Forest structure and regeneration following a mountain pine beetle epidemic in southeastern Wyoming

Forest Ecology and Management 263 (2012) 57–66

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Forest structure and regeneration following a mountain pine beetle epidemic in southeastern Wyoming Lori J. Kayes ⇑, Daniel B. Tinker Department of Botany 3165, 1000 E. University Ave., University of Wyoming, Laramie, WY 82071, USA

a r t i c l e

i n f o

a b s t r a c t

Article history: Received 29 June 2011 Received in revised form 23 September 2011 Accepted 24 September 2011 Available online 21 October 2011

Rocky Mountain forests are currently experiencing a bark beetle epidemic of unprecedented severity and extent. Forest regeneration following bark beetle outbreaks is driven by the survival and density of understory trees (advance regeneration). The composition and density of the advance regeneration may differ substantially from the pre-outbreak overstory and across environmental gradients. We characterized and compared the density and species composition of advance regeneration, residual overstory, and pre-outbreak overstory in stands with varying lodgepole pine density and mortality following a massive mountain pine beetle outbreak in the Medicine Bow Range of Wyoming. Additionally, we examined the influence of moisture conditions, outbreak intensity, and stand characteristics on advance regeneration within these stands. While lodgepole pine experienced considerable mortality, it was still the dominant species in the overstory. Subalpine fir was the dominant species in the advance regeneration. Relative species density of the advance regeneration differed from the pre-outbreak overstory, demonstrating a significant shift towards subalpine fir dominance. Three different lodgepole pine forest types (pure lodgepole pine, aspen-influenced, and spruce-fir) were found prior to the outbreak in the Medicine Bow Range. In general, species composition of the advance regeneration was of the same forest type as the pre-outbreak overstory, indicating that there was very little shift between forest types within individual stands following the outbreak. However, the relative species density of the advance regeneration differed from the pre-outbreak overstory in the spruce-fir and the aspen-influenced forests types, with a much smaller proportion of lodgepole pine occurring in the advanced regeneration. Relative species densities of advance regeneration and residual overstory varied across local moisture conditions and pre-outbreak and lodgepole pine overstory density but not outbreak intensity. Subalpine fir and Engelmann spruce comprised a greater proportion of the overstory and understory in wetter stands while lodgepole pine was a greater proportion on the drier stands. Advance regeneration density was negatively correlated with pre-outbreak and lodgepole pine overstory density and basal area, except for lodgepole pine advance regeneration density which had a weak positive relationship. Succession trajectories are altered in both pure lodgepole pine stands and spruce-fir stands. Based on the density of advance regeneration compared to the pre-outbreak canopy, advance regeneration appears to be a suitable means for regenerating stands following mountain pine beetle outbreaks in the Medicine Bow Range. Relying on advance regeneration may increase heterogeneity in forest structure that may make these forests more resistant to mountain pine beetle attacks in the future. Ó 2011 Elsevier B.V. All rights reserved.

Keywords: Mountain pine beetle Advance regeneration Rocky Mountains Overstory density Lodgepole pine Forest composition

1. Introduction Episodic insect outbreaks and fire are the major disturbance types in many western forests. Such disturbances may impact the overstory, altering successional dynamics and requiring considerable time for forest regeneration. While there is a significant amount of information about forest regeneration following fire in many forest types (e.g., Agee, 1993; Turner et al., 1999), forest ⇑ Corresponding author. Tel.: +1 541 602 9701. E-mail addresses: (D.B. Tinker).

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(L.J.

Kayes),

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0378-1127/$ - see front matter Ó 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2011.09.035

regeneration following insect outbreaks is not well understood and differs from fire in several important ways. For example, stand-replacing fires typically kill all trees in a stand, including small trees; however, following an insect outbreak the understory and small trees are rarely killed and overstory mortality is species specific, based on the species of beetle present (e.g., DeRose and Long, 2010). In addition, most forests have seedlings and saplings in the understory (advance regeneration) that contribute to new stands following disturbance that affect the overstory only. Mortality of overstory trees may release resources that are potentially available for understory vegetation including surviving and establishing trees (e.g., Stone and Wolfe, 1996).

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Bark beetle outbreaks, in particular, are one type of insect outbreak that typically result in overstory mortality due to the preference of the beetles for older, larger diameter trees (Amman, 1977; Shore et al., 2006). Following beetle outbreaks, the majority of stands show some level of advance regeneration. Increased growth of surviving trees due to released resources contributes to the development of new stands following mountain pine beetle (MPB; Dendroctonus ponderosae Hopk.: Romme et al., 1986; Dordel et al., 2008) and spruce beetle (Dendroctonus rufipennis Kirby; Veblen et al., 1991b) outbreaks in the Rocky Mountains. The release of resources may also allow new seedling establishment, as seen following a MPB outbreak in Colorado (Collins et al., 2011) and spruce beetle outbreak in Alaska (Boggs et al., 2008) and the Czech Republic (Jonášová and Prach, 2004). Advance regeneration composition and abundance following bark beetle outbreaks are affected by overstory composition and abundance (Astrup et al., 2008; Nigh et al., 2008; Coates et al., 2009; Vyse et al., 2009; Diskin et al., 2011), microsite conditions (Boggs et al., 2008), management activities (Jonášová and Prach, 2004; Collins et al., 2011) and environmental conditions (Vyse et al., 2009); Coates et al., 2009). Composition and abundance of advance regeneration may differ substantially from the pre-outbreak overstory being comprised of shade tolerance species with slow establishment rates as seen following MPB outbreaks in British Columbia (Nigh et al., 2008; Coates et al., 2009; Vyse et al., 2009) and the Rocky Mountains (DeRose and Long, 2010; Collins et al., 2011). Currently, forests in the western US are experiencing a bark beetle epidemic that is unprecedented in the past 100 years in extent, severity, and duration (e.g. Raffa et al., 2008). Several species of native bark beetle, including the MPB, spruce beetle, western balsam bark beetle (Dryocoetes confusus Swaine), and Douglas-fir beetle (Dendroctonus pseudotsugae Hopkins), are simultaneously affecting over 2.5 M ha of forest in this region. The MPB alone is affecting over 1.5 M ha in southern Wyoming and northern Colorado, resulting in extensive mortality of lodgepole pine. The effects of MPB outbreaks on pre-disturbance stand structure (tree density, basal area and species composition) have been well documented in the Rocky Mountain region in ponderosa (Pinus ponderosa C. Lawson) and lodgepole pine (Pinus contorta Douglas ex Louden var. latifolia Engelm. ex S. Watson: Romme et al., 1986; Dordel et al., 2008; Axelson et al., 2009). Bark beetles can cause up to 70% tree mortality overall, and up to 90% mortality among large trees, across millions of hectares (Cole and Amman, 1980; Romme et al., 1986; Hawkes et al., 2004; Collins et al., 2011). While the effects of bark beetles on overstory structure are well understood there is limited information on forest recovery following beetle outbreaks, particularly an outbreak of this magnitude (but see Collins et al., 2011; Diskin et al., 2011). In the wake of such a large loss of overstory trees, there are inevitable concerns over the future condition and composition of the forest and what, if any, management actions should be taken (Rocca and Romme, 2009). Estimates of total area affected by the current bark beetle outbreak are updated annually typically using aerial surveillance and manual mapping techniques. These techniques are often inaccurate and spatially imprecise because they are a subjective visual estimate of number of recently dead trees only. Thus, they do not provide quantitative information on stand-level beetle activity and/or tree mortality (e.g. Rocca and Romme, 2009). Additionally, these annual estimates of ‘‘spread’’ of the epidemic do not provide any information on the abundance of surviving overstory and understory trees or seedling establishment, i.e., the advance regeneration. These surviving trees and advance regeneration represent the future forests of the region. Understanding the current postoutbreak structure of the forest is critical for making predictions about future structure and function, and informing post-outbreak management planning. To increase understanding of post-out-

break forest structure we addressed two objectives. First, we characterized and compared the community composition and relative species density of advance regeneration, residual overstory, and pre-outbreak overstory in forests dominated by lodgepole pine in the Medicine Bow Range. Second, we determined the influence of local moisture conditions (relatively wet versus relatively dry), outbreak intensity (% lodgepole pine overstory mortality), and stand overstory characteristics (pre-outbreak, total live and dead lodgepole pine, and live post-outbreak overstory density and basal area) on advance regeneration in stands with varying lodgepole pine density and mortality following a massive MPB outbreak. 2. Methods 2.1. Study area The study area was located in forests dominated by lodgepole pine between 2400 and 3000 m elevation in the Medicine Bow Range of the Medicine Bow National Forest (MBNF) in southeastern Wyoming. Lodgepole pine forests comprise 66% of the land cover in the Medicine Bow Range in this elevation band (von Ahlefeldt and Speas, 1996). The area is within an extensive MPB epidemic with virtually all lodgepole pine dominated stands affected by MPB caused mortality that started in the late 1990s. Stands ranged in age from 53 to 239 year old and regenerated following highseverity fire. Mean annual precipitation ranges from 43 cm in the southeastern portion of the range to 76 cm in the northwestern portion of the range. At higher elevations, most precipitation falls as snow between October and May. Temperatures range from an average low 13° C in January to an average high of 22.8° C in July. Precipitation and temperature means were extracted using PRISM Climate Group Data Explorer for latitude and longitude of furthest NW and SE stands (PRISM Climate Group, Oregon State University, http://prismmap.nacse.org/nn/index.phtml?vartype=pptyear0= 2003year1=2003, created 20 Nov 2010). 2.2. Data collection Twenty lodgepole pine dominated stands were selected to represent a range of pre-outbreak lodgepole pine densities and the range of moisture conditions in the MBNF. Half of the stands (n = 10) were located on the southeast side and half (n = 10) on the northwest side of the Medicine Bow Range. Geographic location was used as a proxy for local moisture conditions because stands in the northwest portion of the Medicine Bow Range are generally wetter than stands in the southeast portion due to prevailing weather patterns. Vegetation was sampled in three transects per stand in the summer of 2010 to measure overstory and advance regeneration density and composition. The starting location of a 50-m base line was established near the middle of the stand to avoid edge effects and firewood harvest areas and extended on an east-west bearing. The starting location (Easting and Northing Universal Transverse Mercator (UTM) coordinates) and elevation were recorded using a global positioning system. Three 50-m measurement transects were established running north from the base line at 0, 25 and 50 m. The number, condition, tree (>5 cm dbh) dbh and sapling (<5cm dbh and >1 m height) basal diameter of all stems and saplings were recorded by species in a belt along each measurement transect. The width of the measurement transects varied with tree density and were 1 m wide for very high density stands (>11000 stems per hectare (spha)); 2 m wide for high density sites (>1400 spha): or a 4 m wide for low density sites (<1400 spha). Initially, all measurement transects were 4  50 m but due to the number of stems found we decreased the transect width of high

L.J. Kayes, D.B. Tinker / Forest Ecology and Management 263 (2012) 57–66

density stands. We also recorded mortality status (live or dead) and pitch tube presence. Pitch tubes are masses of resin present on the tree trunk where MPB tunneling began. The number of seedlings (<1 m height) also were counted, by species, in a 2  50 m measurement transect. Species and stand-level density (spha) and basal area were calculated from tree/sapling/seedling data. Pre-outbreak overstory was assumed to include all live trees and dead trees with pitch tubes. The assessment of pre-outbreak overstory may not include recent mortality in non-lodgepole pine species or lodgepole pine snags that have fallen. However, less than 1% of the downed wood was sound and, following bark beetle outbreaks, most lodgepole pine snags do not begin to fall for at least 8 years (Lewis and Thompson, 2011). Similarly, post-outbreak live overstory did not include any trees with pitch tubes since it is assumed that these trees will die within a short time. 2.3. Statistical analysis 2.3.1. Species composition and density We summarized the total (all species combined) advance regeneration (seedlings and saplings), residual live overstory and preoutbreak overstory as mean density, range, and standard deviation per stand. We summarized advance regeneration, live overstory and pre-outbreak overstory for each species as mean density and standard deviation. All data were separated into the following size and mortality classes (seedlings, saplings, total advance regeneration (seedlings and saplings), residual live overstory, total live stems (seedlings, saplings and live overstory), dead overstory and assumed pre-outbreak overstory). Additionally, to compare species composition, we summarized for each species the average relative density per stand and across all stands, and proportion of total basal area for different size and mortality classes. Outbreak intensity was summarized as the mean, range, and standard deviation of percent lodgepole pine mortality of all stands (by density and basal area). Since percent mortality density and proportion of basal area killed were highly correlated (R2 = 0.79) relationships with outbreak intensity were calculated for both but only reported for density. 2.3.2. Comparison between advance regeneration and pre-outbreak overstory We compared community composition based on relative species density per stand occurring in pre-outbreak overstory with advance regeneration using multi-response permutation procedure (MRPP) with Srenson distance and rank transformed data in PCORD (version 6.1, MjM Software, Gleneden Beach, OR, US). MRPP is a non-parametric method of testing differences between a priori groups that results in an A-statistic, representing within-group homogeneity, and a p-value (Mielke and Berry, 2001; McCune and Grace, 2002). For ecological data, A-statistics of 0.10 and higher are considered to have high homogeneity within groups. We used Wilcoxon rank sum tests to examine differences in advance regeneration and pre-outbreak overstory relative density of individual tree species. We examined potential changes in stand-level community composition between advance regeneration and pre-outbreak overstory composition in individual stands by defining forest types using hierarchical cluster analysis and indicator species analysis (ISA: Dufrêne and Legendre, 1973) in PC-ORD (version 6.1, MjM Software, Gleneden Beach, OR, US). Cluster analysis was performed using relative Euclidean distance and Ward’s linkage method on log-transformed density values. We then defined the forest types by the dominant species using ISA. We graphically examined change in stand-level forest type between pre-outbreak overstory and advance regeneration using non-metric multidimensional scaling (NMS: Kruskal, 1964) and MRPP (Mielke and Berry, 2001).

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NMS was performed in PC-ORD using Srenson distance and ‘‘slow and thorough’’ settings for two time periods (pre-outbreak overstory and advance regeneration). PC-ORD ‘‘slow and through’’ settings uses a random starting configuration, 6 axis starting dimensions, 250 runs of real and randomized data with a maximum of 500 iterations each, and an instability criterion of 0.0000001. Pre-outbreak overstory was connected with successional arrows to advance regeneration for the same stand. 2.3.3. Influence of moisture conditions, outbreak intensity and stand characteristics We compared log-transformed density of (1) combined advance regeneration and residual live overstory and (2) advance regeneration without live overstory among different groups representing local moisture conditions, outbreak intensity, and stand characteristics with MRPP using Srenson distance and rank transformed data (Mielke and Berry, 2001; McCune and Grace, 2002). Specific groups compared included moisture conditions (relatively drier southeast and wetter northwest); pre-outbreak and total (live and dead) lodgepole pine overstory density classes - high (>3500 spha), moderate (1000–2300 spha), and low (<1000 spha); total density (overstory and understory) classes - high (>3500 spha), moderately-high (2300–3500 spha), moderately-low (1901–2233 spha), and low (<1900 spha); and outbreak intensity classes - high (>49%), moderate (24–25%) and low (0–25%). Outbreak intensity reflects the current level of mortality in these stands and does not account for the stage of the outbreak. There is potential for continued mortality of lodgepole pine until the epidemic subsides. To further examine the influence of local moisture conditions, stand characteristics and outbreak intensity, we used NMS ordination (Kruskal, 1964) of advance regeneration only (log density). NMS was performed in PC-ORD using Srenson distance and ‘‘slow and thorough’’ settings. The resulting 2-D ordination was overlain with a joint plot indicating the correlation between NMS stand scores and different local moisture conditions (represented by easting and northing UTM coordinates), stand (total sapling and overstory density, pre-outbreak overstory density and basal area, lodgepole pine overstory density) and outbreak intensity (% dead overstory lodgepole pine) and advance regeneration (total and individual species advance regeneration density) variables. To examine patterns related to local moisture conditions evident in MRPP and NMS at the species level, we compared the relative density per stand for individual species by size class (seedling, sapling, live overstory and snags) between dry southwestern and wetter northeastern stands using confidence intervals. 3. Results 3.1. Species composition and density Four tree species were present in both the overstory and advance regeneration: lodgepole pine, subalpine fir (Abies lasiocarpa (Hook.) Nutt., Engelmann spruce (Picea engelmannii Parry ex Engelm.), and quaking aspen (Populus tremuloides Michx.). The density of advance regeneration varied widely from 100 to 12,933 spha for all species combined (see Table 1 for averages and SD). Density of advance regeneration exceeded 1,000 spha in all but three stands. Acceptable stocking levels for lodgepole pine (317 spha) in the MBNF (USDA, 2003) were exceeded in all but one stand. Residual live overstory density was also highly variable, ranging from 117 to 5,567 spha for all species combined. Estimated pre-outbreak overstory density (range 1,133–11,333 spha) was considerably greater than the residual live overstory, but less than advance regeneration. Bark beetle-caused mortality of lodgepole pine ranged from 0% to 70% of overstory lodgepole pine trees

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Table 1 Average (standard deviation) total and individual species density (stems per hectare) for all 20 stands in different size and mortality classes and estimated pre-outbreak overstory. Total live stems include all live stems at the time of sampling (seedlings, sapling and overstory) and Total AdReg includes live seedlings and saplings only. Species

Lodgepole pine Subalpine fir Engelmann spruce Aspen Total

Total live stems

1797 (978) 2700 (2070) 344 (305) 513 (540) 5354 (3171)

Advance regeneration

Overstory

Seedling

Sapling

Total AdReg

Pre-outbreak

Live

Dead

490 (820) 2263 (3191) 237 (489) 382 (879) 3372 (3694)

481 (653) 199 (338) 60 (141) 81 (224) 821 (657)

971 (1220) 2463 (3310) 297 (590) 463 (997) 4193 (3780)

1543 (1549) 238 (256) 54 (92) 51 (109) 1885 (1399)

826 (1336) 238 (256) 48 (82) 51 (109) 1162 (1233)

718 (413) 33 (49) 12 (25) 105 (229) 867 (412)

(average = 37%, SD = 19.6%) and 0–97% (average = 70%, SD = 26%) of overstory lodgepole pine basal area. Two stands showed evidence of spruce mortality due to bark beetles. There were a considerable number of stems in all size categories but the four species differed in their distributions among size classes (Table 1). Subalpine fir was the most abundant seedling overall, accounting for almost 70% of all seedlings (Table 1). However, at the stand level, subalpine fir seedlings comprise 37% of all seedlings on average (Fig. 1a). Four stands contained no seedlings and three stands that contained only lodgepole pine seedlings. Lodgepole pine was the most abundant sapling and live overstory tree accounting for 59% and 71% of stems, respectively (Fig. 1a, Table 1). Lodgepole pine was also the most abundant snag in the overstory due to the recent MPB activity (Fig. 1a, Table 1). Lodgepole pine also occupied the majority of the live and dead overstory basal area accounting for 58% and 86% of basal area, respectively (Fig. 1b). 3.2. Comparison between advance regeneration and pre-outbreak overstory Community composition of stands differed between preoutbreak overstory and advance regeneration based on MRPP

(a)

(A = 0.10, p = 0.0002; Fig. 2), indicating low homogeneity between proportion abundance of species found in the pre-outbreak overstory and advance regeneration. Pre-outbreak overstory was comprised of 82% lodgepole pine, while the advance regeneration was only 23% lodgepole pine (p = 0.02: Fig. 2). Meanwhile, subalpine fir comprised only 13% of the pre-outbreak overstory and 57% of advance regeneration stems (p = 0.05: Fig. 2). There was no difference in the density of Engelmann spruce or aspen between advance regeneration and pre-outbreak overstory (p = 0.95 for both species: Fig. 2). Statistical difference in Engelmann spruce and aspen may have been masked by low sample size of stands with these species present. Both species had higher density in the advance regeneration than the pre-outbreak overstory (Table 1, Fig. 2). While the proportions of the four species shifted following the outbreak, there did not appear to be a major shift in forest type in individual stands based on NMS and MRPP (Fig. 3). Three forest types were evident based on cluster analysis and ISA of pre-outbreak and advance regeneration community composition: (1) pure lodgepole stands, (2) spruce-fir stands, and (3) aspen influenced stands (Fig. 3, Table 2). These three groups retained 63% of information in the cluster analysis. Pure lodgepole stands were indicated by lodgepole pine and were composed of only lodgepole pine in advance regeneration and overstory (Table 2). Lodgepole pine stands changed very little in composition based on the length of the successional arrows (Fig. 3). Aspen influenced stands were indicated by aspen and included all stands with aspen (Table 2). Aspen influenced stands exhibited the largest change in composition based on length of successional arrows (Fig. 3). The remainder of the stands (spruce-fir) were indicated by subalpine fir and Engelmann spruce but contained a mixture of lodgepole pine, Engelmann spruce and subalpine fir (Table 2). Based on cluster analysis and NMS, there was one stand from each forest type (total = 3 stands) that shifted forest types following the outbreak

(b)

Fig. 1. Average relative density per stand (a), and relative overstory basal area (b) for species in different size and mortality categories. PICO = lodgepole pine, ABLA = subalpine fir, PIEN = Engelmann spruce, and POTR = aspen.

Fig. 2. Average relative density per stand by species for total advance regeneration and assumed pre-outbreak overstory. PICO = lodgepole pine, ABLA = subalpine fir, PIEN = Engelmann spruce, and POTR = aspen.

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Axis 2

Pure Lodgepole Pine Aspen Influenced Spruce-fir

Axis 1 Fig. 3. Two-dimensional NMS ordination of understory (seedlings and saplings) advance regeneration and assumed pre-outbreak overstory by forest type. Groupings are from hierarchical cluster analysis and group identification based on indicator species analysis for groups (see Table 2). Arrows connect the pre-outbreak overstory to the understory advance regeneration within the same stand to examine potential changes in forest type. Final stress = 9.30785, axis 1 R2 = 63.8%, axis 2 R2 = 31.3%, cumulative R2 = 95%.

Table 2 Relative abundance (abun) and frequency (freq) of species in different forest types. An asterisk (⁄) indicates that species is an indicator for that group. PICO = lodgepole pine, ABLA = subalpine fir, PIEN = Engelmann spruce, and POTR = aspen. Forest type

Spruce-fir

Species PICO ABLA POTR PIEN

Abun 33 56 0 70

Freq 100 100⁄ 0 65⁄

Pure lodgepole

Aspen influenced

Abun 37 0 0 0

Abun 29 44 100 30

Freq 100⁄ 0 0 0

Freq 100 77 100⁄ 31

(Fig. 3). One stand each with aspen influenced and pure lodgepole pine pre-outbreak overstory shifted to spruce-fir advance regeneration and one stand with spruce-fir pre-outbreak overstory shifted to pure lodgepole pine advanced regeneration. The above results were supported by MRPP which showed no difference in pre-outbreak and advance regeneration density at the stand-level (A = 0.02, p = 0.14). 3.3. Influence of moisture conditions, outbreak intensity and stand characteristics Relative density of advance regeneration and residual overstory were influenced by moisture conditions and stand characteristics but not outbreak intensity based on NMS (Fig. 4) and MRPP (Table 3). The first NMS community axis was related to pre-outbreak overstory density (Fig. 4, Table 4). Easting (stands further east are drier) and lodgepole pine overstory density were correlated with community NMS axis scores of high pre-outbreak overstory

density stands (Fig. 4; Table 4). Lodgepole pine advance regeneration density was positively, but weakly, correlated with community axis scores for stands with high pre-outbreak overstory density (Fig. 4, Table 4). Northing (stand further north are wetter) and outbreak intensity were correlated with community axis scores of low pre-outbreak overstory density stands in NMS (Fig. 4, Table 4). Total and all species advanced regeneration density, except lodgepole pine, were correlated with community axis scores of low pre-outbreak overstory density stands (Fig. 4, Table 4). These results were supported by MRPP which showed significant differences in advance regeneration and residual stand composition between dry southeast and wetter northwest stands, pre-outbreak and lodgepole pine overstory density classes but not outbreak intensity or total stand density classes (Table 3). The second NMS community axis was related to pre-outbreak basal area and density of aspen advance regeneration (Fig. 4, Table 4). Advance regeneration and residual overstory density differed across local moisture conditions of the Medicine Bow Range (Table 3, Fig. 5). Total advance regeneration (seedling and saplings) density was higher on the wetter northwest side than on the dry southeast side (Fig. 5). Total seedling density was also higher on the wetter northwest side than the dry southeast side (Fig. 5). Total sapling and live overstory densities, however, were higher on the dry southeast side than the wetter northwest side (Fig. 5). Lodgepole pine was more abundant in advance regeneration and live overstory in the dry southeast than the wetter northwest (Fig. 5). Subalpine fir, Engelmann spruce and aspen advance regeneration were more abundant in the wetter northwest than the dry southeast (Fig. 5). Live overstory density of subalpine fir and Engelmann spruce were higher in the wetter northwest than the dry southeast

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TOTAL AR PIEN AR ABLA AR Northing

PICO AR

Outbreak Intensity

Total Pre-outbreak Overstory Total PICO Overstory Easting Pre-outbreak Overstory BA

Axis 2

POTR AR

Pre-outbreak Overstory Density Class Low (<1000 spha) Moderate (1001-3500 spha) High (>3500 spha) Axis 1 Fig. 4. NMS of understory (seedlings and saplings) advance regeneration coded by pre-outbreak overstory density classes. Joint plot lines indicate the strength and direction of Pearson correlations (R2 > 0.2) between variables and stand axis scores. Final stress = 10.17799, axis 1 R2 = 43.8%, axis 2 R2 = 48.6%, cumulative R2 = 92.4%. Easting and northing are from UTM coordinates. PICO = lodgepole pine, PIEN = Engelmann spruce, ABLA = subalpine fir, POTR = aspen, AR = advance regeneration density, Total = total overstory and sapling density (spha), total PICO overstory and pre-outbreak overstory = density (spha), BA = basal area.

Table 3 A-statistic and p-values from MRPP for comparisons of residual stand composition (with and without live overstory) within different geographic, mortality, and overstory structure classifications. See methods for definitions of classifications. P-values < 0.05 (in bold) indicate statistical significance. A-statistics > 0.10 (in bold) have high within-group homogeneity. Groups compared

Groups (#)

Dry southeast vs. wetter northwest Outbreak intensity classes Pre-outbreak overstory density classes Lodgepole pine overstory density classes Total stand density classes

With live overstory

2 3 3 4 4

Table 4 Correlations between different overstory, advance regeneration, moisture condition (geographic location) variables and stand community scores from 2-D NMS ordination. PICO = lodgepole pine, PIEN = Engelmann spruce, ABLA = subalpine fir, POTR = aspen. Bold correlations are >0.5. Variable

Axis 1

Axis 2

Lodgepole pine overstory density Pre-outbreak overstory density Easting Total density Pre-outbreak basal area PICO advance regeneration density Outbreak intensity POTR advance regeneration density PIEN advance regeneration density Northing Total advance regeneration density ABLA advance regeneration density

0.716 0.608 0.546 0.472 0.406 0.372 0.307 0.389 0.424 0.455 0.555 0.577

0.004 0.025 0.062 0.012 0.331 0.357 0.177 0.527 0.325 0.111 0.264 0.27

Without live overstory

A

p

A

p

0.10 0.023 0.24 0.28 0.05

0.01 0.27 0.0005 0.0002 0.19

0.10 0.03 0.18 0.21 0.04

0.008 0.19 0.002 0.0009 0.21

(Fig. 5). Aspen had higher live overstory density in the dry southeast than the wetter northwest (Fig. 5). Snag density was similar across local moisture conditions of the Medicine Bow Range for all species.

4. Discussion 4.1. Species composition and density All lodgepole pine dominated stands sampled in southeastern Wyoming contained considerable amounts of advance regeneration. The current advance regeneration is dense enough to restock stands at acceptable levels (based on USDA (2003) stocking density guidelines), if not at pre-outbreak levels, even following the death of most of the overstory. Similar levels of advance regeneration were also found following MPB outbreaks in Colorado (Rocca and

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Fig. 5. Average density (spha) per stand by species for different size classes across different local moisture conditions i.e., dry southeast (SE) and wetter northwest (NW) side of the Medicine Bow Range. PICO = lodgepole pine, PIEN = Engelmann spruce, ABLA = subalpine fir, POTR = aspen, Total Advance Regeneration is seedlings and saplings combined.

Romme, 2009; Collins et al., 2011; Diskin et al., 2011) and British Columbia (Nigh et al., 2008; Coates et al., 2009; Vyse et al., 2009). It is likely that the advance regeneration will experience a growth release and form new overstory as previously observed in the US Intermountain West (Cole and Amman, 1980; Romme et al., 1986; Veblen et al., 1991b; Collins et al., 2011) and Canada (Heath and Alfaro, 1990; Hawkes et al., 2004; Dordel et al., 2008). Species composition of the advance regeneration varied by forest type but all species present in the overstory were also present in the advance regeneration, regardless of shade tolerance. Lodgepole pine, which is often considered shade intolerant (Burns and Honkala, 1990), was abundant in the advance regeneration in all forest types in our study area. Considerable lodgepole pine advance regeneration was also found following MPB outbreaks in Colorado (Collins et al., 2011; Diskin et al., 2011), Idaho (Lewis Murphy et al., 1999), Oregon (Stuart et al., 1989), and British Columbia (Williams et al., 1999; Nigh et al., 2008; Coates et al., 2009; Vyse et al., 2009). This was somewhat surprising, as subalpine fir and Engelmann spruce are more typical shade tolerant advance regeneration tree species (Veblen, 2000; Burns and Honkala, 1990). Aspen, which typically regenerates by sprouting (Burns and Honkala, 1990), was the only deciduous tree species found on our sites. Considerable density of aspen suckers occurred in advance regeneration on sites with aspen in the overstory. Similarly, a pulse of aspen establishment via sprouting was seen following spruce beetle outbreak in Colorado (Nelson, 2009; Collins et al., 2011; Diskin et al., 2011), Utah (DeRose and Long, 2010) and MPB in Canada (Hawkes et al., 2004). In addition to the current advance regeneration, new germinants may establish as the overstory opens further due to continued overstory mortality, loss of needles from dead trees, and snag fall. Establishment of new germinants has been observed following MPB outbreak in Colorado (Collins et al., 2010, 2011) and spruce beetle outbreak in Alaska (Boggs et al., 2008). However, other studies have documented little establishment of new germinants following spruce beetle (Veblen et al., 1991b; DeRose and Long, 2010) or MPB (Astrup et al., 2008; Hawkes et al., 2004) outbreaks. Establishment of new germinants is likely to be species specific and dependent on seed sources and suitable microsites

for establishment (Burns and Honkala, 1990; Astrup et al., 2008; Collins et al., 2011). Seed sources should not be limiting in mature forests, such as these, even for serotinous lodgepole pine (see Aoki et al., 2011). New lodgepole pine and subalpine fir germinants were documented following MPB in Colorado (Collins et al., 2010, 2011), where unlike British Columbia there is not a significant moss layer to inhibit seedling establishment (see Astrup et al., 2008). Regardless of new germinant establishment, no stands completely lacked advance regeneration. While the residual overstory may influence seedling establishment initially, variation in lodgepole pine density has been shown to converge overtime due to infilling in sparse stands and thinning in dense stands (Kashian et al., 2005). Therefore, advance regeneration should be adequate to produce a new overstory in all areas as seen in forest regeneration modeling (see Collins et al., 2011; Diskin, 2010). While the advance regeneration and seedling establishment represent the future structure of these stands, for now there remains a considerable amount of residual overstory of all species in all stands. Currently, there appears to be a lack of conversion to a shade-tolerant species dominated overstory as documented following other beetle outbreaks (Amman, 1977; Veblen et al., 1989, 1991b; DeRose and Long, 2010) largely due to the continued presence of lodgepole pine in the overstory. Similarly, other studies have not found large areas with complete overstory lodgepole pine mortality (Nelson, 2009; Rocca and Romme, 2009; Diskin et al., 2011). However, it is difficult to predict how many of the remaining overstory lodgepole pine will survive the current outbreak. Historically, severe MPB outbreaks have killed up to 100% of the overstory trees (Schmid and Mata, 1996). However, less severe outbreaks have much lower mortality of overstory trees (Cole and Amman, 1980; Hawkes et al., 2004). At current levels of retention, lodgepole pine continues to be the primary overstory species even in the spruce-fir forest type. 4.2. Comparisons between advance regeneration and pre-outbreak overstory MPB outbreak effects on forest succession appear to vary by forest type. In the absence of fire, pure lodgepole pine stand

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trajectories are shifted towards an uneven-aged lodgepole pine forest, while spruce-fir stand trajectories are shifted towards late-seral species dominance. As documented in British Columbia (Nigh et al., 2008; Axelson et al., 2009; Coates et al., 2009; Vyse et al., 2009) and Colorado (Diskin et al., 2011), stands with primarily lodgepole pine in the overstory were dominated by lodgepole pine in the advance regeneration. The pure lodgepole pine forests in this study appear to be ‘‘climax’’ lodgepole pine with lodgepole pine advance regeneration under lodgepole pine overstory. These forests will become uneven-aged lodgepole pine forests with successive MPB outbreaks and the development of lodgepole pine advance regeneration (Amman, 1977; Romme et al., 1986; Sibold et al., 2007; Diskin, 2010). Uneven-aged lodgepole pine stands have also been documented as a result of MPB outbreak or fire in Oregon (Stuart et al., 1989) and Canada (DeLong and Kessler, 2000; Hawkes et al., 2004), and have resulted in increased structural diversity of pure lodgepole pine forests in Rocky Mountain forests (Romme et al., 1986). The dynamics in these pure lodgepole pine stands could change if the current MPB outbreak is affecting smaller diameter trees (Cain and Hayes, 2009; Stockdale et al., 2004) or is of higher intensity than typical outbreaks due to changing climate (Ayres and Lombardero, 2000; Logan et al., 2003; Stireman et al., 2005; Lundquist and Bentz, 2009). While there did not appear to be a major change in forest type between the pre-outbreak overstory and the advance regeneration (Fig. 3), there may be a shift in the overall species composition of spruce-fir stands due to the MPB outbreak. The impact of MPB outbreaks on these stands should be similar to historic outbreaks in ‘‘seral’’ lodgepole pine forests in accelerating succession towards subalpine fir overstory by removing the lodgepole pine overstory (Amman, 1977; Veblen, 2000; Hawkes et al., 2004; Diskin, 2010). Similar acceleration of succession has been seen following other types of overstory disturbance in the Rocky Mountains (Veblen et al., 1989, 1991b). In addition to significant lodgepole pine mortality leading to increase in the relative proportion of shade-tolerant subalpine fir and Engelmann spruce in the overstory, subalpine fir was also the dominant seedling present in the advance regeneration, as found by Diskin et al. (2011). Subalpine fir is a shade-tolerant species and overstory disturbances, such as wind throw (Veblen et al., 1989) and bark beetle outbreaks (Astrup et al., 2008; Nigh et al., 2008; DeRose and Long, 2010; Diskin, 2010), have been shown to shift species composition towards this species in the Rocky Mountains and British Columbia. The majority of the subalpine fir, however, was concentrated in the seedling layer and may not survive to canopy closure (Veblen, 1986; DeRose and Long, 2010). However, if subalpine fir seedlings are released, as seen with mature trees following spruce beetle outbreak (Veblen et al., 1991b), the probability of mortality decreases as growth increases (Kobe and Coates, 1997). Additionally, mature subalpine fir and Engelmann spruce in the overstory provide a seed source for future seedling establishment (Astrup et al., 2008; Collins et al., 2011). All of these factors would contribute to shifting spruce-fir stands from lodgepole pine dominated stands towards spruce-fir dominated stands as demonstrated by Collins et al. (2011). Aspen influenced stands were unique from both spruce-fir and pure lodgepole stands. The majority of these stands contained abundant aspen suckers in addition to significant regeneration of sub-alpine fir. Aspen is generally considered an early-seral species that typically reproduces asexually (Burns and Honkala, 1990). In one year of sampling it was not possible to determine if aspen regeneration were new sprouts or suckers that had existed previously under the canopy. A pulse of aspen sprouting has been documented following disturbances including bark beetle outbreaks (Nelson, 2009; DeRose and Long, 2010; Diskin et al., 2011) and fire (Loope and Gruell, 1973; Brown and DeByle, 1989; Romme et al., 1995). Similarly, multiple MPB outbreaks increased aspen cover

in Utah (Stone and Wolfe, 1996) and Dordel et al. (2008) found that MPB outbreaks in Canada promoted hardwood species in the absence of herbivory. Accession to the overstory for aspen is often limited by browsing (Romme et al., 1995; Dordel et al., 2008; DeRose and Long, 2010). Heavy browsing is possible given that there is an abundant elk herd in the Medicine Bow Range (>7000 individuals; WDGF, 2009). However, Nelson (2009) did not find an increase in browsing with increased aspen sucker densities following MPB outbreak in Colorado. Significant subalpine fir regeneration in most of the aspen influenced stands will likely dominate the overstory in the long term following the decline of aspen (Diskin, 2010; Collins et al., 2011). In addition to bark beetle outbreaks, fire is a major disturbance type that influences lodgepole pine forest development in the Rocky Mountains. While the impact of bark beetle outbreaks on fire susceptibility and fire behavior is still debated (i.e., Bebi et al., 2003; Lynch et al., 2006; Page and Jenkins, 2007; Simard et al., 2010), the result of fire in these forests will be similar. Lodgepole pine forests regenerate after fire (Romme and Knight, 1981; Veblen et al., 1991a). Following fire, lodgepole pine and aspen regenerate vigorously via seeds and sprouts, respectively (Burns and Honkala, 1990). Subalpine fir and Engelmann spruce are slower to regenerate following fire (Burns and Honkala, 1990). If fire were to burn through these forests at any point in the future, the dynamics would shift back towards lodgepole pine dominance in all forest types.

4.3. Influence of moisture conditions, outbreak intensity and stand characteristics Light and moisture regimes, in addition to other factors, affect the growth and survival of advance regeneration (e.g., Pacala et al., 1994; Chen et al., 1996; Kobe and Coates, 1997; Wright et al., 1998; Krasowski and Wang, 2003). We found pronounced differences between the relative and absolute abundances of species, both in the advance regeneration and the pre-outbreak overstory composition, between stands with different relative moisture conditions. Previous studies have shown that different tree species have different moisture requirements for regeneration (Williams et al., 1999; Nigh et al., 2008). Shade intolerant lodgepole pine was more prevalent in both the advance regeneration and the pre-outbreak overstory on drier sites than on more moist sites. Additionally, the prevalence of lodgepole pine in the drier areas accounts for the higher density of these stands, as shade tolerance within a species increases on drier sites (Carter and Klinka, 1992; Williams et al., 1999). Many other factors influence lodgepole pine density, including serotiny, fire interval, and soil fertility (Schoennagel et al., 2003). Subalpine fir and Engelmann spruce are more likely to dominate the overstory in moist sites (Romme and Knight, 1981) and were much more common in the overstory and the advance regeneration in wetter stands. Overstory density significantly influenced the advance regeneration, but the magnitude of the influence differed by tree species. Similar to our findings, overstory density has been shown to decrease the establishment of understory trees in Canada following MPB outbreaks (Astrup et al., 2008; Nigh et al., 2008). Surprisingly, the relationship did not hold true for lodgepole pine advance regeneration, which increased with increasing overstory density. However, similar lodgepole pine advance regeneration has been found in high and low light regimes in British Columbia (Williams et al., 1999). Contrary to our results, Astrup et al. (2008) found that the amount of lodgepole pine advance regeneration decreased with increasing overstory basal area. This discrepancy may be due to lodgepole pine regenerating under lodgepole pine overstory. Stuart et al. (1989) found that in self-perpetuating lodgepole pine stands

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in Oregon, moisture and microclimate were limiting to advance regeneration, rather than light. 4.4. Management implications It appears that active management intervention is not necessary to ensure reforestation following the severe MPB outbreak in the Medicine Bow Range. Using the advance regeneration to restore forests is compatible with natural processes in these forests and is a viable management option. The MPB is a native insect and forests have historically recovered from MPB outbreak via advance regeneration (Romme et al., 1986; Heath and Alfaro, 1990; Sibold et al., 2007). Additionally, relying on the advance regeneration for reforestation should not substantially alter the species composition of these forests, particularly on dry sites dominated by only lodgepole pine. The proportion of late-seral, shade tolerant species may be higher than prior to the outbreak (e.g. Collins et al., 2011) particularly on wet sites. While the relative density of lodgepole pine has decreased, there are still significant density of lodgepole pine stems present in all but one stand. Additionally, as stated above, since lodgepole pine is generally thought to be shade intolerant and to regenerate following disturbance (Burns and Honkala, 1990) it is likely that lodgepole pine density will continue to increase in these stands over time (see Kashian et al., 2005). Fire would also favor lodgepole pine over more shade tolerant species. In areas that exhibit limited advance regeneration, as seen in one stand in the current study and Diskin et al. (2011), recovery to closed canopy forest may take longer (Diskin, 2010). If rapid recovery in areas with low density advance regeneration areas on dry sites or a specific species composition is desired, for example for timber management, planting may be necessary. Predicting the amount and composition of advance regeneration may be possible based on site and stand characteristics. Therefore, locating potential areas with limited advance regeneration or altered species compositions that are in need of reforestation would be possible based on existing information. MPB is likely to be a continuing factor in the forests of southeastern Wyoming. Homogeneity in tree age and size across the landscape appear to have increased the susceptibility of western forests to MPB at the onset of the outbreak (Hicke and Jenkins, 2008; Cain and Hayes, 2009). Forests recovering naturally from advance regeneration are more likely to have a diversity of tree size and age classes both within and among stands. Heterogeneity in tree size and age class at both the landscape and the stand scale may prevent an epidemic of these proportions from occurring in the next generation of Medicine Bow Range forests. Acknowledgements This project was funded by a University of Wyoming NASA Space Grant Consortium Faculty Research Grant. The authors would like to thank Sara Beaver and Carolyn Swift for assistance with all field and lab work; and Bill Romme, Travis Woolley and Dave Shaw for thoughtful reviews of an earlier draft of the manuscript. References Agee, J.K., 1993. Fire Ecology of Pacific Northwest Forests. Island Press, Washington, D.C. Amman, G.D., 1977. The role of mountain pine beetle in lodgepole pine ecosystems: impact on succession. In: Mattson, W.J. (Ed.), The Role of Arthropods in Forest Ecosystems. Springer–Verlag, New York, pp. 3–18. Aoki, C.F., Romme, W.H., Rocca, M.E., 2011. Lodgepole pine seed germination following tree death from mountain pine beetle attack in Colorado. USA. Am. Mid. Nat. 165, 446–451.

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