A temporal shift in resource allocation facilitates flowering before leaf out and spring vessel maturation in precocious species

Abstract

Premise of the Study New growth in the spring requires resource mobilization in the vascular system at a time when xylem and phloem function are often reduced in seasonally cold climates. As a result, the timing of leaf out and/or flowering could depend on when the vascular system resumes normal function in the spring. This study investigated whether flowering time is influenced by vascular phenology in plants that flower precociously before they have leaves. Methods Flower, leaf, and vascular phenology were monitored in pairs of precocious and non‐precocious congeners. Differences in resource allocation were quantified by measuring bud dry mass and water content throughout the year, floral hydration was modelled, and a girdling treatment completed on branches in the field. Key Results Precocious flowering species invested more in floral buds the year before flowering than did their non‐precocious congeners, thus mobilizing less water in the spring, which allowed flowering before new vessel maturation. Conclusions A shift in the timing of resource allocation in precocious flowering plants allowed them to flower before the production of mature vessels and minimized the significance of seasonal changes in vascular function to their flowering phenology. The low investment required to complete floral development in the spring when the plant vascular system is often compromised could explain why flowers can emerge before leaf out.

Reconciling competing hypotheses regarding flower–leaf sequences in temperate forests for fundamental and global change biology

“…For example, the reproductive phenology of species that produce flower from axilary buds set in the previous season may be more independent of leaf phenology than for species with determinate growth (Borchert, 1983; Rathcke & Lacey, 1985; van Schaik et al ., 1993). Previous work also has suggested that differences in xylem anatomy may constrain spring phenology (Lechowicz, 1995), although Savage (2019) determined that for 20 spring‐flowering species, reproductive buds were hydrated primarily by the phloem, suggesting the flowering‐first FLS may be independent of xylem activity.…”

“…This may be particularly important at the high latitudes where selection on flowering time is strong as a result of a shorter growing season (Munguia‐Rosas et al ., 2011). Recent work from Savage (2019) demonstrated that spring flower phenology is less constrained by prior phenological events than leaf phenology, which would allow selection to drive flowering into the early season, producing the flowering‐first FLS. With this hypothesis there is no specific advantage to a species flowering before or after leafing; all that matters is its absolute flowering time.…”

“…One phenological relationship that has long received scientific interest (see Robertson, 1895) and, recently, increased attention (e.g. Gougherty & Gougherty, 2018; Savage, 2019) is the flower‐leaf phenological sequence (FLS) of temperate deciduous woody plants. In a typical model of plant life history, vegetative growth precedes reproduction.…”

“…Long‐term datasets also demonstrate high within‐species variability in FLSs. Despite recent advances in understanding the physiology and evolution of FLSs (Gougherty & Gougherty, 2018; Savage, 2019), most analyses have not directly addressed this variability – potentially slowing progress in predicting how FLSs will respond to climate change. While the literature provides some general correlations between flower and leaf phenology (e.g.…”

Coordination of spring vascular and organ phenology in deciduous angiosperms growing in seasonally cold climates

“…Because of the presumed functional dependency of developing new organs on the vascular system, some authors have suggested that there might be a relationship between leaf phenology (the timing of leaf out) and wood anatomy that is driven by differences in the timing of vascular reactivation in the spring (Lechowicz, 1984; Wang et al ., 1992). However, most studies in the last 20 yr have focused either on bud, leaf and flower phenology or on vascular system development and its regulation by internal and external drivers; it is less common for studies to link multiple organs and/or physiological processes (except see Suzuki et al ., 1996; Kudo et al ., 2015; Gričar et al ., 2017; Lavrič et al ., 2017; Savage, 2019). Thus, today many questions remain regarding whether there is a strong relationship between whole‐organ phenology (bud, leaf and flower phenology) and that of the vascular system in the spring.…”