Forest wildflowers bloom earlier as Europe warms: lessons from herbaria and spatial modelling.

Today plants often flower earlier due to climate warming. Herbarium specimens are excellent witnesses of such long-term changes. However, the magnitude of phenological shifts may vary geographically, and the data are often clustered. Therefore, large-scale analyses of herbarium data are prone to pseudoreplication and geographical biases. We studied over 6000 herbarium specimens of 20 spring-flowering forest understory herbs from Europe to understand how their phenology had changed during the last century. We estimated phenology trends with or without taking spatial autocorrelation into account. On average plants now flowered over 6 d earlier than at the beginning of the last century. These changes were strongly associated with warmer spring temperatures. Flowering time advanced 3.6 d per 1°C warming. Spatial modelling showed that, in some parts of Europe, plants flowered earlier or later than expected. Without accounting for this, the estimates of phenological shifts were biased and model fits were poor. Our study indicates that forest wildflowers in Europe strongly advanced their phenology in response to climate change. However, these phenological shifts differ geographically. This shows that it is crucial to combine the analysis of herbarium data with spatial modelling when testing for long-term phenology trends across large spatial scales.

Climate warming changes synchrony of plants and pollinators.

Climate warming changes the phenology of many species. When interacting organisms respond differently, climate change may disrupt their interactions and affect the stability of ecosystems. Here, we used global biodiversity facility occurrence records to examine phenology trends in plants and their associated insect pollinators in Germany since the 1980s. We found strong phenological advances in plants but differences in the extent of shifts among pollinator groups. The temporal trends in plant and insect phenologies were generally associated with interannual temperature variation and thus probably driven by climate change. When examining the synchrony of species-level plant-pollinator interactions, their temporal trends differed among pollinator groups. Overall, plant-pollinator interactions become more synchronized, mainly because the phenology of plants, which historically lagged behind that of the pollinators, responded more strongly to climate change. However, if the observed trends continue, many interactions may become more asynchronous again in the future. Our study suggests that climate change affects the phenologies of both plants and insects and that it also influences the synchrony of plant-pollinator interactions.

Spring understory herbs flower later in intensively managed forests.

Many organisms respond to anthropogenic environmental change through shifts in their phenology. In plants, flowering is largely driven by temperature, and therefore affected by climate change. However, on smaller scales climatic conditions are also influenced by other factors, including habitat structure. A group of plants with a particularly distinct phenology are the understory herbs in temperate European forests. In these forests, management alters tree species composition (often replacing deciduous with coniferous species) and homogenizes stand structure, and as a consequence changes light conditions and microclimate. Forest management should thus also affect the phenology of understory herbs. To test this, we recorded the flowering phenology of 16 early-flowering herbs on 100 forest plots varying in management intensity, from near-natural to intensely managed forests, in central and southern Germany. We found that in forest stands with a high management intensity, such as Norway spruce plantations, the plants flowered on average about 2 weeks later than in unmanaged forests. This was largely because management also affected microclimate (e.g., spring temperatures of 5.9°C in managed coniferous, 6.7 in managed deciduous, and 7.0°C in unmanaged deciduous plots), which in turn affected phenology, with plants flowering later on colder and moister forest stands (+4.5 d per -1°C and 2.7 d per 10% humidity increase). Among forest characteristics, the percentage of conifers had the greatest influence on microclimate, but also the age, overall crown projection area, structural complexity and spatial distribution of the forest stands. Our study indicates that forest management alters plant phenology, with potential far-reaching consequences for the ecology and evolution of understorey communities. More generally, our study demonstrates that besides climate change other drivers of environmental change, too, can influence the phenology of organisms.

Using herbaria to study global environmental change.

During the last centuries, humans have transformed global ecosystems. With their temporal dimension, herbaria provide the otherwise scarce long-term data crucial for tracking ecological and evolutionary changes over this period of intense global change. The sheer size of herbaria, together with their increasing digitization and the possibility of sequencing DNA from the preserved plant material, makes them invaluable resources for understanding ecological and evolutionary species' responses to global environmental change. Following the chronology of global change, we highlight how herbaria can inform about long-term effects on plants of at least four of the main drivers of global change: pollution, habitat change, climate change and invasive species. We summarize how herbarium specimens so far have been used in global change research, discuss future opportunities and challenges posed by the nature of these data, and advocate for an intensified use of these 'windows into the past' for global change research and beyond.