Carbon starvation as a mechanistic explanation for the gradual decline of savanna ground-layer species under tree encroachment

BACKGROUND: Tropical savannas worldwide have been experiencing woody encroachment, i.e., the rapid increase in density and biomass of woody plants in formerly open environments. In savannas, this process is primarily driven by the absence of fire, which allows woody species to outcompete the herbaceous layer, ultimately leading to losses on ground-layer biodiversity. SCOPE: Causes of savanna encroachment are well documented. However, the mechanisms behind how encroachment exclude typical ground-layer species are not clearly comprehended, and typically classified as a simplistic effect of "shade intolerance". Here we briefly review the encroachment phenomenon, its causes and effects in open savanna vegetation. To develop a mechanistic hypothesis for the gradual decline of ground-layer vegetation, we synthesised leaf trait and physiological data from ground-layer plants. Encroachment changes canopy cover and the light environment, affecting the richness and diversity of ground-layer species and reflecting the progressive transition from open to closed-canopy environments. This pattern may be related to the inability of ground-layer plants to maintain a positive carbon balance under shaded conditions, a physiological state equivalent to carbon starvation. Although species can show significant leaf plasticity in response to light conditions, they depend on carbohydrate reserves stored in underground organs to maintain vital processes when photosynthetic capacity declines. These reserves, however, are finite, ultimately leading to individual mortality and species exclusion. CONCLUSIONS: Shade intolerance alone offers a simplistic explanation to ground layer exclusion under encroachment. We propose that encroachment leads to a physiological response in ground-layer plants changing sink-source aspects in a process analogous to the carbon starvation hypothesis. We suggest that analysing primary metabolism and carbon-based traits is essential to quantify plant persistence and determine the physiological thresholds under encroachment.