Top-down regulation of hemlock woolly adelgid (Adelges tsugae) in its native range in the Pacific Northwest of North America.

The density of insect herbivores is regulated by top-down factors (e.g., natural enemies), bottom-up effects (e.g., plant defenses against herbivory), or a combination of both. As such, understanding the relative importance of these factors can have important implications for the establishment of effective management options for invasive species. Here, we compared the relative importance of top-down and bottom-up factors on the abundance of hemlock woolly adelgid (HWA), Adelges tsugae. HWA is invasive in eastern North America, but its native range includes the Pacific Northwest of North America where it has co-evolved with western hemlock, Tsuga heterophylla. Eastern hemlock, Tsuga canadensis, can also be found planted in city and park settings in the Pacific Northwest and the presence of both host species allowed us to directly compare the importance of predators (top-down) and host plant resistance (bottom-up) on HWA abundance by placing mesh exclusion bags on branches of both species and monitoring HWA abundance over two years. We found no evidence for bottom-up control of HWA on western hemlock (a native host). HWA established more readily on that species than on eastern hemlock on which it is a major pest in eastern North America. We found strong evidence for top-down control in that both summer and winter-active predators significantly reduced HWA densities on the branches of both tree species where predators were allowed access. These findings support the validity of the biological control program for HWA, the goal of which is to reduce outbreak populations of HWA in eastern North America.

Late growing season carbon subsidy in native gymnosperms in a northern temperate forest.

Evergreen tree species that maintain positive carbon balance during the late growing season may subsidize extra carbon in a mixed forest. To test this concept of 'carbon subsidy', leaf gas exchange characteristics and related leaf traits were measured for three gymnosperm evergreen species (Chamaecyparis thyoides, Tsuga canadensis and Pinus strobus) native to the oak-hickory deciduous forest in northeast USA from March (early Spring) to October (late Autumn) in a single year. All three species were photosynthetically active in Autumn. During the Summer-Autumn transition, photosynthetic capacity (Amax) of T. canadensis and P. strobus increased (T-test, P < 0.001) and was maintained in C. thyoides (T-test, P = 0.49), while dark respiration at 20 °C (Rn) and its thermal sensitivity were generally unchanged for all species (one-way ANOVA, P > 0.05). In Autumn, reductions in mitochondrial respiration rate in the daylight (RL) and the ratio of RL to Rn (RL/Rn) were observed in P. strobus (46.3% and 44.0% compared to Summer, respectively). Collectively, these physiological adjustments resulted in higher ratios of photosynthesis to respiration (A/Rnand A/RL) in Autumn for all species. Across season, photosynthetic biochemistry and respiratory variables were not correlated with prevailing growth temperature. Physiological adjustments allowed all three gymnosperm species to maintain positive carbon balance into late Autumn, suggesting that gymnosperm evergreens may benefit from Autumn warming trends relative to deciduous trees that have already lost their leaves.

Fitness and physiology of Adelges tsugae (Hemiptera: Adelgidae) in relation to the health of the eastern hemlock.

The hemlock woolly adelgid, Adelges tsugae Annand is an invasive insect that frequently causes hemlock (Tsuga spp.) mortality in the eastern United States. Studies have shown that once healthy hemlocks become infested by the adelgid, nutrients are depleted from the tree, leading to both tree decline and a reduction of the adelgid population. Since A. tsugae is dependent on hemlock for nutrients, feeding on trees in poor health may affect the ability of the insect to obtain necessary nutrients and may consequently affect their physiological and population health. Trees were categorized as lightly or moderately impacted by A. tsugae based on quantitative and qualitative tree health measurements. Population health of A. tsugae on each tree was determined by measuring insect density and peak mean fecundity; A. tsugae physiological health was determined by measuring insect biomass, total carbon, carbohydrate, total nitrogen, and amino nitrogen levels. Adelges tsugae from moderately impacted trees exhibited significantly greater fecundity than from lightly impacted trees. However, A. tsugae from lightly impacted hemlocks contained significantly greater levels of carbohydrates, total nitrogen, and amino nitrogen. While the results of the physiological analysis generally support our hypothesis that A. tsugae on lightly impacted trees are healthier than those on moderately impacted trees, this was not reflected in the population health measurements. Adelges tsugae egg health in response to tree health should be verified. This study provides the first examination of A. tsugae physiological health in relation to standard A. tsugae population health measures on hemlocks of different health levels.

Effects of Light and Water Availability on the Performance of Hemlock Woolly Adelgid (Hemiptera: Adelgidae).

Eastern hemlock (Tsuga canadensis (L.) Carriere) is a dominant shade-tolerant tree in northeastern United States that has been declining since the arrival of the hemlock woolly adelgid (Adelges tsugae Annand). Determining where A. tsugae settles under different abiotic conditions is important in understanding the insect's expansion. Resource availability such as light and water can affect herbivore selectivity and damage. We examined how A. tsugae settlement and survival were affected by differences in light intensity and water availability, and how adelgid affected tree performance growing in these different abiotic treatments. In a greenhouse at the University of Rhode Island, we conducted an experiment in which the factors light (full-sun, shaded), water (water-stressed, watered), and adelgid (infested, insect-free) were fully crossed for a total of eight treatments (20 two-year-old hemlock saplings per treatment). We measured photosynthesis, transpiration, water potential, relative water content, adelgid density, and survival throughout the experiment. Adelgid settlement was higher on the old-growth foliage of shaded and water-stressed trees, but their survival was not altered by foliage age or either abiotic factor. The trees responded more to the light treatments than the water treatments. Light treatments caused a difference in relative water content, photosynthetic rate, transpiration, and water potential; however, water availability did not alter these variables. Adelgid did not enhance the impact of these abiotic treatments. Further studies are needed to get a better understanding of how these abiotic factors impact adelgid densities and tree health, and to determine why adelgid settlement was higher in the shaded treatments.

Quantifying canopy complexity and effects on productivity and resilience in late-successional hemlock-hardwood forests.

The regrowing forests of eastern North America have been an important global C sink over the past 100+ years, but many are now transitioning into late succession. The consequences of this transition are unclear due to uncertainty around the C dynamics of old- growth forests. Canopy structural complexity (CSC) has been shown to be an important source of variability in C dynamics in younger forests (e.g., in productivity and resilience to disturbance), but its role in late-successional forests has not been widely addressed. We investigated patterns of CSC in two old-growth forest landscapes in the Upper Peninsula of Michigan, USA, to assess factors associated with CSC and its influence on productivity and disturbance resilience (to moderate-severity windstorm). CSC was quantified using a portable below-canopy LiDAR (PCL) system in 65 plots that also had long-term (50-70+ years). inventory data, which were used to quantify aboveground net primary productivity (ANPP), disturbance history, and stand characteristics. We found high and variable CSC relative to younger forests across a suite of PCL-derived metrics. Variation in CSC was driven by species composition and size structure, rather than disturbance history or site characteristics. Recent moderate severity wind disturbance decreased plot-scale CSC, but increased stand-scale variation in CSC. The strong positive correlation between CSC and productivity illustrated in younger forests was not present in undisturbed portions of these late-successional ecosystems. Moderate severity disturbance appeared to reestablish the positive link between CSC and productivity, but this relationship was scale and severity dependent. A positive CSC-productivity relationship was evident at the plot scale with low-severity, dispersed disturbance, but only at a patch scale in more severely disturbed areas. CSC does not appear to strongly correlate With variation in productivity in undisturbed old-growth forests, but may play a very important (and scale/severity-dependent) role in their response to disturbance. Understanding potential, drivers and consequences of CSC in late-successional forests will inform management focused on promoting complexity and old-growth conditions, and illustrate potential inipacts of such treatments on regional C dynamics.

Invasive insect effects on nitrogen cycling and host physiology are not tightly linked.

Invasive insects may dramatically alter resource cycling and productivity in forest ecosystems. Yet, although responses of individual trees should both reflect and affect ecosystem-scale responses, relationships between physiological- and ecosystem-scale responses to invasive insects have not been extensively studied. To address this issue, we examined changes in soil nitrogen (N) cycling, N uptake and allocation, and needle biochemistry and physiology in eastern hemlock (Tsuga canadensis (L) Carr) saplings, associated with infestation by the hemlock woolly adelgid (HWA) (Adelges tsugae Annand), an invasive insect causing widespread decline of eastern hemlock in the eastern USA. Compared with uninfested saplings, infested saplings had soils that exhibited faster nitrification rates, and more needle (15)N uptake, N and total protein concentrations. However, these variables did not clearly covary. Further, within infested saplings, needle N concentration did not vary with HWA density. Light-saturated net photosynthetic rates (Asat) declined by 42% as HWA density increased from 0 to 3 adelgids per needle, but did not vary with needle N concentration. Rather, Asat varied with stomatal conductance, which was highest at the lowest HWA density and accounted for 79% of the variation in Asat. Photosynthetic light response did not differ among HWA densities. Our results suggest that the effects of HWA infestation on soil N pools and fluxes, (15)N uptake, needle N and protein concentrations, and needle physiology may not be tightly coupled under at least some conditions. This pattern may reflect direct effects of the HWA on N uptake by host trees, as well as effects of other scale-dependent factors, such as tree hydrology, affected by HWA activity.

Hemlock woolly adelgid (Hemiptera: Adelgidae) induces twig volatiles of eastern hemlock in a forest setting.

The hemlock woolly adelgid (Adelges tsugae Annand) is an invasive species causing high mortality of eastern hemlock (Tsuga canadensis (L) Carriere) in the forests of eastern North America. Recent findings revealed that sapling eastern hemlocks artificially infested with hemlock woolly adelgid in a plantation setting responded to the insect with an array of induced resin volatile changes. Here we determine if eastern hemlocks growing beneath a forest canopy respond to hemlock woolly adelgid infestation with the same patterns of constitutive and inducible volatile resin production as those plantation specimens. We inoculated previously uninfested branches of mature and immature hemlocks in a central New England forest with hemlock woolly adelgid. We then sampled twig tissue of infested and uninfested trees in late spring, early summer, and mid-autumn, after known intervals of adelgid activity when an induced response might be expected. We identified and quantified resin volatiles by gas chromatography-mass spectrometry. Constitutive levels of total monoterpenoids, sesquiterpenoids, and combined resin volatiles were all several-fold more abundant in forest trees than those previously measured in a plantation setting, pointing to further study of the influence of site factors on hemlock volatile production. Hemlock woolly adelgid infestation induced an array of changes in eastern hemlock's volatile profile, including many-fold increases in benzyl alcohol and methyl salicylate accumulation. Despite differences in constitutive concentrations of volatiles between the two sites, our findings verify that hemlock woolly adelgid elicits patterns of resin volatile induction in forest-grown eastern hemlocks quite similar to those previously observed in plantation grown trees.

Spatially nonrandom tree mortality and ingrowth maintain equilibrium pattern in an old-growth Pseudotsuga-Tsuga forest.

Mortality processes in old-growth forests are generally assumed to be driven by gap-scale disturbance, with only a limited role ascribed to density-dependent mortality, but these assumptions are rarely tested with data sets incorporating repeated measurements. Using a 12-ha spatially explicit plot censused 13 years apart in an approximately 500-year-old Pseudotsuga-Tsuga forest, we demonstrate significant density-dependent mortality and spatially aggregated tree recruitment. However, the combined effect of these strongly nonrandom demographic processes was to maintain tree patterns in a state of dynamic equilibrium. Density-dependent mortality was most pronounced for the dominant late-successional species, Tsuga heterophylla. The long-lived, early-seral Pseudotsuga menziesii experienced an annual stem mortality rate of 0.84% and no new recruitment. Late-seral species Tsuga and Abies amabilis had nearly balanced demographic rates of ingrowth and mortality. The 2.34% mortality rate for Taxus brevifolia was higher than expected, notably less than ingrowth, and strongly affected by proximity to Tsuga. Large-diameter Tsuga structured both the regenerating conspecific and heterospecific cohorts with recruitment of Tsuga and Abies unlikely in neighborhoods crowded with large-diameter competitors (P < 0.001). Density-dependent competitive interactions strongly shape forest communities even five centuries after stand initiation, underscoring the dynamic nature of even equilibrial old-growth forests.

Impacts of dwarf mistletoe on the physiology of host Tsuga heterophylla trees as recorded in tree-ring C and O stable isotopes.

Dwarf mistletoes, obligate, parasitic plants with diminutive aerial shoots, have long-term effects on host tree water relations, hydraulic architecture and photosynthetic gas exchange and can eventually induce tree death. To investigate the long-term (1886-2010) impacts of dwarf mistletoe on the growth and gas exchange characteristics of host western hemlock, we compared the diameter growth and tree-ring cellulose stable carbon (C) and oxygen (O) isotope ratios (δ(13)Ccell, δ(18)Ocell) of heavily infected and uninfected trees. The relative basal area growth of infected trees was significantly greater than that of uninfected trees in 1886-90, but declined more rapidly in infected than uninfected trees through time and became significantly lower in infected than uninfected trees in 2006-10. Infected trees had significantly lower δ(13)Ccell and δ(18)Ocell than uninfected trees. Differences in δ(18)Ocell between infected and uninfected trees were unexpected given that stomatal conductance and environmental variables that were expected to influence the δ(18)O values of leaf water were similar for both groups. However, estimates of mesophyll conductance (gm) were significantly lower and estimates of effective path length for water movement (L) were significantly higher in leaves of infected trees, consistent with their lower values of δ(18)Ocell. This study reconstructs the long-term physiological responses of western hemlock to dwarf mistletoe infection. The long-term diameter growth and δ(13)Ccell trajectories suggested that infected trees were growing faster than uninfected trees prior to becoming infected and subsequently declined in growth and leaf-level photosynthetic capacity compared with uninfected trees as the dwarf mistletoe infection became severe. This study further points to limitations of the dual-isotope approach for identifying sources of variation in δ(13)Ccell and indicates that changes in leaf internal properties such as gm and L that affect δ(18)Ocell must be considered.

Failure under stress: the effect of the exotic herbivore Adelges tsugae on biomechanics of Tsuga canadensis.

BACKGROUND AND AIMS: Exotic herbivores that lack a coevolutionary history with their host plants can benefit from poorly adapted host defences, potentially leading to rapid population growth of the herbivore and severe damage to its plant hosts. The hemlock woolly adelgid (Adelges tsugae) is an exotic hemipteran that feeds on the long-lived conifer eastern hemlock (Tsuga canadensis), causing rapid mortality of infested trees. While the mechanism of this mortality is unknown, evidence indicates that A. tsugae feeding causes a hypersensitive response and alters wood anatomy. This study investigated the effect of A. tsugae feeding on biomechanical properties at different spatial scales: needles, twigs and branches. METHODS: Uninfested and A. tsugae-infested samples were collected from a common garden experiment as well as from naturally infested urban and rural field sites. Tension and flexure mechanical tests were used to quantify biomechanical properties of the different tissues. In tissues that showed a significant effect of herbivory, the potential contributions of lignin and tissue density on the results were quantified. KEY RESULTS: Adelges tsugae infestation decreased the abscission strength, but not flexibility, of needles. A. tsugae feeding also decreased mechanical strength and flexibility in currently attacked twigs, but this effect disappeared in older, previously attacked branches. Lignin and twig tissue density contributed to differences in mechanical strength but were not affected by insect treatment. CONCLUSIONS: Decreased strength and flexibility in twigs, along with decreased needle strength, suggest that infested trees experience resource stress. Altered growth patterns and cell wall chemistry probably contribute to these mechanical effects. Consistent site effects emphasize the role of environmental variation in mechanical traits. The mechanical changes measured here may increase susceptibility to abiotic physical stressors in hemlocks colonized by A. tsugae. Thus, the interaction between herbivore and physical stresses is probably accelerating the decline of eastern hemlock, as HWA continues to expand its range.

Growth, allometry and shade tolerance of understory saplings of four subalpine conifers in central Japan.

The conifers Abies veitchii, A. mariesii, Picea jezoensis var. hondoensis, Tsuga diversifolia dominate in subalpine forests in central Japan. We expected that species differences in shade tolerance and in aboveground and belowground architecture are important for their coexistence. We examined net production and carbon allocation of understory saplings. Although the four species allocated similar amounts of biomass to roots at a given trunk height, the root-zone area of T. diversifolia was greater than that of the three other species. T. diversifolia often dominates shallow soil sites, such as ridge and rocky slopes, and, therefore, a wide spread of lateral roots would be an adaptation to such edaphic conditions. Crown width and leaf and branch mass were greatest for T. diversifolia and A. mariesii, followed in order by A. veitchii and P. jezoensis var. hondoensis. Although leaf mass of P. jezoensis var. hondoensis was lowest among the four species, species differences were not found in the net production per sapling because net production per leaf mass was greatest for P. jezoensis var. hondoensis. The leaf lifespan was longer in the order A. mariesii, T. diversifolia, P. jezoensis var. hondoensis and A. veitchii. The minimum rate of net production per leaf mass required to maintain the current sapling leaf mass (MRNP(LM)) was lowest in A. mariesii and T. diversifolia, and increased in the order of A. veitchii and P. jezoensis var. hondoensis. A. mariesii and T. diversifolia may survive in shade conditions by a lower MRNP(LM) than the two other species. Therefore, species differences in aboveground and belowground architecture and MRNPLM reflected their shade tolerance and regeneration strategies, which contribute to their coexistence.

Fire-mediated pathways of stand development in Douglas-fir/ western hemlock forests of the Pacific Northwest, USA.

Forests dominated by Douglas-fir and western hemlock in the Pacific Northwest of the United States have strongly influenced concepts and policy concerning old-growth forest conservation. Despite the attention to their old-growth characteristics, a tendency remains to view their disturbance ecology in relatively simple terms, emphasizing infrequent, stand-replacing (SR) fire and an associated linear pathway toward development of those old-growth characteristics. This study uses forest stand- and age-structure data from 124 stands in the central western Cascades of Oregon to construct a conceptual model of stand development under the mixed-severity fire regime that has operated extensively in this region. Hierarchical clustering of variables describing the age distributions of shade-intolerant and shade-tolerant species identified six groups, representing different influences of fire frequency and severity on stand development. Douglas-fir trees > 400 years old were found in 84% of stands, yet only 18% of these stands (15% overall) lack evidence of fire since the establishment of these old trees, whereas 73% of all stands show evidence of at least one non-stand-replacing (NSR) fire. Differences in fire frequency and severity have contributed to multiple development pathways and associated variation in contemporary stand structure and the successional roles of the major tree species. Shade-intolerant species form a single cohort following SR fire, or up to four cohorts per stand in response to recurring NSR fires that left living trees at densities up to 45 trees/ha. Where the surviving trees persist at densities of 60-65 trees/ha, the postfire cohort is composed only of shade-tolerant species. This study reveals that fire history and the development of old-growth forests in this region are more complex than characterized in current stand-development models, with important implications for maintaining existing old-growth forests and restoring stands subject to timber management.

Future species composition will affect forest water use after loss of eastern hemlock from southern Appalachian forests.

Infestation of eastern hemlock (Tsuga canadensis (L.) Carr.) with hemlock woolly adelgid (HWA, Adelges tsugae) has caused widespread mortality of this key canopy species throughout much of the southern Appalachian Mountains in the past decade. Because eastern hemlock is heavily concentrated in riparian habitats, maintains a dense canopy, and has an evergreen leaf habit, its loss is expected to have a major impact on forest processes, including transpiration (E(t)). Our goal was to estimate changes in stand-level E(t) since HWA infestation, and predict future effects of forest regeneration on forest E(t) in declining eastern hemlock stands where hemlock represented 50-60% of forest basal area. We used a combination of community surveys, sap flux measurements, and empirical models relating sap flux-scaled leaf-level transpiration (E(L)) to climate to estimate the change in E(t) after hemlock mortality and forecast how forest E(t) will change in the future in response to eastern hemlock loss. From 2004 to 2011, eastern hemlock mortality reduced annual forest E(t) by 22% and reduced winter E(t) by 74%. As hemlock mortality increased, growth of deciduous tree species--especially sweet birch (Betula lenta L.), red maple (Acer rubrum L.), yellow poplar (Liriodendron tulipifera L.), and the evergreen understory shrub rosebay rhododendron (Rhododendron maximum L.)--also increased, and these species will probably dominate post-hemlock riparian forests. All of these species have higher daytime E(L) rates than hemlock, and replacement of hemlock with species that have less conservative transpiration rates will result in rapid recovery of annual stand E(t). Further, we predict that annual stand E(t) will eventually surpass E(t) levels observed before hemlock was infested with HWA. This long-term increase in forest E(t) may eventually reduce stream discharge, especially during the growing season. However, the dominance of deciduous species in the canopy will result in a permanent reduction in winter E(t) and possible increase in winter stream discharge. The effects of hemlock die-off and replacement with deciduous species will have a significant impact on the hydrologic flux of forest transpiration, especially in winter. These results highlight the impact that invasive species can have on landscape-level ecosystem fluxes.

Climate isn't everything: competitive interactions and variation by life stage will also affect range shifts in a warming world.

PREMISE OF THE STUDY: The extent to which climate controls species' range limits is a classic biological question that is particularly relevant given anthropogenic climate change. While climate is known to play a role in species distributions, biotic interactions such as competition also affect range limits. Furthermore, climatic and biotic controls of ranges may vary in strength across life stages, implying complex range shift dynamics with climate change. METHODS: We quantified climatic and competitive influences on growth of juvenile and adult trees of three conifer species on Mt. Rainier, Washington, United States. We collected annual growth data of these trees, which we compared to the competitive environment and annual climate (100 years of data) experienced by each individual. KEY RESULTS: We found that the relationships between growth and climate and between growth and competition differed by life stage and location. Growth was sensitive to heavy snowpack and cold temperatures at high elevation upper limits (treeline), but growth was poorly explained by climate in low elevation closed-canopy forests. Competitive effects on growth were more important for saplings than adults, but did not become more important at either upper or lower range limits. CONCLUSIONS: In all, our results suggest that range shifts under climate change will differ at leading vs. trailing edges. At treeline, warmer temperatures will lead to increased growth and likely to range expansion. However, climate change will have less dramatic effects in low elevation closed-canopy forest communities, where growth is less strongly limited by climate, especially at young life stages.

Factors affecting establishment and recovery of Sasajiscymnus tsugae (Coleoptera: Coccinellidae), an introduced predator of hemlock woolly adelgid (Hemiptera: Adelgidae) on eastern hemlock (Pinales: Pinaceae).

To reduce populations of hemlock woolly adelgid, Adelges tsugae Annand (Hemiptera: Adelgidae), >500,000 Sasajiscymnus tsugae (Sasaji and McClure) (Coleoptera: Coccinellidae) have been released in the Great Smoky Mountains National Park since 2002. To determine factors affecting establishment and recovery of these predatory beetles, 65 single release sites were sampled using beat sheets from 2008 to 2012. Several abiotic and biotic factors were evaluated for their association with establishment and recovery of S. tsugae. Information on predatory beetle releases (location, year of release, number released, and season of release), topographic features (elevation, slope, Beers transformed aspect, and topographic relative moisture index), and temperature data (minimum and maximum temperatures 1 d after release and average minimum and maximum temperatures 7 d after release) were obtained from Great Smoky Mountains National Park personnel. These factors were evaluated using stepwise logistic regression and Pearson correlation. S. tsugae was recovered from 13 sites 2 to 10 yr after release, and the greatest number was recovered from 2002 release sites. Regression indicated establishment and recovery was negatively associated with year of release and positively associated with the average maximum temperature 7 d after release and elevation (generally, recovery increased as temperatures increased). Several significant correlations were found between presence and number of S. tsugae and year of release, season of release, and temperature variables. These results indicate that releases of S. tsugae should be made in warmer (≍10-25°C) temperatures and monitored for at least 5 yr after releases to enhance establishment and recovery efforts.

Decomposing the mid-Holocene Tsuga decline in eastern North America.

The mid-Holocene decline of Tsuga canadensis (hereafter Tsuga) populations across eastern North America is widely perceived as a synchronous event, driven by pests/pathogens, rapid climate change, or both. Pattern identification and causal attribution are hampered by low stratigraphic density of pollen-sampling and radiometric dates at most sites, and by absence of highly resolved, paired pollen and paleoclimate records from single sediment cores, where chronological order of climatic and vegetational changes can be assessed. We present an intensely sampled (contiguous 1-cm intervals) record of pollen and water table depth (inferred from testate amoebae) from a single core spanning the Tsuga decline at Irwin Smith Bog in Lower Michigan, with high-precision chronology. We also present an intensively sampled pollen record from Tower Lake in Upper Michigan. Both sites show high-magnitude fluctuations in Tsuga pollen percentages during the pre-decline maximum. The terminal decline is dated at both sites ca. 5000 cal yr BP, some 400 years later than estimates from other sites and data compilations. The terminal Tsuga decline was evidently heterochronous across its range. A transient decline ca. 5350 cal yr BP at both sites may correspond to the terminal decline at other sites in eastern North America. At Irwin Smith Bog, the terminal Tsuga decline preceded an abrupt and persistent decline in water table depths by approximately 200 years, suggesting the decline was not directly driven by abrupt climate change. The Tsuga decline may best be viewed as comprising at least three phases: a long-duration pre-decline maximum with high-magnitude and high-frequency fluctuations, followed by a terminal decline at individual sites, followed in turn by two millennia of persistently low Tsuga populations. These phases may not be causally linked, and may represent dynamics taking place at multiple temporal and spatial scales. Further progress toward understanding the phenomenon requires an expanded network of high-resolution pollen and paleoclimate chronologies.

Exotic herbivores on a shared native host: tissue quality after individual, simultaneous, and sequential attack.

Plants in nature are often attacked by multiple enemies whose effect on the plant cannot always be predicted based on the outcome of individual attacks. We investigated how two invasive herbivores, the hemlock woolly adelgid (Adelges tsugae) (HWA) and the elongate hemlock scale (Fiorinia externa) (EHS), alter host plant quality (measured as amino acid concentration and composition) when feeding individually or jointly on eastern hemlock (Tsuga canadensis), an important long-lived forest tree that is in severe decline. The joint herbivore treatments included both simultaneous and sequential infestations by the two herbivores. We expected resource depletion over time, particularly in response to feeding by HWA. In contrast, HWA dramatically increased the concentration and altered the composition of individual free amino acids. Compared to control trees, HWA increased total amino acid concentration by 330% after 1 year of infestation. Conversely, EHS had a negligible effect when feeding individually. Interestingly, there was a marginally significant HWA × EHS interaction that suggests the potential for EHS presence to reduce the impact of HWA on foliage quality when the two species co-occur. We suggest indirect effects of water stress as a possible physiological mechanism for our results. Understanding how species interactions change the physiology of a shared host is crucial to making more accurate predictions about host mortality and subsequent changes in affected communities and ecosystems, and to help design appropriate management plans.

The influence of successional processes and disturbance on the structure of Tsuga canadensis forests.

Old-growth forests are valuable sources of ecological, conservation, and management information, yet these ecosystems have received little study in New England, due in large part to their regional scarcity. To increase our understanding of the structures and processes common in these rare forests, we studied the abundance of downed coarse woody debris (CWD) and snags and live-tree size-class distributions in 16 old-growth hemlock forests in western Massachusetts. Old-growth stands were compared with eight adjacent second-growth hemlock forests to gain a better understanding of the structural differences between these two classes of forests resulting from contrasting histories. In addition, we used stand-level dendroecological reconstructions to investigate the linkages between disturbance history and old-growth forest structure using an information-theoretic model selection framework. Old-growth stands exhibit a much higher degree of structural complexity than second-growth forests. In particular, old-growth stands had larger overstory trees and greater volumes of downed coarse woody debris (135.2 vs. 33.2 m3/ha) and snags (21.2 vs. 10.7 m3/ha). Second-growth stands were characterized by either skewed unimodal or reverse-J shaped diameter distributions, while old-growth forests contained bell-shaped, skewed unimodal, rotated sigmoid, and reverse J-shaped distributions. The variation in structural attributes among old-growth stands, particularly the abundance of downed CWD, was closely related to disturbance history. In particular, old-growth stands experiencing moderate levels of canopy disturbance during the last century (1930s and 1980s) had greater accumulations of CWD, highlighting the importance of gap-scale disturbances in shaping the long-term development and structural characteristics of old-growth forests. These findings are important for the development of natural disturbance-based silvicultural systems that may be used to restore important forest characteristics lacking in New England second-growth stands by integrating structural legacies of disturbance (e.g., downed CWD) and resultant tree-size distribution patterns. This silvicultural approach would emulate the often episodic nature of CWD recruitment within old-growth forests.

Hydraulic responses to environmental perturbations in Tsuga canadensis and Betula lenta.

Eastern hemlock (Tsuga canadensis (L). Carr.) is a late-successional species found across the northeastern United States of America that is currently threatened by the exotic pest, hemlock woolly adelgid (Adelges tsugae Annand). Because whole-tree physiological characteristics may scale to influence ecosystem processes, we considered whole-tree hydraulic controls in eastern hemlock and the replacement species black birch (Betula lenta L.). Through a series of misting perturbations, whole-tree resistances (R), capacitances (C) and time constants (tau) were determined from time series sap flux data in eastern hemlock and black birch. Black birch trees responded more rapidly to environmental perturbations than eastern hemlock. Utilizing the step function after applied treatments, whole-tree tau ranged between 9.4 and 24.8 min in eastern hemlock trees compared with 5.9 to 10.5 min in black birch. Species was not a significant predictor of R or C when controlling for tree size. In both species, R decreased with sapwood area and C increased. Our tau results indicate that the loss and replacement of eastern hemlock by black birch will decrease the lag between transpiration and absorption of water from the soil and potentially alter the diurnal pattern of carbon and water uptake.

Deer herbivory alters forest response to canopy decline caused by an exotic insect pest.

Hemlock woolly adelgid (HWA; Adelges tsugae) infestations have resulted in the continuing decline of eastern hemlock (Tsuga canadensis) throughout much of the eastern United States. While the initial impacts of HWA infestations have been documented, our understanding of forest response to this disturbance remains incomplete. HWA infestation is not occurring in isolation but within a complex ecological context. The role of potentially important interacting factors, such as elevated levels of white-tailed deer herbivory, is poorly understood. Despite the potential for herbivory to alter forest successional trajectories following a canopy disturbance, little is known about herbivory-disturbance interactions, and herbivory is rarely considered in assessing forest response to a co-occurring disturbance. We used repeated censuses of deer exclosures and paired controls (400 paired plots) to quantify the impact of deer herbivory on tree seedling species abundance in 10 eastern hemlock ravines that span a gradient in HWA-induced canopy decline severity. Use of a maximum likelihood estimation framework and information theoretics allowed us to quantify the strength of evidence for alternative models developed to estimate the impacts of herbivory on tree seedling abundance as a function of varying herbivore density and canopy decline severity. The exclusion of deer herbivory had marked impacts on the abundance of the studied seedling species: Acer rubrum, Acer saccharum, Betula lenta, Nyssa sylvatica, Quercus montana, and Tsuga canadensis. For all six species, the relationship between seedling abundance and deer density was either exponential or saturating. Although the functional form of the response varied among seedling species, the inclusion of both deer density and canopy decline severity measures consistently resulted in models with substantially greater support. Canopy decline resulted in higher proportional herbivory impacts and altered the ranking of herbivory impacts by seedling species. Our results suggest that, by changing species' competitive abilities, white-tailed deer herbivory alters the trajectory of forest response to this exotic insect pest and has the potential to shift future overstory composition.