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

The costs and effectiveness of chemical defenses in herbivorous insects: a meta-analysis

The evolution of defensive traits and strategies depends on the intensity of selection imposed by natural enemies and on the fitness costs of defenses against these enemies. We tested several hypotheses about the evolution of chemical defenses in plant-feeding insects using a meta-analysis. We analyzed the effectiveness (in terms of prey survival; 159 publications) and costs (in terms of reduction in performance due to defense production; 33 publications) of chemical defenses in various prey-predator systems (140 herbivore species and 124 enemy species). The chemical defenses of insect herbivores, on average, were effective against generalist predators, were not effective against specialist predators and generalist parasitoids, and increased the risk of parasitism by specialist parasitoids. The defenses were more effective against vertebrate than against invertebrate predators and most effective against birds. Defensive compounds synthesized de novo and derived from the herbivore&#39;s food plants did not differ in the magnitude of their effects. Externalization of chemical defenses enhanced their effects on naive vertebrate predators but simultaneously increased the risk of parasitism. The defenses of specialist herbivores were more effective than those of generalists, mostly due to species that sequestered plant allelochemicals for their own defenses. Advertising of chemical defenses by warning display enhanced their effectiveness only against vertebrate predators. Aposematic colors and patterns were more effective warning signals than other types of conspicuous coloration against both experienced and naive vertebrate predators, suggesting that certain colors and/or patterns were more important than conspicuousness for both learning and innate avoidance. The meta-analysis did not reveal physiological costs of the production of chemical defenses across 22 herbivore species, although the results varied strongly with the method used to measure these costs. We conclude that the cost-benefit trade-offs driving the evolution of chemical defenses in herbivorous insects are affected by ecological costs (i.e., increased susceptibility to parasitoids) more than by costs in terms of resources. Still, a favorable cost-benefit ratio, i.e., great effects for a small expenditure, may partly explain the prevalence of chemical anti-predator defenses in insects.</p

Variation in defensive chemistry within a polyphagous Baikal population of Chrysomela lapponica (Coleoptera: Chrysomelidae): potential benefits in a multi-enemy world

Variation in anti-predator chemical defence is frequently observed in natural populations, but its adaptive significance remains debatable. Most populations of the chemically defended leaf beetle, Chrysomela lapponica, are specialized to their host plants, but some populations are polyphagous. We tested the hypothesis that the use of multiple host plants by a Baikal population of C. lapponica results in variation in the composition of its defensive secretions, leading to variation in defence effectiveness against different natural enemies. The secretions of larvae feeding on local host plants differed both in the origin of major components (sequestered or autogeneous) and in chemical profiles. This variation was at least partly associated with differences in the secondary chemistry among the five most abundant plant species used by this population. Larvae feeding on different hosts in nature suffered similar overall mortality from enemies, but the relative contributions of different enemy species (natural enemy profiles) varied among host plant species. Behavioural experiments with three predators and one parasitoid showed that this variation may result from idiosyncratic responses of the enemy species to the composition of the larval defences. These differences allow part of the polyphagous leaf beetle population to escape from the currently most abundant enemy on the host plant species that provides the best protection against this enemy. In this way, the within-population variability in chemical defence, associated with feeding on hosts differing in chemistry, can buffer prey populations against fluctuating pressures of specific enemies

Can Larvae of Forest Click Beetles (Coleoptera: Elateridae) Feed on Live Plant Roots?

Simple SummaryDetailed natural history information is still lacking for many species of soil-dwelling invertebrates. We asked whether the larvae (wireworms) of two click beetle species, which are most abundant in European boreal forests, feed on live roots of forest plants. The weight of root pieces of downy birch, Scots pine, Norway spruce and wavy hair-grass, offered to wireworms in a laboratory experiment, did not decrease, indicating that these larvae did not consume live root tissues. Therefore, Athous subfuscus and Dalopius marginatus should be excluded from the lists of forest pests damaging tree roots.The life histories of many soil-dwelling invertebrates remain poorly studied. The larvae of two click beetle species, Athous subfuscus and Dalopius marginatus, which are most abundant in European boreal forests, are both classified as omnivorous and are included in lists of root-damaging pests. Nevertheless, we are not aware of any direct proof of their ability (or inability) to consume plant roots. In this study, we asked whether these larvae actually feed on the roots of forest plants in the absence of other food sources. Live roots of boreal forest plants, including trees (Betula pubescens, Picea abies and Pinus sylvestris) and grass (Deschampsia flexuosa), were offered to click beetle larvae in a two-month microcosm experiment. The weight of roots placed in vials with the wireworms did not decrease, indicating that the larvae of these click beetle species did not feed on live roots, even in the absence of other food sources. This suggests that the feeding niches of A. subfuscus and D. marginatus larvae are narrower than previously thought and do not include live plant tissues. Therefore, these click beetle species should be excluded from the lists of forest pests damaging tree roots

Ontogenetic changes in insect herbivory in birch (Betula pubesecens): The importance of plant apparency

Several theories aim at predicting changes in the interactions between plants and herbivores over the lifetime of a plant. Hypotheses based on ontogenetic changes in resource allocation to plant defence and in plant apparency lead to partly opposing predictions regarding the differences in levels of herbivory between juvenile and mature plant individuals. We tested these predictions by measuring background foliar losses to insects in saplings and mature trees of downy birch (Betula pubescens) in ten sites along a latitudinal gradient from 60 degrees to 69 degrees N in boreal forests of Northern Europe. The percentage of consumed leaf area increased, and the variation in the levels of herbivory among plant individuals decreased, for tree sizes ranging from small saplings (2-12cm tall) to large saplings (13-80cm tall) and then to mature trees (3-18m tall). Small saplings had higher foliar quality for insects, as indicated by better performance of leafmining larvae of Eriocrania semipurpurella and by greater specific leaf area, compared with large saplings and mature trees. The average percentage of leaf area consumed from a damaged leaf, which reflects the inducibility of local defence responses to insect damage, did not vary among the birch size classes. The foliar losses to insects decreased nearly fivefold with an increase in latitude from 60 degrees to 69 degrees N, but the relative differences in these losses among the birch size classes were independent of latitude. Our findings fit well with the predictions based on a plant apparency hypothesis, but do not support predictions based on ontogenetic changes in resource allocation to plant antiherbivore defences. We conclude that the generally overlooked effects of apparency on plant damage by insects can explain, at least in some cases, the frequently observed lack of correspondence between the levels of plant defences and herbivory.A is available for this article

Local Insect Damage Reduces Fluctuating Asymmetry in Next-year's Leaves of Downy Birch

Insect herbivory imposes stress on host plants. This stress may cause an increase in leaf fluctuating asymmetry (FA), which is defined as the magnitude of the random deviations from a symmetrical leaf shape. We tested the hypothesis that differences in leaf FA among individual shoots of downy birch, Betula pubescens, are at least partly explained by local damage caused by insects in the previous year. Unexpectedly, we found that in the year following the damage imposed by miners, leafrollers and defoliators, damaged birch shoots produced leaves with lower FAs compared to shoots from the same tree that had not been damaged by insects. This effect was consistent among the different groups of insects investigated, but intra-species comparisons showed that statistical significance was reached only in shoots that had been damaged by the birch leaf roller, Deporaus betulae. The detected decrease in leaf FA in the year following the damage agrees with the increases in shoot performance and in antiherbivore defence. The present results indicate that within-plant variation in leaf FA may have its origin in previous-year damage by insects, and that FA may influence the current-year's distribution of herbivory

Vascular plants on the islands and peninsulas of Maloe More (Lake Baikal): patterns of diversity and species turnover

Unique biota of the Lake Baikal region face many threats due to increasing human activities. We documented spatial patterns in diversity of vascular plants, explored effects of natural (bird colonies) and human-induced (tourism) disturbances on species richness of semi-desert and steppe-desert plant communities of 12 islands and 4 peninsulas, and estimated species turnover within a 30-year period. Floras of surveyed islands/peninsulas contained 9 to 143 species; species area relationship followed the power law model. Species richness did not change between 1979 and 2009, but the proportion of ruderal species doubled during this period. Mean relative turnover rate was 1.17% of species per year. The islands with large bird colonies had lower species richness than the islands with small or no colonies. Imposing restrictions on tourist visitation to at least three islands (Zamogoj, Khubyn and Khunuk) is a feasible way to conserve substantial part of regional biodiversity

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

Doubling of biomass production in European boreal forest trees by a four-year suppression of background insect herbivory

Background insect herbivory, i.e. the minor but chronic plant damage caused by insects, is usually considered `negligible' for plants when compared with the severe defoliation associated with forest pest outbreaks. We experimentally tested the hypothesis that the impacts of background herbivory on tree growth and mortality accumulate over years, resulting in much larger effects than usually assumed. In boreal taiga forests near Arkhangelsk (Northern Russia), application of insecticide at 10-day intervals for four growth seasons (June-September of 2014-2017) decreased foliage losses to insects in our study species (early successional deciduous Betula pubescens and Populus tremula; late successional coniferous Picea abies and Pinus sylvestris) from 2.04-6.35% to 0.72-1.18%. The magnitude of the insecticide treatment effect on plant losses to defoliating insects varied considerably among the study species, with the highest effect observed in white birch and the lowest effects in the two late successional species. Across all tree species, insecticide treatment nearly doubled the increase in tree biomass relative to control plots, demonstrating that background insect herbivory has major negative impacts on tree growth and productivity. The insecticide-treated plots showed the largest increase in biomass in Norway spruce and the smallest increase in European aspen when compared to the control plots. The changes in birch growth following the release from insect herbivory were three times greater than the effects of the same level of simulated herbivory in an earlier experiment, thereby hinting at the importance of herbivore-specific elicitors in the growth suppression of trees damaged by insects. The mortality of late successional species in the treatment plots increased nearly three-fold, whereas the mortality of early successional species did not change relative to controls, suggesting an increase in competitiveness of the early successional trees released from herbivory. Thus, in agreement with an earlier modelling study, we conclude that minor herbivore damage, over the long term, substantially reduces biomass production in North European forest trees. Due to differential effects on coexisting tree species, this damage has a pronounced impact on plant competitiveness and affects both the productivity and the structure of boreal forests

Opposite latitudinal patterns for bird and arthropod predation revealed in experiments with differently colored artificial prey

The strength of biotic interactions is generally thought to increase toward the equator, but support for this hypothesis is contradictory. We explored whether predator attacks on artificial prey of eight different colors vary among climates and whether this variation affects the detection of latitudinal patterns in predation. Bird attack rates negatively correlated with model luminance in cold and temperate environments, but not in tropical environments. Bird predation on black and on white (extremes in luminance) models demonstrated different latitudinal patterns, presumably due to differences in prey conspicuousness between habitats with different light regimes. When attacks on models of all colors were combined, arthropod predation decreased, whereas bird predation increased with increasing latitude. We conclude that selection for prey coloration may vary geographically and according to predator identity, and that the importance of different predators may show contrasting patterns, thus weakening the overall latitudinal trend in top-down control of herbivorous insects