Kai Ruohomäki

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.

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.

Realized fecundity in Epirrita autumnata (Lepidoptera: Geometridae) : relation to body size and consequences to population dynamics

Potential fecundity of Epirrita autumnata females is strongly correlated with pupal weight. Adult feeding weakly increases fecundity but does not eliminate its dependence on body size. Daily numbers of eggs laid are positively correlated with body size. However, night minimum temperature is the main determinant of oviposition rate under fluctuating natural temperatures. Adult mortality was estimated to be low in a subarctic forest in autumn. Based on these results, we constructed a simulation model predicting oviposition rate and realized fecundity under given weather conditions. The model indicates that expected realized fecundity strongly depends on female size also under field conditions. This causes selection for large body (abdomen) size which is a probable reason for lack of fine-tuned adult behaviour in E. autumnata. Factors acting during the adult stage can be considered relatively unimportant in the demography of this species; populations are largely regulated by biotic interactions of the larval stage, involving delayed density-dependence. This may be an explanation for population cycles, characteristic for this species.

Tree species diversity influences herbivore abundance and damage: meta-analysis of long-term forest experiments

Plant monocultures are commonly believed to be more susceptible to herbivore attacks than stands composed of several plant species. However, few studies have experimentally tested the effects of tree species diversity on herbivory. In this paper, we present a meta-analysis of uniformly collected data on insect herbivore abundance and damage on three tree species (silver birch, black alder and sessile oak) from seven long-term forest diversity experiments in boreal and temperate forest zones. Our aim was to compare the effects of forest diversity on herbivores belonging to different feeding guilds and inhabiting different tree species. At the same time we also examined the variation in herbivore responses due to tree age and sampling period within the season, the effects of experimental design (plot size and planting density) and the stability of herbivore responses over time. Herbivore responses varied significantly both among insect feeding guilds and among host tree species. Among insect feeding guilds, only leaf miner densities were consistently lower and less variable in mixed stands as compared to tree monocultures regardless of the host tree species. The responses of other herbivores to forest diversity depended largely on host tree species. Insect herbivory on birch was significantly lower in mixtures than in birch monocultures, whereas insect herbivory on oak and alder was higher in mixtures than in oak and alder monocultures. The effects of tree species diversity were also more pronounced in older trees, in the earlier part of the season, at larger plots and at lower planting density. Overall our results demonstrate that forest diversity does not generally and uniformly reduce insect herbivory and suggest instead that insect herbivore responses to forest diversity are highly variable and strongly dependent on the host tree species and other stand characteristics as well as on the type of the herbivore.

Delayed Inducible Resistance in Mountain Birch in Response to Fertilization and Shade

Delayed inducible resistance (DIR) is triggered by artificial or herbivore-caused foliar damage and is manifested as decreased performance of herbivore generation(s) feeding on the trees subsequent to the generation during which the damage took place. DIR is associated with increase in concentrations of foliage phenolics and decrease in nitrogen. The growth-differentiation balance hypothesis, and the carbon-nutrient balance (CNB) hypothesis contained in it, claim that DIR is caused by nutritional stress after defoliation of trees growing on nutrient-poor soils. In these environments, nutrient uptake limits plant growth more strongly than does photosynthesis; that is, carbon-based secondary metabolites (e.g., phenolics) are prone to accumulate. According to the CNB hypothesis, an excess of limiting nutrient(s) or reduced photosynthetic rate should lead to elimination of DIR. We tested this using same-aged Betula pubescens ssp. tortuosa trees of five open-pollinated families growing in a common arboretum in northernmost Finland. In addition to unmanipulated control trees, we had three nutritional treatments during three successive growth seasons: N-fertilization, PK-fertilization adding all nutrients except N, and shading to decrease carbon assimilation. Half of the trees in each treatment were artificially defoliated (50% leaf area) in the second study year, one year before the growth trial with geometrid (Epirrita autumnata) larvae. Tree growth measurements showed that N is the growth-limiting nutrient in our study area. N-fertilization and shading of the trees affected foliage chemistry generally as proposed by the CNB hypothesis. For example, they reduced foliar concentrations of total phenolics and condensed tannins. The birch families differed significantly in foliage chemistry, suggesting genetic differences, but the differences were not associated with fertilizations, shading, or defoliation of the trees. Contrary to fertilizing-shade treatments, changes in leaf chemistry and E. autumnata performance caused by defoliation were not consistent with the CNB hypothesis. For example, defoliation caused significant DIR irrespective of N-fertilization or shading. There were no significant differences among the birch families in performance of the moth larvae or in effects of fertilization, shade, or defoliation on larval performance. These responses to defoliation contrast with those of some other studies, especially those on the Betula resinifera-Rheumaptera hastata system in Alaska, which provide clear support for the CNB as an explanation of DIR. We find methodological differences to be an unlikely explanation for the different results but are unable to propose any single mechanism that will explain the diverse plant responses.

Delayed induced changes in the biochemical composition of host plant leaves during an insect outbreak

Abstract In birch, Betula pubescens, herbivore-induced delayed induced resistance (DIR) of defoliated trees may cause a strong reduction in the potential fecundity of a geometrid folivore Epirrita autumnata. In this study, we examined the biochemical basis of DIR in birch leaves during a natural outbreak of E. autumnata. A set of experimental trees was defoliated at four sites by wild larvae in the peak year of the outbreak, whereas control trees were protected from defoliation by spraying with an insecticide. The biochemical composition of leaves was analysed in the following year and, although the DIR response was weak during this outbreak, causing less than a 20% reduction in the potential fecundity of E. autumnata, some consistent relationships between defoliation, biochemistry and pupal mass of E. autumnata suggested a general biochemical basis for the defoliation-induced responses in birch leaves. Total concentrations of nitrogen, sugars and acetone-insoluble residue (e.g. cell wall polysaccharides, cell-wall-bound phenolics, protein, starch, lignin and hemicellulose) were consistently lower, and total concentrations of phenolics, especially of gallotannins and soluble proanthocyanidins, were higher in the leaves of trees defoliated in the previous year than in those protected from defoliation. The capacity of tannins to precipitate proteins correlated with contents of gallotannins, and was highest in defoliated trees. The pupal mass of E. autumnata showed a strong, positive correlation with concentrations of nitrogen and sugars, and a negative correlation with the acetone-insoluble residue and gallotannins in foliage. Correlations with other measured biochemical traits were weak. The correlation coefficients between biochemical traits and pupal mass consistently had similar signs for both defoliated and insecticide–sprayed trees, suggesting that variation in leaf quality due to defoliation in the previous year was based on similar biochemical traits as variation for other reasons. We suggest that DIR is associated with reduced growth activity of leaves, and may be seen as a delay in the biochemical maturation of leaves in defoliated trees. This explains the high concentration of gallotannins in defoliated trees, a characteristic feature of young leaves. However, the lower content of nitrogen and the higher content of soluble proanthocyanidins in defoliated trees are traits usually characterising mature, not young, leaves, indicating defoliation-induced changes in chemistry in addition to modified leaf age. Our results emphasise the importance of understanding the natural changes in chemistry during leaf maturation when interpreting defoliation-induced changes in leaf biochemistry.

Oviposition Choices of Epirrita autumnata (Lepidoptera: Geometridae) in Relation to Its Eruptive Population Dynamics

We found that oviposition behaviour is indiscriminative in Epirrita autumnata (Lepidoptera, Geometridae), a species known as a periodical pest of birch forests in north-emmost Europe. Oviposition in E. autumnata was not suppressed by low host quality, injured host leaves, or the presence of conspecific eggs or sex pheromone. Oviposition was not limited to host plants, whereas physical characteristics of the substrate were decisive in oviposition site selection. Therefore, the oviposition behaviour of E. autumnata is typical for an outbreak species and certainly contributes to the eruptive population dynamics of the species. Young larvae are responsible for finding a host plant but their capacity for host selection is rather restricted ; larval dispersal cannot compensate for indiscriminative oviposition. Indiscriminative oviposition should not be seen as a phylogenetic constraint in E. autumnata ; more probably, it results from selection in favour of large body size in females which reduces their flying ability.

LEAF VALUE: EFFECTS OF DAMAGE TO INDIVIDUAL LEAVES ON GROWTH AND REPRODUCTION OF MOUNTAIN BIRCH SHOOTS

Most damage caused by invertebrate herbivores is local and limited in extent and may therefore seem inconsequential. However, in addition to providing photosynthates to the whole plant, individual leaves may preferentially feed local sinks, including pri- mordial meristems that develop later. For leaf damage, this may have local consequences and, in the case of preformed meristems, may result in time lags. To investigate such consequences and to determine the degree of independence among shoot modules, we studied shoot traits after damage to individual leaves in long shoots and vegetative and generative short shoots of field-growing mountain birch, Betula pubescens subsp. czere- panovii (Orlova) Hamet-Ahti. For short shoots, the results suggest that, due to the catkin, generative shoots have a higher priority in resource use than vegetative shoots. The overwinter survival of vegetative short shoots was decreased after their young leaves had been damaged early in the previous season. Otherwise, there were no significant effects of leaf damage on vegetative shoots. In generative shoots, leaf damage affected size and reproduction instead of survival. Because leaf damage significantly decreased leaf size-in the generative shoots in the posttreatment year, leaves presumably competed with the catkin for resources within the shoot. Damage also reduced the catkin mass and the mean seed mass in the treatment year. In the post- treatment year, catkin mass and total seed mass were reduced by the treatments, but dif- ferences in the number of seeds and mean seed mass did not quite reach significance. The treatments had no effects on leaf mass of neighbors of vegetative or generative shoots in the treatment year or in the posttreatment year. In the treatment year, removal of long shoot leaves from a growing long shoot did not affect growth of the long shoot, indicating that such growth was supported by resources external to the shoot. However, local effects were evident in the posttreatment year: leaf mass decreased in shoots that developed from axillary buds in long shoots whose supporting leaves had been clipped in the previous year. Consequently, removal of individual leaves may have local effects on shoot survivorship, reproduction, and growth. Timing of damage and shoot type modified the consequences of local leaf damage, and there were no consistent responses for all situations. Due to the limited extent of damage, the effects were not likely to result from nutrient loss due to damage. Instead, consequences of local leaf damage could be explained largely by effects on local sinks and meristem primordia.

Components of male fitness in relation to body size in Epirrita autumnata (Lepidoptera, Geometridae)

Abstract. 1. The effect of body size on different components of male fitness was studied for Epirrita autumnata, a geometrid known for its eruptive population dynamics. Body size is the main determinant of female fecundity in this species.

HIGH LARVAL PREDATION RATE IN NON‐OUTBREAKING POPULATIONS OF A GEOMETRID MOTH

We conducted a two-year predator-exclusion study to assess the magnitude and timing of larval predation in non-outbreaking populations of a geometrid moth, Epirrita autumnata. Laboratory-produced newly hatched larvae were placed on the experimental trees which were assigned to five treatments within two larval densities: (1) all predators, including parasitoids, excluded by mesh bag, (2) birds excluded by cage, (3) ants excluded by glue ring, (4) birds and ants excluded, and (5) control without any predator exclusion. Thereafter, larvae were censused every 3–4 d throughout the five-instar larval period. Mortality of E. autumnata larvae in these populations was high and mostly due to natural enemies. In control trees, only ∼10% of larvae survived, while survival was ∼90% in mesh bags preventing all natural enemies. Bird exclusion significantly improved larval survival, as survival was almost three times higher in trees with cages than in those without cages. On the other hand, ant exclusion did not have any overall effects on larval survival, mostly because ants were only detected in about half of the trees without glue rings. Larvae survived longer in high-density trees from which ants were excluded, but the effect was masked by high mortality, unrelated to ant exclusion, in the late larval season. The results suggest that the effect of ant predation on survival of E. autumnata larvae may be spatially restricted and not important at a larger scale. The same result applies for crab spiders, as they caused high mortality in ∼20% of the study trees. Our results emphasize the importance of considering the spatial scale as well as assessing the impact of multiple predators in order to detect predators affecting survival at the population level. Exclusion of all predation had a significantly stronger effect on larval survival than exclusion of birds alone. Further, mortality was highest during the late larval period, when parasitoids emerge. Thus, a large proportion of larval mortality was most likely due to parasitism. Our results suggest that predation by passerine birds and parasitism may contribute to maintenance of low E. autumnata densities by strong suppression of the number of larvae entering the pupal stage.