Landscape Response to Hemlock Woolly Adelgid in Southern New England 1997-2011

The hemlock woolly adelgid (Adelges tsugae Annand; HWA), a small, aphid-like
insect native to Japan, is currently migrating northward through eastern North
America and threatens to eliminate eastern hemlock (Tsuga canadensis (L.) Carriere),
one of the most abundant, long-lived shade tolerant species, across its range. In
addition, a second invasive pest, the elongate hemlock scale (Fiorinia externa; EHS),
often co-occurs with HWA on hemlock with unknown long-term consequences. The major
objectives of this study were: (1) To characterize the pre-HWA distribution,
composition, and structure of hemlock stands; (2) to characterize the spatial
patterns of damage generated by HWA across southern New England since the time of its
arrival in 1985; (3) to examine environmental and stand factors that are associated
with declines in crown vigor and mortality of hemlock; (4) examine the dynamics of
HWA and EHS in hemlock stands over time; and (5) assess whether there is a difference
in the response of these insects to abiotic conditions (winter temperature, summer
temperature, summer precipitation), and whether the distribution and abundance of
each insect species is dependent on biotic interactions with the co-occurring insect
species. Connecticut Stands (originally sampled in 1997 and 1998) Aerial photographs, photographic overlays, and extensive field study were used to
map and develop GIS overlays of almost 6000 hemlock stands in a 4900 km2 study region
extending from Long Island Sound northward to the Massachusetts border and including
the Connecticut River Valley in Connecticut, USA. Intensive sampling of a random
selection of 114 hemlock stands across the study area was used to document patterns
of hemlock infestation, vigor, and mortality in relation to stand and site
characteristics. Mantel tests were utilized to assess the relative importance of
environmental and stand variables in controlling the intensity of HWA infestation and
damage. Most stands were located along ridge tops, steep hillsides, and narrow
valleys. Hemlock importance values ranged from 22 to 96% and stand densities varied
from 300 to 1450 stems ha-1. Adelgid presence and adelgid-induced hemlock mortality
were found in 88% and 74% of the sampled forests, respectively. Approximately 25% of
stands were logged recently, ranging in intensity from partial hemlock cutting to
large clearcuts. A geographical trend in reduced HWA infestation intensity and tree
mortality and enhanced crown vigor of overstory and understory hemlock occurs from
south to north, coincident with the temporal colonization pattern of HWA. Mantel
analyses indicated that patterns of HWA infestation, hemlock mortality, and crown
vigor were most strongly correlated with latitude. Mortality was also weakly related
to aspect and stand size. Average mortality was highest on western aspects but
exceeded 20% on most slopes. Remaining trees averaged over 50% foliar loss, with no
significant difference among aspects. Results suggest that as HWA becomes abundant,
stands on xeric aspects succumb rapidly, but that stand and landscape variables such
as overstory composition and structure, slope, and elevation, exert little control
over susceptibility or eventual mortality. Ultimately, duration of infestation
controls the intensity of hemlock decline and mortality. Over 4,290 ha of hemlock
forest were eliminated by logging or HWA just within the southern part of our
transect since the mid-1980s, and we predict continued HWA infestation will lead to
unprecedented hemlock loss throughout the northeastern U.S., regardless of site
conditions or location. Massachusetts Stands (originally sampled in 2002-2004) Using aerial photographs, we documented hemlock distribution throughout central
Massachusetts and subsampled 123 stands to examine the spatial pattern of HWA and its
impact on tree vigor and mortality since its arrival in 1989. In the study region,
over 86,000 ha of hemlock forest were mapped in 5,127 stands. White pine (Pinus
strobus), red oak (Quercus rubra), red maple (Acer rubrum), and black birch (Betula
lenta) were common overstory associates. Hemlock abundance increased from south to
north, commonly on western and northwestern slopes. Average stand size was 55 ha,
overstory basal area ranged from 23 to 55m2 ha-1 and overstory stem densities
averaged 993 ha-1. By 2004, 40% of sampled stands were infested, but most stands
remained in good health overall; only 8 stands contained high HWA densities and only
two had lost >50% overstory hemlock. Out of fifteen stand and landscape predictor
variables examined, only latitude and winter climate variables were related to HWA
density. Cold temperatures appear to be slowing the spread and impact of HWA at its
northern extent as HWA infestation intensity and hemlock mortality and vigor were
significantly correlated with average minimum winter temperature. Contrary to
predictions, there was no regional increase in hemlock harvesting. The results
suggest that regional HWA-hemlock dynamics are currently being shaped more by climate
than by a combination of landscape and social factors. The persistence and migration
of HWA continues to pose a significant threat regionally, especially in the northern
portion of the study area, where hemlock dominates many forests. Insect dynamics over time We created a multivariate spatio-temporal model of the joint abundance of HWA and
EHS, which share a host plant. Data on abundance of both insects were examined from
the time the stand was initially sampled and again in 2005, 2007, 2009, and 2011. The
model revealed differences in the way each species responded to weather extremes, and
indicated a commensalism in which high abundance of HWA increased the probability of
subsequent infestation by EHS– but not vice versa. This study provides evidence that
incorporating biotic interactions into a species distribution model indicates whether
a species’ distribution and abundance is dependent on other species in the community,
and importantly, improves estimation of the abiotic niche for species whose abundance
depends on interactions with other species in the community.

铁杉球蚜（Hemlock Woolly Adelgid, Adelges tsugae Annand; 简称HWA）是一种类似蚜虫的小型昆虫，原产于日本。目前该虫正沿北美东部向北扩散，对东部铁杉（Tsuga canadensis (L.) Carriere）构成跨分布区灭绝的威胁——东部铁杉是该区域分布最广、寿命最长的耐阴树种之一。此外，另一种入侵害虫长形铁杉盾蚧（Elongate Hemlock Scale, Fiorinia externa; 简称EHS）常与HWA共同寄生于铁杉之上，二者协同危害的长期后果尚不明确。本研究的主要目标包括：(1) 解析HWA入侵前铁杉林的分布、组成与结构特征；(2) 梳理1985年HWA入侵新英格兰南部以来，该虫造成的危害空间格局；(3) 探究与铁杉冠层活力衰退及植株死亡相关的环境与林分因子；(4) 解析铁杉林中HWA与EHS的种群动态变化；(5) 评估两种昆虫对非生物环境（冬季气温、夏季气温、夏季降水）的响应差异，以及各自的分布与多度是否受共存昆虫的生物交互作用调控。

康涅狄格州样地（1997-1998年首次采样）
研究区域面积达4900平方千米，北抵马萨诸塞州边界，南至长岛海湾，涵盖美国康涅狄格州的康涅狄格河谷。研究团队通过航空照片、影像叠加与大规模野外调查，绘制了该区域近6000块铁杉林的地理分布图与地理信息系统（Geographic Information System, 简称GIS）叠加图层。随后随机选取114块样地开展密集采样，以记录铁杉的侵染、活力与死亡模式，及其与林分和立地特征的关联。本研究采用曼特尔检验（Mantel Test）评估环境与林分变量对HWA侵染强度与危害程度的相对调控作用。
研究区域内多数铁杉林分布于山脊顶部、陡峭山坡与狭窄山谷。铁杉重要值介于22%~96%，林分密度为300~1450株/公顷。88%的采样林分检出HWA，74%的林分出现HWA诱导的铁杉死亡。约25%的样地近期受过采伐，采伐强度从局部铁杉择伐到大规模皆伐不等。从南到北存在HWA侵染强度与树木死亡率降低、冠层及下层铁杉活力提升的地理梯度，与HWA的时间入侵路径一致。曼特尔分析显示，HWA侵染、铁杉死亡与冠层活力的空间格局与纬度相关性最强。死亡率还与坡向和林分规模呈弱相关：西向坡的平均死亡率最高，但多数坡向的死亡率均超过20%。剩余存活树木的平均叶损率超过50%，坡向间无显著差异。结果表明，当HWA种群达到一定丰度时，干旱立地的林分会快速衰亡，但林分与景观变量（如上层林分组成与结构、坡度与海拔）对树木易感性或最终死亡率的调控作用微弱。最终，侵染时长决定了铁杉衰退与死亡的严重程度。自20世纪80年代中期以来，仅研究区域南部就有超过4290公顷的铁杉林因采伐或HWA侵染消失，研究团队预测，无论立地条件与地理位置如何，HWA的持续侵染将导致美国东北部地区出现前所未有的铁杉大规模消亡。

马萨诸塞州样地（2002-2004年首次采样）
研究团队通过航空照片绘制了马萨诸塞州中部全境的铁杉分布地图，并抽取123块样地，以解析1989年HWA入侵以来的危害空间格局及其对树木活力与死亡的影响。研究区域内共绘制了5127块铁杉林，总面积超86000公顷。常见的上层伴生树种包括北美白松（Pinus strobus）、红栎（Quercus rubra）、红枫（Acer rubrum）与黑桦（Betula lenta）。铁杉多度从南到北逐渐升高，常见于西向与西北向山坡。样地平均面积为55公顷，上层林分胸高断面积介于23~55平方米/公顷，上层茎密度平均为993株/公顷。截至2004年，40%的采样样地被HWA侵染，但多数林分整体健康状况良好：仅8块样地的HWA侵染密度较高，仅2块样地的上层铁杉损失超过50%。在15个林分与景观预测变量中，仅纬度与冬季气候变量与HWA密度相关。低温似乎延缓了HWA在其分布北界的扩散与危害，因为HWA侵染强度、铁杉死亡率与活力均与冬季平均最低气温显著相关。与预测相反，该区域的铁杉采伐量并未出现区域性增长。研究结果表明，当前区域尺度的HWA-铁杉种群动态更多受气候调控，而非景观与人为因子的共同作用。HWA的持续定殖与扩散仍对区域构成显著威胁，尤其在研究区域北部，铁杉是多数森林的优势树种。

昆虫种群动态时序分析
研究团队构建了HWA与EHS的联合多度多元时空模型，二者共享铁杉作为寄主植物。研究利用样地初始采样数据，以及2005、2007、2009与2011年的调查数据，分析两种昆虫的多度变化。模型显示两种物种对极端天气的响应存在显著差异，并揭示了一种偏利共生关系：HWA的高丰度会提升后续EHS侵染的概率，但反之不成立。本研究证实，将生物交互作用纳入物种分布模型，可明确揭示物种的分布与多度是否依赖于群落中的其他物种，且重要的是，可提升对那些多度依赖于群落内其他物种交互作用的物种的非生物生态位估计精度。