Annual understory plant recovery dynamics in a temperate woodland mosaic during a decade of ecological restoration

Temperate woodlands are one of the world’s ecosystems in greatest need of ecological restoration, but relatively little is known about their floristic recovery dynamics over decadal timescales. From 2000 to 2012, we monitored understory plant communities in a woodland mosaic in Missouri, USA, as it underwent restoration via prescribed, dormant-season burning and mechanical thinning of red cedar (Juniperus virginiana) and exotic shrubs. Native species richness increased linearly by 36% over this time period, driven primarily by an influx of forb species in thin-soiled upland areas where red cedar was removed. Floristic quality also increased with differential dynamics across local communities; forest floristic quality saturated quickly whereas floristic quality increased gradually over the time series in woodlands and red cedar–dominated woodlands. Species that underlay these patterns were mainly ruderal or matrix forbs and grasses with little dependence on intact, undisturbed habitats. In contrast, conservative species were rare or absent. This case study suggests that understory plant recovery dynamics may be slower in harsher and more degraded sites and faster in more mesic sites within a woodland mosaic. Our observations set a benchmark for woodland understory plant recovery dynamics and indicate that a future restoration challenge is to prioritize the managed translocation of dispersal-limited, conservative species.

Methods
To monitor the influence of restoration activities on herbaceous vegetation, 30 permanent 50-m transects were established in 2000, one year prior to the first prescribed burn. Transects were selected by placing a grid over a topographical map and choosing grid coordinates from a random number table. Transects were evenly distributed among three identifiable plant communities: an upland community dominated by white oak (Quercus alba), a mesic slope community dominated by northern red oak (Q. rubra), paw paw (Asimina triloba), and spicebush (Lindera benzoin), and an invaded community dominated by eastern red cedar (Juniperus virginiana). Transects were separated by =5 m and were selected to maximize elevational gradient. Slope and aspect were uncontrolled. Vegetation was sampled in three strata: ground layer (<0.5 m height), shrub layer (0.5-3 m), and canopy. Ground and shrub layer plant abundance and cover were sampled twice per year (Apr, Jun) in five nested quadrats along each transect. Ground layer quadrats were 0.5 sq-m, and shrub quadrats were 1 sq-m in Apr and 2 sq-m in Jun. Quadrats were offset by five meters between seasons to reduce impact on the vegetation. Herbaceous and shrub layer sampling were conducted in all years 2000-2012 except 2006, when there was little vegetation due to restoration activities. Canopy composition and diameters at breast height were sampled along each transect using a crown line-intercept technique (Cox 1980). Canopy sampling was conducted in 2000, 2004, 2007, and 2012. Following prescribed fires, the percentage of each transect that had burned was also estimated. Plants were initially identified using Steyermark (1963), and taxonomy was subsequently updated to Yatskievych (1999, 2006, 2013). Voucher specimens were deposited at Missouri Botanical Garden. In 2016, Olivia Hajek (a Research Experience Undergraduate) collected environmental data for each quadrat. She measured elevation using a Garmin GPSmap. She measured aspect using a compass. She measured slope using a clinometer; slope was measured over a 3-m distance centered on the quadrat. To calculate a relative radiation index (RRI), we used the formula RRI = cos (180° – O) x sin ß x sin ' + cos ß x cos ', where O = aspect, ß = slope, and ' = latitude (Maren et al. 2015). Canopy cover was estimated using a spherical densiometer. The percent of exposed rock in each quadrat was also recorded based on subjective evaluation on a rank-transformed scale with 0=0% cover, 1=0-5%, 2=5-25%, 3=25-50%, 4=50-75%, 5=75-95%, and 6=95-100%. Burned or cut Juniper stumps were counted within a 2.5-m radius centered on each herb quadrat.

温带林地是全球最亟需生态修复的生态系统之一，但学界对其十年尺度下的植物区系恢复动态仍知之甚少。2000年至2012年，我们对美国密苏里州一处林地镶嵌体的林下植物群落开展了长期监测，该区域正通过休眠季计划火烧、机械疏伐北美圆柏（Juniperus virginiana）与外来灌木的方式实施生态修复。在此期间，本土物种丰富度线性增长36%，这一变化主要源于北美圆柏移除后，薄土高地生境中阔叶草本植物（forb）的大量迁入。植物区系质量同样呈现分异的动态特征：森林群落的区系质量快速趋于饱和，而普通林地与北美圆柏占优群落的区系质量则随监测时长逐步提升。支撑上述变化的物种主要为逸生型或广布型阔叶草本与禾草，它们几乎不依赖完整未受干扰的生境；与之相反，保守型物种（conservative species）则极为罕见甚至缺失。本案例研究表明，在林地镶嵌体中，生境条件更严苛、退化程度更高的区域林下植物恢复动态更为缓慢，而湿润生境则恢复更快。本研究结果为林地林下植物恢复动态建立了基准参照，并指出未来生态修复的核心挑战之一，是优先开展扩散受限的保守型物种的人工迁地定植工作。

研究方法
为监测修复活动对草本植被的影响，我们于2000年（首次计划火烧前一年）布设了30条固定的50米样带。样带布设方式为：在地形图上绘制网格，通过随机数表选取网格坐标确定样带位置。样带均匀分布于3种可明确辨识的植物群落中：以白栎（"Quercus alba"）为优势种的高地群落、以北美红栎（"Q. rubra"）、泡泡树（"Asimina triloba"）与山胡椒（"Lindera benzoin"）为优势种的湿润坡地群落，以及以东部北美圆柏（"Juniperus virginiana"）为优势种的入侵群落。样带间距不小于5米，布设时尽可能覆盖最大的海拔梯度范围。坡度与坡向未做人为控制。
植被调查分为三个层次：地被层（株高<0.5米）、灌木层（0.5-3米）与乔木层。地被层与灌木层的植物多度与盖度每年于4月、6月各调查一次，沿每条样带设置5个嵌套样方开展取样。地被层样方面积为0.5平方米，灌木层样方在4月为1平方米、6月为2平方米。为降低对植被的干扰，两季调查的样方间距设置为5米。
2000年至2012年的所有年份均开展了草本层与灌木层的取样工作，仅2006年除外——该年度因修复活动导致植被覆盖度极低，未开展调查。乔木层的物种组成与胸径则通过冠层线截法（Cox 1980）沿样带开展调查。乔木层调查分别于2000年、2004年、2007年与2012年进行。计划火烧实施后，还会估算每条样带的火烧占比。
植物物种初始鉴定参考Steyermark（1963）的著作，后续分类学命名则依据Yatskievych（1999、2006、2013）的研究进行更新。凭证标本存放于密苏里植物园。
2016年，本科生科研实习项目参与者Olivia Hajek为每个样方收集了环境数据：使用Garmin GPSmap测量海拔高度，使用罗盘测量坡向，使用测斜仪测量坡度——坡度测量范围以样方为中心，覆盖3米距离。为计算相对辐射指数（Relative Radiation Index, RRI），我们采用如下公式：RRI = cos(180° – O) × sinβ × sinφ + cosβ × cosφ，其中O为坡向，β为坡度，φ为纬度（Maren et al. 2015）。乔木层盖度使用球面密度仪进行估算。同时，基于主观评估对每个样方的裸露岩石占比进行分级记录：0级对应0%覆盖度，1级对应0%-5%，2级对应5%-25%，3级对应25%-50%，4级对应50%-75%，5级对应75%-95%，6级对应95%-100%。在每个草本样方为中心的2.5米半径范围内，统计被火烧或砍伐的圆柏伐桩数量。