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1.  Development of a Rain Down Technique to Artificially Infest Hemlocks with the Hemlock Woolly Adelgid, Adelges tsugae 
The hemlock woolly adelgid Adelges tsugae Annand (Hemiptera: Adelgidae), is a non-native invasive pest that has caused widespread decline and mortality of eastern hemlock (Tsuga canadensis (L.) Carr. (Pinales: Pinaceae)) and Carolina hemlock (T. caroliniana Engelm.) in the eastern United States. Our preliminary experiments evaluated the utility of a rain-down technique to induce artificial infestations of A. tsugae on hemlock seedlings en masse. Experiments were conducted in PVC (1 m3) cages topped with poultry wire for placement of A. tsugae-infested branches, and with 1 m2 gridded glue sheets and/or hemlock seedlings placed below to capture adelgid abundance, distribution, and infestation rate data. In the March 2011 experiment, the density of progrediens crawlers (adelgid nymphs, first instars) that rained down inside the PVC cages was significantly higher in the high ovisac treatment compared to the low ovisac treatment, with an estimated 513,000 and 289,000 crawlers per m2 falling beneath each treatment, respectively. Resulting A. tsugae infestation rates on Carolina hemlock seedlings placed inside the cages did not differ between the treatments but were at or above established damage threshold densities for the adelgid. Infestation rates on eastern hemlock seedlings that were placed in cages nine days after the experiment started were below damage threshold levels and did not differ between the treatments. In the May 2011 experiment, the density of sistens crawlers raining down was substantially lower, with 17,000 and 33,000 falling per m2 in the low and high ovisac treatments, respectively. Resulting infestation rates on Carolina hemlock seedlings were extremely low and well below damage threshold levels. Although A. tsugae crawlers were well distributed across the 1 m2 gridded glue sheets placed at the bottom of each cage, hot spots of unusually high crawler density did occur in both experiments. This rain-down technique shows potential for use in an operational tree-breeding program where screening large numbers of hemlock seedlings for resistance to A. tsugae is required.
doi:10.1673/031.014.106
PMCID: PMC4212866  PMID: 25199530
exotic species; host resistance screening; artificial infestation; Tsuga canadensis; Tsuga caroliniana
2.  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
3.  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
4.  Failure under stress: the effect of the exotic herbivore Adelges tsugae on biomechanics of Tsuga canadensis 
Annals of Botany  2013;113(4):721-730.
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.
doi:10.1093/aob/mct286
PMCID: PMC3936583  PMID: 24335663
Biomechanics; Tsuga canadensis; eastern hemlock; Adelges tsugae; HWA; herbivory; invasive; wood density; lignin; tensile strength; flexural strength
5.  Transmission of the Pinewood Nematode, Bursaphelenchus xylophilus, to Slash Pine Trees and Log Bolts by a Cerambycid Beetle, Monochamus titillator, in Florida 
Journal of Nematology  1984;16(1):37-40.
Field-collected adults of the southern pine sawyer, Monochamus titillator (F.) (Coleoptera: Cerambycidae), naturally infested with fourth-stage juveniles (dauerlarvae) of the pinewood nematode, Bursaphelenchus xylophilus (Steiner and Buhrer, 1934) Nickle, 1970, were maturation fed on excised shoots of typical slash pine, Pinus elliottii Engelm. var elliottii, for 21 days. During August 1981, a male and female adult beetle were held in a sleeve cage placed on the terminal of a side branch of each of seven replicate, healthy 10-year-old slash pine trees. All seven branch terminals showed evidence of beetle feeding on the bark after 1 week, and pinewood nematodes were present in wood samples taken near these feeding sites. Four of the seven trees showed wilt symptoms in 4-6 weeks and died about 9 weeks after beetle feeding. Pinewood nematodes were recovered from the roots and trunks of the dead trees. Each of seven replicate slash pine log bolts was enclosed in a jar with a pair of the same beetles used in the sleeve cages. After 1 week, wood underlying beetle oviposition sites in the bark of all replicate log bolts was infested with the pinewood nematode.
PMCID: PMC2618336  PMID: 19295871
Bursaphelenchus xylophilus; Pinus elliottii; Monochamus titillator; maturation-feeding; oviposition
6.  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
7.  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
8.  Ecological boundary detection using Bayesian areal wombling 
Ecology  2010;91(12):3448-3514.
The study of ecological boundaries and their dynamics is of fundamental importance to much of ecology, biogeography, and evolution. Over the past two decades, boundary analysis (of which wombling is a subfield) has received considerable research attention, resulting in multiple approaches for the quantification of ecological boundaries. Nonetheless, few methods have been developed that can simultaneously (1) analyze spatially homogenized data sets (i.e., areal data in the form of polygons rather than point-reference data); (2) account for spatial structure in these data and uncertainty associated with them; and (3) objectively assign probabilities to boundaries once detected. Here we describe the application of a Bayesian hierarchical framework for boundary detection developed in public health, which addresses these issues but which has seen limited application in ecology. As examples, we analyze simulated spread data and the historic pattern of spread of an invasive species, the hemlock woolly adelgid (Adelges tsugae), using county-level summaries of the year of first reported infestation and several covariates potentially important to influencing the observed spread dynamics. Bayesian areal wombling is a promising approach for analyzing ecological boundaries and dynamics related to changes in the distributions of native and invasive species.
PMCID: PMC4024662  PMID: 21302814
Adelges tsugae; boundary analysis; ecotones; edge detection; hemlock woolly adelgid; invasive species; spatial statistics
9.  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
10.  Newly Discovered Transmission Pathway of Bursaphelenchus xylophilus from Males of the Beetle Monochamus alternatus to Pinus densiflora Trees via Oviposition Wounds 
Journal of Nematology  2002;34(4):396-404.
The transmission of Bursaphelenchus xylophilus from Monochamus alternatus males to Pinus densiflora trees via oviposition wounds has been determined. Nematode-infested males, with mandibles fixed experimentally to prevent feeding, were placed for 48 hours with pine bolts containing oviposition wounds that had been made by nematode-free females. After removal of the nematode-infested males, the pine bolts were held for 1 month and then examined for the presence of nematodes. Reproducing nematode populations were recovered from pine bolts that were exposed to male beetles carrying a high number of nematodes. No reproducing nematode population could be recovered from pine bolts exposed to beetles with a small number of nematodes. Nematode reproduction in the pine bolts was not related to the number of oviposition wounds per bolt. Fourth-stage dispersal B. xylophilus juveniles, collected from beetle body surfaces, were inoculated on pine bolt bark 0, 5, 10, and 15 cm away from a single artificial, small hole. These dauer juveniles successfully entered some bolts. The probability of successful nematode reproduction decreased with increased distance between inoculation point and artificial hole. The results indicated that B. xylophilus can move a significant distance to oviposition wounds along the bark surface and enter a tree via the wounds. The new transmission pathway is considered important for the nematode to persist in pine forests such as in North America where pine wilt disease does not occur.
PMCID: PMC2620576  PMID: 19265963
Bursaphelenchus xylophilus; Monochamus alternatus; multiple infection; nematode movement; oviposition wound; Pinus densiflora; transmission
11.  Do water-limiting conditions predispose Norway spruce to bark beetle attack? 
The New Phytologist  2014;205(3):1128-1141.
Drought is considered to enhance susceptibility of Norway spruce (Picea abies) to infestations by the Eurasian spruce bark beetle (Ips typographus, Coleoptera: Curculionidae), although empirical evidence is scarce. We studied the impact of experimentally induced drought on tree water status and constitutive resin flow, and how physiological stress affects host acceptance and resistance.We established rain-out shelters to induce both severe (two full-cover plots) and moderate (two semi-cover plots) drought stress. In total, 18 sample trees, which were divided equally between the above treatment plots and two control plots, were investigated. Infestation was controlled experimentally using a novel ‘attack box’ method.Treatments influenced the ratios of successful and defended attacks, but predisposition of trees to infestation appeared to be mainly driven by variations in stress status of the individual trees over time. With increasingly negative twig water potentials and decreasing resin exudation, the defence capability of the spruce trees decreased.We provide empirical evidence that water-limiting conditions impair Norway spruce resistance to bark beetle attack. Yet, at the same time our data point to reduced host acceptance byI. typographus with more extreme drought stress, indicated by strongly negative pre-dawn twig water potentials.
doi:10.1111/nph.13166
PMCID: PMC4315866  PMID: 25417785
climate change; defence capability; drought stress; host acceptance; Ips typographus; Norway spruce (Picea abies); predisposition; tree physiology
12.  Scatter Hoarding of Seeds Confers Survival Advantages and Disadvantages to Large-Seeded Tropical Plants at Different Life Stages 
PLoS ONE  2015;10(5):e0124932.
Scatter hoarding of seeds by animals contributes significantly to forest-level processes, including plant recruitment and forest community composition. However, the potential positive and negative effects of caching on seed survival, germination success, and seedling survival have rarely been assessed through experimental studies. Here, I tested the hypothesis that seed burial mimicking caches made by scatter hoarding Central American agoutis (Dasyprocta punctate) enhances seed survival, germination, and growth by protecting seeds from seed predators and providing favorable microhabitats for germination. In a series of experiments, I used simulated agouti seed caches to assess how hoarding affects seed predation by ground-dwelling invertebrates and vertebrates for four plant species. I tracked germination and seedling growth of intact and beetle-infested seeds and, using exclosures, monitored the effects of mammals on seedling survival through time. All experiments were conducted over three years in a lowland wet forest in Costa Rica. The majority of hoarded palm seeds escaped predation by both invertebrates and vertebrates while exposed seeds suffered high levels of infestation and removal. Hoarding had no effect on infestation rates of D. panamensis, but burial negatively affected germination success by preventing endocarp dehiscence. Non-infested palm seeds had higher germination success and produced larger seedlings than infested seeds. Seedlings of A. alatum and I. deltoidea suffered high mortality by seed-eating mammals. Hoarding protected most seeds from predators and enhanced germination success (except for D. panamensis) and seedling growth, although mammals killed many seedlings of two plant species; all seedling deaths were due to seed removal from the plant base. Using experimental caches, this study shows that scatter hoarding is beneficial to most seeds and may positively affect plant propagation in tropical forests, although tradeoffs in seed survival do exist.
doi:10.1371/journal.pone.0124932
PMCID: PMC4430353  PMID: 25970832
13.  Negative Feedbacks on Bark Beetle Outbreaks: Widespread and Severe Spruce Beetle Infestation Restricts Subsequent Infestation 
PLoS ONE  2015;10(5):e0127975.
Understanding disturbance interactions and their ecological consequences remains a major challenge for research on the response of forests to a changing climate. When, where, and how one disturbance may alter the severity, extent, or occurrence probability of a subsequent disturbance is encapsulated by the concept of linked disturbances. Here, we evaluated 1) how climate and forest habitat variables, including disturbance history, interact to drive 2000s spruce beetle (Dendroctonus rufipennis) infestation of Engelmann spruce (Picea engelmannii) across the Southern Rocky Mountains; and 2) how previous spruce beetle infestation affects subsequent infestation across the Flat Tops Wilderness in northwestern Colorado, which experienced a severe landscape-scale spruce beetle infestation in the 1940s. We hypothesized that drought and warm temperatures would promote infestation, whereas small diameter and non-host trees, which may reflect past disturbance by spruce beetles, would inhibit infestation. Across the Southern Rocky Mountains, we found that climate and forest structure interacted to drive the 2000s infestation. Within the Flat Tops study area we found that stands infested in the 1940s were composed of higher proportions of small diameter and non-host trees ca. 60 years later. In this area, the 2000s infestation was constrained by a paucity of large diameter host trees (> 23 cm at diameter breast height), not climate. This suggests that there has not been sufficient time for trees to grow large enough to become susceptible to infestation. Concordantly, we found no overlap between areas affected by the 1940s infestation and the current infestation. These results show a severe spruce beetle infestation, which results in the depletion of susceptible hosts, can create a landscape template reducing the potential for future infestations.
doi:10.1371/journal.pone.0127975
PMCID: PMC4441381  PMID: 26000906
14.  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
15.  Responses by Coleoptiles of Intact Rice Seedlings to Anoxia: K+ Net Uptake from the External Solution and Translocation from the Caryopses 
Annals of Botany  2003;91(2):271-278.
This study evaluated the effects of anoxia on K+ uptake and translocation in 3–4‐d‐old, intact, rice seedlings (Oryza sativa L. cv. Calrose). Rates of net K+ uptake from the medium over 24 h by coleoptiles of anoxic seedlings were inhibited by 83–91 %, when compared with rates in aerated seedlings. Similar uptake rates, and degree of inhibition due to anoxia, were found for Rb+ when supplied over 1·5–2 h, starting 22 h after imposing anoxia. The Rb+ uptake indicated that intact coleoptiles take up ions directly from the external solution. Monovalent cation (K+ and Rb+) net uptake from the solution was inhibited by anoxia to the same degree for the coleoptiles of intact seedlings and for coleoptiles excised, ‘aged’, and supplied with exogenous glucose. Transport of endogenous K+ from caryopses to coleoptiles was inhibited less by anoxia than net K+ uptake from the solution, the inhibition being 55 % rather than 87 %. Despite these inhibitions, osmotic pressures of sap (πsap) expressed from coleoptiles of seedlings exposed to 48 h of anoxia, with or without exogenous K+, were 0·66 ± 0·03 MPa; however, the contributions of K+ to πsap were 23 and 16 %, respectively. After 24 h of anoxia, the K+ concentrations in the basal 10 mm of the coleoptiles of seedlings with or without exogenous K+, were similar to those in aerated seedlings with exogenous K+. In contrast, K+ concentrations had decreased in aerated seedlings without exogenous K+, presumably due to ‘dilution’ by growth; fresh weight gains of the coleoptile being 3·6‐ to 4·7‐fold greater in aerated than in anoxic seedlings. Deposition rates of K+ along the axes of the coleoptiles were calculated for the anoxic seedlings only, for which we assessed the elongation zone to be only the basal 4 mm. K+ deposition in the basal 6 mm was similar for seedlings with or without exogenous K+, at 0·6–0·87 µmol g–1 f. wt h–1. Deposition rates in zones above 6 mm from the base were greater for seedlings with, than without, exogenous K+; the latter were sometimes negative. We conclude that for the coleoptiles of rice seedlings, anoxia inhibits net K+ uptake from the external solution to a much larger extent than K+ translocation from the caryopses. Furthermore, K+ concentrations in the elongation zone of the coleoptiles of anoxic seedlings were maintained to a remarkable degree, contributing to maintenance of πsap in cells of these elongating tissues.
doi:10.1093/aob/mcf122
PMCID: PMC4244992  PMID: 12509347
Anoxia; caryopsis; coleoptile; Oryza sativa; osmotic pressure; potassium; uptake; translocation; seedlings; spatial distribution
16.  Planting Sentinel European Trees in Eastern Asia as a Novel Method to Identify Potential Insect Pest Invaders 
PLoS ONE  2015;10(5):e0120864.
Quarantine measures to prevent insect invasions tend to focus on well-known pests but a large proportion of the recent invaders were not known to cause significant damage in their native range, or were not even known to science before their introduction. A novel method is proposed to detect new potential pests of woody plants in their region of origin before they are introduced to a new continent. Since Asia is currently considered to be the main supplier of insect invaders to Europe, sentinel trees were planted in China during 2007-2011 as an early warning tool to identify the potential for additional Asian insect species to colonize European trees. Seedlings (1-1.5 m tall) of five broadleaved (Quercus petraea, Q. suber, Q. ilex, Fagus sylvatica, and Carpinus betulus) and two conifer species (Abies alba and Cupressus sempervirens) were planted in blocks of 100 seedlings at two widely separated sites (one in a nursery near Beijing and the other in a forest environment near Fuyang in eastern China), and then regularly surveyed for colonization by insects. A total of 104 insect species, mostly defoliators, were observed on these new hosts, and at least six species were capable of larval development. Although a number of the insects observed were probably incidental feeders, 38 species had more than five colonization events, mostly infesting Q. petraea, and could be considered as being capable of switching to European trees if introduced to Europe. Three years was shown to be an appropriate duration for the experiment, since the rate of colonization then tended to plateau. A majority of the identified species appeared to have switched from agricultural crops and fruit trees rather than from forest trees. Although these results are promising, the method is not appropriate for xylophagous pests and other groups developing on larger trees. Apart from the logistical problems, the identification to species level of the specimens collected was a major difficulty. This situation could be improved by the development of molecular databases.
doi:10.1371/journal.pone.0120864
PMCID: PMC4439023  PMID: 25993342
17.  Relationships between Community Level Functional Traits of Trees and Seedlings during Secondary Succession in a Tropical Lowland Rainforest 
PLoS ONE  2015;10(7):e0132849.
Most of the previous studies on functional traits focus exclusively on either seedlings or trees. Little knowledge exists on the relationships between community level functional traits of trees and seedlings during succession. Here, we examine variations of the community-level functional traits for trees and seedlings and their correlations along a secondary successional and environmental gradient in a tropical lowland rainforest after shifting cultivation. The results showed that the dynamic patterns in community level functional traits of seedlings were generally consistent with those of the trees during secondary succession. Compared with seedlings, community level traits for trees were less affected by abiotic factors during secondary succession. Correlations between community level functional traits of trees and seedlings were significant for: leaf dry matter content and leaf nitrogen concentration in the 18-year-old fallow; leaf chlorophyll content in the 30-year-old fallow; specific leaf area, leaf dry matter content and leaf nitrogen concentration in the 60-year-old fallow; and leaf nitrogen concentration in old growth. However, these traits except specific leaf area for the tree and seedling communities were all significantly correlated if all the successional stages were combined. Our results suggest that the correlations between community level functional traits of trees and those of seedlings depend on the actual traits and the successional stages examined. However, if all the four successional stages are combined, then four out of five of the community level functional traits for trees could be well predicted by those of the seedlings in the tropical lowland rain forest.
doi:10.1371/journal.pone.0132849
PMCID: PMC4501726  PMID: 26172543
18.  Light and competition gradients fail to explain the coexistence of shade-tolerant Fagus sylvatica and shade-intermediate Quercus petraea seedlings 
Annals of Botany  2013;112(7):1421-1430.
Background and Aims
The coexistence of forest tree species has often been linked to differences among species in terms of their response to light availability during the regeneration stage. From this perspective, species coexistence results from growth–growth or mortality–growth trade-offs along spatial light gradients. Experimental evidence of growth–growth trade-offs in natural conditions is sparse due to various confounding factors that potentially hinder the relationship. This study examined growth hierarchies along light gradients between two tree species with contrasting shade tolerance by controlling potential confounding factors such as seedling size, seedling status, seedling density and species composition.
Methods
Natural regenerated shade-tolerant Fagus sylvatica and shade-intermediate Quercus petraea seedlings were used, and growth rankings over a 4-year period were compared in 8- to 10-year-old tree seedlings.
Key results
No rank reversal occurs between the two species along the light gradient, or along the density, mixture or seedling size gradients. The shade-tolerant species was always the more competitive of the two. Pronounced effects of initial size on seedling growth were observed, whereas the effects of light and competition by neighbours were of secondary importance. The paramount effect of size, which results from the asymmetric nature of interseedling competition, gives a strong advantage to tall seedlings over the long term.
Conclusions
This study extends previous efforts to identify potential drivers of rank reversals in young tree mixtures. It does not support the classical assumption that spatial heterogeneity in canopy opening explains the coexistence of the two species studied. It suggests that spatial variation in local size hierarchies among seedlings that may be caused by seedling emergence time or seedling initial performance is the main driver of the dynamics of these mixed stands.
doi:10.1093/aob/mct200
PMCID: PMC3806531  PMID: 24036670
Rank reversal; seedling growth; density; mixture; niche differentiation; forest dynamics; succession; competition gradient; plant–plant interactions; Fagus sylvatica; Quercus petraea
19.  Seasonal Pattern of Tomato Mosaic Tobamovirus Infection and Concentration in Red Spruce Seedlings 
Tomato mosaic tobamovirus (ToMV) infects red spruce (Picea rubens) and causes significant changes in its growth and physiology. The mechanism of infection and the pattern of virus concentration in seedling roots and needles were investigated. One-year-old red spruce seedlings were obtained from the nursery in April and June 1995 and August 1996 and tested for ToMV using enzyme-linked immunosorbent assay (ELISA). Virus-free seedlings were divided into three treatments: control, root inoculated, and needle inoculated. Two control, five root-inoculated, and five needle-inoculated seedlings were sampled destructively at biweekly intervals for 3 months and then tested for ToMV by ELISA. ToMV was transmitted to seedlings by root but not by needle inoculation. The virus was detected in 67 to 100% of roots but in less than 7% of needles of root-inoculated seedlings. The percent infection of root-inoculated seedlings differed significantly between the April and June and between the April and August inoculation periods. Virus concentration in infected seedling roots increased initially, peaked within 4 weeks postinoculation, and steadily declined thereafter. Significant differences in ToMV concentrations in roots also were detected among inoculation periods and sampling dates. Early spring may represent the optimal time for infection of seedlings, as well as for assaying roots for ToMV.
PMCID: PMC106166  PMID: 16349546
20.  Seasonal Variation in CO2 Efflux of Stems and Branches of Norway Spruce Trees 
Annals of Botany  2007;101(3):469-477.
Background and Aims
Stem and branch respiration, important components of total forest ecosystem respiration, were measured on Norway spruce (Picea abies) trees from May to October in four consecutive years in order (1) to evaluate the influence of temperature on woody tissue CO2 efflux with special focus on variation in Q10 (change in respiration rate resulting from a 10 °C increase in temperature) within and between seasons, and (2) to quantify the contribution of above-ground woody tissue (stem and branch) respiration to the carbon balance of the forest ecosystem.
Methods
Stem and branch CO2 efflux were measured, using an IRGA and a closed gas exchange system, 3–4 times per month on 22-year-old trees under natural conditions. Measurements of ecosystem CO2 fluxes were also determined during the whole experiment by using the eddy covariance system. Stem and branch temperatures were monitored at 10-min intervals during the whole experiment.
Key Results
The temperature of the woody tissue of stems and branches explained up to 68 % of their CO2 efflux. The mean annual Q10 values ranged from 2·20 to 2·32 for stems and from 2·03 to 2·25 for branches. The mean annual normalized respiration rate, R10, for stems and branches ranged from 1·71 to 2·12 µmol CO2 m−2s −1 and from 0·24 to 0·31 µmol CO2 m−2 s−1, respectively. The annual contribution of stem and branch CO2 efflux to total ecosystem respiration were, respectively, 8·9 and 8·1 % in 1999, 9·2 and 9·2 % in 2000, 7·6 and 8·6 % in 2001, and 8·6 and 7·9 % in 2002. Standard deviation for both components ranged from 3 to 8 % of the mean.
Conclusions
Stem and branch CO2 efflux varied diurnally and seasonally, and were related to the temperature of the woody tissue and to growth. The proportion of CO2 efflux from stems and branches is a significant component of the total forest ecosystem respiration, approx. 8 % over the 4 years, and predictive models must take their contribution into account.
doi:10.1093/aob/mcm304
PMCID: PMC2701814  PMID: 18057065
Stem respiration; branch respiration; Picea abies; seasonal variation; temperature; Q10; R10
21.  Mycorrhiza Reduces Adverse Effects of Dark Septate Endophytes (DSE) on Growth of Conifers 
PLoS ONE  2012;7(8):e42865.
Mycorrhizal roots are frequently colonized by fungi of the Phialocephala fortinii s.l. – Acephala applanata species complex (PAC). These ascomycetes are common and widespread colonizers of tree roots. Some PAC strains reduce growth increments of their hosts but are beneficial in protecting roots against pathogens. Nothing is known about the effects of PAC on mycorrhizal fungi and the PAC-mycorrhiza association on plant growth, even though these two fungal groups occur closely together in natural habitats. We expect reduced colonization rates and reduced negative effects of PAC on host plants if roots are co-colonized by an ectomycorrhizal fungus (ECM). Depending on the temperature regime interactions among the partners in this tripartite ECM-PAC-plant system might also change. To test our hypotheses, effects of four PAC genotypes (two pathogenic and two non-pathogenic on the Norway spruce), mycorrhization by Laccaria bicolor (strain S238N) and two temperature regimes (19°C and 25°C) on the biomass of the Douglas-fir (Pseudotsuga menziesii) and Norway spruce (Picea abies) seedlings were studied. Mycorrhization compensated the adverse effects of PAC on the growth of the Norway spruce at both temperatures. The growth of the Douglas-fir was not influenced either by PAC or mycorrhization at 19°C, but at 25°C mycorrhization had a similar protective effect as in the Norway spruce. The compensatory effects probably rely on the reduction of the PAC-colonization density by mycorrhizae. Temperature and the PAC strain only had a differential effect on the biomass of the Norway spruce but not on the Douglas-fir. Higher temperature reduced mycorrhization of both hosts. We conclude that ectomycorrhizae form physical and/or physiological barriers against PAC leading to reduced PAC-colonization of the roots. Additionally, our results indicate that global warming could cause a general decrease of mycorrhization making primary roots more accessible to other symbionts and pathogens.
doi:10.1371/journal.pone.0042865
PMCID: PMC3416760  PMID: 22900058
22.  The Pine Bark Adelgid, Pineus strobi, Contains Two Novel Bacteriocyte-Associated Gammaproteobacterial Symbionts 
Bacterial endosymbionts of the pine bark adelgid, Pineus strobi (Insecta: Hemiptera: Adelgidae), were investigated using transmission electron microscopy, 16S and 23S rRNA-based phylogeny, and fluorescence in situ hybridization. Two morphologically different symbionts affiliated with the Gammaproteobacteria were present in distinct bacteriocytes. One of them (“Candidatus Annandia pinicola”) is most closely related to an endosymbiont of Adelges tsugae, suggesting that they originate from a lineage already present in ancient adelgids before the hosts diversified into the two major clades, Adelges and Pineus. The other P. strobi symbiont (“Candidatus Hartigia pinicola”) represents a novel symbiont lineage in members of the Adelgidae. Our findings lend further support for a complex evolutionary history of the association of adelgids with a phylogenetically diverse set of bacterial symbionts.
doi:10.1128/AEM.03310-13
PMCID: PMC3911223  PMID: 24271164
23.  Differences in Growth Characteristics and Dynamics of Elements Absorbed in Seedlings of Three Spruce Species Raised on Serpentine Soil in Northern Japan 
Annals of Botany  2005;95(4):661-672.
• Background and Aims Serpentine soils are characterized by the presence of heavy metals (Ni and Cr) and excess Mg; these elements often suppress plant growth. Picea glehnii is nevertheless distributed widely on serpentine soils in northern Japan. Growth characteristics were compared among P. glehnii, Picea jezoensis (distributed in the same region) and Picea abies (planted for timber production), and concentrations of elements in various tissues over time and the amount of ectomycorrhizal infection in short roots were evaluated.
• Methods Seedlings of three spruce species were planted in two types of experimental plots, comprising serpentine soil and brown forest (non-serpentine) soil, and these seedlings were grown for 3 years. Growth, ectomycorrhizal infection of short roots, and elemental composition of tissues were examined.
• Key Results The total dry mass of P. glehnii planted on serpentine soil was almost the same as on brown forest soil, and a large number of needles survived to reach later age classes. By contrast, growth of P. jezoensis and P. abies in serpentine soil was significantly less than in brown forest soil, and needle shedding was accelerated. Moreover, roots of seedlings of P. glehnii on serpentine soil were highly infected with ectomycorrhiza, and the concentration of Ni in needles and roots of P. glehnii was the lowest of the three species.
• Conclusions Picea glehnii has a high ability to maintain a low concentration of Ni, and the ectomycorrhizal infection may have the positive effect of excluding Ni. As a result, P. glehnii is more tolerant than the other spruce species to serpentine soil conditions.
doi:10.1093/aob/mci063
PMCID: PMC4246854  PMID: 15650010
Picea glehnii; Picea jezoensis; Picea abies; serpentine soil; growth; needle longevity; ectomycorrhiza; nutrient physiology; metal exclusion
24.  Higher Thermal Acclimation Potential of Respiration but Not Photosynthesis in Two Alpine Picea Taxa in Contrast to Two Lowland Congeners 
PLoS ONE  2015;10(4):e0123248.
The members of the genus Picea form a dominant component in many alpine and boreal forests which are the major sink for atmospheric CO2. However, little is known about the growth response and acclimation of CO2 exchange characteristics to high temperature stress in Picea taxa from different altitudes. Gas exchange parameters and growth characteristics were recorded from four year old seedlings of two alpine (Picea likiangensis vars. rubescens and linzhiensis) and two lowland (P. koraiensis and P. meyeri) taxa. Seedlings were grown at moderate (25°C/15°C) and high (35°C/25°C) day/night temperatures, for four months. The approximated biomass increment (ΔD2H) for all taxa decreased under high temperature stress, associated with decreased photosynthesis and increased respiration. However, the two alpine taxa exhibited lower photosynthetic acclimation and higher respiratory acclimation than either lowland taxon. Moreover, higher leaf dry mass per unit area (LMA) and leaf nitrogen content per unit area (Narea), and a smaller change in the nitrogen use efficiency of photosynthesis (PNUE) for lowland taxa indicated that these maintained higher homeostasis of photosynthesis than alpine taxa. The higher respiration rates produced more energy for repair and maintenance biomass, especially for higher photosynthetic activity for lowland taxa, which causes lower respiratory acclimation. Thus, the changes of ΔD2H for alpine spruces were larger than that for lowland spruces. These results indicate that long term heat stress negatively impact on the growth of Picea seedlings, and alpine taxa are more affected than low altitude ones by high temperature stress. Hence the altitude ranges of Picea taxa should be taken into account when predicting changes to carbon fluxes in warmer conditions.
doi:10.1371/journal.pone.0123248
PMCID: PMC4395334  PMID: 25874631
25.  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

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