Nutrient-mediated tree growth responses are governed by internal resource allocation: intra-organ water-carbon trade-offs and inter-organ carbon concentration gradient

Abstract

Nutrient deposition is reshaping forest productivity, yet the physiological mechanisms linking nitrogen (N) and phosphorus (P) enhancement to tree growth remain incompletely resolved. We propose that internal resource allocation strategies—specifically intra-organ trade-offs between water and carbohydrate resources and inter-organ carbohydrate concentration gradient—mediate nutrient-driven tree growth responses. Using a long-term fertilization experiment in subtropical Cunninghamia lanceolata plantations, we measured relative water content (RWC) and traditional resource concentrations [soluble sugar (SS) concentration; starch (ST) concentration] during drought season. We rank-transformed RWC, SS, and ST within each organ type across all samples. Intra-organ water-carbon trade-offs were quantified as two normalized ratios: ln(RWCrank/SSrank) for RWC:SS and ln(RWCrank/STrank) for RWC:ST, where higher values indicate greater solute dependence for turgor maintenance or greater ST storage volume fraction, respectively. The inter-organ carbon concentration gradient was quantified as differences in SS or ST between leaves and twigs (SSleaf-twig, STleaf-twig) and between absorptive roots and transport roots. We demonstrated three key nutrient-specific responses: (i) N addition promoted transport root ln(RWCrank/SSrank) while enhancing leaf ln(RWCrank/STrank), amplifying STleaf-twig; (ii) P addition reduced leaf and twig ln(RWCrank/SSrank); and (iii) combined N+P addition reduced twig ln(RWCrank/SSrank), while increasing leaf and twig ln(RWCrank/STrank). These reorganization patterns had direct growth consequences: while traditional resource concentrations explained 26.0% of growth variation, incorporating derived attributes increased explanatory power by 43.5% (to 37.3% total variance explained). Notably, the twig ln(RWCrank/STrank) emerged as the single strongest growth predictor, where N+P induced ST dominance correlated with enhanced growth rate. N enrichment enhanced SS dominance in transport roots, a pattern that may occur at the expense of stem growth. Our results establish an internal resource allocation framework that mechanistically links nutrient-mediated carbon management patterns to forest productivity under global change, revealing how N+P co-enrichment synergistically optimizes carbon resource storage and utilization beyond single-nutrient effects.