Genetic and environmental factors behind foliar chemistry of the mature mountain birch.

Previous studies of mountain birch (Betula pubescens spp. czerepanovii) repeatedly have found differences between individual trees in herbivory-related traits, but rarely have yielded estimates of the additive genetic variation of these traits or of their relationship to habitat. We used thirty-year-old birch half-sibs in a northern common garden to estimate the effect of genetics and local microhabitat on resistance-related traits. Genetic estimates of foliar chemistry have been studied only rarely with trees as old as these. Moth performance (Epirrita autumnata), rust (Melampsoridium betulinum) incidence levels, and the general level of natural herbivory damage to individual trees were used as direct measures of birch resistance. Chemical resistance-related traits in plant chemistry included 15 individual phenolics, 16 amino acids, and phenoloxidase activities in the foliage. We also followed birch phenology and growth. Our results show that the genotype of the birch was the most important determinant of phenolic composition and phenoloxidase activity, but that amino acid levels were best explained by the microhabitat of the birch. We also found that the phenology of the birch had a high heritability, although its variation was low. Our results reveal rich genetic variation in birch chemistry.

Extensive tree health monitoring networks are useful in revealing the impacts of widespread biotic damage in boreal forests.

We surveyed the regional distribution of conifer defoliation in Finland with an extensive monitoring network during 1995-2006 (EU Forest Focus Level I). The average defoliation in the whole Finland was 10.3% in pine and 19.9% in spruce. The sharp changes were often related to abiotic and biotic factors. The mean age of the stand explained more than one half of the between-plot variance in defoliation. In a variance component analysis, the main effect of years was negligible, while most of the random variation was due to plot main effect and plot x year interaction. About one fifth of the defoliation could be attributed to abiotic or biotic damage, and there were strong local correlations, e.g., between the changes in defoliation and degree of pine sawfly (Diprionidae) damage. There were clear temporal and spatial patterns in the incidence of the most important causes [Scots pine: Scleroderris canker (Gremmeniella abietina), pine shoot beetles (Tomicus sp.), and pine sawflies (Diprion pini, Neodiprion sertifer); Norway spruce: rust fungi (primarily Chrysomyxa ledi)]. Our results suggest that extensive monitoring networks can reveal useful information about the widespread outbreaks of pest organisms (insects and fungi) already in their increase phases, giving some time for management decisions. In a changing climate, large-scale, regular monitoring of tree health, including abiotic and biotic causes, is more important than ever before.

The significance of ectomycorrhizas in chemical quality of silver birch foliage and above-ground insect herbivore performance.

We tested whether the ectomycorrhizal (ECM) infection level of roots of silver birch (Betula pendula) affects performance of above-ground insect herbivores by increasing available plant biomass, by enhancing availability of nutrients, or by modifying concentration of defense compounds, i.e., phenolics, in birch foliage. Insect performance was determined for a phloem-feeding generalist (Lygus rugulipennis, the European tarnished plant bug), a phloem-feeding specialist (Calaphis flava, the birch aphid), and a chewing generalist (Epirrita autumnata, the autumnal moth larva). Silver birch plantlets had either natural ECM infection level (on average 24% of short roots with ECM), reduced ECM infection level with fungicide (F-, 9% ECM), or enhanced ECM infection level after inoculation with the fungus Paxillus involutus (PI+, 45% ECM) or Leccinum versipelle (LV+, 42% ECM). In general, the most pronounced effect of ECM was observed on growth of plantlets, i.e., stem growth decreased. In PI+-treated plants, leaf biomass also decreased. The effect of mycorrhizal colonization on the host plant's nitrogen (N) and phosphorous (P) concentration was dependent on the mycorrhizal species and experiment. Fungicide treatment did not cause a consistent decrease in nutrients. Finally, defense of birch against herbivory, expressed as foliar phenolic concentration in plantlets, was not modified by ECM. However, E. autumnata had a significantly higher relative growth rate on PI+ plantlets with high leaf N concentration than on LV+ plantlets with low leaf N concentration. The birch aphid C. flava produced significantly less nymphs on birches with enhanced ECM infection levels (PI+ and LV+ plantlets) than on controls. In summary, our data show that the ECM infection level mainly affects the growth parameters of plantlets, whereas effects on leaf chemical quality are minor. Our data show that effects of ECM infection of birch roots on aboveground herbivores are multifaceted and depend on the fungal species forming ectomycorrhiza and also on the degree of specialization and feeding guild of insects.

Reduction in size and fecundity of the autumnal moth, Epirrita autumnata, in the increase phase of a population cycle.

Increasing fecundity with increasing density has been observed for many cyclic herbivore populations, including some forest Lepidoptera. We monitored population density, body size and reproductive capacity of the cyclic lepidopteran, the autumnal moth (Epirrita autumnata, Geometridae), from the early increase phase to the devastating outbreak density in northernmost Norway. Larval density of the species increased exponentially from 1998 to 2002 and remained at the outbreak level also in 2003. Within the same period, the body size and fecundity of individuals reduced as analysed from several parallel datasets on larvae, pupae and adults. In another study area in northernmost Finland, the density increase of the autumnal moth was moderate only, and true outbreak density was not attained during the study. Despite that, a reduction was again detected in the size and fecundity of individuals. Possible factors responsible for the reduced size and fecundity of individuals in the Norwegian population were quantitative shortage of foliage, rapid and delayed inducible resistances of the host, mountain birch (Betula pubescens ssp. czerepanovii), as well as crowding-induced responses of larvae. These factors likely acted in concert, although non-delayed responses to the density were emphasized. Our findings did not support the hypotheses of climatic release, inducible susceptibility of the host tree and mast depression (i.e. lowered chemical defence of the host tree after its mast seeding) as promoters of the fecundity-based density increase of the autumnal moth, since the reduced fecundity in relation to increased density was strongly against the predictions of these hypotheses. Therefore, we suggest that the density increase of autumnal moth populations is promoted by high survival rather than exceptionally high fecundity.

Birch family and environmental conditions affect endophytic fungi in leaves.

We investigated whether variation in foliar endophyte frequency among mountain birch trees from different maternal families was due in part to genetic differences among trees. The effect of different environmental conditions on the susceptibility of these mountain birch families to foliar endophytes was tested. The 3-year study was conducted in two tree gardens (altitudinal difference 180 m) with ten families of mountain birch. The frequency of the commonest endophytic fungus in mountain birch leaves, Fusicladium sp., was significantly affected by mountain birch family, with the ranking of families relative to Fusicladium sp. frequency being consistent from environment to environment. Variation in the frequency of Melanconium sp. was difficult to interpret because of significant family × garden × year interaction. Fusicladium sp. and Melanconium sp. endophytes were most frequent in different tree individuals, families and gardens. We conclude that mountain birch trees show heritable variation in their foliar endophyte frequency, and thus one of the conditions necessary for foliar endophytes of mountain birch trees to be able to affect the evolution of their host plant is fulfilled. However, the effect of mountain birch family on the frequency of endophytic fungi varies depending on the endophytic genera in question and partially also on environmental conditions.

Performance of moth larvae on birch in relation to altitude, climate, host quality and parasitoids.

We studied topographical and year-to-year variation in the performance (pupal weights, survival) and larval parasitism of Epirrita autumnata larvae feeding on mountain birch in northernmost Finland in 1993-1996. We found differences in both food plant quality and parasitism between sites ranging from 80 m to 320 m above sea level. Variation in food plant quality had particularly marked effects on larval survival. The advanced phenology of the birches in relation to the start of the larval period reduced pupal weights. Parasitism rates were different between years and between sites. The clearest site differences were in the proportions of different parasitoid species: Eulophus larvarum was most abundant at the lowest-altitude sites, and Cotesia jucunda at the highest. Differences in the performance of E. autumnata were related to temperature conditions: at higher temperatures, survival and the egg production index were lower, and larval parasitism was higher than at lower temperatures. The higher parasitism at higher temperatures was probably due to greater parasitoid activity during warmer days. In the comparison of different sources of spatial and annual variation in the performance of E. autumnata, the most important factor appeared to be egg mortality related to minimum winter temperature, followed by parasitism and, finally, the variation in food plant quality. If, as predicted, the climate gradually warms up, the effects of warmer summers on the outbreaks of E. autumnata suggest a decrease in outbreak intensity.

Wood ants and a geometrid defoliator of birch: predation outweighs beneficial effects through the host plant.

Soil amelioration by a wood-ant species and its consequences for the larval performance of autumnal moths feeding on mountain birch were studied at various distances from the nest mound. Soil nitrate and ammonium nitrogen did not show any clear relationship with distance. However, trees growing in the mound had over 20% more foliar nitrogen than more distant trees. When moth larvae were experimentally protected from predation, their survival rate and final weight tended to decrease with increasing distance. In a laboratory experiment with detached leaves, the relative growth rate of larvae was roughly 30% higher on leaves from trees located on the mound. Differences in larval performance refute the Plant Stress Hypothesis proposed by T.C.R. White and support P.W. Price's Plant Vigor Hypothesis. Predation by ants was examined along the same gradient in trees with and without a glue band that excluded ants from the canopy. Reduction in the daily survival rate of larvae attributable to ant predation was about 35% in trees growing in the mound and around 5% at a distance of 20 m. Other things being equal, about 25 times more larvae entering the penultimate instar would achieve the pupal stage outside the wood-ant territory than in the vicinity of the mound. While both the fertilizing and predatory influence of wood ants is clear, the domain of predation is much larger than the area where trees and their herbivores can exploit enhanced nutrient levels in and around ant mounds. The existence of undamaged green islands around ant mounds in otherwise totally defoliated mountain-birch forests cannot be explained by soil amelioration by wood ants but rather by their predatory activity.

Decrease in feeding niche breadth of Melasoma lapponica (Coleoptera: Chrysomelidae) with increase in pollution.

We studied host-plant preference and performance of the leaf beetle, Melasoma lapponica, around Severonikel smelter situated in Monchegorsk, Russia. The breadth of feeding niche (Smith's measure) based on both field counts and preference tests decreased with an increase of ambient SO2 concentration, but showed no relationship with either metal pollutants or beetle population densities. In heavily polluted plots (mean annual SO2 concentrations 400-1000 µg/m3) the beetles concentrated on Salix borealis, Whereas in moderately and slightly polluted plots they used other willow species as well. No difference in survival was revealed between M. lapponica fed with leaves of S. borealis from heavily and sloghtly polluted plots. However, performance of larvae fed with Salix caprea and S. Phylicifolia was significantly lower when leaves were collected from heavily polluted plots. In these plots beetles clearly preferred S. borealis, the only species assuring high survival of M. lapponica under strong pollution impact. Decrease in preference of two less favourable hosts, S. caprea and S. phylicifolia, with increase in pollution can therefore be considered as an adaptive response of M. lapponica to pollution-induced changes in host-plant quality.

The host-pathogen system of Gremmeniella abietina (Lagerb.) Morelet and Scots pine; effects of non-pathogenic phyllosphere fungi, acid rain and environmental factors.

Scots pine seedlings (1-yr-old) were inoculated either once, or three times, with the conidia of two saprophytic Honmmema species. After these inoculations, the seedlings were inoculated later with conidia of the pathogenic fungus Gremmeniella abietina (Lagerb.) Morelet. Seedlings received irrigation with simulated acid rain at pH 3, with water of pH 6. or no irrigation, during and after the inoculation treatments, The severity of the symptoms caused by G. abietina, and rhe isolation frequency of endophytic (symptomless) G. abietina and the saprophytes, were measured 11 months after G. abietina inoculation. The isolation frequencies of the two Hormunema species increased significantly in the seedlings inoculated three times with saprophyte conidia. Irrigation treatments did not affect the saprophytes. The disease symptoms caused by G, abietina were positively correlated with tree density. Symptomless G, abietina was isolated most often from the seedlings that had received irrigation at pH b. The isolation frequency was lowest in seedlings with acidic irrigation. The seedlings inoculated three times with conidia of Hormonema sp. 1 had a lower frequency of G. abietina isolations than other seedlings, but the difference was not statistically significant.

Long-term inducible resistance in birch foliage: triggering cues and efficacy on a defoliator.

Heavy damage of the mountain birch foliage, as well as application of small amounts of insect frass to the soil beneath the trees, reduced growth of Epirrita autumnata larvae reared in these trees in the following year. Foliage damage in the previous year decreased larval survival, too. Both foliage damage and insect frass in the soil decreased a fecundity index which combined the effects of size and survival. Because application of small amounts of fertilizers had an effect indistinguishable from that of insect frass, the effect of the frass may base on responses of trees to an increase in soil nutrient concentration in mid-summer. In previously untreated control trees, all performance indices (growth, survival, and egg production) of Epirrita correlated positively with the distance of the birch from the closest birch defoliated in the previous year, indicating "communication" between adjacent trees. Epirrita egg production in trees that had been both defoliated and treated with frass in the previous summer was at least 70% lower than in previously unmanipulated control trees.

Nutrient stress: an explanation for plant anti-herbivore responses to defoliation.

A hypothesis is put forward that the long-lasting inducible responses of trees to herbivores, particularly lepidopteran defoliators, may not be active defensive responses, but a by-product of mechanisms which rearrange the plant carbon/nutrient balance in response to nutrient stress caused by defoliation. When defoliation removes the foliage nutrients of trees growing in nutrient-poor soils, it increases nutrient stress wich in turn results in a high production of carbon-based allelochemicals. The excess of carbon that cannot be diverted to growth due to nutrient stress is diverted to the production of plant secondary metabolites. The level of carbon-based secondary substances decays gradually depending on the rate at which nutrient stress is relaxed after defoliation. In nutrient-poor soils and in plant species with slow compensatory nutrient uptake rates the responses induced by defoliation can have relaxation times of several years. The changes in leaf nitrogen and phenolic content of mountain birch support this nutrient stress hypothesis. Defoliation reduces leaf nitrogen content while phenolic content increases. These responses of mountain birch to defoliation are relaxed within 3-4 years.

Species richness of Macrolepidoptera on Finnish deciduous trees and shrubs.

Species richness of Macrolepidoptera on Finnish trees and shrubs was analysed by means of stepwise regression analysis. The explaining variables were plant frequency, geographical range, plant height, number of relatives and leaf size.Total frequency of the host plant, which correlated strongly with range, explained 57% of the observed variance of lepidopteran species richness on deciduous trees and shrubs. Height of plant and number of relatives explained significantly the residual variation and altogether these three variables explained 71% of the variance of species richness.Analyses at the plant genus level gave similar results and frequency, height and number of relatives explained 78% of the variance of species richness of Macrolepidoptera on deciduous plant genera.When conifers were included in the analysis leaf size also becomes a significant variable. Leaf size can, however, act as a dummy variable which effectively distinguishes conifers from deciduous trees.The validity of different models explaining herbivore species richness on plants is discussed. The results of this study favoured more than earlier studies the importance of relatedness of host plants as a factor which determines the species richness of herbivores.