Eco-evolutionary dynamics of above-belowground interactions in the city

The objective of this thesis was to explore the eco-evolutionary consequences of urbanisation on aboveground and belowground biota communities. Four model plant systems across urban- rural gradients in Belgium: Arabidopsis thaliana, Jacobaea vulgaris, Senecio inaequidens, and Trifolium repens were incorporated, and aboveground arthropods and belowground nematodes were chosen as useful indicators of responses to urbanisation. We firstly revealed the ecological patterns of arthropod and nematode community structure and attempted to identify possible mechanisms behind the ecological changes by linking to plant chemical defences in Chapter 2 and 3. Afterwards common garden experiments were conducted in Chapter 4 to evaluate genetic variation in the phenotypic divergence in plant-herbivore interactions along the urbanisation gradient observed in the Chapter 2. Chapter 2 investigated the interaction network of arthropods, nematodes and secondary metabolites in Arabidopsis thaliana, Jacobaea vulgaris and Senecio inaequidens across the urban-rural gradient in the city of Ghent. Our results showed that urbanisation significantly affected community composition of both arthropods and nematodes in the three plant species, but its effects on community characteristics were often species-specific. In Senecionae species, species richness of arthropods slightly declined along with urbanisation but their diversity did not change. Abundances of total arthropods significantly increased in A. thaliana and J. vulgaris with the increasing levels of urbanisation yet decreased in S. inaequidens. Besides, urban J. vulgaris experienced a higher abundance of herbivores but fewer predators, which is likely attributed to the positive effects of urban warming on herbivores overriding the top-down control. Conversely, urban S. inaequidens had lower numbers of herbivores, likely due to strong bottom-up control through increased concentrations of secondary metabolites although this mechanism seemed to generate a high cost in terms of plant fitness. Urban soil surrounding J. vulgaris was less dominated by fungi, implying increased levels of human disturbance. In Chapter 3, we compared the patterns of nematode communities associated with white clover (Trifolium repens L.) and linked these to a defence trait (HCN) along urban-rural gradients in the cities of Antwerp and Ghent. The results showed that the frequency of HCN within populations significantly decreased with urbanisation in both cities. Urbanisation was markedly correlated with nematode community composition in Antwerp but not with abundances of different feeding guilds, except that plant feeder abundance responded differently to urbanisation depending on the HCN frequency. Urban soils in Antwerp were less bacterially dominated, indicating slow nutrient cycling and a high capacity to retain nutrients. In Ghent, however, urbanisation was unrelated to nematode community structure but differently affected abundances of feeding guilds depending on the clovers’ HCN frequencies. Abundances of plant feeders, fungal feeders, bacterial feeders and microbivores, and total nematodes did not change with HCN frequency in little urbanized areas, but decreased with increasing HCN frequencies in more urbanized locations. The abundance of combined predators and omnivores increased with urbanisation independent of HCN frequencies. These results indicated that plant defence could also help disentangle the effects of urbanisation on soil communities. In Chapter 4, we firstly evaluated phenotypic variation in traits of Arabidopsis thaliana and associated herbivore resistance along an urbanisation gradient, and found that aphid densities significantly increased with urbanisation while plant size did not change, suggesting phenotypic divergence in plant-herbivore interactions. We then assessed genetic variation in these traits when introducing a chewing herbivore (caterpillars of Pieris brassicae) to F1 and a sucking herbivore (the aphid Myzus persicae) to F1 and F2 offspring of field-collected plants. F1 offspring of urban mothers had an increased size, tolerance against P. brassicae and root biomass allocation but lower trichome density, while caterpillar growth rate did not change. They together suggest that higher growth capacity of roots and tolerance to leaf-chewing herbivores were found as an urban adaptation. Plant genotypes of urban origin had smaller inflorescences and lower fitness in the lab, but aphid densities and population growth rate were similar. Seed production was more strongly reduced by M. persicae in urban offspring of the first generation, but this effect disappeared in second-generation offspring. This suggests that the urban adaptations of rosette growth and caterpillar tolerance come at a cost of lower overall fitness as well as lower aphid tolerance, although the latter seems to be a maternal effect. Generally, this thesis highlights that urbanisation is driving eco-evolutionary dynamics across above and belowground biota communities. Plant defence mechanisms are shown to play important roles in regulating species interactions and shaping community structures. Further, this mechanism may play a role in promoting plant invasion. Finally, the properties of cities are emphasized to greatly affect the direction and strength of eco-evolutionary dynamics. More observational and experimental studies are necessary to generalise the patterns of eco- evolutionary dynamics driven by urbanisation