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1.  Laboratory Studies of Feeding and Oviposition Preference, Developmental Performance, and Survival of the Predatory Beetle, Sasajiscymnus tsugae on Diets of the Woolly Adelgids, Adelges tsugae and Adelges piceae  
The suitability of the balsam woolly adelgid, Adelges piceae Ratzeburg (Hemiptera: Adelgidae) as an alternate mass rearing host for the adelgid predator, Sasajiscymnus tsugae Sasaji and McClure (Coleoptera: Coccinellidae) was studied in the laboratory. This predator is native to Japan and has been introduced to eastern hemlock, Tsuga canadensis (L.) Carrière (Pinales: Pinaceae), forests throughout the eastern United States for biological control of the hemlock woolly adelgid, Adelges tsugae Annand (Hemiptera: Adelgidae), also of Japanese origin. Feeding, oviposition, immature development, and adult long-term survival of S. tsugae were tested in a series of no choice (single-prey) and paired-choice experiments between the primary host prey, A. tsugae, and the alternate host prey, A. piceae. In paired-choice feeding tests, the predator did not discriminate between eggs of the two adelgid species, but in the no choice tests the predator did eat significantly more eggs of A. piceae than those of A. tsugae. S. tsugae accepted both test prey for oviposition and preferred to lay eggs on adelgid infested versus noninfested host plants. Overall oviposition rates were very low (< 1 egg per predator female) in the oviposition preference tests. Predator immature development rates did not differ between the two test prey, but only 60% of S. tsugae survived egg to adult development when fed A. piceae compared to 86% when fed A. tsugae. S. tsugae adult long-term survival was significantly influenced (positively and negatively) by prey type and the availability of a supplemental food source (diluted honey) when offered aestivating A. tsugae sistens nymphs or ovipositing aestivosistens A. piceae adults, but not when offered ovipositing A. tsugae sistens adults. These results suggest that the development of S. tsugae laboratory colonies reared on a diet consisting only of A. piceae may be possible, and that the biological control potential of the predator might be expanded to include management of A. piceae in Christmas tree plantations.
doi:10.1673/031.011.6801
PMCID: PMC3385972  PMID: 21867435
Abies fraseri; alternate rearing host; balsam woolly adelgid; biological control; hemlock woolly adelgid; prey suitability; Tsuga canadensis
2.  Visual Ability and Searching Behavior of Adult Laricobius nigrinus, a Hemlock Woolly Adelgid Predator 
Very little is known about the searching behavior and sensory cues that Laricobius spp. (Coleoptera: Derodontidae) predators use to locate suitable habitats and prey, which limits our ability to collect and monitor them for classical biological control of adelgids (Hemiptera: Adelgidae). The aim of this study was to examine the visual ability and the searching behavior of newly emerged L. nigrinus Fender, a host-specific predator of the hemlock woolly adelgid, Adelges tsugae Annand (Hemiptera: Phylloxeroidea: Adelgidae). In a laboratory bioassay, individual adults attempting to locate an uninfested eastern hemlock seedling under either light or dark conditions were observed in an arena. In another bioassay, individual adults searching for prey on hemlock seedlings (infested or uninfested) were continuously video-recorded. Beetles located and began climbing the seedling stem in light significantly more than in dark, indicating that vision is an important sensory modality. Our primary finding was that searching behavior of L. nigrinus, as in most species, was related to food abundance. Beetles did not fly in the presence of high A. tsugae densities and flew when A. tsugae was absent, which agrees with observed aggregations of beetles on heavily infested trees in the field. At close range of prey, slow crawling and frequent turning suggest the use of non-visual cues such as olfaction and contact chemoreception. Based on the beetles' visual ability to locate tree stems and their climbing behavior, a bole trap may be an effective collection and monitoring tool.
doi:10.1673/031.011.11101
PMCID: PMC3281397  PMID: 22220637
biological control; hemlock woolly adelgid; monitoring; predation; Tsuga canadensis; visual cues
3.  Maximizing Oviposition Efficiency when Mass Rearing the Coccinellid, Sasajiscymnus tsugae, a Predator of the Hemlock Woolly Adelgid, Adelges tsugae  
Sasajiscymnus tsugae Sasaji and McClure (Coleeptera: Coccinellidae), is a biological control agent imported for management of hemlock woolly adelgid, Adelges tsugae Annand. In mass rearing S. tsugae, accurate estimation of egg numbers is important because larvae are cannibalistic, especially at higher densities. To determine the most accurate means of estimating egg production, three brands of gauze were compared as oviposition substrates. Curad® gauze provided the most accurate estimate of egg production, and was the most cost effective brand. When eggs were collected from oviposition jars, similar adult yields of S. tsugae occurred between rearing cages infested with 1,650 eggs from gauze compared to eggs on the twigs from within these jars. Additionally, orientation of oviposition jars impacted S. tsugae egg production as significantly more eggs were produced in horizontally oriented oviposition jars.
doi:10.1673/031.010.14112
PMCID: PMC3388978  PMID: 21070172
biological control; invasive species
4.  Bacteriocyte-associated gammaproteobacterial symbionts of the Adelges nordmannianae/piceae complex (Hemiptera: Adelgidae) 
The ISME Journal  2011;6(2):384-396.
Adelgids (Insecta: Hemiptera: Adelgidae) are known as severe pests of various conifers in North America, Canada, Europe and Asia. Here, we present the first molecular identification of bacteriocyte-associated symbionts in these plant sap-sucking insects. Three geographically distant populations of members of the Adelges nordmannianae/piceae complex, identified based on coI and ef1alpha gene sequences, were investigated. Electron and light microscopy revealed two morphologically different endosymbionts, coccoid or polymorphic, which are located in distinct bacteriocytes. Phylogenetic analyses of their 16S and 23S rRNA gene sequences assigned both symbionts to novel lineages within the Gammaproteobacteria sharing <92% 16S rRNA sequence similarity with each other and showing no close relationship with known symbionts of insects. Their identity and intracellular location were confirmed by fluorescence in situ hybridization, and the names ‘Candidatus Steffania adelgidicola' and ‘Candidatus Ecksteinia adelgidicola' are proposed for tentative classification. Both symbionts were present in all individuals of all investigated populations and in different adelgid life stages including eggs, suggesting vertical transmission from mother to offspring. An 85 kb genome fragment of ‘Candidatus S. adelgidicola' was reconstructed based on a metagenomic library created from purified symbionts. Genomic features including the frequency of pseudogenes, the average length of intergenic regions and the presence of several genes which are absent in other long-term obligate symbionts, suggested that ‘Candidatus S. adelgidicola' is an evolutionarily young bacteriocyte-associated symbiont, which has been acquired after diversification of adelgids from their aphid sister group.
doi:10.1038/ismej.2011.102
PMCID: PMC3260495  PMID: 21833037
evolution; genome reduction; insects; symbiosis; Buchnera
5.  Discriminating Tsuga canadensis Hemlock Forest Defoliation Using Remotely Sensed Change Detection 
Journal of Nematology  2002;34(3):213-221.
The eastern hemlock (Tsuga Canadensis) is declining in health and vigor in eastern North America due to infestation by an introduced insect, the hemlock woolly adelgid (Adelges isugue). Adelgid feeding activity results in the defoliation of hemlock forest canopy over several years. We investigated the application of Landsat satellite imagery and change-detection techniques to monitor the health of hemlock forest stands in northern New Jersey. We described methods used to correct effects due to atmospheric conditions and monitor the health status of hemlock stands over time. As hemlocks defoliate, changes occur in the spectral reflectance of the canopy in near infrared and red wavelengths—changes captured in the Normalized Difference Vegetation Index. By relating the differences in this index over time to hemlock defoliation on the ground, four classes of hemlock forest health were predicted across spatially heterogeneous landscapes with 82% accuracy. Using a time series of images, we are investigating temporal and spatial patterns in hemlock defoliation across the study area over the past decade. Based on the success of this methodology, we are no expanding out study to monitor hemlock health across the entire Mid-Atlantic region.
PMCID: PMC2620567  PMID: 19265936
Adelges tsugae; change detection; defoliation; discriminant analysis; discriminating; eastern hemlock; forest; hemlock woolly adelgid; Landsat TM; remote sensing; Tsuga canadensis
6.  Behavior and Daily Activity Patterns of Specialist and Generalist Predators of the Hemlock Woolly Adelgid, Adelges tsugae  
The behavior and daily activity patterns of two specialist predators, Laricobius nigrinus Fender (Coleoptera: Derodontidae) and Sasajiscymnus tsugae, Sasaji and McClure (Coleoptera: Coccinellidae), and a generalist predator, Harmonia axyridis Pallas (Coleoptera: Coccinellidae), of hemlock woolly adelgid, Adelges tsugae (Hemiptera: Adelgidae), were examined using digital video recording in the laboratory. The two specialists are part of a biological control program for A. tsugae, and it is not known if competitive interactions with previously established generalist predators will negatively impact their effectiveness. The behavior and daily activity patterns of adult females of each species were documented in single- and paired-predator assays under simulated spring and summer conditions. Behavior varied qualitatively and quantitatively by species, and did not appear to be highly coordinated temporally or spatially. All species exhibited continuous activity patterns that were punctuated by longer periods of rest. Extensive and intensive searching behavior occurred in all species, with intensive searching being highly variable. Specialist predators appeared to be more selective of feeding and oviposition sites, and rested at more concealed locations than the generalist species. In spring conditions, L. nigrinus had greater activity and a more even behavior distribution than S. tsugae or H. axyridis, which were skewed towards resting. In summer, the latter two species showed increased activity at higher temperatures. Conspecifics significantly altered the time allocated to specific behaviors for L. nigrinus and H. axyridis, resulting in reduced predator effectiveness by reducing time and energy expenditure on activities that directly impact the adelgids. In contrast, S. tsugae conspecifics and all heterospecific combinations showed non-interference. The activity of each species varied with time of day; L. nigrinus was more active at night, while S. tsugae and H. axyridis were more active during the day. All predator groupings maintained a high degree of spatial separation relative to assay size. The use of multiple-predator species combinations that include the specialist predators, is recommended over single-species for biological control of A. tsugae, as temporal and spatial patterns were not highly coordinated. Low-density releases may reduce the potential negative effects of intraspecific competition.
doi:10.1673/031.007.4401
PMCID: PMC2999443  PMID: 20345314
Laricobius nigrinus; Sasajiscymnus tsugae; Harmonia axyridis; predator competition; biological control
7.  Foundation species loss affects vegetation structure more than ecosystem function in a northeastern USA forest 
PeerJ  2013;1:e41.
Loss of foundation tree species rapidly alters ecological processes in forested ecosystems. Tsuga canadensis, an hypothesized foundation species of eastern North American forests, is declining throughout much of its range due to infestation by the nonnative insect Adelges tsugae and by removal through pre-emptive salvage logging. In replicate 0.81-ha plots, T. canadensis was cut and removed, or killed in place by girdling to simulate adelgid damage. Control plots included undisturbed hemlock and mid-successional hardwood stands that represent expected forest composition in 50–100 years. Vegetation richness, understory vegetation cover, soil carbon flux, and nitrogen cycling were measured for two years prior to, and five years following, application of experimental treatments. Litterfall and coarse woody debris (CWD), including snags, stumps, and fallen logs and branches, have been measured since treatments were applied. Overstory basal area was reduced 60%–70% in girdled and logged plots. Mean cover and richness did not change in hardwood or hemlock control plots but increased rapidly in girdled and logged plots. Following logging, litterfall immediately decreased then slowly increased, whereas in girdled plots, there was a short pulse of hemlock litterfall as trees died. CWD volume remained relatively constant throughout but was 3–4× higher in logged plots. Logging and girdling resulted in small, short-term changes in ecosystem dynamics due to rapid regrowth of vegetation but in general, interannual variability exceeded differences among treatments. Soil carbon flux in girdled plots showed the strongest response: 35% lower than controls after three years and slowly increasing thereafter. Ammonium availability increased immediately after logging and two years after girdling, due to increased light and soil temperatures and nutrient pulses from leaf-fall and reduced uptake following tree death. The results from this study illuminate ecological processes underlying patterns observed consistently in region-wide studies of adelgid-infested hemlock stands. Mechanisms of T. canadensis loss determine rates, magnitudes, and trajectories of ecological changes in hemlock forests. Logging causes abrupt, large changes in vegetation structure whereas girdling (and by inference, A. tsugae) causes sustained, smaller changes. Ecosystem processes depend more on vegetation cover per se than on species composition. We conclude that the loss of this late-successional foundation species will have long-lasting impacts on forest structure but subtle impacts on ecosystem function.
doi:10.7717/peerj.41
PMCID: PMC3629072  PMID: 23638378
Adelges tsugae; Eastern hemlock; Hemlock woolly adelgid; Primary productivity; Logging; Nutrient cycling; Soil respiration; Tsuga canadensis; Forest dynamics
8.  Sphaeronema sasseri n. sp. (Tylenchulidae), a Nematode Parasitic on Fraser Fir and Red Spruce 
Journal of Nematology  1985;17(3):346-354.
Sphaeronema sasseri n. sp. is described from Fraser fir and red spruce on Mount Mitchell in North Carolina. Females are distinguished from other species in the genus by body shape, occurrence of body annulations, stylet morphology, head shape, and by several morphometric characters. The nematodes occur in colonies surrounding the bases of lateral and feeder roots, and the infected tissues show a general breakdown of the cortex and bark. The roots appear to be severely damaged by high populations of nematodes. This parasite may be important in the etiology of the slow decline of spruce and fir that has occurred in recent years in the southern Appalachian Mountains.
PMCID: PMC2618459  PMID: 19294105
taxonomy; scanning electron microscopy; spruce decline; fir decline
9.  Assessing the Potential Impacts to Riparian Ecosystems Resulting from Hemlock Mortality in Great Smoky Mountains National Park 
Environmental Management  2009;44(2):335-345.
Hemlock Woolly Adelgid (Adelges tsugae) is spreading across forests in eastern North America, causing mortality of eastern hemlock (Tsuga canadensis [L.] Carr.) and Carolina hemlock (Tsuga caroliniana Engelm.). The loss of hemlock from riparian forests in Great Smoky Mountains National Park (GSMNP) may result in significant physical, chemical, and biological alterations to stream environments. To assess the influence of riparian hemlock stands on stream conditions and estimate possible impacts from hemlock loss in GSMNP, we paired hardwood- and hemlock-dominated streams to examine differences in water temperature, nitrate concentrations, pH, discharge, and available photosynthetic light. We used a Geographic Information System (GIS) to identify stream pairs that were similar in topography, geology, land use, and disturbance history in order to isolate forest type as a variable. Differences between hemlock- and hardwood-dominated streams could not be explained by dominant forest type alone as forest type yields no consistent signal on measured conditions of headwater streams in GSMNP. The variability in the results indicate that other landscape variables, such as the influence of understory Rhododendron species, may exert more control on stream conditions than canopy composition. The results of this study suggest that the replacement of hemlock overstory with hardwood species will have minimal impact on long-term stream conditions, however disturbance during the transition is likely to have significant impacts. Management of riparian forests undergoing hemlock decline should, therefore, focus on facilitating a faster transition to hardwood-dominated stands to minimize long-term effects on water quality.
doi:10.1007/s00267-009-9317-5
PMCID: PMC2717373  PMID: 19495859
Tsuga Canadensis; Hemlock mortality; Hemlock Wooly Adelgid; Great Smoky Mountains National Park; GIS modeling; Stream temperature
10.  Significant Mean and Extreme Climate Sensitivity of Norway Spruce and Silver Fir at Mid-Elevation Mesic Sites in the Alps 
PLoS ONE  2012;7(11):e50755.
Climate forcing is the major abiotic driver for forest ecosystem functioning and thus significantly affects the role of forests within the global carbon cycle and related ecosystem services. Annual radial increments of trees are probably the most valuable source of information to link tree growth and climate at long-term time scales, and have been used in a wide variety of investigations worldwide. However, especially in mountainous areas, tree-ring studies have focused on extreme environments where the climate sensitivity is perhaps greatest but are necessarily a biased representation of the forests within a region. We used tree-ring analyses to study two of the most important tree species growing in the Alps: Norway spruce (Picea abies) and silver fir (Abies alba). We developed tree-ring chronologies from 13 mesic mid-elevation sites (203 trees) and then compared them to monthly temperature and precipitation data for the period 1846–1995. Correlation functions, principal component analysis and fuzzy C-means clustering were applied to 1) assess the climate/growth relationships and their stationarity and consistency over time, and 2) extract common modes of variability in the species responses to mean and extreme climate variability. Our results highlight a clear, time-stable, and species-specific response to mean climate conditions. However, during the previous-year's growing season, which shows the strongest correlations, the primary difference between species is in their response to extreme events, not mean conditions. Mesic sites at mid-altitude are commonly underrepresented in tree-ring research; we showed that strong climatic controls of growth may exist even in those areas. Extreme climatic events may play a key role in defining the species-specific responses on climatic sensitivity and, with a global change perspective, specific divergent responses are likely to occur even where current conditions are less limited.
doi:10.1371/journal.pone.0050755
PMCID: PMC3510186  PMID: 23209823
11.  Fungi Associated with the Hemlock Woolly Adelgid, Adelges tsugae, and Assessment of Entomopathogenic Isolates for Management 
Fungi associated with the hemlock wooly adelgid, Adelges tsugae Annand (Hemiptera: Adelgidae), were collected throughout the eastern USA and southern China. Twenty fungal genera were identified, as were 79 entomopathogenic isolates, including: Lecanicillium lecanii (Zimmermann) (Hypocreales: Insertae sedis), Isaria farinosa (Holm: Fries.) (Cordycipitaceae), Beauveria bassiana (Balasamo) (Hyphomycetes), and Fusarium spp (Nectriaceae). The remaining fungal genera associated with insect cadavers were similar for both the USA and China collections, although the abundance of Acremonium (Hypocreaceae) was greater in China. The entomopathogenic isolates were assayed for efficacy against Myzus persicae (Sulzer) (Homoptera: Aphididae) and yielded mortality ranging from 3 to 92%. Ten isolates demonstrating the highest efficacy were further assessed for efficacy against field-collected A. tsugae under laboratory conditions. Overall, two B. bassiana, one L. lecanii, and a strain of Metarhizium anisopliae (Metchnikoff) (Hypocreales: Clavicipitaceae), demonstrated significantly higher efficacy against A. tsugae than the others. Isolates were further evaluated for conidial production, germination rate and colony growth at four temperatures representative of field conditions. All isolates were determined to be mesophiles with optimal temperature between 25–30° C. In general, conidial production increased with temperature, though two I. farinosa produced significantly more conidia at cooler temperatures. When efficacy values were compared with conidial production and temperature tolerances, Agricultural Research Service Collection of Entomopathogenic Fungi (ARSEF) 1080, 5170, and 5798 had characteristics comparable to the industrial B. bassiana strain GHA.
doi:10.1673/031.010.6201
PMCID: PMC3014804  PMID: 20672977
bioassay; biological control; entomogenous; mycoinsecticides; Tsuga canadensis; Tsuga caroliniana
12.  Effects of Understory Vegetation and Litter on Plant Nitrogen (N), Phosphorus (P), N∶P Ratio and Their Relationships with Growth Rate of Indigenous Seedlings in Subtropical Plantations 
PLoS ONE  2013;8(12):e84130.
Establishing seedlings in subtropical plantations is very important for forest health, succession and management. Information on seedling nutrient concentrations is essential for both the selection of suitable indigenous tree species to accelerate succession of the established plantation and sustainable forest management. In this study, we investigated the concentrations of nitrogen ([N]), phosphorus ([P]), and N∶P ratio in leaves, stems and roots of seedlings of three indigenous tree species (Castanopsis chinensis, Michelia chapensis and Psychotria rubra) transplanted with removing or retaining understory vegetation and litter at two typical subtropical forest plantations (Eucalyptus plantation and native species plantation). We also measured the relative growth rate (RGR) of seedling height, and developed the relationships between RGR and leaf [N], [P] and N∶P ratio. Results showed that treatments of understory vegetation and associated litter (i.e. removal or retained) generally had no significant effects on leaf [N], [P], N∶P ratio and RGR of the transplanted tree seedlings for the experimental period. But among different species, there were significant differences in nutrient concentrations. M. chapensis and P. rubra had higher [N] and [P] compared to C. chinensis. [N] and [P] also varied among different plant tissues with much higher values in leaves than in roots for all indigenous species. RGR of indigenous tree seedlings was mostly positively correlated with leaf [N] and [P], but negatively correlated with leaf N∶P ratio. Considering the low [P] and high N∶P ratio observed in the introduced indigenous tree seedlings, we propose that the current experimental plantations might be P limited for plant growth.
doi:10.1371/journal.pone.0084130
PMCID: PMC3873957  PMID: 24386340
13.  Comparative Chloroplast Genomics Reveals the Evolution of Pinaceae Genera and Subfamilies 
As the largest and the basal-most family of conifers, Pinaceae provides key insights into the evolutionary history of conifers. We present comparative chloroplast genomics and analysis of concatenated 49 chloroplast protein-coding genes common to 19 gymnosperms, including 15 species from 8 Pinaceous genera, to address the long-standing controversy about Pinaceae phylogeny. The complete cpDNAs of Cathaya argyrophylla and Cedrus deodara (Abitoideae) and draft cpDNAs of Larix decidua, Picea morrisonicola, and Pseudotsuga wilsoniana are reported. We found 21- and 42-kb inversions in congeneric species and different populations of Pinaceous species, which indicates that structural polymorphics may be common and ancient in Pinaceae. Our phylogenetic analyses reveal that Cedrus is clustered with Abies–Keteleeria rather than the basal-most genus of Pinaceae and that Cathaya is closer to Pinus than to Picea or Larix–Pseudotsuga. Topology and structural change tests and indel-distribution comparisons lend further evidence to our phylogenetic finding. Our molecular datings suggest that Pinaceae first evolved during Early Jurassic, and diversification of Pinaceous subfamilies and genera took place during Mid-Jurassic and Lower Cretaceous, respectively. Using different maximum-likelihood divergences as thresholds, we conclude that 2 (Abietoideae and Larix–Pseudotsuga–Piceae–Cathaya–Pinus), 4 (Cedrus, non-Cedrus Abietoideae, Larix–Pseudotsuga, and Piceae–Cathaya–Pinus), or 5 (Cedrus, non-Cedrus Abietoideae, Larix–Pseudotsuga, Picea, and Cathaya–Pinus) groups/subfamilies are more reasonable delimitations for Pinaceae. Specifically, our views on subfamilial classifications differ from previous studies in terms of the rank of Cedrus and with recognition of more than two subfamilies.
doi:10.1093/gbe/evq036
PMCID: PMC2997556  PMID: 20651328
chloroplast genome; Cedrus; Cathaya; Pesudotsuga; Pinaceae phylogeny; molecular dating
14.  Fitness dynamics within a poplar hybrid zone: I. Prezygotic and postzygotic barriers impacting a native poplar hybrid stand 
Ecology and Evolution  2014;4(9):1629-1647.
Hybridization and introgression are pervasive evolutionary phenomena that provide insight into the selective forces that maintain species boundaries, permit gene flow, and control the direction of evolutionary change. Poplar trees (Populus L.) are well known for their ability to form viable hybrids and maintain their distinct species boundaries despite this interspecific gene flow. We sought to quantify the hybridization dynamics and postzygotic fitness within a hybrid stand of balsam poplar (Populus balsamifera L.), eastern cottonwood (P. deltoides Marsh.), and their natural hybrids to gain insight into the barriers maintaining this stable hybrid zone. We observed asymmetrical hybrid formation with P. deltoides acting as the seed parent, but with subsequent introgression biased toward P. balsamifera. Native hybrids expressed fitness traits intermediate to the parental species and were not universally unfit. That said, native hybrid seedlings were absent from the seedling population, which may indicate additional selective pressures controlling their recruitment. It is imperative that we understand the selective forces maintaining this native hybrid zone in order to quantify the impact of exotic poplar hybrids on this native system.
doi:10.1002/ece3.1029
PMCID: PMC4063464  PMID: 24967081
Hybrid fitness; hybridization; introgression; postzygotic fitness; reproductive fitness; SNPs
15.  Species-Specific Effects of Woody Litter on Seedling Emergence and Growth of Herbaceous Plants 
PLoS ONE  2011;6(10):e26505.
The effect of litter on seedling establishment can influence species richness in plant communities. The effect of litter depends on amount, and also on litter type, but relatively little is known about the species-specific effects of litter. We conducted a factorial greenhouse experiment to examine the effect of litter type, using two woody species that commonly co-occur in boreonemoral forest—evergreen spruce (Picea abies), deciduous hazel (Corylus avellana), and a mixture of the two species—and litter amount—shallow (4 mm), deep (12 mm) and leachate—on seedling emergence and biomass of three understorey species. The effect of litter amount on seedling emergence was highly dependent on litter type; while spruce needle litter had a significant negative effect that increased with depth, seedling emergence in the presence of hazel broadleaf litter did not differ from control pots containing no litter. Mixed litter of both species also had a negative effect on seedling emergence that was intermediate compared to the single-species treatments. Spruce litter had a marginally positive (shallow) or neutral effect (deep) on seedling biomass, while hazel and mixed litter treatments had significant positive effects on biomass that increased with depth. We found non-additive effects of litter mixtures on seedling biomass indicating that high quality hazel litter can reduce the negative effects of spruce. Hazel litter does not inhibit seedling emergence; it increases seedling growth, and creates better conditions for seedling growth in mixtures by reducing the suppressive effect of spruce litter, having a positive effect on understorey species richness.
doi:10.1371/journal.pone.0026505
PMCID: PMC3197666  PMID: 22028890
16.  Induced Terpene Accumulation in Norway Spruce Inhibits Bark Beetle Colonization in a Dose-Dependent Manner 
PLoS ONE  2011;6(10):e26649.
Background
Tree-killing bark beetles (Coleoptera, Scolytinae) are among the most economically and ecologically important forest pests in the northern hemisphere. Induction of terpenoid-based oleoresin has long been considered important in conifer defense against bark beetles, but it has been difficult to demonstrate a direct correlation between terpene levels and resistance to bark beetle colonization.
Methods
To test for inhibitory effects of induced terpenes on colonization by the spruce bark beetle Ips typographus (L.) we inoculated 20 mature Norway spruce Picea abies (L.) Karsten trees with a virulent fungus associated with the beetle, Ceratocystis polonica (Siem.) C. Moreau, and investigated induced terpene levels and beetle colonization in the bark.
Results
Fungal inoculation induced very strong and highly variable terpene accumulation 35 days after inoculation. Trees with high induced terpene levels (n = 7) had only 4.9% as many beetle attacks (5.1 vs. 103.5 attacks m−2) and 2.6% as much gallery length (0.029 m m−2 vs. 1.11 m m−2) as trees with low terpene levels (n = 6). There was a highly significant rank correlation between terpene levels at day 35 and beetle colonization in individual trees. The relationship between induced terpene levels and beetle colonization was not linear but thresholded: above a low threshold concentration of ∼100 mg terpene g−1 dry phloem trees suffered only moderate beetle colonization, and above a high threshold of ∼200 mg terpene g−1 dry phloem trees were virtually unattacked.
Conclusion/Significance
This is the first study demonstrating a dose-dependent relationship between induced terpenes and tree resistance to bark beetle colonization under field conditions, indicating that terpene induction may be instrumental in tree resistance. This knowledge could be useful for developing management strategies that decrease the impact of tree-killing bark beetles.
doi:10.1371/journal.pone.0026649
PMCID: PMC3197568  PMID: 22028932
17.  Widening of xylem conduits in a conifer tree depends on the longer time of cell expansion downwards along the stem 
Journal of Experimental Botany  2011;63(2):837-845.
The diameter of vascular conduits increases towards the stem base. It has been suggested that this profile is an efficient anatomical feature for reducing the hydraulic resistance when trees grow taller. However, the mechanism that controls the cell diameter along the plant is not fully understood. The timing of cell differentiation along the stem was investigated. Cambial activity and cell differentiation were investigated in a Picea abies tree (11.5 m in height) collecting microsamples at nine different heights (from 1 to 9 m) along the stem with a 4 d time interval. Wood sections (8–12 μm thick) were stained and observed under a light microscope with polarized light to differentiate the developing xylem cells. Cell wall lignification was detected using cresyl violet acetate. The first enlarging cells appeared almost simultaneously along the tree axis indicating that cambium activation is not height-dependent. A significant increase in the duration of the cell expansion phase was observed towards the tree base: at 9 m from the ground, xylem cells expanded for 7 d, at 6 m for 14 d, and at 3 m for 19 d. The duration of the expansion phase is positively correlated with the lumen area of the tracheids (r2=0.68, P < 0.01) at the same height. By contrast, thickness of the cell wall of the earlywood did not show any trend with height. The lumen area of the conduits down the stem appeared linearly dependent on time during which differentiating cells remained in the expansion phase. However, the inductive signal of such long-distance patterned differentiation remains to be identified.
doi:10.1093/jxb/err309
PMCID: PMC3254684  PMID: 22016427
Auxin; cambium; cell differentiation; conduit tapering; Picea abies polar pattern growth
18.  Drought sensitivity of three co-occurring conifers within a dry inner Alpine environment 
Trees (Berlin, Germany : West)  2013;27(1):61-69.
We applied dendroclimatological techniques to determine long-term stationarity of climate-growth relationships and recent growth trends of three widespread coniferous tree species of the central Austrian Alps, which grow intermixed at dry-mesic sites within a dry inner Alpine environment (750 m asl). Time series of annual increments were developed from > 120 mature trees of Picea abies, Larix decidua and Pinus sylvestris. Calculation of response functions for the period 1911 – 2009 revealed significant differences among species in response to climate variables. While precipitation in May – June favoured radial growth of Picea abies and Larix decidua, Pinus sylvestris growth mainly depended on April – May precipitation. P. abies growth was most sensitive to May – June temperature (inverse relationship). Moving response function coefficients indicated increasing drought sensitivity of all species in recent decades, which is related to a decline in soil moisture availability due to increasing stand density and tree size and higher evapotranspiration rates in a warmer climate. While recent trend in basal area increment (BAI) of L. decidua distinctly declined implying high vulnerability to drought stress, moderately shade-tolerant P. abies showed steadily increasing BAI and quite constant BAI was maintained in drought adapted P. sylvestris, although at lowest level of all species. We conclude that synergistic effects of stand dynamics and climate warming increased drought sensitivity, which changed competitive strength of co-occurring conifers due to differences in inherent adaptive capacity.
doi:10.1007/s00468-012-0768-6
PMCID: PMC3750198  PMID: 23976821
Basal area increment; Dendroclimatology; Inner Alpine valley; Radial growth; Moving response function; Tree-ring analysis
19.  Cambial activity related to tree size in a mature silver-fir plantation 
Annals of Botany  2011;108(3):429-438.
Background and Aims
Our knowledge about the influences of environmental factors on tree growth is principally based on the study of dominant trees. However, tree social status may influence intra-annual dynamics of growth, leading to differential responses to environmental conditions. The aim was to determine whether within-stand differences in stem diameters of trees belonging to different crown classes resulted from variations in the length of the growing period or in the rate of cell production.
Methods
Cambial activity was monitored weekly in 2006 for three crown classes in a 40-year-old silver-fir (Abies alba) plantation near Nancy (France). Timings, duration and rate of tracheid production were assessed from anatomical observations of the developing xylem.
Key Results
Cambial activity started earlier, stopped later and lasted longer in dominant trees than in intermediate and suppressed ones. The onset of cambial activity was estimated to have taken 3 weeks to spread to 90 % of the trees in the stand, while the cessation needed 6 weeks. Cambial activity was more intense in dominant trees than in intermediate and suppressed ones. It was estimated that about 75 % of tree-ring width variability was attributable to the rate of cell production and only 25 % to its duration. Moreover, growth duration was correlated to tree height, while growth rate was better correlated to crown area.
Conclusions
These results show that, in a closed conifer forest, stem diameter variations resulted principally from differences in the rate of xylem cell production rather than in its duration. Tree size interacts with environmental factors to control the timings, duration and rate of cambial activity through functional processes involving source–sink relationships principally, but also hormonal controls.
doi:10.1093/aob/mcr168
PMCID: PMC3158687  PMID: 21816842
Cambial activity; forest-stand structure; silver fir (Abies alba); tree-ring formation; tree-to-tree competition; social status; wood anatomy; xylem cell differentiation
20.  Exotic Mammals Disperse Exotic Fungi That Promote Invasion by Exotic Trees 
PLoS ONE  2013;8(6):e66832.
Biological invasions are often complex phenomena because many factors influence their outcome. One key aspect is how non-natives interact with the local biota. Interaction with local species may be especially important for exotic species that require an obligatory mutualist, such as Pinaceae species that need ectomycorrhizal (EM) fungi. EM fungi and seeds of Pinaceae disperse independently, so they may use different vectors. We studied the role of exotic mammals as dispersal agents of EM fungi on Isla Victoria, Argentina, where many Pinaceae species have been introduced. Only a few of these tree species have become invasive, and they are found in high densities only near plantations, partly because these Pinaceae trees lack proper EM fungi when their seeds land far from plantations. Native mammals (a dwarf deer and rodents) are rare around plantations and do not appear to play a role in these invasions. With greenhouse experiments using animal feces as inoculum, plus observational and molecular studies, we found that wild boar and deer, both non-native, are dispersing EM fungi. Approximately 30% of the Pinaceae seedlings growing with feces of wild boar and 15% of the seedlings growing with deer feces were colonized by non-native EM fungi. Seedlings growing in control pots were not colonized by EM fungi. We found a low diversity of fungi colonizing the seedlings, with the hypogeous Rhizopogon as the most abundant genus. Wild boar, a recent introduction to the island, appear to be the main animal dispersing the fungi and may be playing a key role in facilitating the invasion of pine trees and even triggering their spread. These results show that interactions among non-natives help explain pine invasions in our study area.
doi:10.1371/journal.pone.0066832
PMCID: PMC3691272  PMID: 23826154
21.  Multiplex Real-Time PCR for Monitoring Heterobasidion annosum Colonization in Norway Spruce Clones That Differ in Disease Resistance 
A multiplex real-time PCR assay was developed to monitor the dynamics of the Picea abies-Heterobasidion annosum pathosystem. Tissue cultures and 32-year-old trees with low or high resistance to this pathogen were used as the host material. Probes and primers were based on a laccase gene for the pathogen and a polyubiquitin gene for the host. The real-time PCR procedure was compared to an ergosterol-based quantification method in a tissue culture experiment, and there was a strong correlation (product moment correlation coefficient, 0.908) between the data sets. The multiplex real-time PCR procedure had higher resolution and sensitivity during the early stages of colonization and also could be used to monitor the host. In the tissue culture experiment, host DNA was degraded more rapidly in the clone with low resistance than in the clone with high resistance. In the field experiment, the lesions elicited were not strictly proportional to the area colonized by the pathogen. Fungal colonization was more restricted and localized in the lesion in the clone with high resistance, whereas in the clone with low resistance, the fungus could be detected until the visible end of the lesion. Thus, the real-time PCR assay gives better resolution than does the traditionally used lesion length measurement when screening host clones for resistance.
doi:10.1128/AEM.69.8.4413-4420.2003
PMCID: PMC169156  PMID: 12902224
22.  Potato Crop as a Source of Emetic Bacillus cereus and Cereulide-Induced Mammalian Cell Toxicity 
Applied and Environmental Microbiology  2013;79(12):3534-3543.
Bacillus cereus, aseptically isolated from potato tubers, were screened for cereulide production and for toxicity on human and other mammalian cells. The cereulide-producing isolates grew slowly, the colonies remained small (∼1 mm), tested negative for starch hydrolysis, and varied in productivity from 1 to 100 ng of cereulide mg (wet weight)−1 (∼0.01 to 1 ng per 105 CFU). By DNA-fingerprint analysis, the isolates matched B. cereus F5881/94, connected to human food-borne illness, but were distinct from cereulide-producing endophytes of spruce tree (Picea abies). Exposure to cell extracts (1 to 10 μg of bacterial biomass ml−1) and to purified cereulide (0.4 to 7 ng ml−1) from the potato isolates caused mitochondrial depolarization (loss of ΔΨm) in human peripheral blood mononuclear cells (PBMC) and keratinocytes (HaCaT), porcine spermatozoa and kidney tubular epithelial cells (PK-15), murine fibroblasts (L-929), and pancreatic insulin-producing cells (MIN-6). Cereulide (10 to 20 ng ml−1) exposed pancreatic islets (MIN-6) disintegrated into small pyknotic cells, followed by necrotic death. Necrotic death in other test cells was observed only after a 2-log-higher exposure. Exposure to 30 to 60 ng of cereulide ml−1 induced K+ translocation in intact, live PBMC, keratinocytes, and sperm cells within seconds of exposure, depleting 2 to 10% of the cellular K+ stores within 10 min. The ability of cereulide to transfer K+ ions across biological membranes may benefit the producer bacterium in K+-deficient environments such as extracellular spaces inside plant tissue but is a pathogenic trait when in contact with mammalian cells.
doi:10.1128/AEM.00201-13
PMCID: PMC3675918  PMID: 23524678
23.  Ecosystem Function in Appalachian Headwater Streams during an Active Invasion by the Hemlock Woolly Adelgid 
PLoS ONE  2013;8(4):e61171.
Forested ecosystems in the southeastern United States are currently undergoing an invasion by the hemlock woolly adelgid (HWA). Previous studies in this area have shown changes to forest structure, decreases in canopy cover, increases in organic matter, and changes to nutrient cycling on the forest floor and soil. Here, we were interested in how the effects of canopy loss and nutrient leakage from terrestrial areas would translate into functional changes in streams draining affected watersheds. We addressed these questions in HWA-infested watersheds at the Coweeta Hydrologic Laboratory in North Carolina. Specifically, we measured stream metabolism (gross primary production and ecosystem respiration) and nitrogen uptake from 2008 to 2011 in five streams across the Coweeta basin. Over the course of our study, we found no change to in-stream nutrient concentrations. While canopy cover decreased annually in these watersheds, this change in light penetration did not translate to higher rates of in-stream primary production during the summer months of our study. We found a trend towards greater heterotrophy within our watersheds, where in-stream respiration accounted for a much larger component of net ecosystem production than GPP. Additionally, increases in rhododendron cover may counteract changes in light and nutrient availability that occurred with hemlock loss. The variability in our metabolic and uptake parameters suggests an actively-infested ecosystem in transition between steady states.
doi:10.1371/journal.pone.0061171
PMCID: PMC3632569  PMID: 23613803
24.  Temporal and Spatial Profiles of Chitinase Expression by Norway Spruce in Response to Bark Colonization by Heterobasidion annosum 
Pathogen colonization and transcript levels of three host chitinases, putatively representing classes I, II, and IV, were monitored with real-time PCR after wounding and bark infection by Heterobasidion annosum in 32-year-old trees of Norway spruce (Picea abies) with low (clone 409) or high (clone 589) resistance to this pathogen. Three days after inoculation, comparable colonization levels were observed in both clones in the area immediately adjacent to inoculation. At 14 days after infection, pathogen colonization was restricted to the area immediately adjacent to the site of inoculation for clone 589 but had progressed further into the host tissue in clone 409. Transcript levels of the class II and IV chitinases increased after wounding or inoculation, but the transcript level of the class I chitinase declined after these treatments. Transcript levels of the class II and class IV chitinases were higher in areas immediately adjacent to the inoculation site in clone 589 than in similar sites in clone 409 3 days after inoculation. This difference was even more pronounced 2 to 6 mm away from the inoculation point, where no infection was yet established, and suggests that the clones differ in the rate of chitinase-related signal perception or transduction. At 14 days after inoculation, these transcript levels were higher in clone 409 than in clone 589, suggesting that the massive upregulation of class II and IV chitinases after the establishment of infection comes too late to reduce or prevent pathogen colonization.
doi:10.1128/AEM.70.7.3948-3953.2004
PMCID: PMC444825  PMID: 15240268
25.  Root-Associated Ectomycorrhizal Fungi Shared by Various Boreal Forest Seedlings Naturally Regenerating after a Fire in Interior Alaska and Correlation of Different Fungi with Host Growth Responses ▿  
Applied and Environmental Microbiology  2011;77(10):3351-3359.
The role of common mycorrhizal networks (CMNs) in postfire boreal forest successional trajectories is unknown. We investigated this issue by sampling a 50-m by 40-m area of naturally regenerating black spruce (Picea mariana), trembling aspen (Populus tremuloides), and paper birch (Betula papyrifera) seedlings at various distances from alder (Alnus viridis subsp. crispa), a nitrogen-fixing shrub, 5 years after wildfire in an Alaskan interior boreal forest. Shoot biomasses and stem diameters of 4-year-old seedlings were recorded, and the fungal community associated with ectomycorrhizal (ECM) root tips from each seedling was profiled using molecular techniques. We found distinct assemblages of fungi associated with alder compared with those associated with the other tree species, making the formation of CMNs between them unlikely. However, among the spruce, aspen, and birch seedlings, there were many shared fungi (including members of the Pezoloma ericae [Hymenoscyphus ericae] species aggregate, Thelephora terrestris, and Russula spp.), raising the possibility that these regenerating seedlings may form interspecies CMNs. Distance between samples did not influence how similar ECM root tip-associated fungal communities were, and of the fungal groups identified, only one of them was more likely to be shared between seedlings that were closer together, suggesting that the majority of fungi surveyed did not have a clumped distribution across the small scale of this study. The presence of some fungal ribotypes was associated with larger or smaller seedlings, suggesting that these fungi may play a role in the promotion or inhibition of seedling growth. The fungal ribotypes associated with larger seedlings were different between spruce, aspen, and birch, suggesting differential impacts of some host-fungus combinations. One may speculate that wildfire-induced shifts in a given soil fungal community could result in variation in the growth response of different plant species after fire and a shift in regenerating vegetation.
doi:10.1128/AEM.02575-10
PMCID: PMC3126461  PMID: 21441343

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