Vitali Zverev

Mountain birch under multiple stressors – heavy metal‐resistant populations co‐resistant to biotic stress but maladapted to abiotic stress

Stress adaptations often include a trade‐off of weakened performance in nonlocal conditions, resulting in divergent selection, and potentially, genetic differentiation and evolutionary adaptation. Results of a two‐phase (greenhouse and field) common garden experiment demonstrated adaptation of mountain birch (Betula pubescens subsp. czerepanovii) populations from industrially polluted areas of the Kola Peninsula, north‐western Russia, to heavy metals (HM), whereas no adaptations to wind or drought stress were detected in populations from wind‐exposed sites. HM‐adapted seedlings were maladapted to drought but less palatable (co‐resistant) to insect herbivores, even under background HM concentrations. The absence of adaptations to harsh microclimate and the generally high adaptive potential of mountain birch, a critical forest forming tree in subarctic Europe, need to be accounted for in models predicting consequences of human‐driven environmental changes, including the projected climate change.

Factors affecting population dynamics of leaf beetles in a subarctic region: The interplay between climate warming and pollution decline

Understanding the mechanisms by which abiotic drivers, such as climate and pollution, influence population dynamics of animals is important for our ability to predict the population trajectories of individual species under different global change scenarios. We monitored four leaf beetle species (Coleoptera: Chrysomelidae) feeding on willows (Salix spp.) in 13 sites along a pollution gradient in subarctic forests of north-western Russia from 1993 to 2014. During a subset of years, we also measured the impacts of natural enemies and host plant quality on the performance of one of these species, Chrysomela lapponica. Spring and fall temperatures increased by 2.5-3°C during the 21-year observation period, while emissions of sulfur dioxide and heavy metals from the nickel-copper smelter at Monchegorsk decreased fivefold. However, contrary to predictions of increasing herbivory with climate warming, and in spite of discovered increase in host plant quality with increase in temperatures, none of the beetle species became more abundant during the past 20years. No directional trends were observed in densities of either Phratora vitellinae or Plagiodera versicolora, whereas densities of both C. lapponica and Gonioctena pallida showed a simultaneous rapid 20-fold decline in the early 2000s, remaining at very low levels thereafter. Time series analysis and model selection indicated that these abrupt population declines were associated with decreases in aerial emissions from the smelter. Observed declines in the population densities of C. lapponica can be explained by increases in mortality from natural enemies due to the combined action of climate warming and declining pollution. This pattern suggests that at least in some tri-trophic systems, top-down factors override bottom-up effects and govern the impacts of environmental changes on insect herbivores.

Confirmation bias leads to overestimation of losses of woody plant foliage to insect herbivores in tropical regions

Confirmation bias, i.e., the tendency of humans to seek out evidence in a manner that confirms their hypotheses, is almost overlooked in ecological studies. For decades, insect herbivory was commonly accepted to be highest in tropical regions. By comparing the data collected blindly (when the observer was not aware of the research hypothesis being tested) with the results of non-blind studies (when the observer knew what results could be expected), we tested the hypothesis that the records made in the tropics could have overestimated community-wide losses of plant foliage to insects due to the confirmation bias. The average loss of leaf area of woody plants to defoliating insects in Brazil, when measured by a blind method (1.11%), was significantly lower than the loss measured in non-blind studies, both original (5.14%) and published (6.37%). We attribute the overestimation of the community-wide losses of plant foliage to insects in non-blind studies to the unconsciously preconceived selection of study species with higher-than-average levels of herbivory. Based on our findings, we urge for caution in obtaining community-wide characteristics from the results of multiple single-species studies. Our data suggest that we may need to revise the paradigm of the highest level of background insect herbivory in the tropical regions. More generally, we argue that more attention should be paid by ecologists to the problem of biases occurring at the pre-publication phases of the scientific research and, consequently, to the development and the wide application of methods that avoid biases occurring due to unconscious psychological processes.

Consequences of long-term severe industrial pollution for aboveground carbon and nitrogen pools in northern taiga forests at local and regional scales

Boreal coniferous forests act as an important sink for atmospheric carbon dioxide. The overall tree carbon (C) sink in the forests of Europe has increased during the past decades, especially due to management and elevated nitrogen (N) deposition; however, industrial atmospheric pollution, primarily sulphur dioxide and heavy metals, still negatively affect forest biomass production at different spatial scales. We report local and regional changes in forest aboveground biomass, C and N concentrations in plant tissues, and C and N pools caused by long-term atmospheric emissions from a large point source, the nickel-copper smelter in Monchegorsk, in north-western Russia. An increase in pollution load (assessed as Cu concentration in forest litter) caused C to increase in foliage but C remained unchanged in wood, while N decreased in foliage and increased in wood, demonstrating strong effects of pollution on resource translocation between green and woody tissues. The aboveground C and N pools were primarily governed by plant biomass, which strongly decreased with an increase in pollution load. In our study sites (located 1.6-39.7 km from the smelter) living aboveground plant biomass was 76 to 4888 gm(-2), and C and N pools ranged 35-2333 g C m(-2) and 0.5-35.1 g N m(-2), respectively. We estimate that the aboveground plant biomass is reduced due to chronic exposure to industrial air pollution over an area of about 107,200 km2, and the total (aboveground and belowground) loss of phytomass C stock amounts to 4.24×10(13) g C. Our results emphasize the need to account for the overall impact of industrial polluters on ecosystem C and N pools when assessing the C and N dynamics in northern boreal forests because of the marked long-term negative effects of their emissions on structure and productivity of plant communities.

Combined effects of environmental disturbance and climate warming on insect herbivory in mountain birch in subarctic forests: Results of 26-year monitoring

Both pollution and climate affect insect-plant interactions, but the combined effects of these two abiotic drivers of global change on insect herbivory remain almost unexplored. From 1991 to 2016, we monitored the population densities of 25 species or species groups of insects feeding on mountain birch (Betula pubescens ssp. czerepanovii) in 29 sites and recorded leaf damage by insects in 21 sites in subarctic forests around the nickel-copper smelter at Monchegorsk, north-western Russia. The leaf-eating insects demonstrated variable, and sometimes opposite, responses to pollution-induced forest disturbance and to climate variations. Consequently, we did not discover any general trend in herbivory along the disturbance gradient. Densities of eight species/species groups correlated with environmental disturbance, but these correlations weakened from 1991 to 2016, presumably due to the fivefold decrease in emissions of sulphur dioxide and heavy metals from the smelter. The densities of externally feeding defoliators decreased from 1991 to 2016 and the densities of leafminers increased, while the leaf roller densities remained unchanged. Consequently, no overall temporal trend in the abundance of birch-feeding insects emerged despite a 2-3°C elevation in spring temperatures. Damage to birch leaves by insects decreased during the observation period in heavily disturbed forests, did not change in moderately disturbed forests and tended to increase in pristine forests. The temporal stability of insect-plant interactions, quantified by the inverse of the coefficient of among-year variations of herbivore population densities and of birch foliar damage, showed a negative correlation with forest disturbance. We conclude that climate differently affects insect herbivory in heavily stressed versus pristine forests, and that herbivorous insects demonstrate diverse responses to environmental disturbance and climate variations. This diversity of responses, in combination with the decreased stability of insect-plant interactions, increases the uncertainty in predictions on the impacts of global change on forest damage by insects.

High densities of leaf-tiers in open habitats are explained by host plant architecture

1. Crown architecture remains one of the least studied plant traits that influence plant–herbivore interactions. The hypotheses that dense crown architecture of mountain birches from open habitats favours leaf‐tying caterpillars through bottom‐up and/or top‐down effects associated with high leaf connectivity were tested.

Changes in crown architecture as a strategy of mountain birch for survival in habitats disturbed by pollution.

Although trees in polluted areas often exhibit modified growth habits, the immediate causes of changes in crown architecture and their consequences for persistence of plant populations in disturbed habitats are not well understood. We compared individuals of mountain birch, Betula pubescens ssp. czerepanovii, growing in severely disturbed habitats (industrial barrens) surrounding a nickel-copper smelter in north-western Russia, with birches growing in unpolluted habitats. They were found to have shorter heights, a shrubby growth habit, lower depth/width and surface/foliar mass ratios of the crown, higher numbers of dead branches and twisted trunks and higher branching resulting from increased numbers of long shoots and more densely spaced buds than individuals in unpolluted forests. The increased production of long shoots was enabled by their formation not only from the axillary buds of previous-year long shoots but also from the apical buds of short shoots. These latter long shoots develop in the inner part of the crown, thus increasing the crown density. Additionally, birches from industrial barrens better compensated for mechanical damage, such as trunk/shoot removal, compared to birches from unpolluted forest and mountain tundra habitats, presumably due to the larger number of buds formed annually. The specific crown architecture of these birches can be explained by the direct effects of pollution combined with changes in microclimate due to pollution-induced forest decline. The seed progenies of birches from an industrial barren reared in a benign environment produced higher numbers of long shoots than seedlings from other habitats, suggesting that adaptive changes in crown architecture are partially shaped by the selection imposed by long-term pollution impacts. Nearly spherical and compact crowns minimise the impacts of unfavourable environmental conditions on trees and are therefore adaptive. We concluded that the development of specific crown architecture allows mountain birch to dominate in habitats that are severely disturbed by pollution.

Ambient temperatures differently influence colour morphs of the leaf beetle Chrysomela lapponica : Roles of thermal melanism and developmental plasticity

We asked whether ambient temperatures can affect morph frequencies within a subarctic population of the polymorphic leaf beetle Chrysomela lapponica through thermal melanism and/or developmental plasticity. Body temperature increased faster in beetles of dark morph than in beetles of light morph under exposure to artificial irradiation. Dark males ran faster than light males in both field and laboratory experiments, and this difference decreased with increasing ambient air temperature, from significant at 10 °C to non-significant at 20 °C and 26 °C. On cold days (6-14 °C), significantly more dark males than light males were found on their host plants in copula (40.8% and 27.3% respectively); on warm days (15-22 °C) this difference disappeared. Light females produced twice as many eggs as dark females; this difference did not depend on the ambient temperature. The proportion of dark morphs in the progenies of pairs with one dark parent was twice as high as that in the progenies of pairs in which both parents were light, and this proportion was greater when larvae developed at low (10 and 15 °C) than at high (20 and 25 °C) temperatures. We conclude that low temperatures may increase the frequencies of dark morphs in C. lapponica populations due to both the mating advantages of dark males over light males and developmental plasticity. Variation in frequencies of low-fecund dark morphs in the population, caused by among-year differences in temperature together with density-dependent selection, may contribute to the evolutionary dynamics of the colour polymorphism and may influence abundance fluctuations in these leaf beetle populations.

Two Birch Species Demonstrate Opposite Latitudinal Patterns in Infestation by Gall-Making Mites in Northern Europe

Latitudinal patterns in herbivory, i.e. variations in plant losses to animals with latitude, are generally explained by temperature gradients. However, earlier studies suggest that geographical variation in abundance and diversity of gall-makers may be driven by precipitation rather than by temperature. To test the above hypothesis, we examined communities of eriophyoid mites (Acari: Eriophyoidea) on leaves of Betula pendula and B. pubescens in boreal forests in Northern Europe. We sampled ten sites for each of five latitudinal gradients from 2008–2011, counted galls of six morphological types and identified mites extracted from these galls. DNA analysis revealed cryptic species within two of six morphologically defined mite species, and these cryptic species induced different types of galls. When data from all types of galls and from two birch species were pooled, the percentage of galled leaves did not change with latitude. However, we discovered pronounced variation in latitudinal changes between birch species. Infestation by eriophyoid mites increased towards the north in B. pendula and decreased in B. pubescens, while diversity of galls decreased towards the north in B. pendula and did not change in B. pubescens. The percentage of galled leaves did not differ among geographical gradients and study years, but was 20% lower in late summer relative to early summer, indicating premature abscission of infested leaves. Our data suggest that precipitation has little effect on abundance and diversity of eriophyoid mites, and that climate warming may impose opposite effects on infestation of two birch species by galling mites, favouring B. pendula near the northern tree limit.

Background losses of woody plant foliage to insects show variable relationships with plant functional traits across the globe

Summary Despite a long history of research, we lack a comprehensive understanding of the reasons behind pronounced variation in foliar losses to insects among plant species. Our aim was to test the hypothesis that plant functional traits and/or ecological strategies are good predictors of the background losses of woody plant foliage to insects (i.e. losses occurring when herbivore populations are at their ‘normal’ densities) at the global scale. We conducted a quantitative synthesis of published and original data on foliar losses of 793 species of woody plants belonging to 128 families from ca. 500 localities world-wide, representing tropical, temperate and polar climate zones. The background foliar losses to insects varied among plant life forms, increasing from dwarf shrubs to large trees, and were higher in inherently fast-growing species than in slow-growing species. These patterns supported predictions of both the apparency and growth rate (resource availability) hypotheses for data combined across localities, but only outside the tropics. Foliar losses to insects slightly but significantly increased with specific leaf area (SLA) in all climate zones. No differences were noted in background herbivory between woody plant species with deciduous and evergreen foliage, with different shade tolerance and with different successional status. Synthesis. Factors affecting the distribution of herbivory among species of woody plants differed among the climate zones, and the predictive power of at least some of the theories/hypotheses addressing plant–herbivore interactions at large spatial scales varies among climates and/or biomes. The average background losses of woody plant foliage to insects across localities can be predicted from the inherent growth rate of the plant species, its life form and SLA, although these plant characteristics jointly explain only a minor part of the total variation observed in the primary data.