Erkki Haukioja

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.

On the role of plant defences in the fluctuation of herbivore populations.

The role of plant defences in creating cyclic and less regular fluctuations in herbivore density is evaluated on the basis of a case study concerning the birch Betula pubescens and the autumnal moth Oporinia autumnata. Birch strains from the outbreak area of the moth had basically similar but less intense immediate defensive responses when compared with birches from outside the outbreak area. After defoliation, however, birches from the outbreak area had strong intensification of defence mechanisms lasting at least three years while a birch strain originating from outside the outbreak area did not have any such response. Hence, birch defences offer a causal explanation why the moth population will probably not start a new increase immediately after the previous one in the outbreak area. Several density-induced responses of the moth could be explained as adaptations when the defensive tactics of the host tree were known. For example, aggregated larvae grew better than solitary ones on poor birch leaves with strong induced defence (probable diet at high larval densities) while solitary larvae grew better than crowded ones on high quality birch leaves (probable at low densities). Assumptions underlying the plant defence theory on herbivore fluctuations are discussed. The true importance of plant defences is easily masked by increased susceptibility to predation, parasitism, etc. Hence experiments are needed to reveal causal relations. Some experiments able to falsify the theory are proposed, as well as suggestions for avoiding obvious errors in the design of experiments. The evolutionary basis of herbivore fluctuation, as well as the evolution of resource-saving adaptations, is discussed.

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.

Induced Long‐Term Resistance of Birch Foliage against Defoliators: Defensive or Incidental?

The long—term increase in foliage resistance of white birch subjected to artificial defoliation, which has been previously documented, may be a defensive response against leaf predators, or it may be passive deterioration in foliage quality due to lost nutrients. We tested these hypotheses by two experiments in which foliage quality was assayed by the growth response of a geometrid caterpillar that is the trees major herbivore in our area. Fertilization of the soil around defoliated trees did not eliminate the change in foliage quality caused by mechanical damage, contrary to the prediction of the nutrient—stress hypothesis. Another result consistent with the defensive hypothesis was that insect damage was a more effective inducer of changes in birch foliage than mechanical damages was. Artificial defoliation was an effective inducer in a nutrient—poor but not in a nutrient—rich site; this result can be explained by either of the two hypotheses.

Nutrient stress: an explanation for plant anti-herbivore responses to defoliation

SummaryA hypothesis is put forward that the long-lasting inducible responses of trees to herbivores, particularly lepidopteran defoliators, may not be active defensive responses, but a by-product of mechanisms which rearrange the plant carbon/nutrient balance in response to nutrient stress caused by defoliation. When defoliation removes the foliage nutrients of trees growing in nutrient-poor soils, it increases nutrient stress wich in turn results in a high production of carbon-based allelochemicals. The excess of carbon that cannot be diverted to growth due to nutrient stress is diverted to the production of plant secondary metabolites. The level of carbon-based secondary substances decays gradually depending on the rate at which nutrient stress is relaxed after defoliation. In nutrient-poor soils and in plant species with slow compensatory nutrient uptake rates the responses induced by defoliation can have relaxation times of several years. The changes in leaf nitrogen and phenolic content of mountain birch support this nutrient stress hypothesis. Defoliation reduces leaf nitrogen content while phenolic content increases. These responses of mountain birch to defoliation are relaxed within 3–4 years.

Consequences of herbivory in the mountain birch (Betula pubescens ssp tortuosa): importance of the functional organization of the tree

SummaryThree types of experiments indicate that the functional organization of the mountain birch may influence the ways in which the tree responds to simulated or natural herbivory. The first experiment showed that herbivory to both short and long shoot leaves affects plant development but, because growth largely proceeds by resources of the previous year, is manifested only in the year following the damage. The second experiment showed that even partial damage to a single long shoot leaf caused the axillary bud of that leaf to produce a shorter shoot the next year. Therefore, the value of a leaf depends also on the organ which it is subtending. In the third experiment we manipulated the apical dominance of shoots in ramets and caused improvement to leaf quality in extant shoots. Ramets within a tree responded individually, probably mediated by disturbance of the hormonal control because removal of apical buds elicited the response although removal of the same number of basal buds did not. Induced amelioration is a different response to induced resistance. The two responses are triggered by different cues and may occur in the same plant. By altering hormonal balance of shoots it is potentially possible for herbivores to induce amelioration of food quality. The ways in which herbivory is simulated may explain variability of results obtained when herbivory-induced responses in plants have been studied.

Birch leaves as a resource for herbivores: Seasonal occurrence of increased resistance in foliage after mechanical damage of adjacent leaves

SummarySeasonal occurrence of such wound-induced reaction in birch foliage which deteriorates the quality of nearby leaves for herbivores was tested by means of bioassays. Length of the larval period was protracted in two early and mid-summer (larval period!) lepidopteran species as well as in two mid-summer hymenopteran species when larvae were reared on birch leaves whose adjacent leaves had earlier been damaged mechanically. This response was not found for two late-summer hymenopteran species. In a lepidopteran species whose larval period lasts through the whole season, retardation in growth was significant in the beginning of August but notl later. Hence such response of leaves, interpreted as defensive on the part of the birch, was not efficient after leaves had gained their final size. The potential consequences of wound-induced responses of leaves for herbivores are discussed.

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.

Causes of cyclicity of Epirrita autumnata (Lepidoptera, Geometridae): grandiose theory and tedious practice

Abstract Creating multiyear cycles in population density demands, in traditional models, causal factors that operate on local populations in a density-dependent way with time lags. However, cycles of the geometrid Epirrita autumnata in northern Europe may be regional, not local; i.e., successive outbreaks occur in different localities. We review possible causes of cycles of E. autumnata under both local and regional scenarios, including large-scale synchrony. Assuming cyclicity is a local phenomenon, individual populations of E. autumnata display peaks but populations all over the outbreak range fluctuate in synchrony. This concept assumes that the peaks at most localities are so low that they do not lead to visible defoliation and easily remain unnoticed. In this scenario, populations are able to start recovery a few years after the crash, i.e., at the time of the mitigation of detrimental delayed density-dependent factors, such as delayed inducible resistance of the host plant or parasitism. In that case, the same factors that lead to crashes also explain the periodicity of cyclic fluctuations. According to the regional cyclicity scenario, different factors can be important in different phases of the cycle. The key is to identify the factors that tend to produce outbreaks with a periodicity of about 10 years. Initiation of the increase phase seems to coincide with maxima in sunspot activity, but causal connections remain unclear. Climatic factor(s) associated with the solar cycle could contribute to the large-scale geographic synchrony.

Biosynthetic origin of carbon-based secondary compounds: cause of variable responses of woody plants to fertilization?

Summary. We propose that variation in the responses of carbon-based secondary compounds to fertilization in woody plants has a biosynthetic cause. The synthesis of phenylpropanoids and derived compounds (e.g., condensed tannins) competes directly with the synthesis of proteins, and therefore with plant growth, because of a common precursor, phenylalanine. In contrast, the biosynthesis of terpenoids and of hydrolyzable tannins proceeds presumably without direct competition with protein synthesis. Therefore, accelerated plant growth induced by fertilization may cause a reduction in concentrations of phenylpropanoids but may affect less or not at all the levels of other classes of secondary compounds. A meta-analysis based on fertilization experiments with 35 woody plant species supported the predicted differences fertilizing significantly decreased concentrations of phenylpropanoids but not of terpenoids or hydrolyzable tannins.