Foliar fungi on urban trees are important for tree health, biodiversity and ecosystem functioning. Yet, we lack insights into how urbanization influences foliar fungal communities. We created detailed maps of Stockholm region’s climate and air quality and characterized foliar fungi from mature oaks (Quercus robur) across climatic, air quality and local habitat gradients. Fungal richness was higher in locations with high growing season relative humidity, and fungal community composition was structured by growing season maximum temperature, NO2 concentration and leaf litter cover. The relative abundance of mycoparasites and endophytes increased with temperature. The relative abundance of pathogens was lowest with high concentrations of NO2 and particulate matter (PM2.5), while saprotrophs increased with leaf litter cover. Our findings show that urbanization influences foliar fungi, providing insights for developing management guidelines to promote tree health, prevent disease outbreaks and maintain biodiversity within urban landscapes.

Interactions between plants and herbivores are central in most ecosystems, but their strength is highly variable. The amount of variability within a system is thought to influence most aspects of plant-herbivore biology, from ecological stability to plant defense evolution. Our understanding of what influences variability, however, is limited by sparse data. We collected standardized surveys of herbivory for 503 plant species at 790 sites across 116° of latitude. With these data, we show that within-population variability in herbivory increases with latitude, decreases with plant size, and is phylogenetically structured. Differences in the magnitude of variability are thus central to how plant-herbivore biology varies across macroscale gradients. We argue that increased focus on interaction variability will advance understanding of patterns of life on Earth.

Plants interact with a multitude of microorganisms and insects, both below- and above ground, which might influence plant metabolism. Despite this, we lack knowledge of the impact of natural soil communities and multiple aboveground attackers on the metabolic responses of plants, and whether plant metabolic responses to single attack can predict responses to dual attack. We used untargeted metabolic fingerprinting (gas chromatography-mass spectrometry, GC-MS) on leaves of the pedunculate oak, Quercus robur, to assess the metabolic response to different soil microbiomes and aboveground single and dual attack by oak powdery mildew (Erysiphe alphitoides) and the common oak aphid (Tuberculatus annulatus). Distinct soil microbiomes were not associated with differences in the metabolic profile of oak seedling leaves. Single attacks by aphids or mildew had pronounced but different effects on the oak leaf metabolome, but we detected no difference between the metabolomes of healthy seedlings and seedlings attacked by both aphids and powdery mildew. Our findings show that aboveground attackers can have species-specific and non-additive effects on the leaf metabolome of oak. The lack of a metabolic signature detected by GC-MS upon dual attack might suggest the existence of a potential negative feedback, and highlights the importance of considering the impacts of multiple attackers to gain mechanistic insights into the ecology and evolution of species interactions and the structure of plant-associated communities, as well as for the development of sustainable strategies to control agricultural pests and diseases and plant breeding.

Plants interact with a large diversity of microbes and insects, both below and above ground. While studies have shown that belowground microbes affect the performance of plants and aboveground organisms, we lack insights into how belowground microbial communities may shape interactions between aboveground pathogens and insects. We investigated how soil microbiomes and aboveground organisms affect plant growth and development, and whether differences in soil microbiomes influence interactions between aboveground organisms. We conducted a growth-chamber experiment with oak seedlings Quercus robur growing in three soils with similar abiotic soil properties but with distinct natural soil microbiomes. Seedlings were subjected to single or dual attack by powdery mildew Erysiphe alphitoides and aphids Tuberculatus annulatus, either in the presence or absence of prior attack by a free-feeding caterpillar Phalera bucephala. Soil microbiomes were associated with differences in seedling height, and seedlings with multiple aboveground organisms had more but smaller leaves than healthy seedlings. The soil microbiome affected the severity of powdery mildew infection, and mediated the impact of co-occurring aboveground organisms on aphid population size. Our study highlights that plant performance is affected by natural soil microbiomes as well as aboveground organisms, and that natural soil microbiomes can affect interactions between pathogens and insects. These findings are important to understand species interactions in natural systems, as well as for practical applications, such as manipulation of soil microbiomes to manage agricultural pests and diseases.

• Plant pathogen traits, such as transmission mode and overwintering strategy, may have important effects on dispersal and persistence, and drive disease dynamics. Still, we lack insights into how life-history traits influence spatiotemporal disease dynamics.
• We adopted a multifaceted approach, combining experimental assays, theory and field surveys, to investigate whether information about two pathogen life-history traits – infectivity and overwintering strategy – can predict pathogen metapopulation dynamics in natural systems. For this, we focused on four fungal pathogens (two rust fungi, one chytrid fungus and one smut fungus) on the forest herb Anemone nemorosa.
• Pathogens infecting new plants mostly via spores (the chytrid and smut fungi) had higher patch occupancies and colonization rates than pathogens causing mainly systemic infections and overwintering in the rhizomes (the two rust fungi). Although the rust fungi more often occupied well-connected plant patches, the chytrid and smut fungi were equally or more common in isolated patches. Host patch size was positively related to patch occupancy and colonization rates for all pathogens.
• Predicting disease dynamics is crucial for understanding the ecological and evolutionary dynamics of host–pathogen interactions, and to prevent disease outbreaks. Our study shows that combining experiments, theory and field observations is a useful way to predict disease dynamics.

The world is rapidly urbanizing, thereby transforming natural landscapes and changing the abundance and distribution of organisms. However, insights into the effects of urbanization on species interactions, and plant–pathogen interactions in particular, are lacking. We investigated the effects of urbanization on powdery mildew infection on Quercus robur at continental and within-city scales. At the continental scale, we compared infection levels between urban and rural areas of different-sized cities in Europe, and investigated whether plant traits, climatic variables and CO₂ emissions mediated the effect of urbanization on infection levels. Within one large city (Stockholm, Sweden), we further explored whether local habitat features and spatial connectivity influenced infection levels during multiple years. At the continental scale, infection severity was consistently higher on trees in urban than rural areas, with some indication that temperature mediated this effect. Within Stockholm city, temperature had no effect, while local accumulation of leaf litter negatively affected powdery mildew incidence in one out of three years, and more connected trees had lower infection levels. This study is the first to describe the effects of urbanization on plant–pathogen interactions both within and among cities, and to uncover the potential mechanisms behind the observed patterns at each scale. 

1. Plants are attacked by a large diversity of pathogens. These pathogens can affectplant growth and fitness directly but also indirectly by inducing changes in the host plant that affect interactions with beneficial and antagonistic insects. Yet, we lack insights into the relative importance of direct and indirect effects of pathogens on their host plants, and how these effects differ among pathogen species.

2. In this study, we examined four fungal pathogens on the wood anemone Anemone nemorosa. We used field observations to record the impacts of each pathogen species on plant growth and fitness throughout the season, and experimental hand pollination and insect feeding trials to assess whether fitness impacts were mediated by pathogen-induced changes in plant–pollinator and plant–herbivore interactions.

3. Three out of four pathogens negatively affected plant size, and pathogens differed strongly in their effect on plant architecture. Infected plants had lower fitness, but this effect was not mediated by pollinators or herbivores. Even so, two out of four pathogens reduced herbivory on anemones in the field, and we found negative effects of pathogen infection on herbivore preference and performance in feeding trials.

4. Synthesis. Our results are of broader significance in two main respects. First, we demonstrated that pathogens negatively affected plant growth and fitness, and that the magnitude of these effects varied among pathogen species, suggesting that pathogens constitute important selective agents that differ in strength. Second, direct effects on plant fitness were more important than effects mediatedby beneficial and antagonistic insects. In addition, although we did not detect insect-mediated effects on plant fitness, the negative effects of some pathogens on herbivore preference and performance indicate that pathogen communities influence the distribution and abundance of herbivores.

Plants interact with an astonishing diversity of insects and microorganisms. Both above- and belowground, plants are attacked by herbivores and pathogens, and interact with mutualists such as pollinating insects and beneficial microorganisms. Insects and microorganisms interacting with plants may also affect one another when sharing the same host, leading to direct and indirect interactions between plants, microorganisms and insects. These interactions may have important ecological and evolutionary consequences for all involved species, and interaction outcomes might be dependent on the timing of the interaction as well as the abiotic and biotic context. Thus, in order to predict the outcome of plant–microbe–insect interactions, we need insights into how interactions vary over time and space and how these are influenced by biotic context, from the perspective of all involved species.

In this thesis, my overarching aim was to investigate when and where species interact, and to examine the influence of relative timing and biotic context on the outcomes of plant–microbe–insect interactions from a multi-species perspective. I focussed on two study systems, the pedunculate oak Quercus robur and the wood anemone Anemone nemorosa, and the insects and microorganisms associated with these plants. First, I looked into the drivers behind the spatiotemporal distribution of several fungal pathogens on plants. Specifically, I investigated whether life history traits of pathogens were linked to their metapopulation dynamics. Second, I examined the relative importance of direct and insect-mediated effects of these pathogens on plant performance. Third, I conducted multifactorial growth chamber experiments to investigate performance impacts of interactions from the perspectives of all involved species (plant, insect and pathogen). Lastly, I investigated the influence of time of attacker arrival, early arriving attackers and soil microbial communities on interaction outcomes.

I found that life history traits of pathogens were related to some aspects of metapopulation dynamics. These pathogens had direct, negative impacts on plant growth and fitness, while I did not find evidence for insect-mediated effects. For the multifactorial experiments, I observed some impacts of multiple attackers (pathogens and insects) on plant growth, though plants were mostly tolerant to attack. Attackers that shared a host could affect each other’s performances, with effects mostly being asymmetric, though the interaction outcomes were dependent on the time of arrival, early arriving attackers and soil microbial communities.

In conclusion, my findings show that i) life history traits may influence where pathogen species occur in space and time, that ii) direct effects of pathogens on plant fitness can dominate insect-mediated effects, and that iii) the outcome of species interactions is often asymmetric and dependent on relative timing as well as biotic context. By identifying some of the drivers behind, and consequences of, plant–microbe–insect interactions, this thesis contributes to the development of a predictive framework for species interactions.

As the world becomes more and more urbanized, it is increasingly important to understand the impacts of urban landscapes on biodiversity. Urbanization can change local habitat factors and decrease connectivity among local habitats, with major impacts on the structure of natural food webs. However, most studies have focused on single species, or compared rural to urban habitats, which do not inform us on how to design and manage cities to optimize biodiversity. To understand the local and spatial drivers of ecological communities within urban landscapes, we assessed the relative impact of local habitat factors (sunlight exposure and leaf litter) and spatial connectivity on an oak-associated herbivore community within an urban landscape. From the local habitat factors, leaf litter but not sunlight exposure was related to herbivore species richness, with leaf litter contributing to the maintenance of high species richness on isolated trees. Guilds and species differed strongly in their response to local habitat factors and connectivity, resulting in predictable variation in insect community composition among urban oaks. Taken together, our study shows an interactive effect of local and spatial factors on species richness and species composition within an urban context, with guild- and species-specific life histories determining the response of insects to urban landscapes. To maintain biodiversity in the urban landscape, preserving a dense network of local habitats is essential. Moreover, allowing leaf litter to accumulate can be a simple, cost-effective conservation management practice.

Seasonal life history events are often interdependent, but we know relatively little about how the relationship between different events is influenced by the abiotic and biotic environment. Such knowledge is important for predicting the immediate and evolutionary phenological response of populations to changing conditions. We manipulated germination timing and shade in a multi-factorial experiment to investigate the relationship between spring and autumn phenology in seedlings of the pedunculate oak, Quercus robur, and whether this relationship was mediated by natural colonization of leaves by specialist fungal pathogens (i.e., the oak powdery mildew complex). Each week delay in germination corresponded to about 2 days delay in autumn leaf senescence, and heavily shaded seedlings senesced 5–8 days later than seedlings in light shade or full sun. Within seedlings, leaves on primary-growth shoots senesced later than those on secondary-growth shoots in some treatments. Path analyses demonstrated that germination timing and shade affected autumn phenology both directly and indirectly via pathogen load, though the specific pattern differed among and within seedlings. Pathogen load increased with later germination and greater shade. Greater pathogen load was in turn associated with later senescence for seedlings, but with earlier senescence for individual leaves. Our findings show that relationships between seasonal events can be partly mediated by the biotic environment and suggest that these relationships may differ between the plant and leaf level. The influence of biotic interactions on phenological correlations across scales has implications for understanding phenotypic variation in phenology and for predicting how populations will respond to climatic perturbation.