Carbon storage recovery in surviving live lodgepole pine (Pinus contorta var. latifolia) 11 years after mountain pine beetle attack in northern British Columbia, Canada

23 We studied the recovery of tree and stand-level C-storage in a lodgepole pine 24 ( Pinus contorta var. latifolia ) forest in northern British Columbia that experienced 25 substantial (~83%) mortality in 2006-07 (total loss by 2013 = 86%) during a 26 severe mountain pine beetle (MPB) ( Dendroctonus ponderosae ) infestation. 27 Earlier work suggested that this forest recovered positive annual C-storage 3 28 years after attack based on eddy-covariance measurements. We sought to 29 confirm these results by examining C-storage in surviving pine trees using tree 30 core analysis. Average growth release of surviving lodgepole pine trees was 31 392% (range -53% to 2326%) compared to mean decadal growth prior to MPB 32 attack. Nearly 97% of trees underwent a growth release, considerably higher 33 than the 15-75% reported for lodgepole pine in previous studies. Mean annual 34 stem C-storage of the surviving trees in this study was highly correlated (r=0.88) 35 with 10 years of annual net ecosystem productivity estimates made using the 36 eddy covariance technique, indicating that surviving lodgepole pine remain an 37 important part of C-recovery after MPB attack. Mean annual stem C-storage was 38 also highly correlated (r=0.92) with the cumulative percent of downed stems ha -1 39 at the site, suggesting that increased availability of resources is likely assisting the growth release.

D r a f t 4 67 surviving trees to increase their radial and vertical growth rates ( Veblen et al. 68 1991;Dhar and Hawkins 2011;Coyle et al. 2016). Hawkins et al. (2012) and 69 Amoroso et al. (2013) found that pine-dominated stands were able to recover 70 volume rapidly after MPB-outbreaks as a result of significant growth release in 71 surviving trees. Together, these findings strongly support the premise that 72 compensatory growth of surviving trees is responsible for the rapid recovery of 73 stand-level net ecosystem productivity (NEP) after MPB attack, providing 74 significant stand recovery of tree volume (Alfaro et al. 2003;Hawkins et al. 2012;75 Pelz and Smith 2012;Amoroso et al. 2013).

76
Dendrochronology has been used to determine the spatial extent of 77 historic MPB outbreaks to better understand the unprecedented nature of the 78 recent outbreak (Jarvis and Kulakowski 2015). Through tree core analysis, radial 79 growth before and after large disturbances such as MPB-outbreaks can be used 80 to quantify the timing of the disturbance and the growth response of the trees 81 (Alfaro et al. 2003;Amoroso et al. 2013) Growth release following MPB 82 outbreaks has been observed to range from 15-75% in surviving overstory trees 83 and up to 90% for understory trees (Axelson et al. 2009(Axelson et al. , 2010Amoroso et al. 84 2013). Individual surviving trees have been observed to increase their growth by 85 up to ~750% of the pre-outbreak radial growth rate (Amoroso et al. 2013), aiding 86 in the rapid recovery of C-storage, tree stem volume and ecological function of a 87 stand (Hawkins et al. 2012;Alfaro et al. 2015).

88
While past research suggests surviving trees can release following an 89 MPB outbreak (Alfaro et al. 2003;Axelson et al. 2009Axelson et al. , 2010Amoroso et al. D r a f t D r a f t 6 113 2012) and Bowler et al. (2012). The site receives little growing season 114 precipitation (230mm between May and September) and the soils are coarse 115 textured with 34% coarse fragments by volume

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The growth release response of the pine trees were placed into 4 299 categories: low (0-50%), moderate (50-100%), high (100-400%), and very high 300 (>400%; Fig. 3) based on the distributions observed at the site. Smaller trees 301 were more commonly in the very high range of growth release than larger trees 302 (Fig. 3)  D r a f t 23 423 than stands with <70% mortality. Supporting these findings, the high mortality 424 rate (>70%) at our study sites was associated with a high percentage of trees 425 releasing (96.9%) and a high average release of 392%. Our results were also in 426 general alignment with EC measurements of NEP at this site 427 Fig. 4) and scaled-up leaf-level gas-exchange results of Bowler et al. (2012).
428 Together, they suggest that surviving pine trees are a major part of ecosystem C-429 storage recovery after attack.

Effects of stand characteristics and environmental factors on ring widths
432 Size class was expected to affect the growth release and C-storage 433 increase of surviving trees. Smaller trees were expected to have a higher 434 percent release, on the assumption that they were likely younger trees, and 435 therefore more likely to respond to release. However, we also suspected that 436 larger trees should still have a higher C-storage increase as larger trees store 437 more C per unit of radial growth. Smaller trees were not younger than larger 438 trees indicating that they likely had more competitive growing conditions than 439 larger trees before the outbreak. Both were able to respond to decreased 440 competition; however, smaller trees had a higher percent growth release than 441 larger trees (476% vs 308%). Even though smaller trees had a larger percent 442 release, their post-outbreak mean annual ring-width of 0.917 mm was less than 443 the larger tree mean annual ring-width of 1.503 mm. Overall, the effect of 444 diameter class on percent release was significant, with the smaller trees having a D r a f t 24 446 significant relationship. However, Amoroso et al. (2013) found that trees less the 447 20 cm DBH at attack had higher releases, commensurate with our study site 448 release as all surviving trees had diameters less than 20 cm.

449
Higher stand densities may affect the release of the remaining trees. In 450 our study, stand location was found to significantly affect the growth release.
451 Stand densities varied among the eight plot locations (  (Bowler et al. 473 2012;Brown et al. 2012). In years with low tree growth, NEP at the site was 474 negative (Fig. 4). This supports the predictions of Bowler et al. (2012) andBrown 475 et al. (2012) that surviving trees are a major contributor to NEP at our site. While 476 we did observe a relatively strong correlation between NEP and tree C-storage 477 ( Fig. 4; R 2 =0.77) across years in our stand, some of the variation we did observe 478 in our relationship could have been related to shifts of carbon allocation to radial 479 growth in subsequent years as observed by Teets et al. (2018) (Winkler et al. 2012). Coates and Hall (2005) predicted that an even greater 522 increase in canopy transmittance would occur following fall-down of snags as 523 stems and small branches can block a significant amount of light. Hence, the 524 delay in growth response that we observed in understory pine trees were 525 undoubtedly due to the time required for the surviving trees to take advantage of 526 increased light and other resources following the multi-year canopy tree death 527 and gradual fall-down of lodgepole pine that occurred after the MPB attack in 528 British Columbia.