Elena L. Zvereva

Stress Responses of Salix borealis to Pollution and Defoliation

Morphological characters of Salix borealis were monitored during 1994-96 at 10 sites along a transect crossing the heavily polluted surroundings of Severonikel smelter in NW Russia, and analysed with respect to pollution load and density of the principal herbivore, the leaf beetle Melasoma lapponica. Leaf size and shoot growth increased and leaf pubescence decreased with an increase in pollution, whereas variation in other characteristics was not related to pollution load. Leaf fluctuating asymmetry (FA) and leaf pubescence increased with an increase in herbivory, whereas variation in other characters was not related to foliar damage. A field experiment demonstrated that leaf FA and pubescence were high in the year after defoliation. The data on leaf FA, a non-specific stress indicator, suggest that for the extant individuals of S. borealis, defoliation resulted in detectable stress, whereas long-lasting severe pollution by sulphur dioxide and heavy metals caused no measurable stress response and may even stimulate growth of leaves and shoots. Leaf FA of woody plants may serve as an early indicator of the biotic stress caused by herbivory, which expands the use of FA as a tool in helping to compare the relative strengths of different stressing agents.

Delayed induced resistance and increase in leaf fluctuating asymmetry as responses of Salix borealis to insect herbivory

Abstract An outbreak of leaf beetle Melasoma lapponica in two localities around the Severonikel smelter in Kola Peninsula, north-west Russia, resulted in severe defoliation of Salix borealis, observed for the first time in August 1993 and then again in 1994 and 1995. Before the first severe defoliation, in July 1993, performance of M. lapponica larvae in plots with a high beetle density was either better or the same as in low-density plots. However, in 1994 and 1995, the years following severe willow defoliation in high-density plots,  M. lapponica performance (in terms of survival, developmental time and beetle weight) decreased with increasing beetle density. Retarded larval growth in high-density plots was related to a decreased consumption rate, whereas the efficiency of the conversion of ingested food was similar in high- and low-density plots. These results indicate that defoliation triggered delayed induced resistance in S. borealis. Leaf fluctuating asymmetry (FA, a non-specific stress indicator) of this willow species in 1992 was similar in low- and high-density plots, but it increased in high-density plots in 1994, at the same time that detrimental effects on beetle performance were recorded at these sites. Plot-specific indices of beetle performance and FA were negatively correlated both in 1994 and 1995, suggesting that plants stressed by defoliation the previous-year were less favourable for leaf beetles.

Sources of variation in plant responses to belowground insect herbivory: a meta-analysis.

Growing interest in belowground herbivory and the remarkable diversity of the accumulated information on this topic inspired us to quantitatively explore the variation in the outcomes of individual studies. We conducted a meta-analysis of 85 experimental studies reporting the effects of root-feeding insect herbivores (36 species) on plants (75 species). On average, belowground herbivory led to a 36.3% loss of root biomass, which was accompanied by a reduction in aboveground growth (−16.3%), photosynthesis (−11.7%) and reproduction (−15.5%). The effects of root herbivory on aboveground plant characteristics were significant in agricultural and biological control studies, but not in studies of natural systems. Experiments conducted in controlled environments yielded larger effects on plants than field experiments, and infestation experiments resulted in more severe effects than removal studies employing natural levels of herbivory. Simulated root herbivory led to greater aboveground growth reductions than similar root loss imposed by insect feeding. External root chewers caused stronger detrimental effects than sap feeders or root borers; specialist herbivores imposed milder adverse effects on plants than generalists. Woody plants suffered from root herbivory more than herbaceous plants, although root loss was similar in these two groups. Evergreen woody plants responded to root herbivory more strongly than deciduous woody plants, and grasses suffered from root herbivory more than herbs. Environmental factors such as drought, poor nutrient supply, among-plant competition, and aboveground herbivory increased the adverse effects of root damage on plants in an additive manner. In general, plant tolerance to root herbivores is lower than tolerance to defoliating aboveground herbivores.

Responses of terrestrial arthropods to air pollution: a meta-analysis

Background, aim, and scopeArthropods, with over a million species described, are ubiquitous throughout different environments. Knowledge of their responses to human impact is crucial for understanding and predicting changes in ecosystem structure and functions. Our aim was to investigate the general patterns and to identify sources of variation in changes of the diversity, abundance and fitness of terrestrial arthropods (including Arachnida, Collembola and Insecta) in habitats affected by point polluters.Main featuresWe found 134 suitable studies which were published between 1965 and 2007. These data came from impact zones of 74 polluters in 20 countries with the largest representation from Russia (28 polluters), Poland (12 polluters) and the USA (six polluters). The database allowed calculation of 448 effect sizes (i.e. relative differences between measurements taken from polluted and control sites) on the effects of various point polluters like non-ferrous industries, aluminium plants, cement, magnezite, fertilising and chemical plants, power plants, iron- and steel-producing factories. We used meta-analysis to search for general effects and to compare between polluter types and arthropod groups, and linear regression to describe the latitudinal gradient and to quantify relationships between pollution and arthropod responses.ResultsThe overall effect of pollution on arthropod diversity did not differ from zero. However, species richness of soil arthropods (both living on the soil surface and within the soil) tended to decrease, and species richness of herbivores to increase, near point polluters. Abundance of terrestrial arthropods near point polluters decreased in general. This decrease resulted from strong adverse effects on soil arthropods, especially on decomposers and predators. Densities of herbivores increased, but a number of research biases that we discovered in published data may have led to overestimation of the latter effect. The dome-shaped density pattern along pollution gradients was discovered only in 5% of data sets. Among herbivores, only free-living defoliators and sap-feeders demonstrated higher densities in polluted sites; the effects of pollution on other guilds were not significant. Near the polluters, conifers suffered higher increase in damage from herbivores than deciduous woody plants and herbs. Overall effect of pollution on arthropod performance was negative; in particular, individuals from polluted sites were generally smaller than individuals from control sites. This negative effect weakened with increase in duration of the pollution impact, hinting evolution of pollution resistance in populations inhabiting polluted sites. Stepwise regression analysis demonstrated that pollution-induced changes in both the density and performance of arthropods depended on climate of the locality. Negative effects on soil fauna increased with increase in annual precipitation; positive effects on herbivore population density increased with increases in both mean July temperature and annual precipitation.DiscussionWe detected effects of research methodology on the outcome of published studies. Many of them suffer from research bias—the tendency to collect data on organisms or under conditions in which one has an expectation of detecting significant effects. Pseudoreplicated studies (one polluted site contrasted to one control site) frequently reported larger effects than replicated studies (several polluted sites contrasted with several control sites). These methodological flaws especially influenced herbivory studies; we conclude that increase in herbivory in both heavily and moderately polluted habitats is not as frequent as it was earlier suggested. In contrast, the decrease in abundance of predators is likely to be a widespread phenomenon. Thus, our analysis supports the hypothesis that pollution may favour herbivore populations by creating an enemy-free space. Consistent declines in abundance of soil arthropods in impact zones of different polluters suggest that this group can potentially be used in bioindication of pollution-induced changes in terrestrial ecosystems.ConclusionsMain effects of pollution on arthropod communities (decreased abundance of decomposers and predators and increased herbivory) may have negative consequences for structure and services of entire ecosystems. Responses of arthropods to pollution depend on both temperature and precipitation in such a way that ecosystem-wide adverse effects are likely to increase under predicted climate change.Recommendations and perspectivesOur analysis confirmed that local severe impacts of industrial enterprises on biota are well-suited to reveal the direction and magnitude of the biotic effects of aerial pollution, as well as to explore the sources of variation in responses of organisms and communities. Although we analysed the effects of point polluters, our conclusions can be applied to predict consequences of pollution impacts on regional and even global scales. We argue that possible interactions between pollution and climate should be accounted for in the analyses of global change impacts on biota.

Host plant effects on parasitoid attack on the leaf beetle Chrysomela lapponica

Larvae of the leaf beetle Chrysomela lapponica obtain salicyl glucosides (SGs) from the host plant to produce a defensive secretion with salicylaldehyde. In northern Russia, larvae and pupae experience high parasitism by the phorid fly Megaselia opacicornis and tachinid fly Cleonice nitidiuscula. We compared the suitability of the SG-rich Salix borealis and SG-poor S. caprea and S. phylicifolia to Ch. lapponica and tested whether enemy pressure on Ch. lapponica varies among host species that differ in SG content. In the laboratory, survival of Ch. lapponica larvae was higher on S. borealis than on S. caprea and S. phylicifolia, while adult body mass was higher on S. borealis and S. caprea than on S. phylicifolia. In the field, parasitism by both M. opacicornis and Cl. nitidiuscula was greater on beetles from S. borealis than from the SG-poor S. caprea or S. phylicifolia. In a laboratory choice test, the pupal parasitoid M. opacicornis laid similar numbers of eggs on beetles reared on SG-rich and SG-poor willows, suggesting that the host plant-derived defence is not effective against this parasitoid. In a field enemy-exclusion experiment, beetle survival was greatly enhanced by the exclusion of enemies, but survival rates did not differ between S. borealis and S. caprea, although larvae developed faster on S. borealis. On the other hand, parasitism and predation were observed more often on S. borealis than on S. caprea. Thus, beetle larvae perform better but also suffer higher predation and parasitism on S. borealis than on SG-poor willows. Ch. lapponica does not appear to obtain enemy-free space by feeding on SG-rich willow species.

Pheromone specificity in Eriocrania semipurpurella (Stephens) and E. sangii (Wood) (Lepidoptera: Eriocraniidae) based on chirality of semiochemicals

The fifth abdominal segment of femaleEriocrania semipurpurella (Stephens) andE. sangii (Wood) contains a pair of exocrine glands. Hexane extracts of this segment were prepared from both species and analyzed by gas chromatography with simultaneous flame ionization and electroantennographic detection (EAD). For both species, the EAD active peaks were identified as nonan-2-one, (Z)-6-nonen-2-one, and (Z)-6-nonen-2-ol by means of mass spectrometry and comparison of retention indices with those of synthetic standards. Enantiomeric separation of chiral alcohols from the female extracts was achieved by gas chromatographic analysis on a cyclodextrin column. InE. semipurpurella, a mixture of (2S,6Z)-nonen-2-ol and (2R,6Z)-nonen-2-ol (2: I) was found, whereas inE. sangii (2S,6Z)-nonen-2-ol was the predominant enantiomer and only traces of theR enantiomer were indicated by the antennal response. In field tests, a blend of the three compounds was not attractive to conspecific males. A subtractive assay showed that the alcohol in various enantiomeric mixtures was the only attractive compound, whereas addition of (Z)-6-nonen-2-one to the alcohol completely inhibited the attraction of both species. A trapping experiment including a wide range of ratios between theR andS enantiomers showed that baits containing 95–100% of theS enantiomer were attractive to maleE. sangii, whereas males ofE. semipurpurella were attracted to all tested ratios of the enantiomers. However, the response profiles of maleE. semipurpurella differed between populations from southern Sweden, south Finland, and the Kola Peninsula in Russia. In south Sweden males were maximally attracted to a racemic mixture of the alcohols. At the Kola PeninsulaE. semipurpurella was attracted to baits containing 95–100% of theR enantiomer. In south Finland all tested ratios between 0 and 100%R enantiomer trappedE. semipurpurella, but the trap catches appeared to be bimodally distributed with peaks around 15 and 70%R enantiomer. The trapping results suggest the existence of pheromone races or sibling species among the specimens identified asE. semipurpurella.

Activity and heavy metal resistance of non-specific esterases in leaf beetle Chrysomela lapponica from polluted and unpolluted habitats

We compared the general activity and heavy metal resistance of non-specific esterases in two populations of the leaf beetle Chrysomela lapponica from habitats severely contaminated by heavy metals (mostly Ni and Cu) and two populations from unpolluted habitats. Concentrations of Ni and Cu in adult beetles from the most polluted site were 7.7 and 3.6 times higher that in beetles from unpolluted habitats. Larval esterases showed higher activity and lower susceptibility to heavy metals than esterases of adults. Larval esterase activity did not differ between populations from polluted and unpolluted sites, but adult beetles from polluted localities had lower esterase activity than beetles from unpolluted habitats. Both Cu and Ni sulfates in millimolar concentrations in vitro suppressed esterase activity of larvae from unpolluted habitats, but caused no negative effect on esterases of larvae from polluted sites. Similarly, inhibition of adult esterase activity by Ni was stronger in beetles from unpolluted localities than in beetles from polluted localities. This indicates that resistance of non-specific esterases to heavy metals is higher in leaf beetle populations from contaminated environment.

A second life for old data: Global patterns in pollution ecology revealed from published observational studies

A synthesis of research on the responses of terrestrial biota (1095 effect sizes) to industrial pollution (206 point emission sources) was conducted to reveal regional and global patterns from small-scale observational studies. A meta-analysis, in combination with other statistical methods, showed that the effects of pollution depend on characteristics of the specific polluter (type, amount of emission, duration of impact on biota), the affected organism (trophic group, life history), the level at which the response was measured (organism, population, community), and the environment (biome, climate). In spite of high heterogeneity in responses, we have detected several general patterns. We suggest that the development of evolutionary adaptations to pollution is a common phenomenon and that the harmful effects of pollution on terrestrial ecosystems are likely to increase as the climate warms. We argue that community- and ecosystem-level responses to pollution should be explored directly, rather than deduced from organism-level studies.

Effects of leaf pubescence in Salix borealis on host-plant choice and feeding behaviour of the leaf beetle, Melasoma lapponica

Density of leaf trichomes in Salix borealis affected both the choice of individual host plants and feeding behaviour of adults and last instar larvae of the willow feeding leaf beetle, Melasoma lapponica. Beetles clearly preferred shaved disks to unshaved ones taken from the same leaf; this preference was highest in leaves of the most pubescent plants. High leaf pubescence explained the low preference for willow clones from the high density site in among‐site preference trials; shaving significantly increased the consumption of these pubescent willow clones. In no‐choice experiments, the food consumption by both adults and last instar larvae decreased with an increase in leaf pubescence. The time budget of adults did not depend on leaf pubescence of the host plants, however adults compelled to feed on highly pubescent plants changed their feeding sites twice as often as on less pubescent willow clones. Larvae feeding on highly pubescent plants spend moving three times as much time as larvae feeding on less pubescent plants. Combined with our earlier observations on the increase in leaf pubescence in the year(s) following defoliation, these data suggest that leaf hairiness may have contributed to the delayed induced resistance in S. borealis by disturbing the feeding behaviour of M. lapponica.

Fly parasitoid Megaselia opacicornis uses defensive secretions of the leaf beetle Chrysomela lapponica to locate its host

Larvae of the leaf beetle Chrysomela lapponica derive a defensive secretion from salicyl glucosides found in the host plant Salix borealis. This secretion protects beetle larvae from some natural enemies, but does not appear to repel parasitoids. We tested the hypothesis that the fly parasitoid Megaselia opacicornis (Diptera, Phoridae) uses the larval defensive secretion of Ch. lapponica in its search for prey. In the field, nearly 30 times more M. opacicornis individuals were caught on leaves coated with sticky resin next to a source of secretion than on control leaves. In the laboratory, M. opacicornis females laid six times more eggs next to a cotton ball soaked in secretion than next to one soaked in water. Fly females also lay more eggs on prey rich in larval secretion than on secretion-poor prey. In the field, removal of defensive secretion from beetle prepupae resulted in a 7.5-fold reduction of oviposition by fly females. Parasitoids were nearly twice as likely to lay eggs on prepupae, rich in secretion, as on pupae, which contain little secretion. Fly offspring reared from beetle prepupae reached a 21% larger body mass than those reared from pupae. Finally, M. opacicornis females avoided host prepupae already parasitized by the tachinid fly Cleonice nitidiuscula, which possess little secretion. These experiments indicate that host plant-derived defensive secretions are used by this parasitoid for host location. Adaptation of parasitoids to use defensive secretions of hosts may selectively favor an increase in diet breadth in specialist herbivores.