The effects of elevated carbon dioxide on plant-herbivore interactions have been summarized in a number of narrative reviews and metaanalyses, while accompanying elevation of temperature has not received sufficient attention. The goal of our study is to search, by means of metaanalysis, for a general pattern in responses of herbivores, and plant characteristics important for herbivores, to simultaneous experimental increase of carbon dioxide and temperature (ECET) in comparison with both ambient conditions and responses to elevated CO 2 (EC) and temperature (ET) applied separately. Our database includes 42 papers describing studies of 31 plant species and seven herbivore species. Nitrogen concentration and C/N ratio in plants decreased under both EC and ECET treatments, whereas ET had no significant effect. Concentrations of nonstructural carbohydrates and phenolics increased in EC, decreased in ET and did not change in ECET treatments, whereas terpenes did not respond to EC but increased in both ET and ECET; leaf toughness increased in both EC and ECET. Responses of defensive secondary compounds to treatments differed between woody and green tissues as well as between gymnosperm and angiosperm plants. Insect herbivore performance was adversely affected by EC, favoured by ET, and not modified by ECET. Our analysis allowed to distinguish three types of relationships between CO 2 and temperature elevation: (1) responses to EC do not depend on temperature (nitrogen, C/N, leaf toughness, phenolics in angiosperm leaves), (2) responses to EC are mitigated by ET (sugars and starch, terpenes in needles of gymnosperms, insect performance) and (3) effects emerge only under ECET (nitrogen in gymnosperms, and phenolics and terpenes in woody tissues). This result indicates that conclusions of CO 2 elevation studies cannot be directly extrapolated to a more realistic climate change scenario. The predicted negative effects of CO 2 elevation on herbivores are likely to be mitigated by temperature increase.
Aim Latitudinal patterns in biotic interactions, particularly in herbivory, have been widely debated. We conducted a quantitative research synthesis to test whether background losses of woody plant foliage to insects generally decrease from the equator to the poles, and whether geographical gradients in insect herbivory are stronger at higher latitudes than at lower latitudes.Location Global terrestrial ecosystems. MethodsWe used published and original data (3482 point estimates of the percentage of leaf area consumed by insects, collected from 941 species of woody plants in 836 localities world-wide) to analyse the geographical patterns in total losses of plant foliage and in losses to defoliating, leaf mining and leaf galling insects separately, and we searched for climatic factors that can explain the variation in the levels of background insect herbivory across the globe and within climate zones.Result On average, according to published data woody plants lose 7.55% of their leaf area to insects, but 4.73% according to our original data collected in a blinded way. These losses demonstrate a dome-shaped latitudinal pattern: they peak in temperate zones, slightly decrease towards the equator and strongly decrease towards the poles. This pattern is consistent between published and original data, indicating the robustness of the detected relationship between herbivory and latitude. The climatic factors explaining these latitudinal patterns in insect herbivory differ between climate zones. Main conclusionsOur study provides solid support for the hypothesis of a decrease in background herbivory with latitude, but only outside the tropics. For the first time we demonstrate that the latitudinal gradient in insect herbivory across the globe is nonlinear, i.e. its slope differs between the climate zones. In temperate and polar zones, but not in the tropics, background herbivory correlates with mean air temperatures and is therefore likely to increase with climate warming.
The majority of generalisations concerning plant responses to herbivory are based on studies of natural or simulated defoliation. However, effects caused by insects feeding on plant sap are likely to differ from the effects of folivory. We assessed the general patterns and sources of variation in the effects of sap feeding on growth, photosynthesis, and reproduction of woody plants through a meta-analysis of 272 effect sizes calculated from 52 papers. Sap-feeders significantly reduced growth (-29%), reproduction (-17%), and photosynthesis (-27%); seedlings suffered more than saplings and mature trees. Deciduous and evergreen woody plants did not differ in their abilities to tolerate damage imposed by sap-feeders. Different plant parts, in particular below- and above-ground organs, responded similarly to damage, indicating that sap-feeders did not change the resource allocation in plants. The strongest effects were caused by mesophyll and phloem feeders, and the weakest by xylem feeders. Generalist sap-feeders reduced plant performance to a greater extent than did specialists. Methodology substantially influenced the outcomes of the primary studies; experiments conducted in greenhouses yielded stronger negative effects than field experiments; shorter (<12 months) experiments showed bigger growth reduction in response to sap feeding than longer experiments; natural levels of herbivory caused weaker effects than infestation of experimental plants by sap-feeders. Studies conducted at higher temperatures yielded stronger detrimental effects of sap-feeders on their hosts. We conclude that sap-feeders impose a more severe overall negative impact on plant performance than do defoliators, mostly due to the lower abilities of woody plants to compensate for sap-feeders' damage in terms of both growth and photosynthesis.
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 plantfeeding 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's food plants did not differ in the magnitude of their effects. Externalization of chemical defenses enhanced their effects on naïve 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 naïve 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.
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.
Despite the increasing rate of urbanization, the consequences of this process on biotic interactions remain insufficiently studied. Our aims were to identify the general pattern of urbanization impact on background insect herbivory, to explore variations in this impact related to characteristics of both urban areas and insect-plant systems, and to uncover the factors governing urbanization impacts on insect herbivory. We compared the foliar damage inflicted on the most common trees by defoliating, leafmining and gall-forming insects in rural and urban habitats associated with 16 European cities. In two of these cities, we explored quality of birch foliage for herbivorous insects, mortality of leafmining insects due to predators and parasitoids and bird predation on artificial plasticine larvae. On average, the foliage losses to insects were 16.5% lower in urban than in rural habitats. The magnitude of the overall adverse effect of urbanization on herbivory was independent of the latitude of the locality and was similar in all 11 studied tree species, but increased with an increase in the size of the urban area: it was significant in large cities (city population 1-5 million) but not significant in medium-sized and small towns. Quality of birch foliage for herbivorous insects was slightly higher in urban habitats than in rural habitats. At the same time, leafminer mortality due to ants and birds and the bird attack intensity on dummy larvae were higher in large cities than in rural habitats, which at least partially explained the decline in insect herbivory observed in response to urbanization. Our findings underscore the importance of top-down forces in mediating impacts of urbanization on plant-feeding insects: factors favouring predators may override the positive effects of temperature elevation on insects and thus reduce plant damage.
The Latitudinal Biotic Interaction Hypothesis (LBIH) states that the intensity of biotic interactions increases from high to low latitudes. This hypothesis, which may partly explain latitudinal gradients in biodiversity, remains hotly debated, largely due to variable outcomes of published studies. We used meta‐analysis to identify the scope of the LBIH in terrestrial ecosystems. For this purpose, we explored the sources of variation in the strength of latitudinal changes in herbivory, carnivory and parasitism (119 publications) and compared these gradients with gradients in the diversity of the respective groups of animals (102 publications). Overall, both herbivory and carnivory decreased towards the poles, while parasitism increased. The latitudinal gradient in herbivory and carnivory was threefold stronger above 50–60° than at lower latitudes and was significant due to interactions involving ectothermic consumers, studies using standardised prey (i.e. prey lacking local anti‐predator adaptations) and studies aimed at testing LBIH. The poleward decrease in biodiversity did not differ between ectothermic and endothermic animals or among climate zones and was fourfold stronger than decrease in herbivory and carnivory. The discovered differences between the gradients in biotic interactions and biodiversity suggest that these two global macroecological patterns are likely shaped by different factors.
Our 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.
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