Multitrophic plant insect interactions in dependence of belowground processes

Abstract

Most ecologists acknowledge that plants are subject to complex interactions between both below- and aboveground dwelling animals. However, these complex interactions are seldomly investigated simultaneously. In a set of experiments we studied the effects of decomposers, root herbivores and leaf herbivores on plant growth, flower visitation, herbivores and their parasitoids. Our results show that belowground communities affect not only plant growth but also aboveground processes, including plant-pathogen, plant-pollinator and even plant-herbivore-parasitoid interactions. Leaf herbivory reduced plant height, shoot mass, and delayed the onset of flowering of Sinapis arvensis. Furthermore, it negatively affected flowering traits suggesting a decrease in plant attractiveness to pollinators. However, we could not identify any effect of leaf herbivory on flower visitors. Flower visitors were positively influenced by the presence of root herbivores in two independent experiments. This strongly suggests that root herbivores can have an impact on the pollination of Sinapis arvensis. However, we could not find any effect of root herbivory on the measured floral traits (anther size, nectar production, petal size, number of flowers). Although in most experiments the experimental plants faced major herbivore-induced growth changes, plant reproduction (seed set and weight per plant) was similar between herbivory treatments and control plants. These results show the ability of Sinapis arvensis to compensate for leaf and root herbivory. Accordingly, reduced size, delayed start of flowering, reduced flowering period or reduced flower visitation could not be used to predict plant fitness in this annual, cross-pollinated herb. In contrast, decomposers increased plant growth and plant fitness (measured as the number of seeds produced), indicating that mustard may benefit from nutrients provided by decomposers, regardless whether plants are attacked by root herbivores or leaf herbivores, or both simultaneously. We found that the indiv idual presence of either root herbivores or decomposers resulted in increased aphid abundance, demonstrating that the same aboveground plant-insect interaction can be released by different belowground processes. Enhanced aphid densities caused higher numbers of parasitoids. Our results give an insight in the effects of belowground organisms on aboveground organisms and it gets clear that many aboveground patterns could be driven by belowground processes through the plant. Using a different approach we investigated the significance of farming practices in modifying the effects of soil organisms on aboveground systems. Plant biomass in soil from conventional farms exceeded that of soils from organic farms, presumably due to the higher nutrient input in the conventional farming system. Soil defaunation likely mobilized nutrients that increased plant growth. Aphid abundance and Septoria infection was reduced by defaunation but only in organic soils. This suggests that soil organisms in organic farming systems are more important for the augmentation of aphids and the infection rate by Septoria than in conventional systems. Hence, farming practice appears to modify the effect of soil organisms on aboveground organisms, and soil organisms played a major role in organic farming systems. Further, the results indicate that soil organisms may modify higher trophic levels (aphid and pathogen infection) without significantly affecting lower trophic levels (plant growth). Until recently the role of soil biota in modifying the attractiveness of plants to herbivores, pathogens and pollinators has been largely ignored. Particularly in natural habitats where plant species interact with each other, soil biota may play a key role in modifying the insect community associated with plants. Future work needs to focus upon more complex systems consisting of plants and soil biota in different spatial and temporal contexts to better understand the functioning of terrestrial systems.