Julia Koricheva

Regulation of woody plant secondary metabolism by resource availability: hypothesis testing by means of meta-analysis

Our aim in this study was to determine how well phenotypic variation in foliar concentrations of carbon-based secondary compounds (CBSCs) in woody plants can be predicted on the basis of two resource-based hypotheses, i.e. the carbon-nutrient balance (CNB) and growth-differentiation balance (GDB) hypotheses. We conducted a meta-analysis of literature data with respect to responses of CBSCs, carbohydrates and nitrogen to six types of environmental manipulations (fertilization with nitrogen or phosphorus, shading, CO 2 enrichment, drought stress, ozone exposure). Plant responses to nitrogen fertilization, shading and CO 2 enrichment in terms of pooled CBSCs and carbohydrates were consistent with predictions made with the two hypotheses. However, among biosynthetically distinct groups of CBSCs only concentrations of phenylpropanoid-derived compounds changed as predicted; hydrolyzable tannins and terpenoids, in particular, were less responsive. Phosphorus fertilization did not affect concentrations of CBSC or primary metabolites. Plant responses to drought and ozone exposure presumably were driven by plant demands for particular types of compounds (osmolites in the case of drought and antioxidants in the case of ozone exposure) rather than by changes in resource availability. Based on the relative importance of the treatment effects, we propose a hierarchical model of carbon allocation to CBSCs. The model implies that CBSC production is determined by both resource availability and specific demand-side responses. However, these two mechanisms work at different hierarchical levels. The domain of the CNB and GDB hypotheses is at the high hierarchical levels, predicting the total amount of carbon that can be allocated to CBSCs. Predicting altered concentrations of individual CBSCs, i.e. low hierarchy levels, probably demands biosynthetically detailed models which also take into account the history of plant interactions with biotic and abiotic factors.

Ecosystem effects of biodiversity manipulations in European grasslands.

We present a multisite analysis of the relationship between plant diversity and ecosystem functioning within the European BIODEPTH network of plant-diversity manipulation experiments. We report results of the analysis of 11 variables addressing several aspects of key ecosystem processes like biomass production, resource use (space, light, and nitrogen), and decomposition, measured across three years in plots of varying plant species richness at eight different European grassland field sites. Differences among sites explained substantial and significant amounts of the variation of most of the ecosystem processes examined. However, against this background of geographic variation, all the aspects of plant diversity and composition we examined (i.e., both numbers and types of species and functional groups) produced significant, mostly positive impacts on ecosystem processes. Analyses using the additive partitioning method revealed that complementarity effects (greater net yields than predicted from monocultures due to resource partitioning, positive interactions, etc.) were stronger and more consistent than selection effects (the covariance between monoculture yield and change in yield in mixtures) caused by dominance of species with particular traits. In general, communities with a higher diversity of species and functional groups were more productive and utilized resources more completely by intercepting more light, taking up more nitrogen, and occupying more of the available space. Diversity had significant effects through both increased vegetation cover and greater nitrogen retention by plants when this resource was more abundant through N2 fixation by legumes. However, additional positive diversity effects remained even after controlling for differences in vegetation cover and for the presence of legumes in communities. Diversity effects were stronger on above- than belowground processes. In particular, clear diversity effects on decomposition were only observed at one of the eight sites. The ecosystem effects of plant diversity also varied between sites and years. In general, diversity effects were lowest in the first year and stronger later in the experiment, indicating that they were not transitional due to community establishment. These analyses of our complete ecosystem process data set largely reinforce our previous results, and those from comparable biodiversity experiments, and extend the generality of diversity–ecosystem functioning relationships to multiple sites, years, and processes.

META‐ANALYSIS OF SOURCES OF VARIATION IN FITNESS COSTS OF PLANT ANTIHERBIVORE DEFENSES

Plant defense theories predict that allocation to antiherbivore defenses should impose a cost on plants, manifested as a reduction in growth and reproduction. However, the empirical evidence for the existence of such trade-offs is conflicting, suggesting that significant fitness costs of defense arise in some circumstances but not in others. A meta-analysis of 70 studies assessing the relationship between measures of plant defense and growth or reproduction has been conducted to examine the relative importance of several potential sources of variation in the fitness costs of defense. The magnitude of fitness costs varied depending on whether they were measured at the level of phenotype or genotype. The mean magnitude of among-genotype correlations (AGCs) between defense and fitness measures (r = −0.30) was higher than that of among-phenotype correlations (APCs; r = −0.15). Moreover, AGCs tended to be more negative when defense was assessed as the inverse of herbivore densities or damage rather than in ter...

The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis.

Defense against herbivores often changes dramatically as plants develop. Hypotheses based on allocation theory and herbivore selection patterns predict that defense should increase or decrease, respectively, across ontogeny, and previous research partly supports both predictions. Thus, it remains unclear which pattern is more common and what factors contribute to variability among studies. We conducted a meta‐analysis of 116 published studies reporting ontogenetic patterns in plant defense traits and herbivory. Patterns varied depending on plant life form (woody, herbaceous, grass), type of herbivore (insect, mollusk, mammal), and type of defense trait (secondary chemistry, physical defense, tolerance). In woody plants, chemical defense increased during the seedling stage, followed by an increase in physical defenses during the vegetative juvenile stage. Mammalian herbivores showed a strong preference for mature compared to juvenile tissues in woody plants. Herbs experienced a significant increase in secondary chemistry across the entire ontogenetic trajectory, although the magnitude of increase was greatest during the seedling stage. Correspondingly, mollusks preferred young compared to older herbs. Future research investigating growth/defense trade‐offs, allometry, herbivore selection patterns, and ecological costs would shed light on the mechanisms driving the ontogenetic patterns observed.

Numerical responses of different trophic groups of invertebrates to manipulations of plant diversity in grasslands.

Abstract. We studied the effects of plant diversity on abundance of invertebrate herbivores, parasitoids and predators in two grassland communities (one in Switzerland and one in Sweden) in which plant species richness and functional diversity have been experimentally manipulated. Among herbivores, the abundance of only the most sessile and specialised groups (leafhoppers and wingless aphids) was affected by plant diversity. At both sites, numbers of leafhoppers in sweep net samples showed a linear, negative relationship with plant species number whereas numbers of wingless aphids in suction samples increased with the number of plant functional groups (grasses, legumes, and non-legume forbs) present in the plot. Activity of carabid beetles and spiders (as revealed by pitfall catches) and the total number of predators in pitfalls at the Swiss site decreased linearly with increases in the number of plant species and plant functional groups. Abundance of more specialised enemies, hymenopteran parasitoids, was not affected by the manipulations of plant diversity. Path analysis and analysis of covariance indicated that plant diversity effects on invertebrate abundance were mostly indirect and mediated by changes in plant biomass and cover. At both sites, plant species composition (i.e. the identity of plant species in a mixture) affected numbers of most of the examined groups of invertebrates and was, therefore, a more important determinant of invertebrate abundance in grasslands than plant species richness per se or the number of plant functional groups. The presence of legumes in a mixture was especially important and led to higher numbers of most invertebrate groups. The similarity of invertebrate responses to plant diversity at the two study sites indicates that general patterns in abundance of different trophic groups can be detected across plant diversity gradients under different environmental conditions.

Seasonal changes in birch leaf chemistry: are there trade-offs between leaf growth and accumulation of phenolics?

Several plant-herbivore hypotheses are based on the assumption that plants cannot simultaneously allocate resources to growth and defence. We studied seasonal patterns in allocation to growth and putatively defensive compounds by monitoring several chemical and physical traits in the leaves of mountain birch from early June (budburst) to late September (leaf senescence). We found significant seasonal changes in all measured characteristics, both in terms of concentrations (mg g–1) and amounts (mg leaf–1). Changes were very rapid in the spring, slow in the middle of the season, and there was another period of fast changes in the senescing leaves. Co-occurring changes in physical leaf traits and concentrations of several compounds indicated a seasonal decline in foliage suitability for herbivores. Concentrations of protein and free amino acids declined through the growing season whereas individual sugars showed variable seasonal patterns. The seasonal trends of phenolic groups differed drastically: concentrations of soluble proanthocyanidins increased through the season, whereas cell wall-bound proanthocyanidins, gallotannins and flavonoid glycosides declined after an initial increase in young leaves. We failed to find proof that the seasonal accumulation of phenolics would have been seriously compromised by leaf or shoot growth, as assumed by the growth/differentiation balance hypothesis and the protein competition model hypothesis. On the contrary, there was a steady increase in the total amount of phenolics per leaf even during the most active leaf growth.

Meta‐analysis of Trade‐offs among Plant Antiherbivore Defenses: Are Plants Jacks‐of‐All‐Trades, Masters of All?

On the basis of physiological and ecological costs of defense allocation, most plant defense theories predict the occurrence of trade‐offs between resource investment in different types of antiherbivore defenses. To test this prediction, we conducted a meta‐analysis of 31 studies published in 1976–2002 that provided data on covariation of different defensive traits in plant genotypes. We found no overall negative association between different defensive traits in plants; instead, the relationship between defensive traits varied from positive to negative depending on the types of co‐occurring defenses. Evidence of trade‐off was found only between constitutive and induced defenses. Therefore, to a large extent, plants appear to be jacks‐of‐all‐trades, masters of all and may successfully produce several types of defense without paying considerable trade‐offs. Our survey thus provides little evidence that genetic trade‐offs between defensive traits significantly constrain the evolution of multiple defenses in plants.

From genes to ecosystems: a synthesis of the effects of plant genetic factors across levels of organization

Using two genetic approaches and seven different plant systems, we present findings from a meta-analysis examining the strength of the effects of plant genetic introgression and genotypic diversity across individual, community and ecosystem levels with the goal of synthesizing the patterns to date. We found that (i) the strength of plant genetic effects can be quite high; however, the overall strength of genetic effects on most response variables declined as the levels of organization increased. (ii) Plant genetic effects varied such that introgression had a greater impact on individual phenotypes than extended effects on arthropods or microbes/fungi. By contrast, the greatest effects of genotypic diversity were on arthropods. (iii) Plant genetic effects were greater on above-ground versus below-ground processes, but there was no difference between terrestrial and aquatic environments. (iv) The strength of the effects of intraspecific genotypic diversity tended to be weaker than interspecific genetic introgression. (v) Although genetic effects generally decline across levels of organization, in some cases they do not, suggesting that specific organisms and/or processes may respond more than others to underlying genetic variation. Because patterns in the overall impacts of introgression and genotypic diversity were generally consistent across diverse study systems and consistent with theoretical expectations, these results provide generality for understanding the extended consequences of plant genetic variation across levels of organization, with evolutionary implications.

Effects of mycorrhizal fungi on insect herbivores: a meta‐analysis

Mycorrhizal status of the host plant is often ignored in studies on plant-herbivore interactions, but mycorrhizal colonization is known to induce many morphological, physiological, and biochemical changes in host plants, which in turn may alter plant quality as a host for insect herbivores. Both positive and negative effects of mycorrhizal colonization of the host plant on performance and density of insect herbivores have been reported in previous studies. We have conducted a meta-analysis of 34 published and unpublished studies on this topic in order to find out the sources of variation in mycorrhizae effects on insect herbivores. Effects of mycorrhizae on chewing insects depended upon the parameter measured and the degree of herbivore feeding specialization. Density and consumption of chewing insects were higher on mycorrhizal plants, but this did not lead to greater plant damage, presumably because herbivore survival tended to be lower on mycorrhizal plants. Mono- and oligophagous chewers benefited from mycorrhizal colonization of their host plants, whereas performance of polyphagous chewers was reduced on mycorrhizal plants. Among sucking insects, phloem feeders benefited from mycorrhizal infection, but performance of mesophyll feeders was lower on mycorrhizal plants. The type of mycorrhiza was not important for chewing insects, but performance of sucking insects was increased more by arbuscular mycorrhizal fungi (AM) than by ectomycorrhizae (ECM). Among AM inoculation studies, the most commonly used fungal species, Glomus intraradices, tended to have a negative effect on chewer performance, whereas all other fungal species tended to have a positive effect. There was no significant difference in results between studies using inoculation and fungicides, field and laboratory studies, and published and unpublished studies. Mycorrhizal status of the host plant thus influences insect herbivore performance, but the magnitude and direction of the effect depend upon the feeding mode and diet breadth of the insect and the identity of fungi.

Tolerance to herbivory in woody vs. herbaceous plants

Research on plant tolerance to herbivory has been so far largely focussed on herbaceous plants partly due to the implicit assumption that woody plants are inherently lower in their compensatory potential as compared to herbs. However, tolerance to herbivory should be an important part of resistance of woody plants because their apparency to herbivory is high due to a large size and long life span, and their defence systems cannot completely exclude herbivory. Moreover, the longer life span, more complex modularity and higher sectorality of woody plants as compared to herbs imply that compensatory responses in woody plants may take several years to develop, and that consequences of herbivore damage to individual modules may profoundly differ from whole-plant responses. Therefore, short-term studies using branches or ramets as experimental units are likely to underestimate the tolerance of woody plants to herbivory. In addition, defoliation by insects (the most common type of herbivory experienced by woody plants) is less likely to release apical dominance and trigger biomass compensation than mammalian grazing on herbaceous plants. We conclude, therefore, that the seemingly different recovery potentials exhibited by woody and herbaceous plants are more likely to be the consequences of differences between the two types of plants in modular architecture, longevity and the type of herbivory they commonly experience rather than indications of inherent differences in compensatory ability.