Incorporating biotic interactions in phenology

Shifts in the timing of phenological events such as bird migration, leaf unfolding, flowering, and insect emergence, across many taxa and ecosystems are a result of climate change. Phenological shifts depend on different factors and species-specific sensitivity to changes in meteorological variables, therefore when phenological shifts occur within the trophic network we might expect phenological mismatches between interlinked species to occur as a result of climate change, with potential negative effects for biodiversity, ecosystems and the trophic network. However, the availability of data that show how species interactions are affected by climate change is scarce and unified criteria are still lacking on the methodologies studying phenology and biotic interactions. The presented extensive review on the topic allowed the identification of four broad categories of studies that have explored biotic interactions within phenology research and revealed that phenological studies of seasons other than spring are very scarce. This unbalance was also found within biotic interactions research, where mutualistic and obligate interactions, trophic interactions and networks were the main types receiving the most attention compared to other types (i.e., facilitation, competition). Researchers have commonly used co-existence among species as a proxy for biotic interactions, in many cases without any direct measurement of such interactions, while a lack of formal examination in most studies exploring phenological mismatches in response to climate change was also often identified. A conceptual framework was developed for the inclusion of phenology in the study of biotic interactions that categorises research into the conceptualisation and modelling of biotic interactions. Conceptualisation explores phenological data, types of interactions, and the spatiotemporal dimensions, which all determine the representation for biotic interactions within the modelling framework, and the type of models that are applicable. Emerging opportunities were also identified to investigate biotic interactions in phenology research, including spatially and temporally explicit species distribution models as proxies for phenological events and the combination of novel technologies (e.g., acoustic recorders, telemetry data) to quantify interactions. This conceptual framework was applied to a case of study in Ireland, investigating the relevance of different meteorological drivers (maximum and minimum temperature and total precipitation) in the phenology and co-existence of several species linked through the trophic network. Phenological trends towards an earlier phenology in Ireland were identified in terms of advanced date of arrival of migrant birds, first flight of butterflies and moths and green-up (start of the growing season) over the period 2008-2018. A novel analysis developed by van de Pol et al. (2016), the relative sliding time window analyses, was applied in order to identify which meteorological drivers had higher influence on the phenological events of study. Results showed high interannual variability in the time windows at species and group level. We identified common trends between butterflies and moths to show greater influence of temperature time windows when closer to first flight, while in vegetation the opposite pattern was found. Three new indices of phenological change across different trophic levels are presented, these indices allowed to identify potential phenological asynchronies between trophic levels in Ireland and to develop a network of potential interactions based on synchrony among interlinked species