Physiological causes of the age-related decline in pine forest productivity

Background/Question/Methods

A decline in forest Net Primary Production (NPP) with increasing age is one of the most consistent observations in production ecology, but the mechanism causing this decline is still debated. The classic hypothesis (Odum 1969, Science) was that increasing autotrophic respiration (R_a) causes a smaller fraction of Gross Primary Production (GPP) to be available for NPP. However, subsequent research failing to find an increase in R_a lead to the hypothesis that GPP declines with age, causing NPP and R_a to decline (Ryan et al. 1997, Advances in Ecological Research). Previous attempts to unravel the causal nature of the NPP decline have been hampered by the difficulties involved in measuring R_a or GPP on an annual timestep, and in the autocorrelated nature of how GPP is often measured (GPP = NPP + R_a). Here, we use a sap-flow based approach to measure GPP independently of NPP across a chronosequence of warm-temperate loblolly pine (Pinus taeda) forests. Previous biometric research in this chronosequence has demonstrated a 65% decline in pine NPP with increasing age.  
Results/Conclusions

Canopy-weighted stomatal conductance was highly correlated with gas exchange measurements of leaf-level conductance (y = 1.18*x + 0.01, r² = 0.94, p < 0.001), suggesting that the sap-flow method provided accurate measurements of leaf conductance. Summer pine photosynthesis summed from May to September declined linearly from 1300 gC m^-2 in the 15-year-old forest to 600 gC m^-2 in the 97-year-old forest. Thus, there was a strong decline in pine GPP of sufficient magnitude to explain the decline in pine NPP. Consistent with the hypothesis that increasing hydraulic limitation caused the decline in pine GPP, the following was observed with increasing age: light saturated photosynthesis declined, leaf- and canopy-level stomatal conductance declined, the concentration of CO₂ inside leaf airspaces declined, stomatal limitation increased, needle specific leaf area decreased, and the ratio of sapwood area to leaf area increased. We conclude that as these pine trees age and increase in height, photosynthetic rates become increasingly limited by stomatal closure, and the resulting reduced C-uptake leads to reduced NPP. This supports the conceptual model of Ryan et al. (1997, Advances in Ecological Research) and challenges the earlier hypothesis of Odum (1969, Science).