Temperature Effects on the Onset of Sporulation by Phytophthora ramorum on Rhododendron ‘Cunningham's White’

The effect of temperature and moist period on the onset of sporangia production by Phytophthora ramorum on Rhododendron ‘Cunningham's White’ was examined with misted detached leaves held in humid chambers. Following wound inoculation with sporangia, leaves were pre‐incubated at 20°C for either 24 or 72 h prior to placement at six different temperatures (4, 10, 15, 20, 25 and 30°C). The overall mean moist period required for first occurrence of sporulation over all six temperatures was 3.24 days with the 24‐h pre‐incubation time, compared with 1.49 days for the 72‐h pre‐incubation time. Following 24 h pre‐incubation at 20°C and at an incubation temperature of 15°C, sporangia were first collected from leaves following a 24 h incubation. At 10 and 20°C, sporangia were first collected after 48 h, whereas at 4, 25 and 30°C, sporangia were first collected after 3 days. Following 72 h pre‐incubation at 20°C, sporulation generally occurred within 1 day, even at temperatures such at 4 and 30°C that are suboptimal for sporulation. The highest levels of P. ramorum sporulation were observed at 20°C. P. ramorum formed sporangia on host tissue under moist conditions within the same time frame reported for P. phaseoli, P. palmivora and P. nicotianae, but substantially more slowly than certain other species such as P. infestans. Quantifying moisture and temperature conditions for initiation of sporangia production provides knowledge which leads to a greater understanding of the epidemic potential of P. ramorum.     

Effects of Inoculum Density and Wounding on Stem Infection of Three Eastern US Forest Species by Phytophthora ramorum

Seedlings of three Eastern US forest species Quercus rubra (northern red oak), Quercus prinus (chestnut oak) and Acer rubrum (red maple) were inoculated by applying Phytophthora ramorum sporangia to stems at different inoculum densities with and without wounding. Disease occurred in all treatments involving wounds, and no disease was observed in unwounded treatments. Younger seedlings (2–3 years old) did not differ significantly from older seedlings (5–6 years old) in disease incidence, but older seedlings sustained smaller lesions compared with younger seedlings. For both old and young seedlings, disease on wounded stems was observed down to the lowest sporangia concentration utilized (500 sporangia/ml for old seedlings and 100 sporangia/ml for young seedlings). The results show that in the presence of wounding, even very low sporangia concentrations can result in disease, and further suggest that wounding caused by insects and other factors may play an important role in P. ramorum epidemiology in forest environments.     

Stromata, sporangiomata and chlamydosori of Phytophthora ramorum on inoculated Mediterranean woody plants

Three types of multihyphal structures, stromata, sporangiomata and chlamydosori, are described for the plant pathogen Phytophthora ramorum. Their morphology, morphogenesis and position on the host organ were observed by dissecting, compound and scanning electron microscopy. Stromata were consistently formed one to two weeks after zoospore inoculation of detached leaves and fruits of an assortment of Mediterranean sclerophyll shrubs. Stroma initials appeared subcuticularly or subepidermally and developed as small hyphal aggregates by repeated branching, budding, swelling and interweaving, eventually forming a prosenchyma. They always emerged through the adaxial side of the leaf by rupture of the overlying host tissue. Occasionally sporangia and chlamydosori (packed clusters of chlamydospores) were formed on the stromata. Sporangiomata bore short sporangiophores and clusters of 20–100 sporangia and resembled sporodochia of the mitosporic fungi. The biological significance of these multihyphal structures is discussed. Some epidemiological aspects were also studied: several understorey species of the holm oak (Quercus ilex) woodland were susceptible to in vitro infection with three isolates of P. ramorum originally collected from different ornamental hosts. The risk of spread to this ecosystem is evaluated.     

Phytophthora ramorum: a pathogen with a remarkably wide host range causing sudden oak death on oaks and ramorum blight on woody ornamentals

Phytophthora ramorum is an oomycete plant pathogen classified in the kingdom Stramenopila. P. ramorum is the causal agent of sudden oak death on coast live oak and tanoak as well as ramorum blight on woody ornamental and forest understorey plants. It causes stem cankers on trees, and leaf blight or stem dieback on ornamentals and understorey forest species. This pathogen is managed in the USA and Europe by eradication where feasible, by containment elsewhere and by quarantine in many parts of the world. Genomic resources provide information on genes of interest to disease management and have improved tremendously since sequencing the genome in 2004. This review provides a current overview of the pathogenicity, population genetics, evolution and genomics of P. ramorum. Taxonomy: Phytophthora ramorum (Werres, De Cock & Man in't Veld): kingdom Stramenopila; phylum Oomycota; class Peronosporomycetidae; order Pythiales; family Pythiaceae; genus Phytophthora. Host range: The host range is very large and the list of known hosts continues to expand at the time of writing. Coast live oak and tanoak are ecologically, economically and culturally important forest hosts in the USA. Rhododendron, Viburnum, Pieris, Syringa and Camellia are key ornamental hosts on which P. ramorum has been found repeatedly, some of which have been involved in moving the pathogen via nursery shipments. Disease symptoms: P. ramorum causes two different diseases with differing symptoms: sudden oak death (bleeding lesions, stem cankers) on oaks and ramorum blight (twig dieback and/or foliar lesions) on tree and woody ornamental hosts. Useful websites: http://nature.berkeley.edu/comtf/ , http://rapra.csl.gov.uk/ , http://www.aphis.usda.gov/plant_health/plant_pest_info/pram/index.shtml , http://genome.jgi‐psf.org/Phyra1_1/Phyra1_1.home.html , http://pamgo.vbi.vt.edu/ , http://pmgn.vbi.vt.edu/ , http://vmd.vbi.vt.edu./ , http://web.science.oregonstate.edu/bpp/labs/grunwald/resources.htm , http://www.defra.gov.uk/planth/pramorum.htm , http://www.invasive.org/browse/subject.cfm?sub=4603 , http://www.forestry.gov.uk/forestry/WCAS‐4Z5JLL     

Enhanced Recovery of Phytophthora ramorum from Soil Following 30 Days of Storage at 4°C

Chlamydospores of Phytophthora ramorum were used to infest field soil at densities ranging from 0.2 to 42 chlamydospores/cm³ soil. Recovery was determined by baiting with rhododendron leaf discs and dilution plating at time 0 and after 30 days of storage at 4°C, as recommended by USDA‐APHIS. Baiting was slightly more sensitive than dilution plating in recovering P. ramorum immediately following infestation of soil and allowed detection from samples infested with as little as 0.2 chlamydospores/cm³ compared with 1 chlamydospore/cm³ for dilution plating. After 30 days of infested soil storage at 4°C, P. ramorum was detected at significantly (P = 0.05) higher levels than at time 0 with both recovery methods. The results indicate that storage of P. ramorum‐infested soil at 4°C may allow for pathogen activity, such as sporangia production, which may enhance recovery from soil.     

The effect of salinity on the survival,growth, sporulation and infection of Phytophthora ramorum

Phytophthora ramorum has been found in waterways outside infested nurseries, but little is known about its behavior in water. This study examined the effect of salinity on survival, growth, sporulation, and infection. P. ramorum survival and growth was negatively correlated with salt concentration (range of 0–45 g l⁻¹), but showed a level of tolerance even at 45 g l⁻¹. No sporangia were observed in cultures with higher than 20 g l⁻¹ of salt and zoospores were not released from sporangia above 14 g l⁻¹. Water sources with different salinity were used to understand the environment where P. ramorum can survive and infect host material. Water from natural bodies and water amended with different salt concentrations were added to P. ramorum-infested sand and baited with rhododendron leaf disks. Infection decreased with increasing salt concentration and increased with higher initial concentration of P. ramorum. This research helps to better understand the effects of water quality on survival and infectivity of P. ramorum, expanding the potential survey range.     

Impact of sudden oak death on tree mortality in the Big Sur ecoregion of California

The Big Sur ecoregion in coastal California is a botanically and ecologically diverse area that has recently experienced substantial mortality of oak (Quercus spp.) and tanoak (Lithocarpus densiflorus) trees due to the emerging forest disease sudden oak death, caused by the invasive pathogen Phytophthora ramorum. In response to the urgent need to examine environmental impacts and create management response strategies, we quantified the impact of P. ramorum invasion on tree mortality across the Big Sur ecoregion using high-resolution aircraft imagery and field data. Using the imagery, we mapped all detectable oak and tanoak trees possibly killed by P. ramorum infection within redwood-tanoak forests and mixed oak woodlands. To validate and improve our remote assessment, we quantified the number, size, and infection status of host trees in 77 field plots (0.25 ha). The field data showed that our remote assessment underestimated mortality due to the occurrence of dead trees in the forest understory. For each forest type, we developed regression models that adjusted our remote assessments of tree mortality in relation to field observations of mortality and local habitat variables. The models significantly improved remote assessment of oak mortality, but relationships were stronger for mixed oak woodlands (r ² = 0.77) than redwood-tanoak forests (r ² = 0.66). Using the field data, we also modeled the amount of dead tree basal area (m²) in relation to the density of mapped dead trees in mixed oak woodlands (r ² = 0.73) and redwood-tanoak forests (r ² = 0.54). Application of the regression models in a GIS estimated 235,678 standing dead trees in 2005 and 12,650 m² of tree basal area removed from the ecoregion, with 63% of mortality occurring in redwood-tanoak forests and 37% in mixed oak woodlands. Integration of the remote assessment with population estimates of host abundance, obtained from an independent network of 175 field plots (0.05 ha each), indicated similar prevalence of mortality in redwood-tanoak forests (20.0%) and mixed oak woodlands (20.5%) at this time. This is the first study to quantify a realistic number of dead trees impacted by P. ramorum over a defined ecological region. Ecosystem impacts of such widespread mortality will likely be significant.

Evaluation of several commercial biocontrol products on European and North American populations of Phytophthora ramorum

Five commercially available biological control products were tested in vitro with seven isolates of Phytophthora ramorum from North American (NA1, NA2), and European (EU1) populations. The in vitro tests included dual culture methods and detached leaf assays on wounded Rhododendron and Camellia leaves. Variability in response to biocontrol agents among isolates of P. ramorum from North American and European populations was examined. In dual culture tests, both Bacillus subtilis products (Companion® and Serenade®) resulted in better inhibition of the NA1 group than NA2 and EU1. Actinovate® (Streptomyces lydicus) was the least effective of the three bacterial biocontrol agents and there was no difference in percent inhibition among P. ramorum lineages. Two products containing Trichoderma spp. were tested: Plant Helper® (T. atroviride) caused 100% inhibition of all lineages of P. ramorum, while SoilGard? (T. virens) was only about 30% effective. There was great variability among P. ramorum isolates in their response to biocontrol agents. All treatments reduced P. ramorum lesion size on both Rhododendron and Camellia. Combined treatments of Actinovate® with one other BCA did not perform as well as either treatment used individually. Best results were obtained with Serenade® on Rhododendron and Camellia foliage, especially against the NA1 group. Lack of a linear relationship between percent inhibition of P. ramorum by BCAs in vitro and foliar treatments on detached Rhododendron and Camellia leaves indicates that in vitro testing is a poor predictor of BCA performance on plant material.     

The Effect of Exposure to Decreasing Relative Humidity on the Viability of Phytophthora ramorum sporangia

Sporangia of three isolates of Phytophthora ramorum representing three different clonal lineages were subjected to relative humidity (RH) levels between 80 and 100% for exposure periods ranging from 1 to 24 h at 20°C in darkness. Plastic containers (21.5 × 14.5 × 5 cm) were used as humidity chambers with 130 ml of glycerine solution added to each container. Glycerine concentrations corresponded to 100, 95, 90, 85 and 80% RH based on refractive index measurements. Sporangia suspensions were pipeted onto nitrile mesh squares (1.5 × 1.5 cm, 15 micron pore size) which were placed in the humidity chambers and incubated at 20°C in darkness. Following exposure periods of 1, 2, 4, 8, 12 and 24 h, mesh squares were inverted onto Petri dishes of selective medium and sporangia germination assessed after 24 and 48 h. At 100% RH, we observed a mean value of 88% germination after 1 h exposure declining to 18% germination following 24 h incubation. At 95% RH, a steeper decline in germination was noted, with means ranging from 79% at 1 h to less than 1% at 24 h exposure. At 90% RH, no germination was noted after 8 or more h exposure, and values were 57%, 22% and 3% germination for the 1, 2 and 4 h exposures, respectively. Germination was only observed at 1 h exposure for both the 85% RH treatment (52% germination) and the 80% RH treatment (38% germination). The three isolates responded similarly over the range of RH values tested. The germination response of P. ramorum sporangia to RH values between 80% and 100% was comparable to that reported for other Phytophthora species. Knowledge of conditions that affect P. ramorum sporangia germination can shed light on pathogenesis and epidemic potential and lead to improved control recommendations.     

Isolation and characterization of microsatellite markers in Phytophthora ramorum,the causal agent of sudden oak death

We describe specific primers and conditions to amplify two dinucleotide and five trinucleotide microsatellite DNA loci isolated from the oomycete Phytophthora ramorum, the causal agent of sudden oak death. The primer sets were tested on 14–30 isolates from North America and Europe. Seven of 14 loci differentiated between A1 and A2 mating types. All seven loci successfully amplified DNA isolated from infected plant tissue. Four loci may be useful for the diagnosis of P. ramorum because they do not amplify closely related Phytophthora species.     

A comparative study of aluminium and nutrient concentrations in mistletoes on aluminium‐accumulating and non‐accumulating hosts

Mistletoes offer a unique model to study interactions among Al and nutrients in vascular plants, because they grow and reproduce on hosts with distinct Al uptake strategies. We investigated Al distribution and nutrient relations of mistletoes on Al‐accumulating and non‐accumulating hosts. We hypothesised that mistletoes would exhibit similar leaf nutrient and Al concentrations as their host plants, but a strong compartmentalisation of Al when growing on Al‐accumulators. We measured concentrations of N, P, K, Ca, Mg, Cu, Fe, Mn, Zn in leaves and Al in leaves, seeds and branches of Phthirusa ovata and Psittacanthus robustus infecting Miconia albicans, an Al‐accumulator, and Ph. ovata infecting Byrsonima verbascifolia, a non‐Al‐accumulator. High leaf concentrations of Al in Ph. ovata only occurred while parasitizing the Al‐accumulating host; there was no accumulation in branches or seeds. In P. robustus, large concentrations of Al were found in leaves, branches and seeds. Mistletoe seed viability and leaf nutrient concentrations were not affected by Al accumulation. Passive uptake of Al, Ca, Mg, Mn and Cu in mistletoes was evidenced by significant correlations between mistletoes and host leaf concentrations, but not of N, P and K. Al was retranslocated to different plant organs in P. robustus, whereas it was mostly restricted to leaves in Ph. ovata. We suggest that Al might have some specific function in P. robustus, which only parasitizes Al‐accumulator hosts, while the host generalist Ph. ovata can be considered a facultative Al‐accumulator.     

New Insights in the Life Cycle and Epidemics of Phytophthora porri on Leek

White tip, caused by Phytophthora porri, is a devastating disease in the autumn and winter production of leek (Allium porrum) in Europe. This study investigated the disease cycle of P. porri in laboratory and field conditions. Oospores readily germinated in the presence of non‐sterile soil extract at any temperature between 4 and 22°C, with the formation of sporangia which released zoospores. The zoospores survived at least 7 weeks in water at a temperature range of 0 till 24°C. Microscopic examinations revealed that zoospores encysted and germinated on the leek leaf surface and hyphae entered the leaf directly through stomata or by penetrating via appressoria. Oospores were formed in the leaves within 6 days, while sporangia were not produced. By monitoring disease progress in fields with a different cropping history of leek, it could be deduced that P. porri survives in soil for up to 4 years. Disease progress during three consecutive years was correlated with average daily rainfall in the infection period. Disease incidence on leek was reduced when rain splash was excluded by growing the plants in an open hoop greenhouse. Based on these findings, we propose a disease cycle for P. porri in which oospores germinate in puddles, and zoospores reach the leaves by rain splash and survive in water in the leaf axils, from where they infect the plant by direct penetration or via stomata. When conditions become unfavourable, oospores are produced in the leaves which again reach the soil when leaves decay. Secondary spread of the disease by sporangia does not seem to be important.     

A glimpse at future forests: predicting the effects of <Emphasis Type="Italic">Phytophthora ramorum</Emphasis> on oak forests of southern Appalachia

The highly pathogenic Phytophthora ramorum, causal organism of sudden oak death (SOD), is established in forests of the Pacific Northwest (USA) and is threatening invasion of other regions. Given the breadth of its host range, with dozens of asymptomatic ornamental hosts and with oaks, Quercus spp., in the red oak (Erythrobalanus) subgenus particularly susceptible, we investigated the consequences of its invasion and establishment in oak-dominated deciduous forests of the eastern USA. We evaluated the nature and extent of pathogen invasion using vegetation assessments coupled with growth simulations. The woody plant community was assessed in three strata (upper, mid- and lower) and was used to characterize forest composition and structure. Using the Forest Vegetation Simulator (FVS), we then projected woody vegetation growth 50 years into the future with and without the effects of SOD. In forest simulations lacking pathogen invasion, little change in composition or structure is forecasted. Both red oaks and white oaks (subgenus Leucobalanus) increase slightly but significantly over the length of the simulation. In contrast, in SOD-affected forests our projections predict a significant loss of red oaks within 10 years of pathogen invasion. Basal area of white oaks and non-oaks is expected to increase more so in the absence of red oaks. The loss of red oaks to pathogen infection will result in greater increases in red maple, Acer rubrum, and yellow poplar, Liriodendron tulipifera, than in forests free of SOD. Loss of red oak represents a significant loss of hard mast, with potentially devastating consequences for wildlife. Red oak loss will also affect decomposition rates, nutrient cycling, forest structure, and timber values, with consequences for forest health and sustainability.     

Survival of inoculum of the leaf blight fungus Phytophthora colocasiae infecting taro, Colocasia esculenta in the Solomon Islands

Phytophthora colocasiae was successfully isolated by baiting with detergent-treated taro leaf discs 8 cm diameter placed on water slurries of soil, on suspensions of macerated infected leaf lesions or on the washings from petioles of harvested plants. Taro root tips, detached or left on corms, were not susceptible to zoospores of P. colocasiae nor were detached root tips of Lupinus angustifolius. Cubes of taro corm used as baits, and agar selective for Phycomycetes which was inoculated directly with soil, both became too heavily overrun by Phythium splendens to allow detection of P. colocasiae. Investigations indicated that inoculum on lesions of detached leaves and in soil remains viable for only a few days. Petiole bases which comprise the bulk of the ‘tops’ used for vegetative propagation, lost detectable natural inoculum rapidly (2 days) if stored dry, but less rapidly (14 days) if planted immediately in the field. Artifically augmenting surface inoculum with naturally produced sporangia considerably extended the periods of detectability, probably by increasing the chances that a few propagules would survive, especially during dry storage. Incubation of inoculated tops in high humidity led to active infection and sporulation on petioles, especially on cut ends, a situation that might be paralleled under suitable moisture conditions in the field. Of several aroid species tested by artificial inoculation only Alocasia macrorrhiza was susceptible. Natural infection of this plant has not been seen, making it an unlikely alternate host of P. colocasiae under field conditions. Thus perennation between taro crops is effected by shortlived surface propagules and possibly also by mycelium within lesions on petioles. Reduction of the former and prevention of the latter might be achieved by dry storage of tops for 2 to 3 wk.     

Common Factors Drive Disease and Coarse Woody Debris Dynamics in Forests Impacted by Sudden Oak Death

Disease ecology has made important steps in describing how epidemiological processes control the impact of pathogens on populations and communities but fewer field or theoretical studies address disease effects at the ecosystem level. We demonstrate that the same epidemiological mechanisms drive disease intensity and coarse woody debris (CWD) dynamics in natural forest ecosystems impacted by an emerging disease. Sudden oak death (causal agent, Phytophthora ramorum) has caused mortality of tanoak (Notholithocarpus densiflorus) on a spatial scale and rate comparable to other major North American forest diseases caused by invasive pathogens. In pathogen invaded stands, mean CWD masses were 22.4 Mg ha⁻¹ of standing dead tanoak (snags) and 11.5 Mg ha⁻¹ in logs compared to 0.27 and 1.16 Mg ha⁻¹ of snags and logs in an uninvaded stand. Within invaded stands variation in CWD mass and accumulation rates were largely driven by the distribution of pre-disease tanoak biomass and the densities of infected tanoak and California bay laurel (Umbellularia californica) which jointly determine P. ramorum sporulation and disease emergence rates. In a narrow range of community and host characteristics sudden oak death can result in woody debris dynamics similar to discrete disturbances such as fire and forest harvest but it is more common to have lower maximum amounts with slower rates of accumulation than these better studied disturbances. Our results indicate that models of CWD dynamics need to integrate epidemiological processes to predict realistic ecosystem impacts and lead to management applications for forest pathogens.     

Microclimate Impacts Survival and Prevalence of Phytophthora ramorum in Umbellularia californica,a Key Reservoir Host of Sudden Oak Death in Northern California Forests

Phytophthora ramorum, an invasive pathogen and the causal agent of Sudden Oak Death, has become established in mixed-evergreen and redwood forests in coastal northern California. While oak and tanoak mortality is the most visible indication of P. ramorum’s presence, epidemics are largely driven by the presence of bay laurel (Umbellularia californica), a reservoir host that supports both prolific sporulation in the winter wet season and survival during the summer dry season. In order to better understand how over-summer survival of the pathogen contributes to variability in the severity of annual epidemics, we monitored the viability of P. ramorum leaf infections over three years along with coincident microclimate. The proportion of symptomatic bay laurel leaves that contained viable infections decreased during the first summer dry season and remained low for the following two years, likely due to the absence of conducive wet season weather during the study period. Over-summer survival of P. ramorum was positively correlated with high percent canopy cover, less negative bay leaf water potential and few days exceeding 30°C but was not significantly different between mixed-evergreen and redwood forest ecosystems. Decreased summer survival of P. ramorum in exposed locations and during unusually hot summers likely contributes to the observed spatiotemporal heterogeneity of P. ramorum epidemics.     

Decoding the oak genome: public release of sequence data,assembly, annotation and publication strategies

The 1.5 Gbp/2C genome of pedunculate oak (Quercus robur) has been sequenced. A strategy was established for dealing with the challenges imposed by the sequencing of such a large, complex and highly heterozygous genome by a whole‐genome shotgun (WGS) approach, without the use of costly and time‐consuming methods, such as fosmid or BAC clone‐based hierarchical sequencing methods. The sequencing strategy combined short and long reads. Over 49 million reads provided by Roche 454 GS‐FLX technology were assembled into contigs and combined with shorter Illumina sequence reads from paired‐end and mate‐pair libraries of different insert sizes, to build scaffolds. Errors were corrected and gaps filled with Illumina paired‐end reads and contaminants detected, resulting in a total of 17 910 scaffolds (>2 kb) corresponding to 1.34 Gb. Fifty per cent of the assembly was accounted for by 1468 scaffolds (N50 of 260 kb). Initial comparison with the phylogenetically related Prunus persica gene model indicated that genes for 84.6% of the proteins present in peach (mean protein coverage of 90.5%) were present in our assembly. The second and third steps in this project are genome annotation and the assignment of scaffolds to the oak genetic linkage map. In accordance with the Bermuda and Fort Lauderdale agreements and the more recent Toronto Statement, the oak genome data have been released into public sequence repositories in advance of publication. In this presubmission paper, the oak genome consortium describes its principal lines of work and future directions for analyses of the nature, function and evolution of the oak genome.     

Phenology of 16 species of ferns in a subtropical forest of northeastern Taiwan

A knowledge of fern phenology promotes understanding of the biology and ecology of ferns. In this study, the phenology of 16 fern species in a subtropical broadleaf forest (N24°46′, E121°34′) in northeastern Taiwan was monitored from August 1997 to August 2001. Every fern produced both fertile and sterile leaves in each year of the study. Most fertile leaves emerged in February and March, whereas most sterile leaves emerged from May to September. Most leaves reached full expansion during April–July and died during April–August. The average life span of leaves ranged from 4.4 months to 30.3 months. In seven species, fertile leaves lived longer than sterile leaves, but this difference was significant only in Pteris wallichiana. In the other nine species, sterile leaves lived longer than fertile leaves, but the difference was significant only in Cyathea spinulosa, Plagiogyria dunnii, and Plagiogyria adanata. The ephemeral fertile leaves of the two dimorphic species died soon after releasing their spores, at only 5 months of age. However, their sterile leaves survived for over 22 months. The fertile leaves of the other 14 species remained green for almost 2 years after releasing their spores. Sterile leaves remained sterile throughout their lives. Spores matured in May–July and were released in June–August. After spore release, the sporangia detached. No leaf produced a second cohort of sori. Several phenological events, including sterile leaf emergence, leaf expansion and senescence, and spore maturation and release, were significantly positively correlated with temperature but not with precipitation, whereas the emergence of fertile leaves was weakly negatively correlated with temperature and precipitation. However, those correlations varied among different species. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Oak gall wasp infections of Quercus robur leaves lead to profound modifications in foliage photosynthetic and volatile emission characteristics

Oak trees (Quercus) are hosts of diverse gall‐inducing parasites, but the effects of gall formation on the physiology and biochemistry on host oak leaves is poorly understood. The influence of infection by four species from two widespread gall wasp genera, Neuroterus (N. anthracinus and N. albipes) and Cynips (C. divisa and C. quercusfolii), on foliage morphology, chemistry, photosynthetic characteristics, constitutive isoprene, and induced volatile emissions in Q. robur was investigated. Leaf dry mass per unit area (M_A), net assimilation rate per area (A_A), stomatal conductance (g_s), and constitutive isoprene emissions decreased with the severity of infection by all gall wasp species. The reduction in A_A was mainly determined by reduced M_A and to a lower extent by lower content of leaf nitrogen and phosphorus in gall‐infected leaves. The emissions of lipoxygenase pathway volatiles increased strongly with increasing infection severity for all 4 species with the strongest emissions in major vein associated species, N. anthracinus. Monoterpene and sesquiterpene emissions were strongly elicited in N. albipes and Cynips species, but not in N. anthracinus. These results provide valuable information for diagnosing oak infections using ambient air volatile fingerprints and for predicting the impacts of infections on photosynthetic productivity and whole tree performance.