Forest Ecology and Management 341 (2015) 8ndash17

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Forest Ecology and Management

journal homepage wwwelsevier com locate foreco

Permanent forest plots show accelerating tree mortality in subalpineforests of the Colorado Front Range from 1982 to 2013

httpdxdoiorg101016jforeco2014120310378-1127 2015 Published by Elsevier BV

uArr Corresponding author at Dept of Geography University of Nevada RenoMailstop 0154 Reno NV 89557 United States

E-mail address jmsmithcoloradoedu (JM Smith)

Jeremy M Smith auArr Juan Paritsis ab Thomas T Veblen a Teresa B Chapman a

a Department of Geography University of Colorado Boulder CO 80309-0260 United Statesb Laboratorio Ecotono INIBIOMA CONICETndashUniversidad Nacional del Comahue 8400 Bariloche Argentina

a r t i c l e i n f o a b s t r a c t

Article historyReceived 7 August 2014Received in revised form 24 December 2014Accepted 28 December 2014

KeywordsClimate changeDroughtForest demographyPermanent plotsTree mortality

Broad-scale studies have documented widespread increases in tree mortality coincident with warming inthe western USA but variability in patterns and agents of mortality is poorly documented based onmulti-decadal observations of permanently marked trees particularly in Rocky Mountain subalpineforests The current study examines temporal variability in tree mortality based on monitoring gt5000permanently marked trees across a range of topographic positions and stand ages from c 120 togt550 years over a 31-year period in subalpine forests in the Colorado Front Range This study documentsaccelerating rates of annual tree mortality for subalpine fir Engelmann spruce lodgepole pine and lim-ber pine from 1982 through 2013 Over the period from 1982 to 2013 annual mortality rates for all treespecies combined increased from 036 to 103 in old stands (265 to gt550 years since stand-initiatingfires) and from 030 to 072 in young stands (120 years since fire) Tree populations at sites oftopographically moister locations and where competition was less due to presence of canopy openingsexperienced initially lower rates of tree mortality but all populations experienced higher mortality ratesafter c 2008 In comparison with the 1953ndash1994 period the frequency of extreme high temperatures inearly summer increased after the mid-1970s and more markedly after 2000 Over time the contributionof early summer (July) conditions to annual drought has increased This pattern of climatic variability hasbeen coincident with and conducive to a two and a half fold increase in the average annualized tree mor-tality rates for the total tracked tree population from the relatively cool and wet 1982ndash1994 period to thewarmer and drier 2008ndash2013 period Tree mortality attributable to bark beetles over the 1982ndash2013period was minor except for western balsam bark beetle (Dryocoetes confusus) which since 2008 hasaccounted for about 12 of the subalpine fir deaths Overall our findings indicate that even in the absenceof lethal bark beetle outbreaks conifer mortality apparently associated with moisture stress has recentlyincreased in subalpine forests in the Colorado Front Range

2015 Published by Elsevier BV

1 Introduction

Late 20th and early 21st century increases in tree mortalitymanifested either as gradual increases in background tree mortal-ity rates or pulses of forest die-off have been widely documentedacross the western USA and associated with rising regional tem-peratures (van Mantgem et al 2009 Williams et al 2013)Although broad-scale studies clearly document widespreadincreases in tree mortality with warming the relative roles ofbiotic agents and rising temperatures is still poorly understoodThe linkage of tree mortality to temperature is based on twonon-mutually exclusive suites of mechanisms (1) increasing

physiological damage (sensu Anderegg et al 2013) due to greaterwater deficits under higher temperatures in habitats where treegrowth and survival is limited by water availability (Breshearset al 2005 Williams et al 2013) and (2) temperature-inducedincreases in the populations and lethality of insects and pathogensthat kill trees (Raffa et al 2008 Hicke et al 2006) The latter suiteof mechanisms includes both the directly favorable effects of war-mer temperatures on insect populations such as Dendroctonus barkbeetles and reduction in host tree defenses under diminishedwater availability to trees (ie predisposition of trees to lethalinsect attack Raffa et al 2008) Despite important advances inunderstanding the physiology underlying drought-induced treedeath (reviewed by Anderegg et al 2012) and the effects of tem-perature on reproductive rates and survivorship of insects lethalto trees (reviewed by Bentz et al 2010) the ecological and climaticcontexts that result in different patterns of tree mortality across a

JM Smith et al Forest Ecology and Management 341 (2015) 8ndash17 9

range of tree species remain poorly documented Relatively fewstudies identify evidence of lethal agents at the level of the individ-ual tree (Das et al 2011) in contrast to numerous broad-scalestudies that document pulses of tree mortality from aerial observa-tions of stands where mortality mechanisms at the tree-level aredifficult to ascertain (Williams et al 2013)

Since the mid-1990s the forests of Colorado have experiencedprofound pulses of tree mortality coincident with warmer temper-atures and episodes of reduced precipitation that have affected allthe common tree species of the subalpine forests (Bigler et al2007 Worrall et al 2010 Colorado State Forest Service 2012)Sudden and massive mortality of conifers since the mid-1990s inColorado is well documented in relation to outbreaks of bark bee-tles primarily mountain pine beetle (MPB Dendroctonus pondero-sae) affecting lodgepole pine (Pinus contorta) limber pine (Pinusflexilis) and ponderosa pine (Pinus ponderosa) and spruce bark bee-tle (SBB Dendroctonus rufipennis) affecting Engelmann spruce(Picea engelmannii) (Chapman et al 2012 Colorado State ForestService 2012) Less well documented is the extensive mortalityof subalpine fir (Abies lasiocarpa) attributed to western balsam barkbeetle (WBBB Dryocoetes confusus Negron and Popp 2009Colorado State Forest Service 2012) Increases in background treemortality in the absence of evidence of bark beetle infestationare also evident in subalpine forests in Colorado (Bigler et al2007 van Mantgem et al 2009 Anderegg et al 2014)

The influences of warming temperatures and increased waterdeficits are likely to vary across coarse-scale gradients of moistureavailability related to precipitation elevation and local topo-graphic position For example modeling of the drivers of tree mor-tality rates in coniferous forests in Californiarsquos Sierra Nevadamountain range indicates that mortality is best explained by waterdeficit in water-limited (low-elevation) forests whereas favorableeffects of warmer temperatures on mortality rates in energy-limited (high-elevation) forests implies a greater role for insect-caused tree death in those forests (Das et al 2013) At a coarsespatial scale in mountain ranges where the higher elevations arerelatively humid a simple elevation-based dichotomy betweenwater-limited and energy-limited forests is practical but in manyhigh elevation forest habitats in the western USA dry conditionslimit tree growth For example tree radial growth sampled across25 widely dispersed sites at elevations of 3000ndash3350 m in the sub-alpine forests of the Colorado Front Range showed contrastingresponses to annual variability in moisture availability accordingto local topographic positions from xeric to mesic and hydric siteconditions (Villalba et al 1994) The dominant response patternwas one of reduced tree growth at xeric sites in conjunction withwarmer temperatures (Villalba et al 1994) Analogously a 9-yearrecord (1999ndash2007) of continuous eddy flux observations at a siteof c 105 year old conifers at 3050 m forest in the Colorado FrontRange showed that longer growing season length resulted inreduced net ecosystem productivity (NEP) and that the negativeimpact of an earlier start of spring on annual NEP was due to treegrowth dependence on snowmelt water through most of the grow-ing season (Hu et al 2010) Water deficits resulting from reducedsnow packs and earlier spring snowmelt limit NEP in subalpine for-ests of the Front Range and potentially may lead to elevated ratesof tree mortality Thus in the current study we examine tree mor-tality patterns in relation to climate variability including timingand severity of monthly water deficits from 1982 to 2013 acrossa range of different topographic settings affecting soil moistureavailability in the subalpine zone of the Colorado Front Range

Attributing regional trends in tree mortality to climate changerests on the un-tested assumption that the effects of climatechange are the same for young and old forests (Luo and Chen2013) In some studies decadal-scale changes in tree mortalityhave been attributable to stand development processes and are

not necessarily driven by climate change (Lutz and Halpern2006 Thorpe and Daniels 2012) In old forests however tree mor-tality is often assumed to be in an equilibrium state in which it ismatched by recruitment implying that the effects of endogenousprocesses on mortality rates are weak so that changes in ratesshould reflect climate change (Luo and Chen 2013) While theexistence of an equilibrium between mortality and recruitmentin old forests has long been a contested assumption in forest ecol-ogy (Connell and Sousa 1983 Veblen 1992) a recent study of treemortality in boreal forests in Canada documented higher climate-change driven increases in mortality rates in young compared toold forests (Luo and Chen 2013) Thus in the current study weexamine mortality rates for stands of different successional statusand ages ranging from c 120 to gt550 years

Key to understanding the pathways linking tree mortality todrought is recognition that lsquolsquonot all droughts are created equalrsquorsquo(Anderegg et al 2013) in terms of severity seasonality timingand relative contributions of higher temperature and reduced pre-cipitation In the current study we take advantage of the long-termmonitoring of climate at stations near (mostly within 100ndash2000 m)the monitored tree populations to examine associations of mortal-ity patterns with local climate variability based on a range ofmonthly to annual drought measures as well as daily extremes ofhigh summer temperatures In particular given previous researchin the study area linking reduced NEP to earlier start of spring overthe 9-year period from 1999 to 2007 (Hu et al 2010) we soughtevidence of a shift towards earlier dates of high temperaturesand water deficits in late spring and summer

In the current study we report the results of monitoring treemortality from 1982 to 2013 in 40 permanent plots containinggt5000 permanently marked trees in subalpine forest near theUniversity of Colorado Mountain Research Station in Arapaho-Roosevelt National Forest The stand by stand analyses applied inthe current study allow consideration of how stand compositionage successional status and topographic position may influencethe effects of climate variability on tree mortality The researchreported here addresses the following three questions (1) Howhave tree mortality rates for the four common conifer species inthese forests changed over this 31-year period in relation to annualto decadal-scale climate variability (2) What are the relative con-tributions of biotic agents (insects and pathogens) versus abioticfactors (ie water stress) to the observed patterns of tree mortal-ity (3) Do the observed tree mortality patterns and relations withclimatic variation differ according to site factors (ie topographicposition) and stand attributes (ie stand age composition andsuccessional status)

2 Methods

21 Study area and site selection for permanent forest plots

The study took place in Arapaho-Roosevelt National Forestlocated on the eastern slope of the Colorado Front Range The FrontRange is a fault block range which trends northndashsouth along themargin of the Great Plains to the east and is bordered by severalranges of the Rocky Mountains to the west The majority ofprecipitation falls as snow in winter and spring due to westerlyairflow though storms also result from easterly cyclonic flow orsummer convective activity and move upslope from the plains(Greenland 1989) Average annual precipitation is approximately700 mm most of which occurs as snow Mean average annual tem-perature is around 17 C and ranges from a maximum annual aver-age of 31 C to a minimum annual average of 09 C (C-1 climatedata 1953ndash2012) Soils in the study area are derived from glacialtill and primarily consist of loamy-skeletal cryoboralfs though

10 JM Smith et al Forest Ecology and Management 341 (2015) 8ndash17

more organic cryohemist soils are found at poorly-drained sites(Veblen 1986a)

Tree data are based on monitoring of 40 permanent forest plotsinstalled in the early 1980s in an area of subalpine forest near theCU Mountain Research Station and Niwot Ridge Biosphere Reservein Arapaho-Roosevelt National Forest (Fig 1 Table 1 Appendix ASupplementary Material) Data from three of these 40 plots wereutilized in the western North American tree mortality data synthe-sis of van Mantgem et al (2009) Dominant tree species in the plotsare limber pine (P flexilis) lodgepole pine (P contorta var latifolia)subalpine fir (A lasiocarpa) and Engelmann spruce (P engelmannii)Quaking aspen (Populus tremuloides) is also present in low abun-dance in three of the plots

Plot installation began in 1982 and was guided by the goal ofincluding a maximum range of stand ages and topographic posi-tions while excluding sites with any history of logging (Veblen1986a) Ten large plots (c 50 50 m) were installed in 1982ndash83(7 plots) and 1986 (3 plots) and each contain an average of over400 permanently tagged and mapped living and standing dead

Fig 1 Map of the study area showing the location of permanent plots in the vicinity oCounty Colorado Black dots indicate the presence of large permanent plots (1ndash10) and doaround fine-scale canopy gaps and reflect the forest composition of their neighboring m

trees (gt4 cm diameter-at-breast-height dbh) Individual plot sizevaries (Table 1) due to differences in stand density because thesampling goal was to include approximately 400 trees in each plotPlots were subjectively located in sectors of forest not disturbed bylogging (ie lacking cut stumps) The six largest plots (BW2 3MRS4 5 7 and BL6) are situated along a topographic-moisturegradient of older (ie gt250 years) stands at xeric sites dominatedby limber pine or lodgepole pine to mesichydric stands of Engel-mann spruce and subalpine fir Species abundance along with treeage and size for these six plots are detailed in an initial study ofstand dynamics (Veblen 1986a) Four plots (MRS1 8 9 and 10)are relatively even-aged (c 120 year-old) post-fire stands ofprimarily lodgepole pine Due to their proximity and similar struc-tures plots MRS8 9 and 10 were combined into a single unit foranalyses Thirty smaller (c 10 10 m) plots installed in 1983 aresituated around fine-scale canopy gaps near selected larger plotsdescribed above and contain an average of 40 trees in younglodgepole pine-dominated stands (Gaps 1ndash5 near MRS1) olderlodgepole pine with Engelmann spruce and subalpine fir (Gaps

f the CU Mountain Research Station and Niwot Ridge Biosphere Reserve in Boulderts with gray circles indicate the presence of smaller gap plots Gap plots are situatedain plot The black triangle represents the location of the C-1 climate station

Table 1Permanent plot descriptors organized into older versus younger stands

Plot name Plot size(sq m)a

Year of plotinstallation

Initialpopulationsize

Live basal areain 2007(sq mha)

Standage (yrs)

Topographicposition

Successional status

Old standsBW2 2592 1982 374 476 265 Xeric Successional from limber pine to Engelmann spruce and subalpine firBW3 810 1982 282 935 255 Mesic Successional with Engelmann spruce subalpine fir and lodgepole pineMRS4 1944 1982 515 767 355 Xeric Successional with Engelmann spruce subalpine fir and lodgepole pineMRS5 2916 1982 425 532 554 Hydric Compositional equilibrium with Engelmann spruce and subalpine firBL6 1944 1982 416 765 462 Mesic Compositional equilibrium with Engelmann spruce and subalpine firMRS7 2916 1983 496 557 375 Xeric Successional with Engelmann spruce subalpine fir and limber pineGaps at MRS4 1706 1983 408 59 355 XericMesic Successional with Engelmann spruce subalpine fir and lodgepole pineGaps at BL6 1277 1983 273 869 462 Mesic Compositional equilibrium with Engelmann spruce and subalpine fir

Young standsMRS1 1134 1982 834 688 120 Xeric Lodgepole pine dominated stem-exclusion phaseMRS8 9 amp 10 1404 1986 871 686 120 XericMesic Lodgepole pine dominated stem-exclusion phaseGaps at MRS1 461 1983 173 41 120 Xeric Lodgepole pine dominated stem-exclusion phase

a For aggregated plots plot size refers to the sum of the areas of the component plots

JM Smith et al Forest Ecology and Management 341 (2015) 8ndash17 11

6ndash20 near MRS4) and older spruce-fir stands (Gaps 21ndash30 nearBL6) These gaps originated from treefalls or are small naturalopenings in the forest as opposed to originating from timbercutting

Each plot or group of plots was classified by successional statusand as hydric mesic or xeric based on topographic position asdetailed in Veblen 1986a (Table 1) Topographic classification ofthe soil moisture status of each site is confirmed by radial growthresponses to interannual climatic variability (Villalba et al 1994)Thus in plots classified as xeric radial tree growth is positivelycorrelated with spring to early summer precipitation and nega-tively correlated with spring to early summer temperature (egplots BW2 MRS 4 MRS7) In contrast in the hydric plot MRS5radial growth is positively correlated with springndashsummer temper-ature and is not correlated with precipitation The climate-growthresponses of the mesic plots (BW3 and BL6) were intermediatebetween the xeric and hydric plots (Villalba et al 1994)

22 Monitoring of tree mortality in the permanent forest plots

A mortality census of dead trees was conducted for each plot atthree-year intervals since plot installation dates until 1994 (eg1985 1988 1991 and 1994) Tree mortality was again monitoredin 2007 2010 and 2013 During a census the species of each deadtree was recorded and its status as dead standing or fallen Mortal-ity caused by bark beetles was inferred from presence of beetle exitholes and beetle galleries which allowed the identification of thedifferent types of beetles MPB SBB WBBB and engraver beetles(Ips spp) The 2007 mortality census preceded any local effectsof the regional MPB event that has massively affected nearby for-ests since 2004 (Chapman et al 2012) During the 2007 mortalitycensus only one limber pine was observed to have been killed byMPB and two others were under attack whereas in the 2010 and2013 mortality censuses 17 and 44 trees respectively were killedby bark beetles of different types (mostly WBBB) Since barkbeetles were an insignificant mortality agent prior to 2008 treemortality over the 31-year time period is compared for twoequal-length periods lacking bark beetle outbreaks and a shorterperiod with significant bark beetle activity 1982ndash1994 1995ndash2007 and 2008ndash2013 The pre- and post-1995 time periods werefurther distinguished by less and more severe water deficitsrespectively (Fig 2)

We report the tree mortality results as annualized mortality(M) by species and for all species combined for individual plotsand groups of plots based on the number of live trees at the timeof permanent plot installation in 1982ndash83 and 1986 using the

following formula (dTiT)P frasl 100 = M where dT represents thenumber of trees that died (combined or by species) in the numberof years included in time period P and iT represents the initial livetree count at time of plot installation In 2007 a complete census ofall the plots was conducted including measurement of diametergrowth of all tagged trees as well as in-growth of smaller trees intothe gt4 cm dbh size class Thus although tree mortality is reportedas annualized mortality for the three comparison periods here thetotal change in the tree population size considering in-growth aswell as mortality for the c 25 year period ending in 2007 can befound in Smith (2012)

We note that tree mortality was not measured annually butrather at intervals of 3 or more years and then totaled for periodsof 12 13 or 6 years Thus the annualized mortality is a standardi-zation procedure allowing comparison of total mortality in periodsof different lengths This is important because the absence of dataon annual variability in mortality rates precludes the application ofmost statistical evaluations of the tree mortality data

23 Moisture deficits and relationships with tree mortality

Annual and monthly moisture deficits were calculated using amodified Thornthwaite method (Willmott et al 1985 Gavinet al 2006) based on daily records from the Niwot Ridge C-1 cli-mate station (Fig 1) Monthly means of average maximum andminimum temperature and monthly sums of precipitation werecalculated from daily measurements for the period 1982ndash2012(httpcultercoloradoeduNWT) Variability in these climaticparameters is assessed graphically for the study period Giventhe lack of measurement of annual variability in tree mortalityrates we did not perform statistical modeling of relationshipsbetween annual mortality and annual climatic variables (Daset al 2013)

24 Maximum daily temperature record

To assess the potential effects on tree mortality of temporalchanges in the onset of warm temperatures during late springand early summer we plotted 5-day running means of daily max-imum temperatures from the first of June until the end of Augustfor an arbitrary threshold of 24 C over the period 1953ndash2012using the daily climate record from the C-1 station For each yearwe record the date at which the 5-day mean maximum dailytemperature first reached the threshold temperature Dates aremeasured in days from June 1st

Fig 2 (a) Annual moisture deficits (C-1) for 1982ndash2012 (bndashe) Monthly moisture deficits for 1982ndash2012 Gray shaded areas represent annual moisture deficits (mm) andblack shaded areas represent monthly contribution for (b) June (c) July (d) August and (e) September Totals of 177 255 and 285 trees died during the 1982ndash1994 1995ndash2007 and 2008ndash2013 periods respectively

12 JM Smith et al Forest Ecology and Management 341 (2015) 8ndash17

3 Results

31 Tree mortality patterns from 1982 through 2013

Over the full 31-year monitoring period ending in 2013 therewas a strong increase in tree mortality both for the aggregate treepopulation and consistently for each plot or group of plots Andwith time the increase in tree mortality became a more uniformlyaccelerating trend across stands of different composition age andsite characteristics Of the total of 5067 trees gt4 cm dbh initiallytagged at the dates of plot installations (1982 1983 or 1986)totals of 177 255 and 285 trees died during the 1982ndash19941995ndash2007 and 2008ndash2013 periods respectively (Fig 2)

All stands young and old show large increases in annualizedmortality rates for all species combined over the 32-year monitor-ing period (Fig 3) Comparison of annualized mortality rates forthe 1982ndash1994 and 2008ndash2013 periods indicate a range from alow of a 35 increase for the 15 small gap plots at MRS4 to a12-fold increase for plot BL6 For all species aggregated each standalso records a higher annualized mortality rate in 2008ndash2013 com-pared to the 1995ndash2007 period (Fig 3)

Four of the six old stand plots recorded substantial increases(range from 40 to gt200) in mortality rates from the 1982ndash1994 to 1995ndash2007 (Fig 3) when water deficits were also increas-ing (Fig 2) One exception is plot MRS5 which is the only hydric

site (a bog forest) where warmer conditions have a positive influ-ence on radial tree growth measured from 1899 to 1991 (Villalbaet al 1994) The other exception is plot BW2 which is a late seralstand in which the more shade-tolerant subalpine fir and Engel-mann spruce are successionally replacing the shade-intolerantlimber pine and quaking aspen (Veblen 1986a)

Although all the gap plots exhibit large increases in mortalityrates from the 1982ndash1994 to 2008ndash2013 periods the trends foryoung and old gap plots differ for the 1982ndash1994 and 1995ndash2007comparison (Fig 3) The gap plots in the young stands at MRS1increased in mortality rate whereas the gap plots in the old standsat MRS4 and BL6 declined in mortality rates between 1982ndash1994and 1995ndash2007 (Fig 3) The mortality rates in the gap plots atMRS1 are less than in the closed canopy young stands (MRS1 andMRS 8 9 and 10) which is consistent with less intensive self-thinning during the stem-exclusion stage under more open canopyconditions (Fig 3) During the 2008ndash2013 period of elevated mor-tality mortality rates in the gap plots at old stand BL6 are also lessthan in the adjacent closed canopy BL6 plot

In the 6 old stands all the conifers showed large increases inaverage mortality rates from 1982ndash1994 to 2008ndash2013 with sub-alpine fir increasing by 300 lodgepole pine by 250 limber pineby 85 and Engelmann spruce by 38 (Table 2 Fig 4) Initiallyduring the 1982ndash1994 period the species with the highest mortal-ity rate varied widely among plots For example initially limber

Fig 3 Mean annualized mortality for each plot or group of plots from 1982 to 2013 as a percent of the initial live tree count Mortality values are presented for three mainperiods of observation (1) 1982ndash1994 (2) 1995ndash2007 and (3) 2008ndash2013

JM Smith et al Forest Ecology and Management 341 (2015) 8ndash17 13

pine had the highest mortality rate in the late seral stand BW2whereas Engelmann spruce had the highest rate in the adjacentstand BW3 (Fig 4) The most dramatic increases in plot-level mor-tality rates are for subalpine fir in MRS5 BL6 and the gap plots atBL6 but not until the 2008ndash2013 period (Fig 4) These two sitesare hydric and mesic respectively and are the oldest stands inthe study In contrast to the other old stands which were late-seralstages these stands are in compositional equilibrium (Veblen1986a) In contrast to the high mortality rate of subalpine fir inmost plots in 2008ndash2013 it remained relatively low in the xericlate seral stand BW2

Prior to 2007 no tree mortality in the permanent plots wasattributed to MPB or other bark beetles despite field inspectionof newly dead trees for evidence of lethal biotic agents In 2007one limber pine in plot MRS7 had been killed by MPB and twoother living limber pines in MRS7 were already attacked in thatyear After 2007 bark beetles become a significant agent of mortal-ity Among the 125 tree deaths recorded for the 2008ndash2010 period64 were attributed to MPB 64 to unknown or Ips beetles and08 to WBBB (Table 3) During the 2011ndash2013 period when 160trees died there was a sharp increase in deaths attributed to WBBBwhich accounted for 20 of the tree deaths (Table 3) Despite thisupsurge in beetle-killed trees c 79 of the trees that died during2008ndash2013 did not show any symptoms of beetle attack Even inthe case of subalpine fir which had the highest percentage of

Table 2Mean annualized mortality by species and period per plot type

Subalpine fir Lodgepole pine

1982ndash1994

1995ndash2007

2008ndash2013

1982ndash1994

1995ndash2007

MRS1 000 000 000 037 055MRS8 9 amp 10 000 001 000 027 044Gaps at MRS1 000 000 000 026 031Gaps at MRS4 013 013 033 011 005Gaps at BL6 053 039 153 000 000Mean mortality in young

stands000 001 000 030 043

Mean mortality in old stands 017 015 068 004 007Mean mortality in all stands

combined013 012 055 014 021

deaths attributable to a biotic agent (WBBB) more than 73 ofthe tree deaths were not attributable to a biotic agent

32 Coincidence of tree mortality with recent interannual climatevariability

Annual Thornthwaite moisture deficits show an increasingfrequency of severe droughts from 1982 to 2013 but also exhibitsubstantial interannual variability (Fig 2a) The mean deficit for1982ndash1994 of 42 mm (plusmn35 mm SD) is significantly less than themean deficit of 65 mm (plusmn43 mm SD p lt 0001 Wilcoxon rankedsum test) for the 1995ndash2007 period The mean annual deficit from2008 to 2012 is 50 mm (plusmn24 mm SD) but the shorter time perioddoes not allow for a valid comparison of means The two highestannual deficits occurred in 2000 and 2003 (c 124 and 129 mmrespectively) and are followed by another high deficit in 2005 (c114 mm) and moderately high deficits in 2009 and 2010 (gt80 mm)

Monthly moisture deficits were recorded for June throughSeptember (Fig 2bndashe) The percent contribution of each month toannual moisture deficit shifts over time implying more severewater deficits earlier in the summer as well as greater deficits inlate summer Severe annual droughts can be associated withextreme monthly water deficits in either August or July Monthlywater deficit for August was the greatest overall contributor toannual deficits with an average deficit of c 21 mm and a 404

Engelmann spruce Limber pine

2008ndash2013

1982ndash1994

1995ndash2007

2008ndash2013

1982ndash1994

1995ndash2007

2008ndash2013

106 000 000 000 000 000 000061 000 000 000 000 000 000039 000 000 000 000 004 010000 022 011 037 006 000 000000 024 017 006 000 000 000069 000 000 000 000 002 000

014 012 011 016 007 004 013034 010 010 014 005 004 011

Fig 4 Mean annualized mortality by species for six old stands from 1982 to 2013as a percent of the initial live tree count Mortality values are presented for threemain periods of observation (1) 1982ndash1995 (2) 1995ndash2007 and (3) 2008ndash2013Species codes are as follows ABLA subalpine fir PICO lodgepole pine PIENEngelmann spruce PIFL limber pine

Table 3Percentage of tree deaths attributed to mortality agents during the 2008ndash2010 and2011ndash2013 periods

Percentage of tree deaths

Biotic agents 2008ndash2010 2011ndash2013N = 125 N = 160

Mountain pine beetle 64 50Pine engraver beetle (Ips sp) 24 00Unknown beetles 40 13Spruce bark beetle 00 13Western balsam bark beetle 08 200

No apparent biotic agent 864 724

Fig 5 Days after June 1st when the 5-day running mean of maximum dailytemperature reached 24 C (filled circles)

14 JM Smith et al Forest Ecology and Management 341 (2015) 8ndash17

contribution to the cumulative annual moisture deficit for the1982ndash2012 period (Fig 2d) The contribution of August waterdeficits remains similar over the 31 year period However the con-tribution of July to the total annual deficit increases sharply after1992 (Fig 2c) implying a shift towards earlier water stress duringthe summer season Likewise the peak contributions of June andSeptember occur in 2006 and 2010 respectively suggesting bothearly and later seasonal droughts since the early 2000s

Consistent with the trend towards earlier summer water stressthe frequency of years during which the 5-day running means ofdaily maximum temperatures exceeds a threshold of 24 C is muchgreater after 1994 (Fig 5) From 1953 to 1976 the 24 C thresholdwas reached in only a single year In contrast after 2000 all yearsexcept one reach the 24 C threshold It is noteworthy that sincethe late 1980s the 24 C threshold was reached in most years priorto early July indicating a long warm season (Fig 5)

4 Discussion

41 Limitations of results

Any conclusions about causation of tree death must be tem-pered for several reasons Statistical modeling of climate predictorsof annual mortality was not performed because the censuses ofmortality conducted at 3ndash13 year intervals did not yield a validmeasure of annual variability in annualized mortality rates Evenif annual tree mortality had been statistically related to annual cli-mate variables the long lags between drought events and treedeaths previously demonstrated for these tree species (Bigleret al 2007) make attribution of death events to particular yearsdifficult Furthermore in the absence of long-term physiologicalmonitoring of the trees it is difficult to determine actual mecha-nisms of death Although we propose that high temperatures anddrought are directly involved in the mechanisms of tree deathwe cannot exclude the possibility that climate is predisposing treesto undetected lethal biotic agents

42 Tree mortality in relation to climate variability

The principal finding of this study is that despite some varia-tions attributable to differences in stand structure (gaps and suc-cessional status) and to site there has been a marked increase inannualized mortality rates for all the conifer populations moni-tored in 1982ndash2013 Comparison of the first two monitoring peri-ods indicates that at sites other than the bog forest and therelatively open canopy late seral stand BW2 mortality ratesclimbed steeply during the warmer and drier 1995ndash2007 periodDuring the 2008ndash2013 period tree mortality rates increased forall populations ndash for all species combined there was a two and ahalf fold increase in annualized mortality rates between 1995ndash2007 and 2008ndash2013 At the level of individual plots or groups ofgap plots the increases in annualized mortality rates range froma low of a 35 increase to a 12-fold increase when the annualized

JM Smith et al Forest Ecology and Management 341 (2015) 8ndash17 15

mortality rates of 1982ndash1994 and 2008ndash2013 periods are com-pared Although changes in mortality rates for the first two moni-toring periods varied among stands two thirds of the old standsbegan to record substantial increases (range from 40 to gt200)in mortality rates from the 1982ndash1994 to 1995ndash2007 periods

The steep increase in mortality rates documented in the currentstudy are not attributable mainly to bark beetles populationswhich are well known to have erupted in Colorado forests duringthe 1990s (Chapman et al 2012 Colorado State Forest Service2012) Evidence of bark beetle attack is easily seen particularlyin the form of pitch tubes and beetle galleries so that it is unlikelythat beetle-attacked trees would not have been recognized in ourperiodic measurements of tree mortality In the permanent plotsprior to 2007 MPB caused a negligible number of tree deathsand even in 2008ndash2013 accounted for only 56 of tree deathsLikewise SBB has infested large populations of trees across Colo-rado since the late 1990s including heavily infested stands onlyc 30 km to the northwest of our study area in Rocky MountainNational Park But again mortality caused by SBB was negligiblebefore 2007 and in the 2008ndash2013 period accounted for lt1 ofthe tree deaths The biotic agent which has contributed signifi-cantly to recent tree mortality is WBBB which in 2008ndash2013 wasresponsible for 115 of the deaths of subalpine fir

Infestation of subalpine fir by western balsam bark beetles is akey component of a phenomenon described as lsquolsquosubalpine firdeclinersquorsquo (Colorado State Forest Service 2012)

Chronic levels of subalpine fir decline are increasingly commonin subalpine forests in Colorado and may involve infection by rootdisease fungi which weaken trees and make them susceptible toattack by WBBB (Worrall et al 2004 Negron and Popp 2009) Inour study we identified WBBB galleries but we did not sample orexcavate roots for fungal pathogens Little research has been con-ducted on subalpine fir decline in Colorado and the findings ofthe present study may be the first to quantify its importance inthe death of subalpine fir at a stand scale Research conducted else-where has shown that a reduced rate of radial growth increasedthe susceptibility of subalpine fir to successful attack by WBBB(Bleiker et al 2003) Thus the warmer and drier climatic condi-tions in our study area over recent decades and associated reduc-tion in radial growth rates of subalpine fir in our permanentplots (Villalba et al 1994 Smith 2012) would predispose treesto successful attack by WBBB

Although warmer and drier climatic conditions undoubtedlypredispose all the conifers to successful attack by bark beetles(Raffa et al 2008 Hart et al 2014) 75 of the tree deaths in2008ndash2013 in the permanent plots could not be directly attributedto bark beetles While we recognize the difficulty of attributingtree death to a single factor the lack of evidence of beetle attack(eg pitch tubes and galleries) on trees killed within three yearsof field inspection implies that either previously unidentified bioticagents that do not leave obvious signs on the dead trees contrib-uted to tree death or that tree death is attributable to physiologicaldamage related to water stress Although determination of thephysiological mechanisms by which trees died was beyond thescope of our study we hypothesize that either the direct or predis-posing effects of drought play a primary role in increasing back-ground tree mortality rates in our permanent plots At multi-decadal time scales since the early 1900s the subalpine forest zoneof the Front Range is characterized by warming trends as measuredby various temperature parameters (Saunders et al 2008 Rayet al 2008 Baron et al 2009) The shift toward warmer conditionswhen combined with static or decreasing levels of precipitationhas led to increased occurrence of more severe droughts affectingforests across large parts of the western USA (Breshears et al2005 Williams et al 2013) Under warmer temperatures of recentdecades variability in precipitation related to variability in climate

drivers such as the El Nintildeo-Southern Oscillation the Pacific Deca-dal Oscillation and the Atlantic Multidecadal Oscillation (AMO)appears to be promoting more severe droughts in the southernRocky Mountains (McCabe and Dettinger 1999 McCabe et al2004) Variability in these same climate drivers has previouslybeen shown to be a dominant driver of tree-ring reconstructedwildfire activity (Veblen et al 2000 Schoennagel et al 20052007 Sibold and Veblen 2006 Sherriff and Veblen 2008) and barkbeetles (Hart et al 2014) in the Southern Rockies over the pastseveral centuries

A trend towards increased frequencies of annual water deficitsis evident in the weather records from our study site and equallyimportant is the evidence of increased frequency of late spring toearly summer high temperature extremes and shifts in the sea-sonal timing of drought Subsequent to 1991 there is an apparentshift towards a greater contribution of early summer water deficitsto the annual water deficit consistent with the earlier appearanceof high daily maximum temperatures of 24 C after the late 1980sSimilarly Hu et al (2010) found that earlier snowmelt results inearlier growth initiation but also in an overall lengthening of thegrowing season which reduces productivity for these species inour study area Analogously retrospective tree-ring reconstruc-tions of tree mortality suggest that drought seasonality may differ-entially affect tree mortality For example Bigler et al (2007)showed that Engelmann spruce and subalpine fir in the ColoradoFront Range exhibited lagged (by 5ndash11 years) mortality followingearly season drought but more rapid mortality following late sea-son drought These findings once again highlight the probabilitythat timing of drought may be an important determinant of themechanistic pathway to tree death (Anderegg et al 2013)

43 Variability in mortality patterns related to site and standdevelopment

Despite the ubiquity of increased mortality rates across all theconifer species and across all stands in our study there wereimportant variations in the timing and the magnitude of increasedtree mortality according to stand attributes and site conditions Forexample the late seral stand BW2 exhibited a decline in tree mor-tality from the 1982ndash1994 to 1995ndash2007 period This was due toan initially higher rate of tree mortality of the early seral specieslimber pine during the first period Stand BW2 is a c 265-yearold post-fire stand dominated by a post-fire cohort of limber pinewhich is gradually being replaced by more shade-tolerant Engel-mann spruce and subalpine fir (Veblen 1986a) The small numbersof trees dying in 1995ndash2007 in BW2 may reflect the open canopy ofthis stand as well as the much younger ages (lt150 years) of thesespecies populations compared to the other old stands (Veblen1986a) Although successional dynamics in this stand appearedto account for the initially higher and then lower mortality ratesby the third period (2008ndash2013) the mortality rate of limber pinewas double its initial rate Stand MRS5 also exhibited a decreasein tree mortality of subalpine fir and essentially no change forEngelmann spruce between the 1982ndash1994 and the 1995ndash2007period This is a bog forest where under warmer and drier climaticconditions waterlogged soils prevented trees from experiencingwater stress as also shown by the positive correlation of treegrowth with warmer temperatures at this site (Villalba et al1994) With further warming and drought in 2008ndash2013 howeverboth species in stand MRS5 experienced substantial increases inmortality

In the late seral stand MRS4 as expected the seral specieslodgepole pine on average had a higher mortality rate than theshade-tolerant subalpine fir and Engelmann spruce This was espe-cially evident during 2008ndash2013 when the mortality rate of lodge-pole pine was nearly three times as great as the other two conifers

Fig 4 Mean annualized mortality by species for six old stands from 1982 to 2013as a percent of the initial live tree count Mortality values are presented for threemain periods of observation (1) 1982ndash1995 (2) 1995ndash2007 and (3) 2008ndash2013Species codes are as follows ABLA subalpine fir PICO lodgepole pine PIENEngelmann spruce PIFL limber pine

Table 3Percentage of tree deaths attributed to mortality agents during the 2008ndash2010 and2011ndash2013 periods

Percentage of tree deaths

Biotic agents 2008ndash2010 2011ndash2013N = 125 N = 160

Mountain pine beetle 64 50Pine engraver beetle (Ips sp) 24 00Unknown beetles 40 13Spruce bark beetle 00 13Western balsam bark beetle 08 200

No apparent biotic agent 864 724

Fig 5 Days after June 1st when the 5-day running mean of maximum dailytemperature reached 24 C (filled circles)

14 JM Smith et al Forest Ecology and Management 341 (2015) 8ndash17

contribution to the cumulative annual moisture deficit for the1982ndash2012 period (Fig 2d) The contribution of August waterdeficits remains similar over the 31 year period However the con-tribution of July to the total annual deficit increases sharply after1992 (Fig 2c) implying a shift towards earlier water stress duringthe summer season Likewise the peak contributions of June andSeptember occur in 2006 and 2010 respectively suggesting bothearly and later seasonal droughts since the early 2000s

Consistent with the trend towards earlier summer water stressthe frequency of years during which the 5-day running means ofdaily maximum temperatures exceeds a threshold of 24 C is muchgreater after 1994 (Fig 5) From 1953 to 1976 the 24 C thresholdwas reached in only a single year In contrast after 2000 all yearsexcept one reach the 24 C threshold It is noteworthy that sincethe late 1980s the 24 C threshold was reached in most years priorto early July indicating a long warm season (Fig 5)

4 Discussion

41 Limitations of results

Any conclusions about causation of tree death must be tem-pered for several reasons Statistical modeling of climate predictorsof annual mortality was not performed because the censuses ofmortality conducted at 3ndash13 year intervals did not yield a validmeasure of annual variability in annualized mortality rates Evenif annual tree mortality had been statistically related to annual cli-mate variables the long lags between drought events and treedeaths previously demonstrated for these tree species (Bigleret al 2007) make attribution of death events to particular yearsdifficult Furthermore in the absence of long-term physiologicalmonitoring of the trees it is difficult to determine actual mecha-nisms of death Although we propose that high temperatures anddrought are directly involved in the mechanisms of tree deathwe cannot exclude the possibility that climate is predisposing treesto undetected lethal biotic agents

42 Tree mortality in relation to climate variability

The principal finding of this study is that despite some varia-tions attributable to differences in stand structure (gaps and suc-cessional status) and to site there has been a marked increase inannualized mortality rates for all the conifer populations moni-tored in 1982ndash2013 Comparison of the first two monitoring peri-ods indicates that at sites other than the bog forest and therelatively open canopy late seral stand BW2 mortality ratesclimbed steeply during the warmer and drier 1995ndash2007 periodDuring the 2008ndash2013 period tree mortality rates increased forall populations ndash for all species combined there was a two and ahalf fold increase in annualized mortality rates between 1995ndash2007 and 2008ndash2013 At the level of individual plots or groups ofgap plots the increases in annualized mortality rates range froma low of a 35 increase to a 12-fold increase when the annualized

JM Smith et al Forest Ecology and Management 341 (2015) 8ndash17 15

mortality rates of 1982ndash1994 and 2008ndash2013 periods are com-pared Although changes in mortality rates for the first two moni-toring periods varied among stands two thirds of the old standsbegan to record substantial increases (range from 40 to gt200)in mortality rates from the 1982ndash1994 to 1995ndash2007 periods

The steep increase in mortality rates documented in the currentstudy are not attributable mainly to bark beetles populationswhich are well known to have erupted in Colorado forests duringthe 1990s (Chapman et al 2012 Colorado State Forest Service2012) Evidence of bark beetle attack is easily seen particularlyin the form of pitch tubes and beetle galleries so that it is unlikelythat beetle-attacked trees would not have been recognized in ourperiodic measurements of tree mortality In the permanent plotsprior to 2007 MPB caused a negligible number of tree deathsand even in 2008ndash2013 accounted for only 56 of tree deathsLikewise SBB has infested large populations of trees across Colo-rado since the late 1990s including heavily infested stands onlyc 30 km to the northwest of our study area in Rocky MountainNational Park But again mortality caused by SBB was negligiblebefore 2007 and in the 2008ndash2013 period accounted for lt1 ofthe tree deaths The biotic agent which has contributed signifi-cantly to recent tree mortality is WBBB which in 2008ndash2013 wasresponsible for 115 of the deaths of subalpine fir

Infestation of subalpine fir by western balsam bark beetles is akey component of a phenomenon described as lsquolsquosubalpine firdeclinersquorsquo (Colorado State Forest Service 2012)

Chronic levels of subalpine fir decline are increasingly commonin subalpine forests in Colorado and may involve infection by rootdisease fungi which weaken trees and make them susceptible toattack by WBBB (Worrall et al 2004 Negron and Popp 2009) Inour study we identified WBBB galleries but we did not sample orexcavate roots for fungal pathogens Little research has been con-ducted on subalpine fir decline in Colorado and the findings ofthe present study may be the first to quantify its importance inthe death of subalpine fir at a stand scale Research conducted else-where has shown that a reduced rate of radial growth increasedthe susceptibility of subalpine fir to successful attack by WBBB(Bleiker et al 2003) Thus the warmer and drier climatic condi-tions in our study area over recent decades and associated reduc-tion in radial growth rates of subalpine fir in our permanentplots (Villalba et al 1994 Smith 2012) would predispose treesto successful attack by WBBB

Although warmer and drier climatic conditions undoubtedlypredispose all the conifers to successful attack by bark beetles(Raffa et al 2008 Hart et al 2014) 75 of the tree deaths in2008ndash2013 in the permanent plots could not be directly attributedto bark beetles While we recognize the difficulty of attributingtree death to a single factor the lack of evidence of beetle attack(eg pitch tubes and galleries) on trees killed within three yearsof field inspection implies that either previously unidentified bioticagents that do not leave obvious signs on the dead trees contrib-uted to tree death or that tree death is attributable to physiologicaldamage related to water stress Although determination of thephysiological mechanisms by which trees died was beyond thescope of our study we hypothesize that either the direct or predis-posing effects of drought play a primary role in increasing back-ground tree mortality rates in our permanent plots At multi-decadal time scales since the early 1900s the subalpine forest zoneof the Front Range is characterized by warming trends as measuredby various temperature parameters (Saunders et al 2008 Rayet al 2008 Baron et al 2009) The shift toward warmer conditionswhen combined with static or decreasing levels of precipitationhas led to increased occurrence of more severe droughts affectingforests across large parts of the western USA (Breshears et al2005 Williams et al 2013) Under warmer temperatures of recentdecades variability in precipitation related to variability in climate

drivers such as the El Nintildeo-Southern Oscillation the Pacific Deca-dal Oscillation and the Atlantic Multidecadal Oscillation (AMO)appears to be promoting more severe droughts in the southernRocky Mountains (McCabe and Dettinger 1999 McCabe et al2004) Variability in these same climate drivers has previouslybeen shown to be a dominant driver of tree-ring reconstructedwildfire activity (Veblen et al 2000 Schoennagel et al 20052007 Sibold and Veblen 2006 Sherriff and Veblen 2008) and barkbeetles (Hart et al 2014) in the Southern Rockies over the pastseveral centuries

A trend towards increased frequencies of annual water deficitsis evident in the weather records from our study site and equallyimportant is the evidence of increased frequency of late spring toearly summer high temperature extremes and shifts in the sea-sonal timing of drought Subsequent to 1991 there is an apparentshift towards a greater contribution of early summer water deficitsto the annual water deficit consistent with the earlier appearanceof high daily maximum temperatures of 24 C after the late 1980sSimilarly Hu et al (2010) found that earlier snowmelt results inearlier growth initiation but also in an overall lengthening of thegrowing season which reduces productivity for these species inour study area Analogously retrospective tree-ring reconstruc-tions of tree mortality suggest that drought seasonality may differ-entially affect tree mortality For example Bigler et al (2007)showed that Engelmann spruce and subalpine fir in the ColoradoFront Range exhibited lagged (by 5ndash11 years) mortality followingearly season drought but more rapid mortality following late sea-son drought These findings once again highlight the probabilitythat timing of drought may be an important determinant of themechanistic pathway to tree death (Anderegg et al 2013)

43 Variability in mortality patterns related to site and standdevelopment

Despite the ubiquity of increased mortality rates across all theconifer species and across all stands in our study there wereimportant variations in the timing and the magnitude of increasedtree mortality according to stand attributes and site conditions Forexample the late seral stand BW2 exhibited a decline in tree mor-tality from the 1982ndash1994 to 1995ndash2007 period This was due toan initially higher rate of tree mortality of the early seral specieslimber pine during the first period Stand BW2 is a c 265-yearold post-fire stand dominated by a post-fire cohort of limber pinewhich is gradually being replaced by more shade-tolerant Engel-mann spruce and subalpine fir (Veblen 1986a) The small numbersof trees dying in 1995ndash2007 in BW2 may reflect the open canopy ofthis stand as well as the much younger ages (lt150 years) of thesespecies populations compared to the other old stands (Veblen1986a) Although successional dynamics in this stand appearedto account for the initially higher and then lower mortality ratesby the third period (2008ndash2013) the mortality rate of limber pinewas double its initial rate Stand MRS5 also exhibited a decreasein tree mortality of subalpine fir and essentially no change forEngelmann spruce between the 1982ndash1994 and the 1995ndash2007period This is a bog forest where under warmer and drier climaticconditions waterlogged soils prevented trees from experiencingwater stress as also shown by the positive correlation of treegrowth with warmer temperatures at this site (Villalba et al1994) With further warming and drought in 2008ndash2013 howeverboth species in stand MRS5 experienced substantial increases inmortality

In the late seral stand MRS4 as expected the seral specieslodgepole pine on average had a higher mortality rate than theshade-tolerant subalpine fir and Engelmann spruce This was espe-cially evident during 2008ndash2013 when the mortality rate of lodge-pole pine was nearly three times as great as the other two conifers

JM Smith et al Forest Ecology and Management 341 (2015) 8ndash17 15

mortality rates of 1982ndash1994 and 2008ndash2013 periods are com-pared Although changes in mortality rates for the first two moni-toring periods varied among stands two thirds of the old standsbegan to record substantial increases (range from 40 to gt200)in mortality rates from the 1982ndash1994 to 1995ndash2007 periods

The steep increase in mortality rates documented in the currentstudy are not attributable mainly to bark beetles populationswhich are well known to have erupted in Colorado forests duringthe 1990s (Chapman et al 2012 Colorado State Forest Service2012) Evidence of bark beetle attack is easily seen particularlyin the form of pitch tubes and beetle galleries so that it is unlikelythat beetle-attacked trees would not have been recognized in ourperiodic measurements of tree mortality In the permanent plotsprior to 2007 MPB caused a negligible number of tree deathsand even in 2008ndash2013 accounted for only 56 of tree deathsLikewise SBB has infested large populations of trees across Colo-rado since the late 1990s including heavily infested stands onlyc 30 km to the northwest of our study area in Rocky MountainNational Park But again mortality caused by SBB was negligiblebefore 2007 and in the 2008ndash2013 period accounted for lt1 ofthe tree deaths The biotic agent which has contributed signifi-cantly to recent tree mortality is WBBB which in 2008ndash2013 wasresponsible for 115 of the deaths of subalpine fir

Infestation of subalpine fir by western balsam bark beetles is akey component of a phenomenon described as lsquolsquosubalpine firdeclinersquorsquo (Colorado State Forest Service 2012)

Chronic levels of subalpine fir decline are increasingly commonin subalpine forests in Colorado and may involve infection by rootdisease fungi which weaken trees and make them susceptible toattack by WBBB (Worrall et al 2004 Negron and Popp 2009) Inour study we identified WBBB galleries but we did not sample orexcavate roots for fungal pathogens Little research has been con-ducted on subalpine fir decline in Colorado and the findings ofthe present study may be the first to quantify its importance inthe death of subalpine fir at a stand scale Research conducted else-where has shown that a reduced rate of radial growth increasedthe susceptibility of subalpine fir to successful attack by WBBB(Bleiker et al 2003) Thus the warmer and drier climatic condi-tions in our study area over recent decades and associated reduc-tion in radial growth rates of subalpine fir in our permanentplots (Villalba et al 1994 Smith 2012) would predispose treesto successful attack by WBBB

Although warmer and drier climatic conditions undoubtedlypredispose all the conifers to successful attack by bark beetles(Raffa et al 2008 Hart et al 2014) 75 of the tree deaths in2008ndash2013 in the permanent plots could not be directly attributedto bark beetles While we recognize the difficulty of attributingtree death to a single factor the lack of evidence of beetle attack(eg pitch tubes and galleries) on trees killed within three yearsof field inspection implies that either previously unidentified bioticagents that do not leave obvious signs on the dead trees contrib-uted to tree death or that tree death is attributable to physiologicaldamage related to water stress Although determination of thephysiological mechanisms by which trees died was beyond thescope of our study we hypothesize that either the direct or predis-posing effects of drought play a primary role in increasing back-ground tree mortality rates in our permanent plots At multi-decadal time scales since the early 1900s the subalpine forest zoneof the Front Range is characterized by warming trends as measuredby various temperature parameters (Saunders et al 2008 Rayet al 2008 Baron et al 2009) The shift toward warmer conditionswhen combined with static or decreasing levels of precipitationhas led to increased occurrence of more severe droughts affectingforests across large parts of the western USA (Breshears et al2005 Williams et al 2013) Under warmer temperatures of recentdecades variability in precipitation related to variability in climate

drivers such as the El Nintildeo-Southern Oscillation the Pacific Deca-dal Oscillation and the Atlantic Multidecadal Oscillation (AMO)appears to be promoting more severe droughts in the southernRocky Mountains (McCabe and Dettinger 1999 McCabe et al2004) Variability in these same climate drivers has previouslybeen shown to be a dominant driver of tree-ring reconstructedwildfire activity (Veblen et al 2000 Schoennagel et al 20052007 Sibold and Veblen 2006 Sherriff and Veblen 2008) and barkbeetles (Hart et al 2014) in the Southern Rockies over the pastseveral centuries

A trend towards increased frequencies of annual water deficitsis evident in the weather records from our study site and equallyimportant is the evidence of increased frequency of late spring toearly summer high temperature extremes and shifts in the sea-sonal timing of drought Subsequent to 1991 there is an apparentshift towards a greater contribution of early summer water deficitsto the annual water deficit consistent with the earlier appearanceof high daily maximum temperatures of 24 C after the late 1980sSimilarly Hu et al (2010) found that earlier snowmelt results inearlier growth initiation but also in an overall lengthening of thegrowing season which reduces productivity for these species inour study area Analogously retrospective tree-ring reconstruc-tions of tree mortality suggest that drought seasonality may differ-entially affect tree mortality For example Bigler et al (2007)showed that Engelmann spruce and subalpine fir in the ColoradoFront Range exhibited lagged (by 5ndash11 years) mortality followingearly season drought but more rapid mortality following late sea-son drought These findings once again highlight the probabilitythat timing of drought may be an important determinant of themechanistic pathway to tree death (Anderegg et al 2013)

43 Variability in mortality patterns related to site and standdevelopment

Despite the ubiquity of increased mortality rates across all theconifer species and across all stands in our study there wereimportant variations in the timing and the magnitude of increasedtree mortality according to stand attributes and site conditions Forexample the late seral stand BW2 exhibited a decline in tree mor-tality from the 1982ndash1994 to 1995ndash2007 period This was due toan initially higher rate of tree mortality of the early seral specieslimber pine during the first period Stand BW2 is a c 265-yearold post-fire stand dominated by a post-fire cohort of limber pinewhich is gradually being replaced by more shade-tolerant Engel-mann spruce and subalpine fir (Veblen 1986a) The small numbersof trees dying in 1995ndash2007 in BW2 may reflect the open canopy ofthis stand as well as the much younger ages (lt150 years) of thesespecies populations compared to the other old stands (Veblen1986a) Although successional dynamics in this stand appearedto account for the initially higher and then lower mortality ratesby the third period (2008ndash2013) the mortality rate of limber pinewas double its initial rate Stand MRS5 also exhibited a decreasein tree mortality of subalpine fir and essentially no change forEngelmann spruce between the 1982ndash1994 and the 1995ndash2007period This is a bog forest where under warmer and drier climaticconditions waterlogged soils prevented trees from experiencingwater stress as also shown by the positive correlation of treegrowth with warmer temperatures at this site (Villalba et al1994) With further warming and drought in 2008ndash2013 howeverboth species in stand MRS5 experienced substantial increases inmortality

In the late seral stand MRS4 as expected the seral specieslodgepole pine on average had a higher mortality rate than theshade-tolerant subalpine fir and Engelmann spruce This was espe-cially evident during 2008ndash2013 when the mortality rate of lodge-pole pine was nearly three times as great as the other two conifers

16 JM Smith et al Forest Ecology and Management 341 (2015) 8ndash17

(Fig 4) In contrast in the gaps at MRS4 the mortality rate was con-sistently lower for lodgepole pine than the two shade-tolerantconifers Under the open canopy conditions of the gap plots lodge-pole pine mortality may be reduced due to greater availability oflight or soil moisture and other soil-mediated resources due to lessbasal area in the gaps (59 versus 767 m2ha Table 1) Similarly inthe pure stands of lodgepole pine its mortality rate was lower inthe gap plots than in the adjacent closed canopy MRS1 stand orthe nearby closed canopy MRS8-10 stands in all three monitoringperiods and markedly so in the most recent period (Table 2) Againbasal area in the gaps was only 41 versus 688 and 686 m2ha inthe closed canopy pure lodgepole pine stands (Table 1) Thus inboth old (c 355 years) and young (c 120 years) post-fire standsgap conditions partially ameliorated the increase in mortality rateof lodgepole pine over the 31-year period of warming

In mesic old-growth stands adult mortality rates have longbeen inferred to be higher for subalpine fir than Engelmann sprucebased on tree age frequency distributions and treefall rates(Oosting and Reed 1952 Veblen 1986b) Indeed the consistentlyhigher adult mortality rates of subalpine fir in combination with itshigher fecundity and shorter longevity relative to Engelmannspruce have long been argued to explain how differences in life his-tory traits contribute to the coexistence of these two species in oldstands (Oosting and Reed 1952) The current study is the first lon-gitudinal study to clearly document greater mortality for subalpinefir compared to Engelmann spruce The most salient pattern at BL6which is an archetype of a mesic old spruce-fir forest in which agestructures indicate coexistence of both dominant tree species(Veblen 1986a) in both the closed canopy stand and in the gapsis the consistently higher rate of mortality of subalpine fircompared to Engelmann spruce For all old stands combined treemortality rates were higher for subalpine fir than Engelmannspruce in all three time periods

The greater climate sensitivity of tree mortality in young standsfound elsewhere (Luo and Chen 2013) could only be evaluated forlodgepole pine in our study because this was the only dominantspecies in both young and old stands During all time periods mor-tality rates were higher for this species in closed canopy youngpost-fire stands compared to the 355-year old stand (MRS4) asexpected given that these stands were in a self-thinning stage(sensu Oliver and Larson 1996) However the increase in mortalityrates over time was actually less for lodgepole pine in the youngstands than in the 355-year old stand Thus the limited data avail-able in the current study did not support the hypothesized greatersensitivity of mortality in young stands to climate change

5 Conclusion

Monitoring of permanent forest plots is essential for quantify-ing rates and proximate causes of tree mortality at time scales ofseveral decades and to spatially relate mortality patterns to standand site attributes This study documents an accelerating rate ofannual tree mortality rates for subalpine fir Engelmann sprucelodgepole pine and limber pine based on monitoring marked pop-ulations of gt5000 trees from 1982 through 2013 Increased treemortality rates during this period coincided with recent increasesin the frequency of severe annual moisture deficits and of monthlymoisture deficits Over time higher maximum daily temperaturesare being recorded earlier in the summer and the contribution ofearly summer (July) conditions to annual drought conditions hasincreased This pattern of climatic variability has been coincidentwith and conducive to a two and a half fold increase in the averageannualized tree mortality rates for the total tracked tree popula-tion from the relatively cool and wet 1982ndash1994 period to thewarmer and drier 2008ndash2013 period Although unidentified biotic

agents affecting all tree species cannot be ruled out as a directcause of tree death the weight of the evidence suggests that waterstress appears to be contributing to an increase in background treemortality Notably tree mortality attributable to bark beetles ndash themost reliably observed lethal biotic agent in these forests ndash overthe 1982ndash2013 period was minor except for WBBB which since2008 has accounted for about 12 of the subalpine fir deathsOverall our findings suggest that the effects of higher tempera-tures and moisture stress either as direct causes of tree death orin combination with potentially increasing bark beetle populationsunder regional climate warming will likely continue to accelerateconifer mortality rates in Coloradorsquos subalpine forests

Acknowledgements

This research was supported by the United States NationalScience Foundation (awards 0825823 0743498 and 1262687) aJohn W Marr Ecology Fund Grant a CU Graduate School Disserta-tion Completion Fellowship and through a grant from the UnitedStates Geological Survey as part of the Western Mountain Initiative(a USGS global change research project) and the Cordillera ForestDynamics Network (CORFOR) Logistical support andor data wereprovided by the NSF supported Niwot Ridge Long-Term EcologicalResearch project and the University of Colorado MountainResearch Station We thank three anonymous reviewers for helpfulcomments on the manuscript

Appendix A Supplementary material

Supplementary data associated with this article can be found inthe online version at httpdxdoiorg101016jforeco201412031

References

Anderegg WRL Berry JA Field CB 2012 Linking definitions mechanisms andmodeling of drought-induced tree death Trends Plant Sci 17 (12) 693ndash700httpdxdoiorg101016jtplants

Anderegg L Anderegg W Berry J 2013 Not all droughts are created equaltranslating meteorological drought into woody plant mortality Tree Physiol 33(7) 672ndash683 httpdxdoiorg101093treephystpt044

Anderegg WRL Anderegg LDL Berry JA Field CB 2014 Loss of whole-treehydraulic conductance during severe drought and multi-year forest die-offOecologia 175 11ndash23 httpdxdoiorg101007s00442-013-2875-5

Baron J Schmidt T Hartman M 2009 Climate-induced changes in high elevationstream nitrate dynamics Glob Change Biol 15 1777ndash1789 httpdxdoiorg101111j1365-2486200901847x

Bentz BJ Reacutegniegravere J Fettig CJ Hansen EM Hayes JL Hicke JA Kelsy RGNegroacuten JF Seybold SJ 2010 Climate change and bark beetles of the westernUnited States and Canada direct and indirect effects Bioscience 60 602ndash613httpdxdoiorg101525bio20106086

Bigler C Gavin D Gunning C Veblen TT 2007 Drought induces lagged treemortality in a subalpine forest in the Rocky Mountains Oikos 116 1983ndash1994httpdxdoiorg101111j20070030-129916034x

Bleiker KP Lindgren BS Maclauchlan LE 2003 Characteristics of subalpine firsusceptible to attack by western balsam bark beetle (Coleoptera Scolytidae)Can J For Res 33 1538ndash1543 httpdxdoiorg101139X03-071

Breshears D Cobb N Rich P Price K Allen C Balice R Romme W Kastens JFloyd M Belnap J Anderson J Myers O Meyer C 2005 Regional vegetationdie-off in response to global-change-type drought Proc Natl Acad Sci 102(42) 15144ndash15148 httpdxdoiorg101073pnas0505734102

Chapman T Veblen TT Schoennagel T 2012 Spatio-temporal patterns ofmountain pine beetle activity in the southern Rocky Mountains Ecology 932175ndash2185 httpdxdoiorg10189011-10551

Colorado State Forest Service 2012 Report on the Health of Coloradorsquos ForestsForest Stewardship Through Active Management lthttpcsfscolostateedupdfs137233-forestreport-12-wwwpdfgt

Connell JH Sousa WP 1983 On the evidence needed to judge ecological stabilityor persistence Am Nat 121 (6) 789ndash824

Das A Battles J Stephenson NL van Mantgem PJ 2011 The contribution ofcompetition to tree mortality in old-growth coniferous forests For EcolManage 261 1203ndash1213 httpdxdoiorg101016jforeco201012035

Das AJ Stephenson NL Flint A Das T van Mantgem PJ 2013 Climaticcorrelates of tree mortality in water- and energy-limited forests PLoS One 8 (7)e69917 httpdxdoiorg101371journalpone0069917

JM Smith et al Forest Ecology and Management 341 (2015) 8ndash17 17

Gavin DG Hu FS Lertzman K Corbett P 2006 Weak climatic control of stand-scale fire history during the Late Holocene Ecology 87 1722ndash1732 lthttpgeographyuoregonedugavinsoftwarehtmlgt

Greenland D 1989 The climate of Niwot Ridge Front Range Colorado USA ArctAlp Res 21 (4) 380ndash391

Hart SJ Veblen TT Eisenhart KS Jarvis D Kulakowski D 2014 Droughtinduces spruce beetle (Dendroctonus rufipennis) outbreaks across northwesternColorado Ecology 95 930ndash939 httpdxdoiorg10189013-02301

Hicke JA Logan JA Powell J Ojima DS 2006 Changing temperatures influencesuitability for modeled mountain pine beetle (Dendroctonus ponderosae)outbreaks in the western United States J Geophys Res ndash Biogeosci 111G02019 httpdxdoiorg1010292005JG000101 12 pp

Hu J Moore DJP Burns SP Monson RK 2010 Longer growing seasons lead toless carbon sequestration in a subalpine forest Glob Change Biol 16 771ndash783httpdxdoiorg101111j1365-2486200901967x

Luo Y Chen YH 2013 Observations from old forests underestimate climatechange effects on tree mortality Nat Commun 4 httpdxdoiorg101038ncomms2681

Lutz JA Halpern CB 2006 Tree mortality during early forest development along-term study of rates causes and consequences Ecol Monogr 76 257ndash275httpdxdoiorg1018900012-9615(2006)076[0257TMDEFD]20CO2

McCabe GJ Dettinger MD 1999 Decadal variations in the strength of ENSOteleconnections with precipitation in the western United States Int J Climatol19 1399ndash1410 httpdxdoiorg101002(SICI)1097-0088(19991115)1913lt1399AID-JOC457gt30CO2-A

McCabe GJ Palecki MA Betancourt JL 2004 Pacific and Atlantic Oceaninfluences on multidecadal drought frequency in the United States Proc NatlAcad Sci USA 101 4136ndash4141 httpdxdoiorg101073pnas0306738101

Negron JF Popp JB 2009 The flight periodicity attack patterns and life historyof Dryocoetes confusus Swaine (Coleoptera Curculionidae Scolytinae) thewestern balsam bark beetle in North Central Colorado Western North Am Nat69 447ndash458 httpdxdoiorg1033980640690404

Oliver CD Larson BC 1996 Forest Stand Dynamics John Wiley amp Sons Inc NewYork NY 520 pp

Oosting HJ Reed JF 1952 Virgin spruce-fir of the Medicine Bow MountainsWyoming Ecol Monogr 22 69ndash91

Raffa KF Aukema BH Bentz BJ Carroll AL Hicke JA Turner MG RommeWH 2008 Cross-scale drivers of natural disturbances prone to anthropogenicamplification the dynamics of bark beetle eruptions Bioscience 58 501ndash517httpdxdoiorg101641B580607

Ray A Barsugli J Averyt K 2008 Climate Change in Colorado A Synthesis toSupport Water Resources Management and Adaptation Report for The WesternWater Assessment for the Colorado Water Conservation Board 53 pp

Saunders S Montgomery C Easley T 2008 Hotter and Drier The Westrsquos ChangedClimate Report for The Rocky Mountain Climate Organization and the NaturalResources Defense Council 64 pp

Schoennagel T Veblen TT Romme WH Sibold JS Cook ER 2005 ENSO andPDO variability affect drought-induced fire occurrence in Rocky Mountain

subalpine forests Ecol Appl 15 2000ndash2014 httpdxdoiorg10189004-1579

Schoennagel T Veblen TT Kulakowski D Holz A 2007 Multidecadal climatevariability and climate interactions affect subalpine fire occurrence westernColorado (USA) Ecology 88 2891ndash2902 httpdxdoiorg10189006-18601

Sherriff RL Veblen TT 2008 Variability in firendashclimate relationships inponderosa pine forests in the Colorado Front Range Int J Wildland Fire 1750ndash59 httpdxdoiorg101071WF07029

Sibold J Veblen TT 2006 Relationships of subalpine forest fires in the ColoradoFront Range with interannual and multidecadal-scale climatic variation JBiogeogr 33 833ndash842 httpdxdoiorg101111j1365-2699200601456x

Smith JM 2012 An Examination of Background Tree Mortality and Mountain PineBeetle Disturbance in Subalpine Forests of the Front Range of Colorado USAPhD Dissertation Department of Geography University of Colorado 257pp

Thorpe HC Daniels LD 2012 Long-term trends in tree mortality rates in theAlberta foothills are driven by stand development Can J For Res 42 1687ndash1696 httpdxdoiorg101139x2012-104

van Mantgem PJ Stephenson NL Byrne JC Daniels LD Franklin JF Fuleacute PZHarmon ME Larson AJ Smith JM Taylor AH Veblen TT 2009Widespread increase of tree mortality rates in the western United StatesScience 323 521ndash524 httpdxdoiorg101126science1165000

Veblen TT 1986a Age and size structure of subalpine forests in the Colorado FrontRange Bull Torrey Bot Club 113 (3) 225ndash240

Veblen TT 1986b Treefalls and the coexistence of conifers in subalpine forests ofthe central Rockies Ecology 67 (3) 644ndash649

Veblen TT 1992 Regeneration dynamics In Glenn-Lewin DC Peet RK VeblenTT (Eds) Plant Succession Theory and Prediction Chapman amp Hall Londonpp 152ndash187

Veblen TT Kitzberger T Donnegan J 2000 Climatic and human influences onfire regimes in ponderosa pine forests in the Colorado Front Range EcolAppl 10 1178ndash1195 httpdxdoiorg1018901051-0761(2000) 010[1178CAHIOF]20CO2

Villalba R Veblen TT Ogden J 1994 Climatic influences on the growth ofsubalpine tress in the Colorado Front Range Ecology 75 1450ndash1462

Williams A et al 2013 Temperature as a potent driver of regional forest droughtstress and tree mortality Nat Clim Change 3 292ndash297 httpdxdoiorg101038nclimate1693

Willmott CJ Rowe CM Mintz Y 1985 Climatology of the terrestrial seasonalwater cycle J Climatol 5 589ndash606

Worrall JJ Sullivan Kelly F Harrington Thomas C Steimel Joseph P 2004Incidence host relations and population structure of Armillaria ostoyae inColorado campgrounds For Ecol Manage 192 191ndash206 httpdxdoiorg101016jforeco200401009

Worrall JJ Marchetti S Egeland L Mask Eager T Howell B 2010 Effects andetiology of sudden aspen decline in southwestern Colorado USA For EcolManage 260 638ndash648 httpdxdoiorg101016jforeco201005020