Long-term physiological insights of cone production as related to carbon isotope fractionation in stone pine forests of northern Spain

Variation in life-history and ecophysiological traits has key ecological significance in plants, in which environmental changes play a central role throughout their life cycles. Stone pine (Pinus pinea L.) is one of the most characteristic species of the Mediterranean basin that is able to grow under harsh, limiting conditions and is typically defined as a masting species. Considering the high economical value associated with edible nut production, the masting habit of stone pine has been a main concern for forest management of the species. Here, we investigate the masting mechanism through characterization of temporal changes in tree ring-width (TRW), ecophysiological (cellulose Δ¹³C and δ¹⁸O) and cone yield patterns for five monospecific stands in north-central Spain. The regional positive (r = 0.41, SE = 0.25) and negative (r = –0.89, SE = 0.49) relationships involving tree growth vs. Δ¹³C and δ¹⁸O, respectively, suggest drought impairing carbon uptake via stomatal regulation for water saving occurring in the area during the period of 1960–2016. Increasingly positive relationships between TRW and Δ¹³C indicate intensifying impacts of drought on tree performance over time. By analyzing Δ¹³C–yield interannual dynamics, we found variable coupling of cone production with leaf-level gas exchange during the 4-year reproductive cycle of the stone pine. Particularly, the strongly positive relationships between Δ¹³C and yield with a 3-year lag, corresponding to strobili development and pollination, vanished and became non-significant in the recent decades. Thus, weather conditions during conelet emergence are not driving anymore cone production, which initially was sink-limited. In contrast, the relationships between Δ¹³C and a 1-year lagged yield, i.e. when cone enlargement and seed maturation occur, largely increased over the study period running from nearly zero (1960–1989 period) to above 0.50 (1987–2016 period) indicating a recent source limitation of reproduction driven by a harsher climate. Our results provide evidence that, although cone yield does not impose a penalty on aboveground biomass increments, it is becoming progressively limited by warming-induced effects of drought on tree ecophysiological performance.