactions between the galleries of Dendroctonus ponderosae and Orthotomicus latidens 109 Appendix F15. Photographs of interactions between the galleries of Dendroctonus ponderosae, Ips pint and Orthotomicus latidens 110 Appendix F16. Photographs of interactions between the galleries of secondary bark beetles: Ips pini, Hylurgops spp. and/or Dendroctonus murrayanae, Orthotomicus latidens, and Pseudips mexicanus Appendix F17. Photographs of interactions between the galleries of Orthotomicus latidens and Pseudips mexicanus 112 Appendix F18. Photographs of interactions between the galleries of secondary bark beetles: Ips pini, Hylurgops spp. and/or Dendroctonus murrayanae and/or Hylastes spp., and ambrosia beetles ('pin-holes' characteristics) 113 Appendix F19. Miscellaneous observations in the diagnosis, and/or the difficulties to ascertain the 'true' agent of tree mortality carpenter ants rot and decay fungus Woodpeckering holes rot and decay fungus 114 Appendix F20. Miscellaneous observations of the interactions between the galleries of Dendroctonus ponderosae and Orthotomicus latidens that tunneled randomly, intermixing with/into Dendroctonus ponderosae gallery (potentially due to their overwintering behavior or maturation feedings of the teneral/adults from the previous summer?) 115 Appendix G. References of the agent of lodgepole pine mortality Appendix Gl: identification of adult bark beetles associated under the bark The bark beetles associated with the trees were identified either from visual inspection of the adult(s), if present, or from their associated reproductive galleries. This appendix details the characteristics of the adult insects. Adults of Dendroctonus ponderosae are dark brown to black and range from 3.7-7.5 mm long, with females normally larger than males (Unger 1993). Adults of Ips pini range from dark reddish brown to nearly black, with sizes from 3.5-4.2 mm long (Hopping 1964). Adults of Hylurgops spp. are reddish brown to black in color, depending on species, and ranges between 3.1-5.7 mm, with a more slender appearance than D. ponderosae (Furniss and Carolin 1977, Wood 1982b). Adults of Orthotomicus latidens are dark reddish brown and ranges from 2.3-3.6 mm long (Wood 1982b), distinguishable from I. pini and P. mexicanus due to its smaller size. Adults of Pseudips mexicanus are dark reddish brown and approximately 3.6-5.0 mm long (Struble 1970, Wood 1982b). Adults of Dendroctonus murrayanae have dark brown to black body with reddish brown elytra, and ranging from 5.0 to 7.3 mm in size (Keen 1952, Wood 1982b). Adults of Pityogenes spp. are dark reddish brown to nearly black, and range from 1.8-3.7 mm long, while adults of Pityophthorus spp. are yellowish brown to almost black, ranging from 0.8-3.2 mm in size (Reid 1955, Bright and Stark 1973, Bright 1976,1981). Ambrosia beetles are dark reddish brown to black and depending on the species, ranges from 2.0-3.7 mm in measurement (Borden 1988, Daterman and Overhulser 2002). Among the two most common ambrosia beetles, Trypodendron lineatum is 2.7-3.5 mm long, with the adults ranging from brown to black, distinguished by their bicolored elytra, usually with 116 five dark stripes alternating with four lighter stripes (Wood 1957,1982b). In contrast, Gnathotrichus spp. are dark reddish brown to almost black in color, and on average about 3.7 mm in length (Daterman and Overhulser 2002), with a longer, slender appearance, compared to the stouter Trypodenderon lineatum. Most pine engravers can be identified to species and sex based on their antennal club or secondary sexual characters and by the number and shape of their declivital spines at the end of the beetles' elytra (Hopping 1963a, Lanier and Cameron 1969). Ips pini has four spines, while O. latidens and P. mexicanus with only three spines. All three species can be distinguished via the antenna club, mean size, and differences in their declivital characteristics (/. pini: Fig. 7,8,26,27 in Hopping 1963a, O. latidens: Fig. 3,4,20 in Hopping 1963c, P. mexicanus: Fig. 1,2,21 in Hopping 1963a, Lanier and Cameron 1969). The distinguishing characteristics for I. pini entail the four spines, with the third spine in males being the largest, elongated or sub-capitated, whereas females possess a short, conical third spine, identical to the second spine (Fig. 7,8,9 in Hopping 1964, Fig. 45 in Bright 1976). In I. pini, the sutures of the antennal club are bi-sinuate (Fig. 92 in Bright 1976, Fig.2 in Angst and Lanier 1979). For O. latidens, the males' third declivital spines are larger and longer, shaped like a 'long cylinder7, compared to females with a smaller third declivital spine, which is shaped more like a 'tapered triangle' (Fig. 42 in Bright 1976, Miller and Borden 1985), and the suture of antenna club is broadly sinuate to nearly straight (Fig. 89 in Bright 1976). In P. mexicanus, the sutures of the antenna club are strongly arcuate. On the frons, males have a prominent median tubercle on the epistomal margin, whereas the females exhibit a bare spot in that area with a small carina or a shallow fovea. Most males have a longer third 117 spine, which extend in parallel, than the females, with the spine turning obliquely inwards (Fig. 7,8 in Lanier and Cameron 1969, Hopping 1963b). Hylurgops spp. have an anteriorly constricted pronotum, or more slender appearance than the Dendroctonus genus, and is more likely found at the base or the roots of the tree(Bright 1976, Wood 1982b). Dendroctonus murrayanae can be distinguished from Hylurgops spp. or D. ponderosae from the stout appearance characteristic of the genus Dendroctonus or based on the presence of a median longitunidal, subcarinate line located above the epistomal process (Fig. 2 in Furniss and Kegley 2008). Synonymous with the common name of twig beetles, Pityogenes spp. and Pityophthorus spp. are among the smallest of bark beetles. Males of Pityogenes spp. have two or three large teeth-like spines on their elytral declivity, and females have a deeply excavated frons. Pityophthorus spp. are so numerous that to identify them can be challenging. One difference between Pityogenes spp. and Pityophthorus spp. are their antennal clubs, compressed with two sutures in Pityogenes spp., but chitinized septa in Pityophthorus spp. (Bright and Stark 1973, Bright 1976,1981). Appendix G2. identification of bark beetle galleries under the bark The common method of identifying the beetles associated with trees is based on the characteristics of beetle galleries, after most of the parent bark beetles or their broods have re-emerged and dispersed to seek, feed, and reproduce in other hosts. The common gallery features, including the length and shape of the gallery of D. ponderosae and the secondary bark beetles are included as a reference guide to identify the beetles associated with the mortality of the tree surveyed (BCMoF 1994) (Appendix F). 118 Dendroctonus ponderosae is a monogamous species, and females normally initiate the construction of a long, nearly straight, vertical egg gallery in the soft inner cambium beneath the bark. The gallery has a characteristic hook, or J-shaped, where the beetle entered, with the gallery initially heading downward, then ascending diagonally for about 3-5 cm, before turning upward, slightly grooving, following the grain of the wood (Wood 1982b, Gibson et al. 2009) (Appendix Fl). Galleries are approximately 30 cm long under optimal conditions, however, length may approach 1.5 m (Reid 1962b, Safranyik and Carroll 2006). Ips pini is a polygamous species, with one male creating a nuptial chamber to mate with up to seven females, which individually create galleries of 13-25 cm long (Furniss and Carolin 1977) (Appendix F2). Orthotomicus latidens is monogamous, with the female constructing up to four egg gallery arms of 2-3 cm long for each of the arm, which extends from the male-initiated nuptial chamber (Reid 1999) (Appendix F4). Pseudips mexicanus is polygamous, with the males mating up to three females. Females construct galleries of approximately 5 cm long on each of the arms (Smith et al. 2009) (Appendix F5). The harem size for each can be inferred from the number of egg galleries by the females, which radiates from the nuptial chamber initiated by males, except for O. latidens since this species is always monogamous. Ips pini and O. latidens galleries radiate from the nuptial chamber to produce an X or Y or star shaped galleries (Fig. 5,6 in Kegley et al. 1997 vs. Fig. 23 in Bright and Stark 1973), while P. mexicanus create an almost circular curving of a C or S shaped galleries radiating away from the nuptial chambers (Fig. 5 in Hopping 1963b, Fig. 1in Smith et al. 2009). The galleries of I. pini and O. latidens can be differentiated based on their sizes, 119 spacing of the egg niches, and lengths of the galleries (Appendix F2 vs. Appendix F4). Females of O. latidens lay their eggs singly on both sides of tunnel of the egg gallery at an average rate of 0.95 egg niches/mm, almost double the rate of I. pini at 0.54 egg niches/mm (Miller and Borden 1985). In term of size, the adults of O. latidens are smaller (2.3-3.6 mm) than I. pini (3.5—4.2 mm), and produce shorter galleries (each arm approximately 3 cm long, vs. each arm approximately 13-25 cm in length). These differences of size, higher density of egg niches, and gallery characteristics help distinguish each species based on their ovipositional behaviour and their gallery systems. The sour sap bark beetles of the genera Hylurgops and Hylastes are known to vector the ophiostomatoid fungus, Leptographium wageneri (W.B.Kendr.) M.J. Wingf., which causes the black-stain root disease, exhibiting symptoms of a dark stain on the tracheids of the phloem (Schweigkofler et al. 2005). This black stain signature is used to distinguish the Hylurgops spp. from D. murrayanae since larvae of both species often overlap when they occur together in the root crowns region of the tree (Bright 1976, Wood 1982b) (Appendix F3, Appendix F6, Appendix F9). Though Hylastes macer (LeConte) is more commonly associated with the Leptographium fungus, with 63-75% association vs. Hylurgops porosus (LeConte) at only 30% (Schweigkofler et al. 2005), Hylurgops porosus is probably the more important vector (Safranyik et al. 1999a, 2000, 2004). Thus, galleries with dark stains were assumed to predominantly have originated from Hylurgops spp. (Appendix F3). Dendroctonus murrayanae, monogamous like other Dendroctonus spp., attack individual trees at low densities, not in groups, constructing galleries of 13-23 cm in length. 120 Dendroctonus murrayanae laid their eggs in a strung-out mass on the more downward or inward-curved side of the gallery in a shallow excavation. The larvae exhibit aggregated feeding while leaving trails of red frass (BCMoF 1994, Furniss and Kegley 2008) (Appendix F6). Pityogenes spp. and/or Pityophthorus spp. frequently occur on smaller trees, or smaller branches/larger twigs/thinner barks of larger trees. They produce star-shaped galleries, with multiple branches of tunnelling from five to ten females from the nuptial chamber, similar but considerably smaller tunnels than those of I. pini or O. latidens (Bright and Stark 1973, Bright 1976,1981) (Appendix F7). Ambrosia beetles are sapwood borers. Their galleries are easily distinguishable from the other bark beetles galleries, based on their characteristic 'pin-hole' tunnels with black stain fungi discolouring the entrance of their tunnel on the phloem (Daterman and Overhulser 2002) (Appendix F8). Ambrosia beetles produce an extensive network of three-dimensional galleries, extending primarily into the woody tissue. The chambers or cradles for larvae development branch several times, above and below the main tunnel. Ambrosia beetles often occur on the larger trees of at least 10 cm in diameter (Wood 1957, 1982b). Although wood borers are not bark beetles, they are found quite extensively in dead trees, together with other phloeophagous insects (Wilson 1975). Wood borers also tunnel into the hardwood, but can be distinguished from ambrosia beetles by their larger larval sizes, the wider galleries going in random directions leaving a trail of roughen wooden shavings, or D-shaped or larger O-shaped tunnels, boring into the sapwood (Appendix Fll). 121 Aside from damage by insects, including in the roots (Appendix F10), the presences of other deformities and/or pathogens on lodgepole pine were also examined. The most abundant of them all, in the younger stands, was the fungi Peridermium harknessii Moore, which causes western gall rust on the pines (Peterson 1960). Western gall rusts exhibit symptoms such as trunk cankers and branch galls on lodgepole pine (Appendix Fll). The formations of those woody galls were the product of fungal infection, resulting in the cambial cells to divide rapidly. This pathogen is an obligate parasite that requires live host to successfully propagate, which is a potential mortality agent of lodgepole pine by itself if the trees were heavily infested, or increases the susceptibility of mortality by subsequent colonizations from bark beetles. 122 Appendix H: Size relationships of trees with various signs of bark beetle activity The dominant density distribution of Dendroctonus ponderosae can be split based on the stand's maturity levels; beetles in the 'young' stands were predominantly in trees of at least 10 cm versus the older stands in trees of at least 15 cm. When the trees were associated with the complex of secondary bark beetles or D. ponderosae and with other bark beetles, the hosts were more likely to be larger and taller, in comparison to the trees with individual secondaries only, in the absence of D. ponderosae. For example, 81% (161/200) of the secondary bark beetles associated with D. ponderosae presence were in the larger trees (d: 14.0 cm, Ti: 15.1 m), compared to the remainder 19% of the trees with secondaries, but without D. ponderosae (39/200) (d: 9.1 cm, fi: 10.4 m). When the density distribution of secondary bark beetles were examined in comparison to those of D. ponderosae, those bark beetles were closely associated to one other, with their highest distribution to resemble those at the mean diameters of D. ponderosae. These could vary depending on the stand dynamics. In 'young' stands, the density distribution of secondaries associated with D. ponderosae were generally lower to indicate that not all the D. ponderosae mortalities were occupied by secondary bark beetles. In the 'old' stands, the density distributions of the secondary bark beetles were close to or lower than those of D. ponderosae, since not many young susceptible trees were left in the more mature stands, with the majority of those larger diameter trees normally had been colonized by D. ponderosae. 123 Individual secondary bark beetles Although individual species of secondary bark beetles were associated with the dead trees at a lower rate (around 25% or less), I. pini were found almost exclusively in the intermediate diameter tree class of younger stands around 10 cm (distribution: 5.7-17.1 cm) and very low in the 'old' stands. When the density distribution of I. pini was plotted, the beetles were found in smaller diameter trees than those of D. ponderosae and/or most secondary bark beetles; I. pini had a density distribution that closely resembles those of the complex of secondary bark beetles. Hylurgops spp. and/or D. murrayanae were the most abundant secondary bark beetles associated with the dead trees (171/373), with a mean of 13.3 cm. These insects were found in trees around 10 cm in the 'young' stands or 15 cm or more in the 'old' stands, similar to D. ponderosae. Galleries of 0. latidens were found in dead trees with a mean of 12.6 cm. Such trees occurred slightly more in Mackenzie (29/48) than the 'older7 stands of Crassier Creek and Chief Lake combined (17/48), but had the highest presence of individual secondary bark beetles presence in the 'old' stands than most of the other bark beetles or when compared to the individual younger stands (Table 8). Their distribution were more spread out from the mean, towards the relatively smaller diameter trees when associated with D. ponderosae or I. pini in the 'old' and 'young' stands respectively. When O. latidens.was found with I. pini, O. latidens were found in smaller trees than the majority of I. pini. Trees with P. mexicanus was among the lowest frequency of secondary bark beetles in the stands associated with the dead trees (27/373). These trees had a mean diameter of 124 12.5 cm. When evidence of P. mexicanus was present, the insects were most commonly associated with D. ponderosae (presence: absence ratio of 5.8), and occasionally with 0. latidens (ratio of 0.4). Since there are very few observations of P. mexicanus, the graphs of their density distribution is often not evenly distributed (non-bell shaped curve) when plotted in each individual site. Pityogenes spp. and/or Pityophthorus spp., or the twig beetles were the least frequently recorded (25/373). They occurred in the smaller diameters and twigs (mean: 8.6 cm), mostly beyond the main bole area surveyed. While the lower diameter distribution of associated trees overlapped with D. ponderosae, the diameter distribution most closely matched the distribution of /. pini as they would peak in the smaller diameter than I. pini. Ambrosia beetles were distributed in the largest diameter trees on average (d: 15.0 cm, h: 16.0 m), compared to any other bark beetles including D. ponderosae. 125 Other biotic disturbances: root collar damage by Insects, wood borers and western gall rust The four most abundant disturbance agents associated with the dead trees (n: 373), except for root collar damage and western gall rusts that included live trees (n: 251) as well, are Hylurgops spp. and/or D. murrayanae at 46% (171/373), root collar damage at 38% (238/624), and western gall rust at 35% (221/624), and the wood borers at 30% (113/373). Root collar damage occurrences and their density distributions were similar to those of secondary bark beetles. Both groups followed closely the density distribution of trees with signs of D. ponderosae, having the focal peak point at the mean diameters of D. ponderosae. The difference between root collar damage and D. ponderosae was the former occurred at lower density than the distribution means of the latter, but extended their distribution towards the smaller diameter classes, and only occasionally in the larger trees of the older stands. The signs of trees colonized by wood borers closely resembled those of the secondary bark beetles, with lower density and more spread out distributions over the smaller diameters of tree colonized by D. ponderosae. The fungal parasite infections of western gall rust (Endocronartium harknessii) did not show any correlation with the other disturbance agents, and were found in stands with trees of mean diameter 6.5 cm and 7.9 m. The density distribution that showed the highest peaks around lodgepole pine are 9 cm or less in all types of stands, with almost all the infections were recorded solely in the Mackenzie Forest District. 126 Interactions among the bark beetles and with other biotic disturbances The interactions between two individual species of bark beetles were cross-compared in two ways, by including or excluding the presence of the other bark beetles, or by excluding the presence of the secondary species examined. The individual species of the secondary bark beetles were associated most often with D. ponderosae (all had ratios of presence to absence of 2.7 or higher). Dendroctonus ponderosae was found with I. pini 79% of the time (55/70), with Hylurgops spp. and/or D. murrayanae 88% of the time (151/171), with O. latidens 73% of the time (35/48), with P. mexicanus 85% of the time (23/27). Dendroctonus ponderosae was rarely found in the same tree with Pityogenes spp. and/or Pityophthorus spp., 56% of the time (14/25), but was found most frequently with ambrosia beetles, 91% association (70/77) (Table 8). Among the individual secondary bark beetles, Hylurgops spp. and/or D. murrayanae had the highest interactions, in relative numbers and percentages, with the other species of secondaries, comparable to those with D. ponderosae. These insects were found in the same tree as /. pini at 86% of the time (60/70), O. latidens at 69% of the time (33/48), P. mexicanus at 85% of the time (23/27), Pityogenes spp. and/or Pityophthorus spp. at 72% of the time (18/25), and ambrosia beetles at 94% of the time (72/77). Pityogenes spp. and/or Pityophthorus spp. were among the smallest bark beetles in this study, which was found among the smallest of the dead trees (d: 8.6 cm, h: 10.3 m). When Pityogenes spp. and Pityophthorus spp. occurred individually on their own, the trees were smaller and shorter (d: 5.0 cm, fi: 5.5 m). While, ambrosia beetles were almost always 127 associated with the largest and tallest dead trees (d: 15.0 cm, ft: 16.0 m). Their highest association was with D. ponderosae at 94% of the time (72/77) (d: 15.3 cm, ft: 16.2 m). In the realm of exclusive interactions between two species of bark beetles only, D. ponderosae exhibited the highest exclusive interaction with Hylurgops spp. and/or D. murrayanae at 23% (39/171) of the total occurrences. Ips pini never occured in the same trees with O. latidens only or P. mexicanus only. Pseudips mexicanus was not associated exclusively with any bark beetles, except with O. latidens on some occasions. Similarly, no associations were detected between Pityogenes spp. and/or Pityophthorus spp. with any other species of bark beetles, except with I. pini only. Insects that feed around the root collar were also frequently associated with D. ponderosae, in 64% of the occurrences (152/238). Root collar damage was associated with the assemblage of secondary bark beetles 63% of the time (150/238), and Hylurgops spp. and/or D. murrayanae 55% of the time (131/238). Those three groups of interactions were found in larger trees (d: 13.8-14.1 cm, h: 14.8-15.2 m) in comparison to those without root collar damage by insects (d: 8.5-10.7 cm, h: 10.7-12.7 m). Analogously, wood borers had a high correlation with all the four groups, including root collar damage by insects, at a rate of around 80% or higher. Trees with wood borer activity had signs of secondary bark beetle activity 96% of the time (109/113), D. ponderosae 85% of the time (96/113), Hylurgops spp. and/or D. murrayanae 84% of the time (95/113), and root collar damage by insects 79% of the time (89/113). 128 The fungus disease, western gall rust, had no correlation with the bark beetles or the non-bark beetle groups. In general, the disease were found on the larger trees (d: 7.911.7 cm, ti: 9.3-13.1m). 129 Appendix I: Case study of Mac3-C: The perfect mortality-storm from a combined effect of stand density and maturity from secondaries The goal of setting up Mac3-C in 2010 was to demonstrate the role of bark beetle outbreaks as an important agent of lodgepole pine mortality and their continuous significance in the stands, especially the secondary bark beetles at the post-outbreak stage after the main wave of mortality at the outbreak stage by D. ponderosae. Sometimes, such cases of high mortality by secondaries were considered an outlier, when the samples were irregularly detected, or the rate of mortality was higher or lower than the conventional mean, but such issues were also caused by a limited sample size or limited monitoring periods or less common events requiring certain predisposition factors or due to preconceived bias and a narrow scope of predetermined conclusion in hindsight, before collecting, examining, or interpreting the field data. The evaluation of a worst case scenario of tree mortality by outbreaks of secondary bark beetles can provide additional insights on the bark beetles populations at the post-outbreak stage, in their associations among the dead and their interactions with the live residuals lodgepole pines. For that reason, an additional plot (Mac3-C) was 'randomly' selected and surveyed for meeting the profile criteria as a high risk stand for mortality by secondary bark beetles. Mac3-C is a young, high density, pure lodgepole pine plot with 40 live and 27 dead pines (d: 7.3 cm, 1i: 9.6 m) (Table 4), and it is a good example of a stand with a more severe situation of a secondary bark beetle outbreak, I. pini in particular. In general, 54% of the dead trees contained an assemblage of secondary bark beetles (200/373), and in Mac3-C, the secondaries were associated in the stand at the rate of 35% (24/67), or with the dead trees at 89% (24/27), which was much higher than the 54% average. 130 Normally, the role of an individual species of secondary bark beetles as an agent of tree mortality was insignificant; however, this was not the case for I. pini in Mac3-C. Ips pini was associated with the dead trees at an average rate of 19% (70/373) in the 15 plots, but more than a quarter of I. pini were detected in the single plot of Mac3-C (19/67), or a 70% association with the dead trees of Mac3-C (19/27), which was at least three times higher than the 19% average. Among the 27 dead pines, the following bark beetles were associated at a higher rate even, where D. ponderosae was found in 85% of the trees (23/27), and Hylurgops spp. and/or D. murrayanae 78% of the time (21/27). The presence of P. mexicanus 11% of the time (3/27), and 0. latidens 7% of the time (2/27), were almost negligible in comparison. Root collar damage by insects were examined on all 67 live and dead lodgepole pines in the stand, where the rate of infestation was one out of every three pines (22/67) (Tables 8 and 9). The classic paradigm was the younger the stands, the smaller the mean diameter and the shorter the mean height of the lodgepole pines. This proved agreeable with the field observations and/or in the comparisons made between the stands. For example, the high density 'young' plot of Mac3-C (d: 7.3 cm, Ti: 9.6 m) was contrasted against the polar opposite of the low density 'old' plot of CLk-A (d: 16.6 cm, h: 18.8 m). In general, the difference in diameter sizes between the presence and absence of bark beetles was approximately double, and the magnitude of the height differences was between a half-fold to a one-fold increase. For example, the presence of D. ponderosae in the 15 overall plots (d: 13.6 cm, fi: 14.8 m), versus their absence (d: 6.0 cm, fi: 8.0 m) was approximately double in measurements; in Mac3-C, the presence (d: 10.3 cm, f>: 12.9 m) to 131 absence (d: 5.8 cm, ft: 7.9 m) was slightly less than double; and in the lower density 'older' site (CLk-A), the presence (d: 20.9 cm, ft: 22.0 m) to absence (d: 12.4 cm, ft: 15.5 m) remained high, though the least different between the three comparisons. The presence of bark beetles was mostly found in the larger and taller lodgepole pines, in comparison to the absence of bark beetles in the trees, where the healthy and dead trees without bark beetles were smaller and shorter. This was generally true for all species of bark beetles in all type of plots, except for the very low numbers or almost non-occurrences of I. pini and Pityogenes spp. and/or Pityophthorus spp. in the 'older' plots. If the stands were grouped according to the maturity level ('young' or 'old'), the trees with D. ponderosae were smaller and shorter (d: 9.8-12.2 cm, ft: 11.7-12.9 m) in the younger stands in Mackenzie (Mac3-C, Mac3-B, Mac2-B, Macl-B), than those of the older stands (d >15 cm, ft >15 m) in Mackenzie (Mac4-B), Crassier Creek (CCk-A) or Chief Lake (CLk-A). The complex of secondary bark beetles mimicked closely the distribution of D. ponderosae. The only minor difference is trees with secondaries were slightly smaller and shorter. For example, the measurements of the dead trees associated with the secondary bark beetles in Mac3-C (d: 9.6 cm, ft: 12.0 m) and CLk-A (d: 17.7 cm, ft: 19.0 m), were relatively similar to the measurements of D. ponderosae in Mac3-C (d: 10.3 cm, fi: 12.9 m) and CLk-A (d: 20.9 cm, ft: 22.0 m). The reverse of the classic paradigm, as above, occurred only in the low density 'old' stand (CLk-A), where the presence of certain secondaries such as /. pini, O. latidens, P. mexicanus and ambrosia beetles were associated with the smaller and shorter lodgepole pines, in comparison to their absence. Some possible explanations for the phenomena in 132 CLk-A were the low presence of the secondary bark beetles, thus, skewing and lowering the mean diameters, mean heights and their ranges, or the lower availability of suitable hosts and higher presence of live 'residuals' that are more resistant to bark beetles, or possibly, the more mature stand conditions were not the best for the populations of secondaries to increase to outbreak levels to cause 'residual' mortality. Lodgepole pine mortality associated with bark beetles can be highly variable from stand to stand, depending on the interactions of bark beetles with the pine densities and/or with the plot maturity. Two comparisons of tree mortality by bark beetles were made between Mac3-C with the other plots; the first being the similarity of some of the plots to Mac3-C, and the second, the differences in the plots in stand density and stand maturity to Mac3-C. The measurements of Mac3-C and the 15 overall plots were standardized as the baseline for ail the comparisons. Ratios among stands, as comparable indicators of mortality associated-agents The most noticeable difference between Mac3-C with the other plots was the ratio of dead to live lodgepole pines. Ratio was used as a relative measure of the interactions, in the relative comparisons between the plots. The higher the ratio number, the higher the proportion of dead to live trees within the plot. The advantage of using ratio to compare the presence to absence was the adjustment was made automatically on the appropriate scale, relative to the plot density, since the ratio of other than 1.0 represents the severity of the mortality agent, values above 1.0 meant higher presence than absence, and anything below 1.0 signified more absent than present. For example, if the ratio is 2.0, the occurrences of 133 present to absent of that mortality agent is twice as high, and a ratio of 0.5 meant the numbers present to absent is half of that. The first three comparisons (Mac3-B, Mac2-B, Mac4-B) were highly similar in density and maturity to Mac3-C, though there were some minor differences. The commonality among these plots was their high density of lodgepole pines (>60 stems/plot) and as 'young' stands, except for Mac4-B that was an older mature stand (Table 4). Mac3-C had a ratio of 0.7, compared to the other 3 plots with similar density, where their ratio were 2.0 or higher, while the overall ratio of all the 15 plots was around 1.5. This implies that the lower value of Mac3-C had more live trees than dead trees, within the stand. In term of meeting the goals of this study, the lower the ratio, the higher the potential availability of hosts for the secondary bark beetles, as long as the residuals were within the suitable range as viable hosts, which was the case for Mac3-C (ratio: 0.7, d: 7.3 cm, h: 9.6 m) (Table 4). In the second part of the comparison, the goal was to vary the stand density and stand maturity, but still be as inclusive as possible in examining the interactions between the guilds of bark beetles with their lodgepole pine hosts. Several inherent variability in density and maturity within the plots were contrasted against Mac3-C (high density 'young' plot): the four variable plots had the characteristics of a very high density 'young' plot (Macl-B), a medium density 'young-old' plot (Mac5-A), a medium density 'old' plot (CCk-A), and a low 'old' density plot (CLk-A) (Table 4). Among these plots, the ratio of dead to alive trees for the very high density plot was 1.3, for the 'young-old' and 'old' stands of medium density 134 were slightly above 2.0, and for the low density old' stand was 6.0. All the values were well above Mac3-C ratio of 0.7, or all plots had lower abundance of live residuals than Mac3-C. The ratio of presence to absence of D. ponderosae was fairly high and consistent in all the plots, at a ratio of 0.5 or higher, except for the very high density plot of Macl-B at 0.1. One probable explanation for the Macl plots was Macl-A and Macl-B were 'younger' stands, where the trees were smaller in diameters (d: 5.6 cm), shorter in heights fh: 7.0), and of limited suitability as hosts for D. ponderosae. The assemblage of secondary bark beetles had similar ratios of presence to absence of 0.5 or higher within all plots, except for Macl-B. Most of those ratios followed closely the trends of D. ponderosae, except for some minor differences. Those differences were due to plot to plot variations, including the availability of larger trees or more mature plots, which effectively limits the numbers of mortality to some extent, or potentially the number of suitable hosts for D. ponderosae and the subsequent increase in the populations of secondary bark beetle, as the case for Macl. The more distinct the deviation in stand density or maturity from Mac3-C or the 15 overall plots, the higher the variability between the ratios of dead to live trees; the average ratio of presence to absence in D. ponderosae and secondary bark beetles (d: 13.0-13.6 cm, h: 14.2-14.8 m) for the 15 overall plots were both 0.5; in Mac3-C, the ratios were 0.5 and 0.6 respectively (d: 9.6-10.3 cm, ft: 12.0-12.9 m); in a high density 'young' stand (Mac3-B), or in a plot similar to Mac3-C, the presence of D. ponderosae and secondary bark beetles were more similar, at 0.8 and 0.6 (d: 9.8-9.9 cm, 1h: 11.5-11.7 m) than in the polar opposite stand of Mac3-C or a low density 'older' stand (CLk-A), where the two ratios were proportionally higher at 1.0 and 3.7 (d: 17.7-20.9 cm, fi: 19.0-22.0 m). 135 The differences in ratio demonstrates the complexity of the maturity of the stand, as a direct measure of the numbers of dead to live trees, or as an indirect measure of more suitable hosts for the bark beetles from the larger and taller trees. Mac3-C had the highest ratio of I. pini at 0.4, which was minorly significant in comparison to the overall and the other plots (ratios of 0-0.2). The ratios of presence to absence of Hylurgops spp. and/or D. murrayanae, O. latidens, P. mexicanus in Mac3-C (0.5, ~0, ~0) were not significantly different from the overall measurements (0.4,0.1, ~0). However, in certain plots, some species of secondary bark beetles were found more concentrated in the 'young-old' or 'old' plots. Hylurgops spp. and/or D. murrayanae and ambrosia beetles had the highest ratio of presence to absence at 1.1and 0.8 in medium dense 'young-old' plot (Mac5-A), well above the average ratio of 0.4 and 0.1in the 15 overall plots. Orthotomicus latidens had the highest ratio of presence to absence in low density 'old' plot (CLk-A) at 0.6, compared to the average ratio of 0.1 from the 15 overall plots. Pseudips mexicanus had one of the lowest ratios of presence to absence among the associations of bark beetles in the stands (0.1 or less), regardless of plot density or maturity level. Similarly, the presence to absence ratio of the non-bark beetle elements (root collar damage by insects and wood borers) in Mac3-C and Mac3-C type of plots were more similar to the 15 overall plot, than the non-Mac3-C type of plots, which had greater variation: the 15 overall plots had ratios of 0.6 for root collar damage and 0.2 for wood borers, Mac3-C type of plots had ratios of 0.4-0.8 for root collar damage by insects and 0.1-0.4 for wood borers, the non-Mac3-C type of plots, in this case CLk-A, had the highest ratios of 3.7 for root collar 136 damage and 2.5 for wood borers. These last 2 ratios were 5 times or higher, in some stands, than the average ratios observed in the overall plots. For the fungus disease of western gall rust, the ratio for Mac3-C type of plots can vary from 0.2 to 0.9 compared to the 15 overall plots (0.5), but the highest ratio was found in the very high density 'young' stand (Macl-B) at 1.8, at least twice or more, higher than the average ratios. Among all, western gall rust was the only mortality agent associated with the smaller and shorter lodgepole pines (d: 5.5-7.9 cm, fi: 8.1-10.6 m) in all plots, except in Macl-B, relative to those trees that did not had any western gall rusts (d: 6.6-13.3 cm, h: 6.9-14.5 m). In summary, these ratios indirectly supports the warrant for a more detailed inspection of Mac3-C, with its low stand ratio of 0.7 (high amount of 'residuals') and qualifying as a high 'risk' stand for potential tree mortality from outbreaks of secondaries, in particular I. pini that was recorded at a ratio of 0.4 (above the average values from any of the other stands surveyed). 137 Exception than the rule: Higher associations of secondary bark beetles in Mac3-C The highlight of Mac3-C was the percentage of I. pini found associated most abundantly with the lodgepole pines. Mac3-C was not an unusual plot, as the presence to absence ratio of D. ponderosae and the complex of secondary bark beetle in Mac3-C and the 15 overall plots were similar at around 0.5. One of the reason for the more pronounced increase in /. pini was because of the higher abundance of live residuals (ratio: 0.7), and the trees in Mac3-C were highly suitable potential hosts for I. pini, as the plot was a monoculture plantation of intermediate, pole-sized diameter of lodgepole pines (d: 5.7-17.1 cm, h: 5.8-20.0 m). The pine engravers were seldom found on the larger trees in the older plots, possibly due to the beetles occurring at the higher canopy levels or above the sampled area, since unlike smaller trees, the larger ones were more fully utilized by D. ponderosae, limiting the 'free' resources available for subsequent use by the secondaries to cause potential outbreaks. Since I. pini is a moderately aggressive bark beetle that occasionally outbreak given the proper circumstances, in this case, the initial host abundance from the dead trees of D. ponderosae outbreak, new mortality of nearby live residuals was predicted when the increase in population of I. pini was sufficient to overcome the defenses of the pole-sized trees, which disregard whether the trees were healthy or had been weaken by D. ponderosae or compromised by any secondary bark beetles or the other mortality agents. Hylurgops spp. and/or D. murrayanae was found in the largest of trees, with the differences between their presence and absence from the trees was approximately the 138 doubling of the diameters size or heights of the trees, displaying differences ranging from 4.1 to 9.1 cm and 3.8 to 8.3 m. For O. latiden, their presence was most noticeable in the older plots, and for P. mexicanus, no correlation of plot density or stand maturity affected the distribution of this species. Each stand had its own characteristic interactions between stand density and maturity, or indirectly, the signature of interactions between the insects and hosts. In this manner, the presence of Pityogenes spp. and/or Pityophthorus spp. was associated with the smallest of trees among all the recorded bark beetles in most sites, and were not present in the older sites, possibly due to the unsampled regions at higher canopy level, where there is a higher availability of exclusive phloem material for them and less suitable for D. ponderosae. However, the beetles were associated with the larger trees (d: 7.3-14.6 cm, h: 9.6-14.6 m) when present in the stand, than their absence in the smaller trees (d: 5.8-10.8 cm, fi: 7.7-12.3 m). In contrast, ambrosia beetles was found among the largest of trees in all the compared sites, except for Mac3-C and CLk-A. The differences between their presence (d: 10.2-18.4 cm, h: 11.7-18.2 m) and absence (d: 5.7-9.8 cm, fi: 7.7-12.3 m) from the trees was approximately the doubling of the diameters size, but less so in height. Mac3-C had a similar trend of the general interactions of the 15 overall plots for Pityogenes spp. and/or Pityophthorus spp., where they were found among the smallest of trees, but no ambrosia was found in this plot. 139 Summary of case study of Mac3-C, in comparison to similar type of stands The average value of the 15 plots, or within a plot, is subject to random fluctuations, since the resulting mean is only an arbitrary series of measurements of the most frequent values recorded, not an absolute dictum; in this case, the majority of the data was collected from the 'young' residual stands in Mackenzie, and the mean value of this case study primarily reflect the pole-sized diameter lodgepole pines of Mackenzie, which Mac3-C did not deviate from the overall measurements. The purpose of these comparisons of the interactions, means and ratios were to differentiate the plots, since any deviations from the mean, signify that some characteristics of the bark beetles or the non-bark beetle elements were correlated as major agents of tree mortality under different circumstances, or by varying the density or maturity levels. In the younger stands of Mackenzie (Mac3-C, Mac3-B, Mac2-B, Macl-B), the bark beetles and root collar damage by insects were associated with lodgepole pine of diameters around 8-10 cm, versus the older stands of Mackenzie (Mac4-B), Crassier Creek (CCk-A) or Chief Lake (CLk-A), which was around 13 cm or more: D. ponderosae (dy0Ung: 9.8-10.3 cm vs. d0id: 15.4-20.9 cm), I. pini (dyg: 8.7-10.2 cm vs. 0id: 16.7-19.5 m), and root collar damage by insects (f»yg: 11.4-12.1 m, h0id: 14.3-20.1 m). The reverse was true with western gall rust, found associated with the smaller trees (d: 5.5-7.9 cm, Ti: 8.1-10.6 m), relative to their absence (d: 6.6-13.3 cm, fi: 6.9-14.5 m). If the stands were grouped according to their maturity, the individual secondary bark beetles in the younger stands of Mackenzie, were mostly associated to the larger trees (d: 7.4-15.6 cm, fi: 10.3-13.2 m) versus the average-sized tree in the plots (d: 5.8-7.3 cm, fi: 7.8-9.6 m). However, those trees with secondaries in the younger stands were smaller and shorter than those from the older stands (d: 12.8-22.5 cm, fi: 16.7 -24.7 m). The assemblage of secondary bark beetles was the main mortality agent associated with the dead trees in Mac3-C. Among the individual or groups of secondaries, the most significant secondary bark beetles in Mac3-C was I. pini, found most abundantly (ratio 0.4) in this stand than any other stands, and was associated with the dead trees as the second best model (AIC: 58) after secondary bark beetles (AIC: 39) (Table 10B). The presence to absence ratio is a gauge of the stand density and maturity, but is also an indirect measure of the stand as a suitability index for secondary bark beetles. The highest ratio of 0.4 in /. pini in Mac3-C is an example exhibiting the species preference for a high density 'young' stand. In general, Hylurgops spp. and/or D. murrayanae was found most abundantly among the individual species of secondary bark beetles, in all the different stages of the stands, but 'young-old' stand (Mac5-A) works best for them, since the ratio of 141 1.1 indicates an increase of at least two-fold or more than the other sites. Orthotomicus latidens was predominantly associated with the dead trees in the 'older' stands (CLk-A or CCk-A) at ratios of 0.4 and 0.2. In summary, Mac3-C is a high-risk plot of pure lodgepole pine, perfect to examine the rate of mortality from secondary bark beetles. Host abundance, or the availability of residual pines in the plot highly influence the population dynamics of bark beetles in Mac3-C, with the rise of one population into the outbreak phase, corresponding to a drop for another species, which in turn cause an extended period of mortality among the 'ripe residuals' on overtime. 142 Appendix Jl. Distribution of diameter-at-breast height (in cm) of lodgepole pine with frass, and their association with Dendroctonus ponderosae and secondary bark beetles Lodgepole pines Any secondary with frass Dendroctonus bark beetles ponderosae (+> Lodgepole pines with frass (+) I- 8.9 (5.7-14.6) presence (+) absence* (-) Ips pini Pseudips mexicanus W mSiia (+) Pityogenes spp. and/or Ambrosia beetles Pityophthorus spp. Dendroctonus murrayanae (+) j|g||| Hylurgops spp. Orthotomicus latidens and/or (+) (+) W (+) •.msmOe. 9.7 (7.3-14.6) 8.9 (5.7-14.6) 8.5 Orthotomicus latidens presence*(+) absence (-) 8.1 8.6 Pseudips mexicanus presence (+) absence* (-) 8.1 Pityogenes spp. and/or Pltyophthorus spp. MSii •SH presence'(+) 7.9 (5.7-10.7) 8.4 (7.3 -10.7) 7.9 (5.7-10.7) 8.3 (6.5-10.7) 7.2 (5.7-8.2) 8.3 (7.3-10.7) absence' (-) 9.5 (5.7-14.6) 10.4 (7.3-14.6) 9.1 (5.7-13.6) 8.9 (5.7 -10.9) 10.5 (7.3 -14.6) 9.3 (9.0-9.5) 8.1 8.1 8.6 (5.7-13.6) 8.7 (5.7-10.9) 8.1 Ambrosia beetles JjL. presence*(+) 8.1 absence* (-) 8.9 (5.7-14.6) 8.1 8.1 8.7 (7.3-10.7) 7.8 (5.7-10.7) i£9i 9.7 (7.3-14.6) 8.6 (5.7 -14.6) * The interactions of the two terms may include the presence of (1) Dendroctonus ponderosae, or (2) any secondary bark beetles, or (3) others/non-bark beetles (root collar damage by insects, wood borers, or western gall rust) * In contrast, the second relationship showed the absence of the 'horizontal' term (opposite of cross-interactions) with the hosts, with the only residuals are the non-bark beetles (others: root collar damage by insects, wood borers, or western gall rust) 144 Appendix J2. Distribution of height (in m) of lodgepole pine with frass, and their association with Dendroctonus ponderosae and secondary bark beetles Any secondary Lodgepole pines with frass Dendroctonus bark beetles ponderosae Ips pini Hylurgops spp. Orthotomicus latidens and/or Dendroctonus murrayanae Pseudips mexicanus Pityogenes spp. Ambrosia beetles and/or Pityophthorus spp. (+) (+) (+) <+) W (+) (+) (•) <+) 11.3 (7.2-17.1) 12.4 (8.4-17.1) 11.4 (7-2-17.1) 11.0 (7.2.-13.8) 11.6 (7.2-13.8) 12.0 (8.4-17.1) 12.3 (10.5-13.8) 11.0 (7.2-13.5) 11.1 9.8 (7.2-11.6) 9.4 13.1 (9.4-17.1) 10.9 (8.4-17.1) 11.0 (7.2-13.5) 10.8 (7.2-17.1) 11.5 (8.4-17.1) 11.3 (7.2-17.1) - 12.7 (8.4-17.1) 12.2 (8.4-13.8) 12.9 (11.0-13.8) 12.3 (8.4-17.1) 12.5 (10.5-13.8) (10.5-13.5) 7.7 (5.7-9.2) 7.7 (5.7-9.2) 7.5 (5.7-9.0) 5.7 8.1 Lodgepole pines with frass presence*(+) absence' (-} Dendroctonus ponderosae presence*(+) 12.4 (8.4-17.1) 12.1 I -^ U:*.^-1-ss absence* (-) 7.7 (5-7-9.2) 7.3 (5.7 -9.0) 8.1 Any secondary bark beetles Mi presence*(+) 11.4 (7.2-17.1) 12.7 (8.4-17.1) absence* (-) 9.4 9.8 (7.2-11.6) Ips plnl presence (+) 11.0 (7.2-13.8) (8.4 -13.8) 13.1 (9.4-17.1) 13.1 (9.4-17.1) 11.5 (7.2-13.8) 12.2 11.1 (8.4-13.8) 12.3 (10.5-13.8) 11.0 (7.2-13.5) 12.7 (11.0-13.8) 12.5 (11.0-13.8) 11.3 (7.2-13.5) 11.4 (8.4-17.1) 11.8 (10.5-13.1) 11.1 lar-to. absence (- 10.5 17.1 Hylurgops spp. and/or Dendroctonus murrayanae j. presence'(+) 11.6 (7.2-13.8) 11.5 (7,2-13.8) 12.9 (11.0-13.8) absence' (-) 10.9 (8.4-17.1) 11.9 (8.4-17.1) _ 10.4 (8.4-13.1) - continue next page • 145 - 11.1 "•* - tmrr.f- -v .••I.-jp-.-TItr-ir j-jtf -• 10.0 (9.5 -10.5) <»> 0 - continuation Hylurgops spp. Orthotomicus and/or latidens Dendroctonus murrayanae Lodgepole pines Any secondary with frass Dendroctonus bark beetles ponderosae Ips pini (+> (+) M (+) 12.0 18.4-17.1) 12.3 (8.4-17.1) 11.1 (8.4-13.8) 12.7 (11.0-13.8) 11.0 12.5 (9.4-13.5) 10.9 (7.2-13.5) 12.3 (10.5-13.8) 12.5 (10.5-13.8) 12.3 (10.5-13.8) 12.5 (11.0-13.8) 10.8 12.3 (8.4 -17.1) 10.1 (+) (+} Pseudips mexicanus Pityogenes spp. and/or Ambrosia beetles Pityophthorus spp. W W H Orthotomicus latidens presence*(+) absence*(-) (7.2-13.5) 12.1 11.1 (10.5-13.8) (9.5-13.2) 11.2 12.6 (11.1-13.5) IO.9" (7.2-13.5) 11.1 (7.2-13.5) 11.9 (10.5 -13 5) 11.1 (10.5 -13.8) 10.9 (7.2-13.1) 11.7 (8.4-17.1) 9.4 (7.2-11.6) 11.3 2 -13.5) (9.5 -13.2) 11.9 (10.5-13.5) 13.1 (8.4-17.1) 13.5 (13.1-13.8) Pseudips mexicanus etem presence (+) mm absence (-) mm ~ (7.2-17.1) 12.1 flii&S; LjM (7.2-13.1) Pityogenes spp. arid/or Pityophthorus spp. presence (+) .5 -13. absence (-) 11.5 (8.4-17.1) 12.6 11.0 (8.4-17.1) (8.4-13.8) 12.0 (9.0-13.8) 11.1 11.1 11.0 11.7 (7.2-13.8) 11.1 Ambrosia beetles 3L irrrffi'ifiiftirfiiii presence*(+) 11.1 absence (-) 7.2-17.1) 12.4 (8.4-17.1) (7.2-13.8) f 11.9 (8.4-17.1) 11.1 11.1 12.5 (10.5-13.8) 10.9 (7.2-13.5) The interactions of the two terms may include the presence of (1) Dendroctonus ponderosae, or (2) any secondary bark beetles, or (3) others/non-bark beetles (root collar damage by insects, wood borers, or western gall rust) * In contrast, the second relationship showed the absence of the 'horizontal' term {opposite of cross-interactions) with the hosts, with the only residuals are the non-bark beetles (others: root collar damage by insects, wood borers, or western gall rust) 146 0 Appendix J3. Distribution of diameter-at-breast height (in cm) of lodgepole pine with frass, and their association with bark beetles, root collar damage by insects or other interactions New mortality Lodgepole pines Dead (live to dead) Residuals (live) with frass (2009 and 2010) (2009 to 2010) (2009 to 2010) (+) (+) Mac3<* (dead) (2010) Mac3-C* (live) (2010) Root collar damage by insects Others: Wood borers Others: Western gall rust (+) (+) (+) 8.8 (5.7-13.6) 8.6 (5.7-10.7) 8.0 (5.7-10.2) 9.3 (7.3-13.6) 10.1 (9.5-10.7) 8.8 7.7 (5.7-8.7) 5.7 W H (+) (+) 8.3 (5.7-13.6) 10.2 (8.1-14.6) 8.3 (5.7-10.7) 8.2 10.6 10.7 0 Lodgepole pines with frass «rtfiaaiMii presence (+) 8.9 (5.7-14.6) M Mil 9.8 (8.2-10.9) __ Dendroctonus ponderosae I presence (+) absence (-) (7.3-14.6) (8.2-10.9) 7.7 (5.7-9.2) (7.3-13.6) (8.1-14.6) 7.6 (5.7-9.0) 9.2 7.1 (5.7-8.4) 8.2 (7.4 -10.2) 7.8 (5.7-9.2) Any secondary bark beetles •zw.m presence (+) 8.6 (5.7-10.7) 8.0 (5.7-14.6) 9.8 (8.2 -10.9) (5.7-13.6) 10.9 (9.0-14.6) 5.7-10.7) 8.9 (5.7-13.6) 8.5 (5.7-13.1) 9.6 (8.2 -10.9) 8.3 (5.7-13.6) 9.1 (9.0-9.2) 8.3 (5.7 -10.7) 8.8 8.6 (5.7- 13.6) (5.7-10.7) (5.7-13.6) (8.1-10.9) (9.5-10.7) (6.5-10.2) 8.5 (5.7 -13.6) 5.7 8.0 (5.7-9.2) (5.7 -10.2) absence (-) Ipspini presence (+) 9.2 11.4 (8.1-14.6) absence' (-) (8.1-14.6) (8.1-10.2) Hylurgops spp. and/or Dendroctonus murrayanae i i Hf n T 8.1 presence (+) absence' (-) .7-10. 2-10. 9.2 (5.7-14.6) 0 7-10.7) 8.5 (5.7-13.6) 10.2 (8.1-14.6) - continue next page • 147 0 8.2 continuation Orthotomicus latidens Mi 0 7.6 (5.7-9.5) 7.6 (5.7-9.5) 6.6 (5.7-7.4) 8.3 (5.7-10.7) 8.2 9.6 (8.1-13.6) 10.7 8.5 (6.5-10.2) 9.0 10.7 0 8.4 (7.3-9.5) 10.1 (9.5-10.7) 7.4 10.6 7.1 (5.7-8.4) 8.2 9.1 (5.7-13.6) 5.7 5.7-8.2) (5.7-10.7) presence*(+) 8.6 (5.7-14.6) 8.2 7.4 (5.7-9.5) absence* (-) 9.0 (5.7-13.6) 10.6 (10.2 -10.9) 9.2 (6.5 -13.6) (8.1-9.2) 8.6 8.2 8.1 •Hai •Min 9,0 10.6 (5.7-14.6) (10.2-10.9) 8.5 (5.7-13.6) 14.6 8.8 Pseudips mexicanus *s presence'(+) (7.3-10.7) absence*(-) (7.3-9.5) m (8.1-14.6) 8.1 (5.7 -10.2) Pityogenes spp. and/or Pityophthorus spp. presence (+) 7.9 15.7-10.7) 7.3 (5.7-9.0) 10.6 absence*(-) 5.7-14.6 (10.2 -10.9) 9.8 (7.3 -13.6) 9.5 (7.3-13.6) 10.2 (8.1-14.6) 5.7-8.4) 6.5 (5.7-7.4) 8.9 (8.2 -10.2) Ambrosia beetles 8.1 0 0 8.2 8.9 (5.7-13.6) 8.6 (5.7 -10.7) 8.0 (5.7 -10.2) (+) (+) (+) Root collar damage by insects Others: Wood borers Others: Western gall rust presence (+) absence'(-) 8.9 (5.7 -14.6) w 9.8 (8.2-10.9) 8.3 (5.7-13.6) 10.2 (8.1-14.6) (+) M (+) (2009 and 2010) (2009 to 2010) (2009 to 2010) Lodgepole pines with frass Dead New mortality Residuals (live) (live to dead) f 8.3 (5.7-10.7) M M (2010) (2010) Mac3-C* (dead) Mac3-C* (live) The interactions of the two terms may include the presence of (1) Dendroctonus ponderosae or (2) secondary bark beetles with the hosts, with some of them interacting with non-bark beetles/others (root collar damage by insects, wood borers, or western gall rust) * In contrast, the second relationship showed the absence of the 'horizontal' term (opposite of cross-interactions) with the hosts, with the only residuals are the non-bark beetles (others: root collar damage by insects, wood borers, or western gall rust) * Mac3-C was surveyed on 2010 only, without any prior information of the stand for mortality monitoring (2009) 148 Appendix J4. Distribution of height (in m) of Iodgepoie pine with frass, and their association with bark beetles, root collar damage by insects or other interactions New mortality (live to dead) Residuals (live) Dead Lodgepole pines (2009 and 2010) (2009 to 2010) (2009 to 2010) with frass (+) (+) (+) Iodgepoie pines with frass -fti. "..".'V presence*(+) absence (-) Root collar damage by insects Others: Wood borers Others: Western gall rust (+) (+) (+) (+) (+) _ 11.3 (7.2-17.1) 13.1 (12.9-13.2) 10.6 (7.2-13.8) 12.3 (9.4-17.1) 12.4 (8.4-17.1) 13.1 (12.9-13.2) 11.3 (8.4-13.8) 13.2 (9.4-17.1) Dendroctonus ponderosae presence'(+) Mac3-C* (live) (2010) (+> ^ *. Mac3-C* (dead) (2010) • 11.3 (9.0-13.5) - 8.5 -• --~ ' ' w*-' . ... . 11.3 (8.4-13.8) 12.3 (9.5-13.8) 10.0 (7.2-12.9) (8.4-13.8) (13.5-13.8) (11.0-12.9) sssss 10.2 9.9 (7.2 -11.6) 9.8 (7.2 -11.6) 9.4 (7.2-11.3) (9.0-11.3) 9.8 (8.5-11.1) 11.3 (9.0-13.5) 11.4 (8.4 -13.8) (9.5-13.8) (7.2 -12.9 (8.4-13.8) 12.3 (9.5-13 8) 9.6 (7.2-11.3) 13.7 (13.5-13.8) (7.2-12 9) Any secondary bark beetles presence*(+) 11.4 (7.2-17.1) (12.9-13.2) (7.2 -13.8 (9.7-17.1) absence (- Ips pini mmmfcsaoaj 1 presence (+) 9.7-13.1 absence (-) 11.3 (9.0 -13.5) 11.2 13.3 (9.4-17.1) 13.1 (9.4-17.1) (9.4-12.9) Hylurgops spp. and/or Dendroctonus murrayanae « 13.1 presence (+) (7.2-13.8) absence (-) 10..9 (8.4-17.1) (12.9-13.2) 4H 11.3 (9.0-13.5) 10.9 (7.2-13.8) 10.3 (8.4-12.9) 12.3 (9.4-17.1) - continue next page - 149 12.8 (11.1-13.8) 10.3 (8.4-13.1) 10.6 9.5 (8.5-10.2) . - continuation New mortality Lodgepole pines Dead (live to dead) Residuals (live) with frass (2009 and 2010) (2009 to 2010) (2009 to 2010) H W W W 12.0 (8.4-17.1) 13.2 10.6 17.1 11.0 13.0 (12.9 -13.1) (7.2 -12.9) 12.3 (10.5-13.8) 13.2 11.6 10.8 (7.2-17.1) 13.0 (12.9-13.1) Mac3-C* (dead) (2010) Mac3<* (live) (2010) Root collar damage by insects Others: Wood borers Others: Western gall rust W (+) (+) W <+) Orthotomicus latidens Hta presence*(+) absence*(-) (7.2 -13.5) v "mi"' niiMifri»"iVTIHl 0 0 10.6 11.1 (8.4-13.8) (8.4-13.8) 10.7 (9.4-13.1) 11.3 (9.0-13.5) 8.5 11.7 (9.5 -13.8) 10.3 (9.5-11.0) 10.0 11.4 (9.4-13.1) 13.5 12.3 (10.5 -13.8) 13.7 (13.5 -13.8) 11.0 10.6 (9.4-13.1) 9.5 9.9 (7.2-12.9) (7.2-12.9) Pseudips mexicanus MM presence*(+) 13.1 13.5 12.1 (9.4-17.1) 10.2 (9.0-11.3) (10.5-13.8) wmmsmm absence*(-) 10.0 (7.2-12.9) 8.5 Pityogenes spp. and/or Pityophthorus spp. presence (+) absence' (-) 17.2-13.5) 11.5 (8.4 -17.1) (9.5-13.2) (7.2 -11.6) 13.0 (12.9-13.1) 11.3 (8.4-13.8) 12.3 (9.4-17.1) 10.2 m n.i MAVkm 11.1 absence*(-) 11.3 (7.2-17.1) 11.1 13.1 (12.9-13.2) 10.6 (7.2-13.8) 12.3 (9.4-17.1) 11.3 (9.0-13.5) 8.5 11.3 (8.4-13.8) Hi 12.3 (9.5 -13.8) t The interactions of the two terms may include the presence of (1) Dendroctonus ponderosae or (2) secondary bark beetles with the hosts, with some of them interacting with non-bark beetles/others (root collar damage by insects, wood borers, or western gall rust) * In contrast, the second relationship showed the absence of the 'horizontal' term (opposite of cross-interactions) with the hosts, with the only residuals are the non-bark beetles (others: root collar damage by insects, wood borers, or western gall rust) * Mac3-C was surveyed on 2010 only, without any prior information of the stand for mortality monitoring (2009) 150 (7.2-11.0) 10.5 (8.5 -12.9) 11.4 (8.4 -13.8) (9.0-11.3) Ambrosia beetles presence'(+) 11.5 (9.5 -13.5) JM. 10.0 (7.2-12.9) Appendix K: Size relationships of trees with frass with bark beetle activity If lodgepole pines were associated to D. ponderosae, the trees were larger and taller (12/21) (d: 9.7 cm, fi: 12.4 m) than trees without D. ponderosae (9/21) (d: 7.7 cm, ft: 9.8 m) (Table 11, Appendix I). Any trees associated to D. ponderosae, with any interactions between D. ponderosae and secondaries or non-bark beetles, were larger (d: 8.4-10.1 cm, Ti: 11.9-13.7 m), than the trees in the absence of D. ponderosae (d: 5.3-8.1cm, fi: 9.4-11.1 m) (Table 11). Within the secondary bark beetle castes, I. pini was associated the highest with all the other bark beetles. For example, among the 11 Hylurgops spp. and/or D. murrayanae found, they were associated from highest to lowest in the following order: I. pini (10/11), followed by D. ponderosae (6/11) and Pityogenes spp. and/or Pityophthorus spp. (6/11); for O. latidens, this species was associated the highest with I. pini (6/7) and D. ponderosae (6/7); for P. mexicanus, the highest interaction was with I. pini (7/7) and D. ponderosae (6/7) (Table 11, Appendix I). One common features among the secondary bark beetles interactions were the more uniform distribution of measurements of the tree diameter (d: 8.5-8.6 cm), less so in tree height fh: 11.0-12.3 m). In their absence, the trees were slightly larger in diameter (d: 9.011.0 cm), but comparable in tree height measurement (fi: 10.8-13.1 m). The overall relative similarity of measurements was possibly due to the limited sample size. The only obvious observation of host selection was the presence of I. pini in smaller lodgepole pines (18/21) (d: 8.5 cm, ft: 11.0 m), in comparison to their absence (3/21) (d: 11.0 cm, fi: 13.1 m) (Appendix I). 151 From the four surviving green residuals, all trees had some secondary bark beetles (4/4), I. pini in half of them (2/4), failed or ongoing colonization of D. ponderosae in half of them (2/4), and 0. latidens and P. mexicanus in one of the tree for each species (Appendix I). The one tree with P. mexicanus, was found also associated with D. ponderosae and I. pini. This sort of multiple layers of interactions between the secondary bark beetles demonstrate the lethal potential of secondaries as a possible mortality agent of weaken trees. In this case, as an opportunist, in others, as the aggressor species that attacked live residuals, for example, several of the live trees were exclusively infested with an individual secondary species such as I. pini (1/2) or O. latidens (1/1) (Table 11). The twig bark beetles, Pityogenes spp. and/or Pityophthorus spp. was associated with the smaller diameter trees (d: 7.9 cm, h: 11.0 m) versus their absence from the trees (d: 9.5 cm, fi: 11.5 m). This generalization of smaller trees associated with twig beetles was true for all the twig beetle interactions with the other groups, but the difference in magnitude was most noticeable in their interaction with O. latidens (d: 7.2 cm, fi: 11.1 m), versus the absence of the twig beetles, in the presence of O. latidens only (d: 10.5 cm, Ti: 13.1 m) (Appendix I). In contrast, ambrosia beetles were found the least among the frass trees (1/21). For that reason, no comparisons were made, since the sample size was limited, and insufficient to exhibit even the weakest of any interactions. Root collar damage by insects were found in 62% (13/21) (d: 8.8 cm, fi: 11.3 m) of the trees with frass. Root collar damage by insects were most commonly associated with the complex of secondary bark beetles (12/13), followed by I. pini (11/13) D. ponderosae 152 (9/13), Hylurgops spp. and/or D. murrayanae (5/13), 0. latidens (5/13), P. mexicanus (5/13), and with Pityogenes spp. and/or Pityophthorus spp. (4/13) (Table 11, Appendix I). Wood borers were found in 14% of the trees with frass (3/21). All were associated with the complex of secondary bark beetles (3/3) and I. pini (3/3), and two out of the three trees were associated with the other mortality agents, except for their absence in ambrosia beetles (Appendix I). One possibility for the highest association of I. pini with the wood borers was the attractions to the host volatiles of weaken trees, or the presence of new mortality, which signal the presence of a suitable host, in addition to the emitted pheromones by the secondaries. 38% (8/21) of the trees with frass had western gall rusts, which had the highest association with the complex of secondary bark beetles (8/8), followed by I. pini (7/8) (Table 11). The recorded observation that only two trees were associated with D. ponderosae, versus the presence of secondaries in all the interactions with western gall rusts exhibited the differences in behaviors and colonization preferences between D. ponderosae and /. pini; Dendroctonus ponderosae is more likely to attack healthy, vigorous tree of larger diameter because the phloem nutrition of those trees are highest when they had not been compromised; in contrast to secondary bark beetles, particularly I. pini that are moderately aggressive, will attack almost any weakened hosts, including ones with western gall rust. In summary, 21 trees with frass were associated with bark beetles. The highest among them were /. pini (18/21), followed by D. ponderosae (13/21), Hylurgops spp. and/or D. murrayanae (11/21), Pityogenes spp. and/or Pityophthorus spp. (8/21), 0. latidens (7/21), 153 and P. mexicanus (7/21) (Table 11). The presence of D. ponderosae in the lodgepole pine was associated with the larger and taller trees (d: 9.7 cm, f>: 12.4 m), versus their absence (d: 7.7 cm, f>: 9.8 m). In contrast, the presence of I. pini and Pityogenes spp. and/or Pityophthorus spp. were associated with the smaller trees (d: 7.9-8.5 cm, fi: 11.0 m), in comparison to their absence (d: 9.5-11.0 cm, ft: 11.5-13.1 m). Most secondary barkbeetles, excluding I. pini were associated with trees of slightly smaller, if not comparable, in diameter size and heights in their presence (d: 8.6 cm, ft: 11.6-12.3 m), versus their absence (d: 9.09.2 cm, ft: 10.8-11.0 m) (Appendix I). 154 Appendix L: Justification for grouping Hyiurgops spp. and Dendroctonus murrayanae in the same category The two most common bark beetles at the root collar regions, Hyiurgops spp. and/or D. murrayanae, were found very similarly within their habitat environments, including their numbers, occurrences and interactions with each other or with other bark beetles. In total, the grouped measurements of bark beetles of the roots, Hyiurgops spp. (d: 13.3 cm, fi: 14.7 m) and D. murrayanae (d: 13.5 cm, ft: 14.8 m), had comparable diameter and height (d: 13.3 cm, ft: 14.6 m), similar to the average combined measurements of their individual occurrences. This comparison of the two showed some overlapping, and was combined into one category because both had some similarities in the measurements, so as not to underevaluate the presence of one or the other. 155