Context-dependent response of the trait-related flowering pattern in sub-Mediterranean grasslands

The timing of flowering is a key component of community assembly, being critical to competition for resources or avoidance of stress. In grasslands, the functional differentiation of species inside the community drives the flowering pattern, so that each phenological phase relates to a specific set of functional traits. Although the temporal dimension is an important factor in determining species assemblages, how plant traits respond to the heterogeneity of resource availability has been identified mostly through observations of spatial variations. To understand the role of temporal variation of resources in the species assemblage processes, we performed a trait-based phenological study in sub-Mediterranean grasslands (central Apennines). We counted flowering shoots of species of three plant communities along a productivity gradient in 1 m × 1 m plots, during the growing season. We calculated the mean proportions of flowering shoots of species sharing traits related to resource acquisition and stress tolerance and analysed their relations with soil temperature, soil humidity, and canopy height, comparing their temporal patterns using indicator species analysis, redundancy analysis, variation partitioning, and generalized linear modeling. Our results highlighted that the temporal gradient, which synthesizes the variation trend of the environmental conditions and vegetation structure of the grassland communities during the growing season, is a major factor in determining the trait-based flowering pattern. In the early flowering phases, there is a predominance of species with strategies of slow resource acquisition and storage but rapid growth rate, while in the periods with optimal environmental conditions, the blooming species are the ones with strategies of slow growth rate and more efficient resource acquisition, conservation, and use. No common patterns emerged among plant communities for the late flowering species from mid-summer to autumn. We also observed that the shift in soil temperature, soil relative humidity and canopy height among communities reflected a modification over time of the flowering expression of some traits, such as leaf anatomy and persistence, type of storage organ, and vertical space occupation. Harsh conditions filter species with resource-retaining strategies, drought resistance, and avoidance ability, whereas in productive conditions, competition for light promotes the coexistence of species with dissimilar resource acquisition strategies on a fine spatial scale. This seems to substantiate the hypothesis that the functional response to the seasonal variation in environmental conditions largely retraces the modifications, at the community level, of the functional composition across spatial resource gradients. Our results show that the amplitude of the environmental fluctuations influences the type and number of strategies positively filtered by the system. Environmental fluctuations in time influenced the trait-related flowering pattern more in highly productive conditions (having the highest differences in soil relative humidity and canopy height between spring and summer) than in less productive ones. In fact, in productive conditions, the phenological responses to environmental fluctuations are mostly related to traits that limit competition with dominant species by spatial niche segregation (vegetative propagation, vertical space occupation, and plant height) and to species that fit their life cycle to the variation of environmental conditions, through different life and leaf span. Conversely, such traits showed weaker trends in the driest community, where the flowering pattern was less dependent on temporal fluctuations of environmental conditions. These findings are consistent with the fluctuation niche theory, based on the different growth/phenological response of species to the variation of resource availability over time.