Long-Term Impacts of the Hemlock Woolly Adelgid on Forest Carbon at Harvard Forest 2008-2011

The abundance of eastern hemlock (Tsuga canadensis) in eastern US forests has declined since the 1950s owing to the introduction of the non-native insect, hemlock woolly adelgid (HWA, Adelges tsugae). In southern New England, eastern hemlock is being replaced by the deciduous tree species, black birch (Betula lenta). To date there is little understanding of whether hemlock loss will fundamentally alter ecosystem C balance and component fluxes. In this study, we use a comparative approach to study potential changes in C fluxes and storage and N cycling associated with HWA-induced hemlock decline and replacement. The stands include primary- and secondary-growth hemlock forests (230 and 132 years old, respectively), recently disturbed stands (5 and 18 years old) that now have rapidly growing black birch saplings, and a mature black birch stand of age similar to the second-growth hemlock stand. We addressed the question of whether the quantity and distribution of C pools in black birch forests are the same as those found in the hemlock stands they replace and, if so, over what time scales. We found that if HWA did not infest hemlock stands in central MA, C stocks in these secondary stands could still increase by at least 30% over a period of 100 years. Girdling, intended to simulate HWA infestation, resulted in a large transfer of C from live biomass to coarse woody debris five years after treatment, but had little effect on total ecosystem C content. A former hemlock stand killed by HWA and now dominated by black birch saplings also had a large pool of highly decayed CWD and a rapidly aggrading C pool in live biomass. C pools in biomass in a mature, secondary growth black birch stand 135 years since pastureland abandonment were as large as those in a primary-growth hemlock stand 235 years of age. We also found that aboveground net primary production was higher in the aggrading black birch stand and significantly so at 18-years post-HWA compared to the secondary-hemlock stand it would likely replace. Rapid forest regrowth was accompanied by significantly higher rates of N uptake from the soil but also higher N-use efficiency because most of the N taken up from the soil was allocated to the production of wood with a high C-to-N ratio. In contrast to patterns of aboveground production, the rate of soil respiration was lowest in the young stands and not significantly different from the second-growth hemlock stand, suggesting little net effect of stand replacement on soil C efflux. The leaf litter decomposition study showed that black birch litter decomposed more rapidly than hemlock litter but that there was no effect of stand type on the rate of decomposition. Analyses of extracellular microbial exoenzyme activity painted a more nuanced pattern of variation among stands, with fine root biomass the only weakly explanatory variable. Based on this analysis, it appears that ecosystem C storage is resilient to the loss of hemlock because of vigorous regrowth by black birch. These results suggest that forests affected by HWA in southern New England will remain a sink for atmospheric CO2 despite reorganization of stand structure and species composition.自20世纪50年代以来，美国东部森林中的东部铁杉（Tsuga canadensis）种群丰度因外来昆虫铁杉球蚜（hemlock woolly adelgid, HWA, Adelges tsugae）的传入而持续下降。在新英格兰南部地区，东部铁杉正被落叶树种黑桦（Betula lenta）所取代。迄今为止，学界对铁杉消失是否会从根本上改变生态系统碳平衡及其组分通量仍知之甚少。 本研究采用比较研究方法，探究与铁杉球蚜诱导的铁杉衰退及植被替代相关的碳通量（C fluxes）、碳储量（C storage）与氮循环（N cycling）的潜在变化。研究样地涵盖原始生长林与次生生长林型的铁杉林（树龄分别为230年与132年）、近期受干扰的样地（受干扰时长分别为5年与18年，当前已生长出快速发育的黑桦幼树），以及一片与次生铁杉林树龄相近的成熟黑桦林。本研究旨在解答两个核心问题：其一，黑桦林碳库的数量与分布是否与其所取代的铁杉林一致？其二，若一致，该一致性的时间尺度为何？ 研究发现，若马萨诸塞州中部的铁杉林未遭受铁杉球蚜侵染，这些次生铁杉林的碳储量在100年内仍可至少提升30%。环剥（girdling）处理——用于模拟铁杉球蚜侵染——在处理五年后导致大量碳从活生物量转移至粗木质残体（coarse woody debris, CWD），但对生态系统总碳含量影响甚微。一处曾受铁杉球蚜侵染致死、如今以黑桦幼树为优势种的原铁杉林，同样拥有大量高度腐解的粗木质残体碳库，以及活生物量中快速累积的碳库。一处因弃牧已有135年的成熟次生黑桦林，其生物量碳库规模可与树龄235年的原始生长铁杉林相当。 我们还发现，处于快速恢复阶段的黑桦林的地上净初级生产力（aboveground net primary production）更高，在受铁杉球蚜侵染18年后的样地中，该生产力显著高于其将取代的次生铁杉林。森林快速恢复的同时，土壤氮吸收速率显著提升，但氮利用效率也更高——因为从土壤吸收的大部分氮被分配至碳氮比更高的木材生产中。与地上生产力模式不同，年轻样地的土壤呼吸（soil respiration）速率最低，且与次生铁杉林无显著差异，这表明林分更替对土壤碳排放的净影响极小。叶片枯落物分解研究显示，黑桦枯落物的分解速率快于铁杉枯落物，但林分类型对分解速率并无影响。胞外微生物胞外酶活性（extracellular microbial exoenzyme activity）的分析则揭示了林分间更为复杂的变异模式，仅细根生物量可作为微弱的解释变量。 基于上述分析可知，由于黑桦的旺盛恢复，生态系统碳存储对铁杉消失具有恢复力。这些结果表明，尽管新英格兰南部受铁杉球蚜影响的森林发生了林分结构与物种组成的重组，但其仍将作为大气CO₂的汇持续存在。