Phloemophagous and xylophagous insects, their parasitoids, predators and inquilines in the branches of the most important oak species in Serbia

Altogether 26 species of phloemophagous and xylophagous insects, 47 species of parasitoids, 14 species of predators and 7 species of inquilines were identified on the branches of Quercus cerris, Q. frainetto, Q. petraea and Q. robur, diameter 3–15 cm, at 24 sites in Serbia over the period 1992–1996. The greatest number of the identified species were taken from Q. petraea branches (66), followed by Q. cerris (49), Q. frainetto (48) and Q. robur (43). Among the identified phloemophagous and xylophagous insects, the most frequent and the most abundant species were Scolytus intricatus, Agrilus angustulus and Xylotrechus antilope. The most frequent and the most abundant parasitoid was Ecphylus silesiacus. In some samples, the species Entedon ergias, Cheiropachus quadrum and Dendrosoter protuberans were also among the more abundant parasitoids. The most significant predator was the species Tilloidea unifasciata, and the most significant inquilines were the species Poecilothrips albopictus and Asynapta pectoralis.     

Morphological and physiological reactions of young deciduous trees (Quercus robur L., Q. petraea [Matt.] Liebl., Fagus sylvatica L.) to waterlogging

One-year-old seedlings of Quercus robur L., Q. petraea (Matt.) Liebl. and Fagus sylvatica L. were cultivated in lysimeters and subjected to waterlogging for 17 weeks, interrupted by a five-week drainage period during summer. The growth of Q. robur was less affected by waterlogging than that of Q. petraea and Fagus. Waterlogging resulted in the formation of adventitious roots in Q. robur and Q. petraea, but not in Fagus. In contrast to Fagus, Q. robur and, to a lesser extent, Q. petraea were able to generate roots even below the water table. The hydraulic conductance of the excised root systems, the stomatal conductance and, in Fagus, the leaf water potential and the leaf-mass related hydraulic conductance were decreased by waterlogging. The decrease in the hydraulic conductance was largest in Fagus, and smallest in Q. robur. The roots of Fagus responded to anaerobic conditions with an increase in ethanol concentration. The measurements of nitrate reductase activities in roots and leaves provided no indications of a persistent contribution of NO₃ ⁻ metabolism to the alleviation of waterlogging-induced stress. It is concluded that Q. robur and, to a lesser extent, Q. petraea can tolerate waterlogging periods better than Fagus due to a different pattern of root formation, and to a better adjustment of leaf biomass production to the hydraulic conductivity of the root system. This revised version was published online in June 2006 with corrections to the Cover Date.     

Insights into drought adaptation of two European oak species revealed by nucleotide diversity of candidate genes

Nucleotide diversity, correlations to environmental conditions, and deviations from standard neutral models were examined in eight candidate genes for drought response of European oaks Quercus petraea and Quercus robur. Baseline genetic parameters were calculated and deviation from neutrality was tested using Tajima’s D, and Fu and Li’s D and F statistics. Population structure was investigated using differentiation indices and Bayesian clustering. Similar values of total nucleotide diversity were found in both species with significant higher diversity at non-synonymous sites in Q. robur while the number of haplotypes was significantly higher in Q. petraea. Significant population differentiation was found for three genes in Q. petraea and for one gene in Q. robur. Within four genes, strong correlations were found between the local temperature–precipitation regime and the allele frequencies of six alleles, of which three were private to Q. petraea. Using various population genetic and Bayesian tests for neutrality, four outlier single nucleotide polymorphisms (SNPs) under putative selection were detected in two of the analyzed genes. Significant differentiation and strong allelic correlation to environmental conditions support preceding gene expression profiling experiments, where functional impact of candidate genes in drought response has been revealed. Q. petraea populations were found to be more differentiated as compared to Q. robur—this could be linked to the higher adaptive potential of this species under arid conditions.     

Flooding effects on starch partitioning during early growth of two oak species

Pedunculate (Quercus robur L.) and sessile (Q. petraea [Matt.] Liebl.) oaks are the most common oak species in Western Europe. They are known to display different ecological requirements, particularly relative to root hypoxia induced by flooding: In a glasshouse study of seedlings, we quantified the effects of flooding on starch mobilization from cotyledons and starch partitioning. Growth and distribution of lateral roots were also measured. The above-ground growth of Q. robur was less affected by flooding than that of Q. petraea which failed to develop a second flush. Root growth was also severely inhibited, particularly in Q. petraea. In Q. robur, lateral root initiation as well as elongation was restricted to the soil surface layer. Flooding markedly reduced total growth and concentrations of in all components except stems. Starch mobilization from cotyledons was delayed by flooding, especially in Q. robur seedlings. Under flooding, the decrease of cotyledons dry mass and starch content in Q. robur was lower than in Q. petraea, whereas Q. robur displayed larger growth than Q. petraea. The features of carbohydrate management may be crucial in the observed differences in flooding tolerance of these species.     

Regeneration of oaks (Quercus robur/Q. petraea) and three other tree species during long-term succession after catastrophic disturbance (windthrow)

In broadleaved temperate forests in Europe, oak (Quercus robur/Q. petraea) regeneration is reported to be weak or absent. However, most work concern seedlings or saplings, studied relatively few years. We studied a Picea abies stand in Sweden, windthrown and logged (all stems harvested) in 1969, testing the hypothesis that oaks regenerate in the long term among competing tree species after catastrophic disturbance. In 2011, after 40 years/growth seasons, we recorded live and dead trees in the new stand and investigated the surroundings, competition, and succession. The following trees, up to 26 m tall, colonized: Sorbus aucuparia, Betula pendula/B. pubescens, Fagus sylvatica, Q. robur/Q. petraea, and Corylus avellana (a shrub). Betula dominated, and only Fagus was regenerating in 2011. Sorbus had produced most of the dead trees, mainly or partly through intraspecific competition. In the stand, compared to the surroundings, Quercus, Picea, and Alnus glutinosa were under-represented, and Sorbus, Betula, and Fagus were over-represented. Yet, the density of Quercus was far from negligible; 48 large trees/ha. Most of the oaks (74 %) were co-dominant trees and many grew near Sorbus. Thus, oaks can survive and grow fast among pioneer trees and browsing animals, a conclusion which is supported by the literature (nine studies identified). High mortality of Sorbus is part of a long-term succession, where Fagus might come to dominate. However, Quercus likely will persist, in low density. We propose three key traits contributing to long-term persistence of Q. robur/Q. petraea in European temperate forests: long life span, ecological plasticity, and resistance to disturbances.     

Differential response of two Central-European oak species to single and combined stress factors

We studied the effects of repeated defoliation and drought, which are considered to be most effective in triggering oak decline, on the Central-European oak species Quercus robur L. and Quercus petraea [Matt.] Liebl. Three-year-old saplings were subjected to artificial defoliation in two consecutive years and to drought stress, applied singly or in combination. Differences in the morphological, anatomical and physiological responses to these stress factors among treatments and between species were tested in a 3-year experiment. Drought stress lowered the pre-dawn and the afternoon leaf-water potentials in both species, irrespective of additional defoliation. The relative water content of the leaves was unaffected by drought stress; but, in Q. robur, it decreased in trees subjected to defoliation and to the combination of drought stress and defoliation. When repeated defoliation and drought stress were applied within the same growing season, the leaf-to-air difference in the partial pressure of water vapour (w) explained most of the variation in the daily integral of the stomatal conductance to water vapour (g _{s day sum}) in Q. petraea; however, in Q. robur, the hydraulic conductance of the twigs was the most powerful predictor variable. In the same year, the actual hydraulic conductance was correlated with g _{s day sum} in Q. robur, but not in Q. petraea. The studied parameters of gas exchange and biomass production revealed that Q. robur recovered more rapidly from stress than did Q. petraea. We hypothesize that this is due to Q. roburs lower responsiveness to the environmental variable w and its higher responsiveness to internal hydraulic conductance compared to Q. petraea. This revised version was published online in May 2005 with corrections to Table 4.     

Hybridisation and colonisation dynamics in European oaks

Summary

Extensive hybridisation between the two sympatric species Quercus petraea and Q.robur is suggested by the near lack of genetic differentiation between the two species and supported by controlled crosses and mating system analysis in mixed stands. Further ecological and genetic evidence suggest that hybridisation does not impede the ecological specialisation of the two species, raising the issue of its evolutionary significance in oaks. Preferential unidirectional hybridization (pollen Q. petraea to ovule Q. robur) has been shown in various mixed stands and facilitates the introduction of sessile oak in existing pedunculate stands. If this unidirectional trend is reinforced in later backcrosses, then hybridisation leads to the dispersal of Q. petraea in existing stands of Q. robur. Hybridisation can therefore be seen as a ‘pollen-mediated’ dispersal mechanism, and has most likely contributed to the rapid migration of Q. petraea in Europe. Given the extant distribution of the species in Europe, migration through pollen swamping should be seen at the edges of the natural distribution of Q. petraea where the demographic imbalance of the two species will reinforce backcrosses.     

Distinct male reproductive strategies in two closely related oak species

Reproductive strategies of closely related species distributed along successional gradients should differ as a consequence of the trade‐off between competition and colonization abilities. We compared male reproductive strategies of Quercus robur and Q. petraea, two partly interfertile European oak species with different successional status. In the studied even‐aged stand, trees of the late‐successional species (Q. petraea) grew faster and suffered less from intertree competition than trees of the early‐successional species (Q. robur). A large‐scale paternity study and a spatially explicit individual‐based mating model were used to estimate parameters of pollen production and dispersal as well as sexual barriers between species. Male fecundity was found to be dependent both on a tree's circumference and on its environment, particularly so for Q. petraea. Pollen dispersal was greater and more isotropic in Q. robur than in Q. petraea. Premating barriers to hybridization were strong in both species, but more so in Q. petraea than in Q. robur. Hence, predictions based on the competition–colonization trade‐off are well supported, whereas the sexual barriers themselves seem to be shaped by colonization dynamics.     

Ectomycorrhizal fungal communities of pedunculate and sessile oak seedlings from bare-root forest nurseries

In this study, we present the detailed molecular investigation of the ectomycorrhizal (ECM) community of Quercus petraea and Quercus robur seedlings grown in bare-root forest nurseries. In all tested oak samples, mycorrhizal colonization was nearly 100%. Morphological observation and molecular investigations (sequencing of fungal ITS rDNA) revealed a total of 23 mycorrhizal taxa. The most frequent and abundant fungal taxa were Hebeloma sacchariolens, Tuber sp., and Peziza sp.; from the detected fungal taxa, 20 were noted for Q. petraea and 23 for Q. robur. Depending on the nursery, the species richness of identified ECM fungal taxa for both oak species ranged from six to 11 taxa. The mean species richness for all nurseries was 5.36 and 5.82 taxa per Q. petraea and Q. robur sample, respectively. According to the analysis of similarity, ECM fungal communities were similar for Q. petraea and Q. robur (R = 0.019; p = 0.151). On the other hand, detected fungal communities were significantly different between nurseries (R = 0.927; p < 0.0001). Using the Spearman rank correlation, it was determined that the ectomycorrhizal diversity (in terms of richness, the Shannon diversity, evenness, and Simpson dominance indices) is significantly related to the soil parameters of each nursery. We conclude that individual nursery may be considered as separate ecological niches that strongly discriminate diversity of ECM fungi.     

Geometric morphometric analyses of leaf variation in four oak species of the subgenus Quercus (Fagaceae)

Abstract

This paper defines a protocol for the study of leaf morphology and morphometric relationships among Quercus frainetto, Quercus robur, Quercus petraea and Quercus pubescens. Leaf shapes were investigated in an attempt to characterize and discriminate among these four species. Landmark and outline data were compared in order to ascertain their relative efficacy for describing variation in leaf morphology. MANOVA was performed to assess intra‐specific differentiation and to compare the distribution of variance in individuals, populations and species. A strong correlation was found between landmark and outline datasets of the four species: both methods proved capable of discriminating among the four species. Finally, a Two‐Block Partial Least‐Squares analysis was performed for each species in order to assess the correlation between intra‐specific shape variation and environmental factors.     

Deciduous and semi-deciduous oak forests (<Emphasis Type="Italic">Quercus robur,Q. petraea</Emphasis> and <Emphasis Type="Italic">Q. pyrenaica</Emphasis>) floristic composition in the Northwest Iberian Peninsula

Oak forests in the Northwest Iberian Peninsula represent climax communities with a high floristic diversity of vascular plants. This study presents data from 189 botanical samples randomly collected in stands of deciduous and semi-deciduous oak as Quercus robur (98), Q. petraea (50) and Q. pyrenaica (41). Within these stands, 187 species or subspecies were identified, in addition to 20 genera and 68 families, all of them present in forests of Quercus robur. A total of 126 species occur in more than five relevés. The largest number of species corresponds to Poaceae (22), Fabaceae (19) and Rosaceae (14). The biological spectrum is dominated by hemicryptophytes, with mainly Atlantic and Sub-Atlantic floristic elements. The distribution of the stands has been studied by using Two-Way Indicator Species Analysis, obtaining like pseudo-species, with shrubby and arborea form, the following ones: Fagus sylvatica, Castanea sativa, Sorbus aucuparia, Corylus avellana, Crataegus monogyna, Pyrus cordata, Erica arborea, Frangula alnus and Cytisus scoparius.     

A set of primers for the amplification of chloroplast microsatellites in Quercus

The increase in demand for the certification of oak seed lots, as well as control of the geographical origin of oak wood, has led us to develop powerful genetic markers permitting us to discriminate among provenance regions. With the aim of detecting new chloroplast variants, we have identified 17 potential cpSSRs motifs from available oak sequences and tested their variability among French oak populations. Six loci were polymorphic at the intraspecific level in Quercus petraea and Q. robur. Moreover, conservation of the primer pairs was checked on a set of 21 forest tree species and they were all shown to work well on several Quercus species, and even within Fagacaea.     

Evidence for hybridization and introgression within a species-rich oak (<Emphasis Type="Italic">Quercus</Emphasis> spp.) community

Background  

Analysis of interspecific gene flow is crucial for the understanding of speciation processes and maintenance of species integrity. Oaks (genus Quercus, Fagaceae) are among the model species for the study of hybridization. Natural co-occurrence of four closely related oak species is a very rare case in the temperate forests of Europe. We used both morphological characters and genetic markers to characterize hybridization in a natural community situated in west-central Romania and which consists of Quercus robur, Q. petraea, Q. pubescen s, and Q. frainetto, respectively.     

Strength and variability of postmating reproductive isolating barriers between four European white oak species

The identification and quantification of the relative importance of reproductive isolating barriers is of fundamental importance to understand species maintenance in the face of interspecific gene flow between hybridising species. Yet, such assessments require extensive experimental fertilisations that are particularly difficult when dealing with more than two hybridising and long-generation-time species such as oaks. Here, we quantify the relative contribution of four postmating reproductive isolating barriers consisting of two prezygotic barriers (gametic incompatibility, conspecific pollen precedence) and two postzygotic barriers (germination rate, early survival) from extensively controlled pollinations between four oak species (Quercus robur, Quercus petraea, Quercus pubescens and Quercus pyrenaica) that have been shown to frequently hybridise in natural populations. We found high variation in the strength of total reproductive isolation between species, ranging from total reproductive isolation to advantage toward hybrid formation. As previously found, Q. robur pollen was unable to fertilise Q. petraea due to a strong reproductive isolating mechanism. On the contrary, Q. pubescens pollen was more efficient at fertilising Q. petraea than conspecific pollen. Overall, prezygotic barriers contribute far more than postzygotic barriers to isolate species reproductively, suggesting a role for reinforcement in the development of prezygotic barriers. Conspecific pollen precedence reduced hybrid formation when pollen competition was allowed; however, presence of conspecific pollen did not totally prevent hybridization. Our results suggest that pollen competition depends on multiple ecological and environmental parameters, including species local abundance, and that it may be of uppermost importance to understand interspecific gene flow among natural multispecies populations.     

Outlier loci highlight the direction of introgression in oaks

Loci considered to be under selection are generally avoided in attempts to infer past demographic processes as they do not fit neutral model assumptions. However, opportunities to better reconstruct some aspects of past demography might thus be missed. Here we examined genetic differentiation between two sympatric European oak species with contrasting ecological dynamics (Quercus robur and Quercus petraea) with both outlier (i.e. loci possibly affected by divergent selection between species or by hitchhiking effects with genomic regions under selection) and nonoutlier loci. We sampled 855 individuals in six mixed forests in France and genotyped them with a set of 262 SNPs enriched with markers showing high interspecific differentiation, resulting in accurate species delimitation. We identified between 13 and 74 interspecific outlier loci, depending on the coalescent simulation models and parameters used. Greater genetic diversity was predicted in Q. petraea (a late‐successional species) than in Q. robur (an early successional species) as introgression should theoretically occur predominantly from the resident species to the invading species. Remarkably, this prediction was verified with outlier loci but not with nonoutlier loci. We suggest that the lower effective interspecific gene flow at loci showing high interspecific divergence has better preserved the signal of past asymmetric introgression towards Q. petraea caused by the species' contrasting dynamics. Using markers under selection to reconstruct past demographic processes could therefore have broader potential than generally recognized.     

Development and Characterization of Genomic and Gene-Based Microsatellite Markers in North American Red Oak Species

Oaks (Quercus: Fagaceae) are ecological and economic keystones of many forested ecosystems but effective genetic management strategies are hindered by high levels of phenotypic plasticity within species and frequent hybridization among them. These same features, however, make oak communities suited for the study of speciation, hybridization, and genetic adaptation. Efforts to develop new and to adapt existing genomic resources to less-studied members of this genus should not only improve oak conservation and management but also aid the study of fundamental evolutionary processes. Here, we present a suite of 27 highly polymorphic simple sequence repeat (SSR) markers tested in four North American red oak (Quercus section Lobatae) species: Q. rubra, Q. ellipsoidalis, Q. coccinea, and Q. velutina. Five markers are genomic SSRs (gSSRs) — four novel and one previously transferred from Q. petraea — and 22 are gene-based SSRs derived from Q. robur and Q. petraea expressed sequence tags (EST-SSRs). Overall, levels of polymorphism detected with these primer pairs were high, with gene diversity (H _e) averaging 0.66 across all loci in natural populations. In addition, we show that EST-SSR markers may have the potential to detect divergent selection at stress-resistance candidate genes among closely related oak species.     

Genetic evidence of reproductive isolation in a remote enclave of Quercus pubescens in the presence of cross-fertile species

Peripheral populations may be crucial for understanding processes underlying adaptive genetic variation. Their evolution and ecology are driven by various genetic and demographic processes, such as selection, gene flow and bottleneck. Peripheral populations often experience a reduction in density resulting in the Allee effect. The presence of interfertile species increases the opportunity for hybridisation, which allows for a rescue from the Allee effect, but at the risk of genetic extinction through introgression. In this article we investigated a peripheral population of Quercus pubescens, a European tree species. The study population is located in Poland, several hundred kilometres northwards from the main species range. Due to geographic separation, the study population exists under strong pressure of introgression from potentially inter-fertile Q. petraea and Q. robur, which are the only common oaks in Poland. The intermediate morphology between typical Q. pubescens and a common oak species found in the study population supports the introgression hypothesis, which could be in line with the earlier studies of this species complex conducted in the main range of Q. pubescens. Alternatively, the intermediate morphology could reflect the founder effect or selection at an ecological extreme. We attempted to verify these hypotheses using microsatellites and a reference of common oak species. The results showed that the study population is genetically distinct from both Q. petraea and Q. robur. Additionally, the population is characterised by a low effective population size and limited gene dispersal. This suggests that the study population reveals strong reproductive isolation from common species, implying alternative sources of atypical morphology.     

Conservation of Nuclear SSR Loci Reveals High Affinity of <Emphasis Type="Italic">Quercus infectoria</Emphasis> ssp. <Emphasis Type="Italic">veneris</Emphasis> A. Kern (Fagaceae) to Section <Emphasis Type="Italic">Robur</Emphasis>

Conservation of 16 nuclear microsatellite loci, originally developed for Quercus macrocarpa (section Albae), Q. petraea, Q. robur (section Robur), and Q. myrsinifolia, (subgenus Cyclobalanopsis) was tested in a Q. infectoria ssp. veneris population from Cyprus. All loci could be amplified successfully and displayed allele size and diversity patterns that match those of oak species belonging to the section Robur. At least in one case, limited amplification and high levels of homozygosity support the occurrence of “null alleles” caused by a possible mutation in the highly conserved primer areas, thus hindering PCR. The sampled population exhibited high levels of diversity despite the very limited distribution of this species in Cyprus and extended population fragmentation. Allele sizes of Q. infectoria at locus QpZAG9 partially match those of Q. alnifolia and Q. coccifera from neighboring populations. However, sequencing showed homoplasy, excluding a case of interspecific introgression with the latter, phylogenetically remote species. Q. infectoria ssp. veneris sequences at this locus were concordant to those of other species of section Robur, while sequences of Quercus alnifolia and Quercus coccifera were almost identical to Q. cerris.     

Seeing the forest through the trees: comprehensive inference on individual mating patterns in a mixed stand of Quercus robur and Q. petraea

Background and Aims

Sexual reproduction is one of the most important moments in a life cycle, determining the genetic composition of individual offspring. Controlled pollination experiments often show high variation in the mating system at the individual level, suggesting a persistence of individual variation in natural populations. Individual variation in mating patterns may have significant adaptive implications for a population and for the entire species. Nevertheless, field data rarely address individual differences in mating patterns, focusing rather on averages. This study aimed to quantify individual variation in the different components of mating patterns.

Methods

Microsatellite data were used from 421 adult trees and 1911 seeds, structured in 72 half-sib families collected in a single mixed stand of Quercus robur and Q. petraea in northern Poland. Using a Bayesian approach, mating patterns were investigated, taking into account pollen dispersal, male fecundity, possible hybridization and heterogeneity in immigrant pollen pools.

Key Results

Pollen dispersal followed a heavy-tailed distribution (283 m on average). In spite of high pollen mobility, immigrant pollen pools showed strong genetic structuring among mothers. At the individual level, immigrant pollen pools showed highly variable divergence rates, revealing that sources of immigrant pollen can vary greatly among particular trees. Within the stand, the distribution of male fecundity appeared highly skewed, with a small number of dominant males, resulting in a ratio of census to effective density of pollen donors of 5·3. Male fecundity was not correlated with tree diameter but showed strong cline-like spatial variation. This pattern can be attributed to environmental variation. Quercus petraea revealed a greater preference (74 %) towards intraspecific mating than Q. robur (36 %), although mating preferences varied among trees.

Conclusions

Mating patterns can reveal great variation among individuals, even within a single even-age stand. The results show that trees can mate assortatively, with little respect for spatial proximity. Such selective mating may be a result of variable combining compatibility among trees due to genetic and/or environmental factors.     

Population differentiation of sessile oak at the altitudinal front of migration in the French Pyrenees

To assess the effects of altitude on the level and structure of genetic diversity, a genetic survey was conducted in 12 populations of sessile oak (Quercus petraea) located between 130 and 1660 m in two parallel valleys on the northern side of the Pyrenees Mountains. Genetic diversity was monitored at 16 nuclear microsatellite loci and 5 chloroplast DNA (cpDNA) markers. The cpDNA survey suggested that extant populations in both valleys shared the same source populations from the plain. There was no visible trend of nuclear genetic diversity along altitude, even if indirect estimates of effective population sizes revealed a consistent reduction at higher altitudes. Population differentiation, although low, was mostly present among populations of the same valleys and reached similar levels than differentiation across the range of distribution of sessile oak. Contribution to the overall differentiation in the valleys was mostly due to the genetic divergence of the highest populations and the altitudinal variation of allelic frequencies at a few loci. Bayesian inference of migration between groups of populations showed that gene flow is preferentially unidirectional from lower altitudes in one valley to other groups of populations. Finally, we found evidence of clonal reproduction in high altitude populations. The introgression of Quercus robur and Quercus pubescens was also more frequent at the altitudinal margin suggesting that this mechanism may have contributed to the present migration and adaptation of Q. petraea and may also facilitate its future upslope shift in the context of climate change.