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Forests 7 (8): 171 (2016)
University of British Columbia. BRAES Institute
Dhar, Amalesh
Parrott, Lael
Hawkins, Christopher D.B.
The mountain pine beetle (Dendroctonus ponderosae Hopkins) (MPB) has infested and killed millions of hectares of lodgepole pine (Pinus contorta var. latifolia Engelm) forests in British Columbia, Canada, over the past decade. It is now spreading out of its native range into the Canadian boreal forest, with unknown social, economic and ecological consequences. This review explores the ramifications of the MPB epidemic with respect to mid-term timber supply, forest growth, structure and composition, vegetation diversity, forest fire, climate change, and ecosystem resilience. Research confirms that, in British Columbia, all of these variables are more significantly impacted when salvage logging is used as management response to the outbreak. We conclude that appropriate management in response to MPB is essential to ensuring ecologically resilient future forests and reliable mid-term timber supplies for affected human communities. We highlight knowledge gaps and avenues for research to advance our understanding in support of sustainable post-disturbance forest management policies in British Columbia and elsewhere.
ReviewAftermath of Mountain Pine Beetle Outbreak inBritish Columbia: Stand Dynamics, ManagementResponse and Ecosystem ResilienceAmalesh Dhar 1,*,†, Lael Parrott 1 and Christopher D.B. Hawkins 21 Okanagan Institute for Biodiversity, Resilience, and Ecosystem Services (BRAES), University of BritishColumbia, Okanagan Campus, 1177 Research Road, Kelowna, BC V1V 1V7, Canada; lael.parrott@ubc.ca2 Yukon Research Centre, Whitehorse, YK Y1A 5K4, Canada; chawkins@yukoncollege.yk.ca* Correspondence: amalesh@ualberta.ca; Tel.: +1-780-492-6538; Fax: +1-780-492-4323† Present address: Department of Renewable Resources, University of Alberta, 847 General Services Bldg,Edmonton, AB T6G 2H1, Canada.Academic Editors: Jarmo K. Holopainen and Timothy A. MartinReceived: 9 June 2016; Accepted: 2 August 2016; Published: 5 August 2016Abstract: The mountain pine beetle (Dendroctonus ponderosae Hopkins) (MPB) has infested andkilled millions of hectares of lodgepole pine (Pinus contorta var. latifolia Engelm) forests in BritishColumbia, Canada, over the past decade. It is now spreading out of its native range into theCanadian boreal forest, with unknown social, economic and ecological consequences. This reviewexplores the ramifications of the MPB epidemic with respect to mid-term timber supply, forest growth,structure and composition, vegetation diversity, forest fire, climate change, and ecosystem resilience.Research confirms that, in British Columbia, all of these variables are more significantly impactedwhen salvage logging is used as management response to the outbreak. We conclude that appropriatemanagement in response to MPB is essential to ensuring ecologically resilient future forests andreliable mid-term timber supplies for affected human communities. We highlight knowledge gapsand avenues for research to advance our understanding in support of sustainable post-disturbanceforest management policies in British Columbia and elsewhere.Keywords: climate change; forest disturbance; forest resilience; mid-term timber supply; stand dynamics1. IntroductionThe mountain pine beetle (MPB) (Dendroctonous ponderosae Hopkins) is part of the natural systemin British Columbia’s pine forests and it helps to maintain biological diversity and functionally healthylandscapes [1]. The MPB can be found in pine forests from western Canada to northern Mexico [2].Generally, lodgeple pine (Pinus contorta var. latifolia Engelm) is the most common host, but other pinespecies including ponderosa pine (P. ponderosa Laws), whitebark pine (P. albicaulis Engelm.), westernwhite pine (P. monticola Dougl.), limber pine (P. flexilis James), coulter pine (P. coulteri D. Don) andScots pine (P. sylvestris L.) are also suitable hosts [3]. The female beetles lay their eggs along thesides of vertical galleries they excavate in the inner bark of the mature tree. Once the eggs hatch,the beetle larvae feed on the phloem tissue of the tree and disrupt nutrient flow and eventuallystart damaging the host plant [3]. In addition, beetles are also vectors of three blue stain symbioticfungi (Grosmannia clavigera Robinson-Jeffrey & R.W. Davidson, Ophiostoma montium (Rumbold) vonArx., and Leptographium longiclavatum Lee, Kim and Breuil), which contribute to beetle success [4–6].Although MPB broods can be reared without their symbiotic fungi [7], the fungi have a positiveinfluence on the survival of beetle broods by (i) exhausting tree defenses during mass-attack [8];(ii) expediting the development of immature beetles [9]; and (iii) increasing phloem nutrients [10–12].Forests 2016, 7, 171; doi:10.3390/f7080171 www.mdpi.com/journal/forestsForests 2016, 7, 171 2 of 19Beetles usually overwinter as larvae, completing their development the following spring, pupatingin June or July, and finally the adults emerge in mid to late summer [3]. Generally large and slowgrowing trees are the preferred beetle host due to their inability to resist the establishment of adults inthe phloem layer [13,14]. Control or prevention of beetle infestation is particularly difficult as beetlesspend most of their life cycle protected under the bark [15]. However, in addition to extreme wintertemperatures (<´40 ˝C) [3], unseasonable temperatures in the early or late development stage of thebeetle could lead to high mortality [16].An outbreak is dependent on the size of the beetle population, climate and degree of susceptiblestands distributed over the landscape and stand characteristics such as species composition, diameter,age, and stand density [17]. Based on dendroecological studies, four to five MPB outbreaks occurredin BC during the last century, with an average duration of ~10 years [18,19], while in the northernRocky Mountains of the United States, MPB outbreaks occur every 20 to 40 years and typically lastfor ~6 years [20]. The rate of spread and severity of the current outbreak is the largest recordedin the history of Canada, infesting >20 million hectares of pine forest in western Canada [21,22].Climate change (winter minimum temperatures that are too warm to cause beetle larval mortality) andeffective forest management (e.g., harvest regulation, fire suppression that maintained an abundantmature pine tree population across the landscape leading to homogenous stand structures) areconsidered major factors which expedited the expansion of MPB outbreaks in BC and the spread east ofthe Rocky Mountains to boreal jack pine (Pinus banksiana Lamb.) forests [19–22]. Typically, MPB attacklarge or old individuals (diameter >20 cm or >60 years of age) of pine. However, due to the severityof the current outbreak, MPB even attacked young pine trees (diameter ď7.5 cm or ď13 years age)if no mature trees were available [23]. MPB impacts are far reaching and have undoubtedly alteredstand and landscape structure as well as having severe consequences on BC’s interior forest industry.The mid-term timber supply (portion of the timber that would be available for harvest within themiddle of the normal management cycle which is generally 30–70 years in interior BC) [24] has beenespecially affected, as well as different ecosystem services (water supply, non-timber forest, products,habitat suitability, scenic beauty, carbon storage, nutrient cycling etc.) provided by the forest [25].In spite of significant advancement in research on management of forest disturbance [3,14,17],none of this knowledge can solely mitigate the problem, and management still depends onsanitation harvesting to control infestations by removing infested trees, use of prescribed fire,insecticides (monosodium methanearsonate (MSMA)), semiochemicals, or pheromones used ontrap trees [26–28]. Unfortunately, the effectiveness of some of these direct management approaches(sanitation, insecticide, semiochemicals) does not last more than 2 years, some have a negative effect onthe environment (insecticide), and some require higher cost, skills, and labour (sanitation, prescribedfire) to implement [26,28–30]. Thus, with the high intensity of attack, management efforts wereeventually shifted to salvage logging (clear cut) operations to capture as much of the economicvalue of dead timber as possible before the wood deteriorated and may slow the spread of beetlesto other areas. While large-scale salvage logging in some areas may be an appropriate economicresponse, harvesting all the killed timber is not possible, nor is it feasible or practical, and may beunsound ecologically due to its negative impact [23,31–33]. Regardless of the choice of mitigationstrategy, forest managers must conscientiously continue to conserve forest values such as biodiversity,hydrology, soil, as well as stand structure and age class distribution [32]. The impacts of this colossaloutbreak, coupled (compounded) with large-scale salvage operations will likely lead to conditionsoutside the natural range of disturbances that these ecosystems have experienced historically [14,31,33].Information regarding the response of pine-dominated ecosystems to disturbances such as fire andharvesting is available [2,34–36]; however, it is still unclear whether stand dynamics will respondsimilarly with respect to a large-scale beetle epidemic. Therefore, understanding how MPB-attackedstands will develop and characterize the future landscape is essential for assessing the impendingimpacts on ecological and socioeconomic conditions.Forests 2016, 7, 171 3 of 19Considerable studies have been conducted to determine the post beetle stand dynamics across theMPB impacted areas in western Canada. However, this information needs to be gathered, synthesized,and presented in such way that it is widely available and understandable to managers, practitioners,and researchers alike. We have, therefore, compiled this review to describe post beetle dynamics acrossthe landscape in western Canada with an emphasis on BC. The outcome of this review will assist theinitiation of sustainable forest management policies for MPB impacted areas in BC and elsewhere.2. Stand Structure and CompositionFrom different studies, it is well documented that MPB outbreaks play an important role indirecting ecological process and the dynamics of lodgepole pine forests [1,14,23,37–40]. Moreover,beetle infestations are viewed as stand-releasing disturbances that favour the release of existingsuppressed and understory trees which then form a new forest (e.g., [1,18,39–42]). In the absenceof fire, MPB outbreaks exert widespread influence upon stand succession processes in favour ofshade tolerant or semi shade tolerant species in even-aged pine forests [1,37,39,43]. However, forestmanagement practices before (e.g., fire suppression) and after (e.g., salvage logging) beetle attack mayalso play a vital role in the composition and size structure of understory and overstory species [33].It is well established that structure and compositional development of salvage-logged (equivalentto clear cut) stands are significantly different from those of unsalvaged stands [32,44] as artificialregeneration with planting of nursery-grown tree seedlings is the basis of reforestation activity. In BC,nursery-grown tree seedlings such as lodgepole pine or hybrid spruce (Picea glauca Moench Voss ˆPicea engelmannii Parry) or subalpine fir (Abies lasiocarpa Hook. Nutt.) are used to facilitate thereforestation of salvage logged stands [45]. Stands developing from salvage-logged areas may thushave a simplified stand structure and composition as well as lower plant species richness and/ordiversity as compared to unsalvaged forest left to naturally regenerate [32,46–50].In unsalvaged stands, residual stand structure and composition play a vital role in developmentof the future forest [23,32,44]. Although the forests of central BC appear to have been devastated by themountain pine beetle, studies of residual stand structure in many locations revealed that this was notthe case for unsalvaged stands, as abundant residual green trees, regenerating saplings and seedlingsof currently acceptable commercial tree species remain in the stands [51–55]. The recruitment rate andspecies composition of new regeneration after MPB attack are variable across the landscape (differentcombinations of species and densities). Several recent studies reported successful recruitment withabundant regeneration beneath the tree layer after MPB attack [40,53–58] while others reporteda slow recruitment process with substantially lower regeneration density [1,21,59]. However,Amoroso et al. [55] concluded that ingress of natural regeneration was slow in the first few yearsafter MPB attack but there was a strong pulse of recruitment 10–20 years post disturbance. This couldbe the main the reason why some of the areas had low levels of recruitment. In addition, poor substratesand soil moisture, or availability of viable seed sources may also interrupt seedling recruitment [21,59].Considering species composition, MPB-attacked forests are undergoing substantialconversion—moving from lodgepole pine to more shade-tolerant species in most areas ofBC [43,54,55,59,60]. Shade tolerant subalpine fir and interior spruce are the most dominant understoryspecies [1,54,55,59,60] followed by low-to-moderate shade tolerant species such as lodgepole pineand Douglas-fir [1,40,61]. This implies that MPB-caused mortality results in the rapid conversion ofstands from lodgepole pine to shade-tolerant conifers (i.e., subalpine fir, interior spruce) [60,62] andaccelerates the conversion of even-aged stands to uneven-aged stands [23,37,55].3. Growth Response of Residual Live TreesDue to MPB attack, forest changes will primarily be related to species abundance, composition andcondition of residual secondary structure/trees [39,40,63]. As attacked trees die and more light reachesto the forest floor, advanced regeneration [20,64] and understory vegetation [46] display enhancedgrowth rates [42,55]. The radial growth rate depends on the amount of MPB-induced mortality [40]Forests 2016, 7, 171 4 of 19as well as the abundance and condition (vigour) of residual overstory and understory species [39,62].Previous studies suggested that enhanced radial growth of the residual overstory generally startedwithin three to five years of MPB attack [2]. Temporally, this is the grey stage of the stand (the greystage follows the red stage (needles turn red and are still on the tree) and the needles turn grey and falloff the tree). Studies showed that the residual overstory grows at rates similar to [1,39,65] or greaterthan [66] trees that have never been suppressed. After the death of larger pine trees, healthy vigorousunderstory species exhibited increased radial growth compared to healthy overstory trees, althoughthe extent of response varied among species and sites [42,55]. Generally, after the beetle attack, shadetolerant species (i.e., Douglas-fir (Pseudotsuga menziesii Mirbel. Franco); Picea glauca (Moench) Voss ˆP. englemanii Parry) demonstrated the greatest radial growth among understory species whereas shadeintolerant species (i.e., lodgepole pine, trembling aspen (Populus tremuloides Michx.)) had the bestgrowth response among overstory trees and in most cases, the degree of radial growth increasedwith increased pine mortality [42,55]. Considering the mean annual growth response, both residualoverstory and understory trees species showed variable growth responses [42,55,67] and in someinstances reached up to 400% from the pre-MPB conditions [67].Generally, MPB attacks older trees (>60 years of age) and if we consider the growth pattern ofpine trees, it reveals that peak productivity can be achieved 24–60 years after stand development anddeclines thereafter to 16%–48% of maximum values by the age of 200–350 years [68–70]. Therefore,disturbance caused by MPB “resets” the pine development to an earlier and possibly more productivestage and killed pine volume can be offset by the increased growth [42,55,67,68].4. Mid-Term Timber SupplyThe current MPB epidemic has already killed a cumulative total of 723 million m3 of pine (53% ofthe total merchantable pine volume) in BC and approximately 752 million m3 (56%) will likely bekilled by 2018, in addition to another 2% by 2023 [22]. As a result, the BC Ministry of Forests increasedthe allowable annual cut (AAC) by 14.5 million m3 from the pre-outbreak AAC level to capture asmuch economic value from the resource available as possible [71]. The AAC in some forest districts(e.g., Vanderhoof and Quesnel) has been increased more than twofold the pre-outbreak levels [72].This means timber previously allotted for logging in the coming decades is instead being harvestedover just a few years in the near term. It was anticipated that the increased AAC could last only 5to 15 years due to a gradual deterioration in wood quality (shelf life varies with climate) of beetle-killedtrees, accessibility, location, lack of milling facilities, and market conditions. With such a loss in useabletimber stock, it is inevitable that sustainable levels of harvesting will have to be adjusted downwardafter the pine beetle outbreak, especially in timber supply areas heavily dependent on pine trees.It was estimated that there will be a precipitous drop of approximately 12.6 million m3 in the provinceand approximately 75% in central BC (Prince George forest district) below pre-outbreak levels [71,73].This AAC drop is projected to last for several decades because a forest requires 60–80 years toregenerate as a mature stand. Moreover, a significant number of young lodgepole pine stands havebeen attacked as well, and they were generally considered non-susceptible to the mountain pinebeetle [72]. This implies that the pine beetle outbreak and exacerbated beetle-induced mortality andsalvage uplifts constitute a dearth of mature forest habitat and ecosystem services as well as a mid-termtimber supply decline. However, the overall impact on mid-term timber supply could be differentdepending on the management policy.Several studies have revealed that a large percentage of MPB-impacted unsalvaged stands haveenough (well-spaced, ě900 healthy stems ha´1 >4 m in height or 700 stems ha´1 >6 m in height) orbasal area (~10 m2¨ha´1) residual secondary structure (seedling, sapling and mature trees that survivedafter MPB attack) that could provide at least 150 m3¨ha´1 of timber within thirty years (mid-term) ofthe MPB attack [23,51,52,54,67]. In central BC (Prince George forest district with an estimated areaof 55,000 km2), a severely MPB impacted area, Hawkins et al. [54] reported that depending on stand age,44%–98% of attacked stands have enough secondary stand structure (sufficient stems ě 900 stem ha´1Forests 2016, 7, 171 5 of 19> 4 m height and < 7.5 cm DBH) to contribute to the mid-term timber supply. In this assessmentthey did not include residual mature trees (DBH > 7.5 cm); if these trees were included, then theoverall percentage would be much higher than indicated in the report. Similarly, Dhar et al. [67]reported that the vast majority of stands had greater, and often much greater, than 10 m2¨ha´1 basalarea of residual secondary structure (>4 cm DBH) in the post-beetle condition. This could easilyprovide mid-term timber supply within the desired time frame. In another study, Coates et al. [51]reported that only 20%–25% of stands needed some level of management intervention to achieve themid-term timber supply goal. Even though the climate in BC is exceptionally variable, for most ofthe unsalvaged stands, mid-term timber supply shortfalls may not be a large concern [51,52,54] aspreviously projected [74].The modelling approaches for the post beetle stand condition also revealed that a greatproportion of MPB attacked stands have the potential to contribute to mid-term timber supplywithout further management activities [54,75]. Different types of models such as SORTIE-ND,PrognosisBC and their hybrids are mainly used to predict the dynamics of MPB-attacked standsin BC. Among them, SORTIE-ND is intensively applied to predict future or mid-term timber supplyanalysis across BC [51,54,75–78]. Based on projections by Hawkins et al. [54], stands with a minimumof 900 stems/ha (tree > 4 m height but < 7.5 cm DBH) of residual secondary stand structure canreach minimum merchantable volumes (150 m3¨ha´1) in most of the age classes within 30 yearsafter MPB attack. A similar result was also reported by Coates [75] in central BC. In another study,Coates et al. [51] indicated that stands with healthy, vigorous, and well-spaced advanced regenerationmay develop rapidly following MPB attack and can contribute harvestable volumes of 200–300 m3¨ha´1within 25–40 years, which is greater than target timber production (150 m3¨ha´1) for MPB-infectedstands in BC. Similarly, Pousette [78] showed that a significant number of MPB killed stands incentral BC can contribute mid-term merchantable timber within 30 years of MPB attack. In an earlierstudy Coates and Hall [76], suggested that after MPB-induced pine mortality, residual spruce inwell-stocked stands with good basal area recovered to pre-attack basal areas within 50 years in two offour experimental stands in BC. For both mature and immature stands, Runzer et al. [77] suggestedthat the best option for MPB-impacted stands would be to allow the stand to develop naturally withoutintervention and harvest them to assist with mid-term timber supply. Likewise, field inventoriesalso suggested that a significant number of MPB-attacked stands have the potential to contribute tomid-term timber supply without further management. Moreover, retention of stands with suitableresidual stems can shorten rotation age greatly [52] compared to starting a new plantation after logging.Finally, it has been recommended that if there is a need to continue salvage logging, then thosestands which do not meet the mid-term timber supply minimum volume requirement should beselected and stands or portions of stands that will be economically viable through the mid-term shouldbe retained [52]. This could be accomplished using partial cutting, by selectively logging the dead anddying pine from mixed stands. Leaving economically viable trees such as Douglas-fir or clumps ofspruce and fir can compensate for a portion of mid-term timber in the decades after the pine is gone.However, the challenge after catastrophic forest disturbances is to strategically assess what shouldand should not be harvested in the short and medium terms. The goal is to create the most favourabletimber supply and habitat supply forecast possible where management decisions come from integratedapproaches by considering ecological, economical and societal values.5. Forest FireGenerally, it is hypothesized that MPB-induced tree mortality affects fire behavior by alteringthe flammability, continuity, and structure of fuels [79–82]. Moreover, the fuel profile such as surface,ladder, and crown fuels are expected to change with time since outbreak, potentially altering firebehavior and fire risk. After tree death, needles fade to red within a year of attack (red stage) andrisks of ignition, torching, and canopy fire are expected to increase due to lower leaf moisture content(10 times lower in foliar moisture content compared to green needles), non-fiber carbohydrates andForests 2016, 7, 171 6 of 19fats, which increase flammability [83,84]. Approximately 3 to 10 years (gray stage) after the beetleattack, trees drop their needles and twigs and become exposed in the upper crown [81], which likelyincreases the forest floor fuels [81,82]. Therefore, it is expected that surface fires will be more likelyto spread into the canopy during the gray stage [85] and salvage logging is a recommended methodof forest management to reduce the fire hazard [80–82]. However, MPB and its impacts on fuelaccumulation and subsequent fire hazard are poorly understood: some studies have suggested higherprobability or severity of fire following beetle outbreak [66,79,80], while others suggest a decreasedfire probability [2,86], or no evidence of any relationship between MPB and active fire [34–36,87–89].Based on an extensive literature review, Jenkins et al. [80] concluded that both rates of fire spread andfire-line intensities were higher in the current outbreak’s stands than in endemic stands. Similarly,Lynch et al. [79] reported that MPB mortality in the mid-1970s increased the odds of burning in 1988by 11% over unaffected areas in Yellowstone National Park, USA, whereas Alfaro et al. [2] suggestedthat there was no significant relationship in the frequency of beetle outbreak related to fire frequencyin BC and they also found a positive relationship between MPB attack severity and less frequent fire.Similarly, Simard et al. [86] reported that the MPB outbreak in Greater Yellowstone may reduce theprobability of active crown fires in the short term (up to 35 years after a beetle outbreak) by thinninglodgepole pine canopies. Likewise, a recent study in western USA claimed that the observed effectof MPB infestation on the area burned in 2002–2013 appears negligible at broad spatial extents [36].Meigs et al. [89] claimed that following MPB outbreak, fire likelihood is neither higher nor lower thanin non-MPB-affected forests in the Pacific Northwest of USA. Many studies emphasize the importanceof climate rather than fuels as the primary driver of wild fires [34,35,87,90]. According to these studies,weather conditions such as extremely dry, gusty conditions with a sustainable ignition event andtopography are the main driving factors in the occurrence of forest fire as opposed to MPB. There isthus no clear conclusion about the interaction of MPB-induced mortality and forest fire, and the debatepersists. Further comprehensive study is required to answer this question by keeping in mind that thescience of fire behaviour is very complex as many factors can influence how a fire will act and thereare a number of unknowns when it comes to predicting fire behaviour in MPB infested stands.6. Carbon DynamicsEmpirical and theoretical evidence suggests that MPB disturbances may not necessarily decreasecumulative carbon (C) productivity (i.e., total productivity over multiple years to decades). In fact,intermediate- severity disturbances (e.g., MPB) may accelerate, maximize, or even regulate ecosystemcycling and production [66,91,92]. However, there is ongoing debate about the impact of MPB oncarbon dynamics due to the variability in research findings among the different studies [93–100].Some studies reported that the MPB outbreak has a direct impact on carbon dynamics as tree mortalityreduces the rate of forest carbon uptake and increases future emissions by excessive heterotrophicrespiration and thus forests are being converted from net carbon sinks to carbon sources [93–95,101].According to Kurz et al. [94], net greenhouse gas production over 21 years will be 990 Mt carbondioxide equivalents (CO2e) in MPB-impacted areas in BC, which will affect the carbon dynamicsand exacerbate global climate change. A similar observation was also reported by Foley et al. [93].However, flux tower-based observations and recent modelling conclude that MPB-killed forests are notchanging from net carbon sinks to net carbon sources [96,97,102,103]. In fact, the healthy residual treesin MPB killed stands are sequestrating carbon at higher rates due to the rapid change of forest structureand composition [96,99–102]. Based on a recent study, Arora et al. [103] estimated that the currentMPB outbreak in BC's forests could accumulate 328 Mt less carbon by 2020 while changing climateand increasing atmospheric CO2 concentration could enhance carbon uptake equal to a cumulativesink of around 900–1060 Mt C, which is almost three times higher than the total loss. A comparableresult has also been reported from field-based growth dynamics studies [42,55,67]. All of these studiesreport that residual tree species showed enhanced radial growth after beetle attack, leading to rapidcarbon uptake by the residual tree species that compensates for losses due to tree mortality. Therefore,Forests 2016, 7, 171 7 of 19it can be suggested that the overall MPB impact on carbon dynamics is not as severe as previouslypredicted [93–95]; in fact, frequent moderate-severe MPB disturbances may stimulate C productivityof the forest stands [68,103].7. Species Range ExpansionClimate change projections predict that a large portion of BC’s central interior is expected tobecome drier while the northeastern portion is projected to become wetter [104]. This will influencespecies’ geographic ranges, with species shifting northward and to higher elevations as well asimpacting primary ecosystem processes like succession and disturbance [105]. The current climaticchange projections suggest that many BC tree species’ (i.e., Larix occidentalis Nutt., natural hybridsof Picea englemannii and Picea gluca; Abies lasiocarpa (Hooker) Nuttall, Tsuga heterophylla (Raf.) Sarg.,Thuja plicata Donn ex D.Don) distributions are predicted to shift their geographic ranges and some ofthese species are already found in the understory of MPB-impacted pine dominant forests [104,105].MPB outbreaks may facilitate the shift of geographic distribution for those species by opening gaps inthe forest canopy and breaking the “biological inertia” [106] of the mature pine trees that have beenin holding for a long time. This opening of the canopy thus potentially permits the establishmentof climatically better adapted trees present in the understory layer. Although such species could,in theory, be planted after salvage logging as a means of assisting range shifts, knowing which speciesto plant would require considerable research effort.8. BiodiversityThe current MPB outbreak has direct impact on species richness and diversity for understory andherbaceous flora and fauna, [46,54,55,60,107–109] as MPB-caused mortality emulates a thinning fromabove, which allows more growing space (light, water, nutrients, etc.) for understory vegetation [43].Details of MPB impact on vegetation diversity are discussed in the species composition and ecosystemresilience sections of this manuscript; thus, this section only treats the impact of MPB outbreaks onwildlife species. Various studies have revealed that MPB outbreaks have either direct (altering foodand forage availability), indirect (altering habitat suitability), or mixed impacts on wildlife [110–112].According to Martin et al. [111], bird species richness did not decline in stands having up to60% pine mortality but showed a strong negative impact when mortality exceeded 75% [113].Drever et al. [114], however, reported that the percent of red-attacked pines positively correlated tospecies richness of woodpeckers and negatively correlated to richness of other forest birds. In anotherstudy, Walters et al. [115] found that the abundance of tree sap eater migratory northern flickers(Colaptes auratus L.) and red-naped sapsuckers (Sphyrapicus nuchalis B.) decreased in MPB-killedstands. Similarly, Bonnot et al. [116] reported that wildlife species that depend on the forest covershowed less abundance when the dead trees drop their foliage. On the contrary, the occurrenceand abundance of shrub species are strongly associated with abundance of many small mammalssuch as Trowbridge’s shrew (Sorex trowbridgii B.) and Pacific water shrew (S. bendirii M.) [115] andwell as with ungulate species that browse the new growth. Lastly, the management response toan MPB-impacted stand will also affect fauna. Salvaged stands, for example, will lose significantunderstory structure, modifying forage availability and habitats. Impacts of salvage logging alsoextend to the aquatic environment, causing increased sedimentation of rivers, modified flow regimes,and increased water temperatures. All of these impacts have been shown to affect fish habitat andspawning grounds [117–120]. Fully documenting the response of flora and fauna to MPB outbreaks andsubsequent management interventions would require detailed and long-term studies across differentgeographic locations.9. Ecosystem ResilienceEcological resilience is the capacity of an ecosystem to maintain its identity, functions,and processes after disturbance [121]. Resilience of managed forest ecosystems can be enhancedForests 2016, 7, 171 8 of 19by management actions that maintain the complexity of forest structure and dynamics from thestand to landscape scale [122,123]. Natural disturbances, when they occur within the natural range ofvariation for a particular ecosystem, serve to increase forest complexity by creating stand and landscapescale heterogeneity and can thus promote forest resilience. Forest management and harvestingthat create patchy mosaics of even-aged stands can also contribute to landscape scale heterogeneity,while selective harvesting, for example, can lead to stand scale heterogeneity. Such interventions,that promote complex forest structure, may increase forest resilience to disturbance and environmentalchange [123]. However, management actions such as large-scale replanting of a single species or firesuppression, as well as unprecedented levels of natural disturbance, can also serve to greatly reduceforest complexity, by simplifying forest structure at stand or landscape scales, thus reducing resilience.The adaptive cycle (Figure 1) provides a conceptual model of ecosystem reorganisation and growthfollowing disturbance. As an ecosystem moves through this cycle, it is more or less resilient at differentphases. We will use this model to describe how the combined effects of MPB-caused disturbance andmanagement can influence forest ecosystem resilience.Lodgepole pine is a disturbance-adapted species that persists in landscapes despite repeatedMPB outbreaks and wildfire [124]. Compared to stand-replacing disturbances (e.g., wildfire),MPB outbreaks are intermediate (generally 30%–50% mortality) disturbances that leave substantialsecondary stand structure [14,54,124]; thus, under post MPB conditions, forest recovery proceedsrelatively quickly. If beetle-impacted stands are managed by salvage logging then a significantalteration occurs in the backloop of the ecosystem reorganization phase (α) of the adaptive cycle,potentially shifting the system to a less resilient state (pathway A in Figure 2). A combination ofMPB attack and salvage logging diminishes the capacity for re-establishment of pre-disturbancecommunities, affects biogeochemical and hydrological processes, and develops a homogeneouslandscape structure and composition [23,32,44,105]. In addition, salvage logging after MPB attack alsonegatively affects water quality, aquatic habitats and soil erosion [23,117,125–127]. Impairment ofecosystem recovery is one of the important ecological consequences of MPB-impacted salvage-loggedforests. After disturbance, large ecological legacies can remain, which play crucial roles in ecosystemrecovery and influence ecosystem processes for decades or centuries [128,129]. Salvage logging afterdisturbance (e.g., MPB attack) removes most of the biological legacies from the system, which leads tofurther damage of an already disturbed ecosystem [32]. The organisms in such a system may becomemaladapted due to interactive effects of two simultaneous disturbances (e.g., beetle attack and salvagelogging) [32]. Moreover, salvage logging creates a homogeneous landscape structure and compositionand a reduction in plant species richness and/or diversity [47–50]. As in most cases post logging(after timber harvest), stand recovery is facilitated through artificial regeneration with planting ofnursery-grown tree seedlings. In the long run, such uniform landscapes are typically less resilientto disturbances and often experience more pest outbreaks than natural heterogeneous and complexforests [130–132]. In addition, any disturbance initiated in one part of a homogeneous landscape caneasily be transmitted to other parts under favourable environmental conditions and can devastatethe whole landscape [133,134]. Conversely, after natural disturbance, unsalvaged stands create aheterogeneous landscape structure with a mosaic of even-aged and uneven-aged patches [43,135].These heterogeneous forests can recover faster than the salvage-logged stands as a significant portionof biological legacies (e.g., surviving trees, snags and logs, patches of intact vegetation, seedbanksin tree crowns or in the soil) of that particular ecosystem remain intact [136–138]. This allows theforest to remember its genetic, compositional and structural pre-harvest condition to build a newcomplex ecosystem [139], which, due to its increased heterogeneity, may be more adaptable to achanging climate and less susceptible to future disturbances [32,140]. Lastly, organisms are typicallybest adapted to the disturbance regimes under which they evolved [141,142]. Diverse and spatiallyheterogeneous natural systems are thus more resilient than homogeneous systems by providingsupport for all functional groups (pollinator, primary producers, herbivores etc.) and persistence ofecological function over time [143,144] (pathway B in Figure 2).Forests 2016, 7, 171 9 of 19MPB-caused mortality increases diversity and complexity of the forests [46,54,55,60,107–109],which can be explained within the “intermediate disturbance hypothesis” whereby the highest speciesdiversity can be achieved at intermediate rates and intensity of disturbance [145]. Under suchconditions, ecosystems tend to have a mixture of pioneer and climax species [32], which makes theforest more diverse, complex and stable by including more pathways of energy flow [146]. In a recentstudy, Pec et al. [108] mentioned that understory community diversity and productivity increasedacross a gradient of increasing pine tree mortality. A similar observation was also reported by Stoneand Wolfe [46] in northern Utah and Kovacic et al. [107] in eastern Colorado. In another study, Perovichand Sibold [60] reported that stands with MPB outbreak had greater diversity in age classes and speciescomposition. In addition, natural disturbances generate tremendous amounts of dead wood, whichcan be used as habitats for many saproxylic (i.e., organisms that depend, during at least part oftheir life cycle, upon the dead or dying wood of moribund or dead trees, or upon other saproxylicorganisms) species [147]. Based on a study by Müller et al. [148], European spruce bark beetle(Ips typographus) infestations improved the habitat of several endangered saproxylic beetles. In manycases, the presence or abundance of saproxylic species are used as bio-indicators of sustainable forestmanagement [149,150] and positive indications of forest resilience. Dead wood can also significantlycontribute to soil development by increasing soil fertility of poor sites [151]. In addition, removing deadtrees by salvage logging is directly linked to soil drying and compaction, which alters the understoryplant species composition, abundance and richness [47].Forests 2016, 7, 171 9 of 18 and species composition. In addition, natural disturbances generate tremendous amounts of dead wood, which can be used as habitats for many saproxylic (i.e., organisms that depend, during at least part of their life cycle, upon the dead or dying wood of moribund or dead trees, or upon other saproxylic organisms) species [147]. Based on a study by Müller et al. [148], European spruce bark beetle (Ips typographus) infestations improved the habitat of several endangered saproxylic beetles. In many cases, the presence or abundance of saproxylic pecies are used as bio‐indicators of ustainable forest management [149,150] and positive indications of forest resilience. Dead wood can also significantly contribute to soil development by increasing soil fertility of poor sites [151]. In addition, removing dead trees by salvage logging is directly linked to soil drying and compaction, which alters the understory plant species composition, abundance and richness [47]. Figure 1. Adaptive cycle of a complex adaptive system. The arrows indicate the speed of change in the cycle: short, narrowly spaced arrows indicate slow change while long arrows indicate rapid change. The exit from the adaptive cycle at the left suggests where in the cycle the potential of the system can leak away and where a switch into a system with lower productivity and organization is most likely to occur. “r” denotes growth and exploitation of abundant resources, “K” denotes conservation, competitiveness, niche specialization for stabilization, “Ω” denotes release and new opportunities through disturbance, and “α” denotes recovery through reorganization (adapted from [121]). The pathway that a forest ecosystem follows in the adaptive cycle after an MPB outbreak is thus highly dependent on the nature and intensity of management interventions. Too much salvage logging can lead to a system of greatly decreased resilience (Figure 2, pathway A) and thus increased susceptibility to future disturbances. Many authors have argued that this is one of the main reasons why the current MPB outbreak is in an epidemic stage in Canada [105]. Due to previous forest management policies, most of the MPB impacted Canadian pine forests were even‐aged and homogenous in structure [22,43,44,152,153]. This relatively homogenous landscape, in conjunction with warming climates (warmer summer, mild winter), allowed the beetle population to spread exponentially. Present‐day post‐beetle forest management by salvage logging should thus seek to minimize such future disturbance events by, for example, planting a greater heterogeneity of species. Pathway B in Figure 2 represents an alternative and more resilient future forest. This forest is diverse, heterogeneous in spatial and vertical structure, maintains the memory of biological legacies, and Figure 1. Adaptive cycle of a complex adaptive system. The arrows indicate the speed of change in thecycle: short, narrowly spaced arrows indicate slow change while long arrows indicate rapid change.The exit from the adaptive cycle at the left suggests where in the cycle the potential of the systemcan leak away and where a s itch into a system with lower productivity and organization is mostlikely t occur. “r” denotes growth and exploitation of abundant resources, “K” d notes conservation,competitiveness, niche specialization for st bilization, “Ω” den tes release and n w opportunitiesthrough disturbance, and “α” denotes recovery through reorganization (adapted from [121]).The pathway that a forest ecosyste follows in the adaptive cycle after an MPB outbreak isthus i ly ependent on the nature and intensity of m nag me t int rve tions. Too much salvageloggin can lead to a system of greatly decrease lience (Figure 2, pathway A) and thus increasedsusceptibility to future disturbances. Many authors have argued that this is one of the ai whythe current MPB outbreak is in an epidemic stage in Canada [105]. Due to previous forest managementForests 2016, 7, 171 10 of 19policies, most of the MPB impacted Canadian pine forests were even-aged and homogenous instructure [22,43,44,152,153]. This relatively homogenous landscape, in conjunction with warmingclimates (warmer summer, mild winter), allowed the beetle population to spread exponentially.Present-day post-beetle forest management by salvage logging should thus seek to minimize suchfuture disturbance events by, for example, planting a greater heterogeneity of species. Pathway B inFigure 2 represents an alternative and more resilient future forest. This forest is diverse, heterogeneousin spatial and vertical structure, maintains the memory of biological legacies, and supports a rangeof ecological processes that are connected across scales of space and time. Such a complex forestis more capable of system-level adaptation and re-organisation in response to future disturbances.Post-MPB outbreak management should seek to promote this complexity from the stand to thelandscape scale.Forests 2016, 7, 171 10 of 18 supp rts a range of ecological processes that are connected across scales of space and time. Such a co plex forest is more capable of system‐level adaptatio and re‐organisation in response to future disturbances. Post‐MPB outbreak management should seek to pr ote this c plexity from t e stand to the landscape scale. Figure 2. Adaptive cycles of MPB‐impacted lodgepole pine forests through the lens of forest management policy. Less resilient forest stands can develop if salvage logging is used as a means of forest management (Pathway A), while more resilient forest stands can be developed in the absence of salvage logging (Pathway B). 10. Conclusions The current MPB outbreak in BC crosses ecological, social and economic boundaries and its management goes beyond insect management. However, this literature review suggests that (i) a significant percent of residual secondary trees survived the beetle attack, (ii) stands in the current epidemic area appear to be recovering rapidly and in most cases can significantly contribute to mitigating the loss of mid‐term timber supply, (iii) the occurrence of the MPB epidemic has resulted in more structurally and compositionally diverse forest stands, (iv) MPB‐caused tree mortality may accelerate some tree species’ geographic range expansion resulting from changing climatic conditions and (v) a comparatively small percentage of unsalvaged stands require management intervention for achieving mid‐term timber supply goals. In addition, MPB‐impacted, unsalvaged stands are likely to be more complex and heterogeneous in structure and, therefore, more ecologically resilient than stands developed following salvage logging. It is also critical that abundant numbers of live and dead standing trees be retained for wildlife habitat, and that forest understories are protected to allow rapid recovery and readjustment of the ecosystem [105]. Moreover, this new dimension of forest structure opens up the opportunity to design forests that are more diverse and more resilient to climate change, pest outbreaks and other unforeseen challenges that are sure to follow [123]. Post‐beetle management should seek to reconcile social, ecological and economic objectives, retaining a patchwork of the best residual stands at the landscape scale, combined with salvage logging if necessary in stands where economic and ecological recovery objectives can best be met using this approach. However, ecological and economic impacts of the current mountain pine beetle outbreak need not be considered an unmitigated disaster. It is evident that lodgepole pine forests (at the stand and landscape level) in BC have experienced similar or even multiple outbreaks in the past and have naturally recovered over a short period of time [1,40]. We recommend the adoption of an ecosystem Figure 2. Adaptive cycles of MPB-impacted lodgepole pine forests through the lens of forestanage ent policy. Less resilient forest stands can develop if salvage logging is used as a eans offorest management (Pathway A), while more resilient forest stands can be developed in the absence ofsalvage logging (Pathway B).10. ConclusionsThe cu rent MPB outbreak in BC cros es ec logical, soci l and economic boundaries andits management go s beyo d insect management. However, this literature review suggests th t( ) a s gnificant percent of residual secondary trees survived the be tle attack; (ii) stands in the currentepide ic area appear to be r c ering ra idly and i st c ses i ific tly c tribute toitigating the loss of id-ter ti ber supply; ( i) the occurrence of the PB epide ic has resultedin ore str ct ra ly a c ositiona ly diverse forest stands; (iv) PB-caused tree ortality ayaccelerate so e tree species’ geographic range expansion resulting fro changing cli atic conditionsan (v) a co paratively s a l percentage of unsalvaged stands require anage ent intervention forachie i i -ter ti er s l goals. In addition, PB-i pacted, unsalvage stands are likely tobe co plex and het rogeneous in struct re and, therefo , more ecologically resilient tha standsdevelop d following salva e logging. It is also critical tha abundant numbers of liv and dead standingtrees be retained for w ldlife habitat, and tha forest understories are p otect d to allow rapid recoveryand readjustment of the eco yst m [105]. Moreover, this new dim nsion of forest structure pens up theForests 2016, 7, 171 11 of 19opportunity to design forests that are more diverse and more resilient to climate change, pest outbreaksand other unforeseen challenges that are sure to follow [123]. Post-beetle management should seek toreconcile social, ecological and economic objectives, retaining a patchwork of the best residual standsat the landscape scale, combined with salvage logging if necessary in stands where economic andecological recovery objectives can best be met using this approach. However, ecological and economicimpacts of the current mountain pine beetle outbreak need not be considered an unmitigated disaster.It is evident that lodgepole pine forests (at the stand and landscape level) in BC have experiencedsimilar or even multiple outbreaks in the past and have naturally recovered over a short period oftime [1,40]. We recommend the adoption of an ecosystem service-based, integrated forest managementpolicy that seeks to maintain forest complexity and resilience from stand to landscape scales (see forexample: [44,123,154]). Lastly, management decisions should be made using a combination of the bestavailable data, local knowledge, professional judgment, and long term cost-benefit assessments thattake into account the state of the future forest as well as the realization that MPB is an integral part ofpine forest ecosystems in BC and most of its range.Acknowledgments: This research was supported by a grant to Lael Parrott from the Natural Science andEngineering Research Council of Canada (grant No. NET GP 434810-12) to the TRIA Network, with contributionsfrom Alberta Agriculture and Forestry, Foothills Research Institute, Manitoba Conservation and WaterStewardship, Natural Resources Canada—Canadian Forest Service, Northwest Territories Environment andNatural Resources, Ontario Ministry of Natural Resources and Forestry, Saskatchewan Ministry of Environment,West Fraser and Weyerhaeuser. We also thankful to two anonymous reviewers for their constructive suggestionsthat greatly improved the overall manuscript.Conflicts of Interest: The authors declare no conflict of interest.References1. Axelson, J.; Alfaro, R.; Hawkes, B. Influence of fire and mountain pine beetle on the dynamics of lodgepolepine stands in British Columbia, Canada. For. Ecol. Manag. 2009, 257, 1874–1882. [CrossRef]2. Alfaro, R.I.; Campbell, E.; Hawkes, B.C. Historical Frequency, Intensity and Extent of Mountain Pine BeetleDisturbance in British Columbia; MPB Working Paper 2009-30; Natural Resources Canada, Canadian ForestService, Pacific Forestry Centre: Victoria, BC, Canada, 2010; p. 52.3. Safranyik, L.; Carroll, A.L. The Biology and Epidemiology of the Mountain Pine Beetle in LodgepolePine Forests. The Mountain Pine Beetle: A Synthesis of Biology, Management, and Impacts on Lodgepole Pine;Safranyik, L., Wilson, B., Eds.; Natural Resources Canada: Victoria, BC, Canada, 2006; pp. 3–66.4. 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Aftermath of Mountain Pine Beetle Outbreak in British Columbia: Stand Dynamics, Management Response and Ecosystem Resilience
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