Global pattern and controls of biological nitrogen fixation under nutrient enrichment: A meta-analysis.

Biological nitrogen (N) fixation (BNF), an important source of N in terrestrial ecosystems, plays a critical role in terrestrial nutrient cycling and net primary productivity. Currently, large uncertainty exists regarding how nutrient availability regulates terrestrial BNF and the drivers responsible for this process. We conducted a global meta-analysis of terrestrial BNF in response to N, phosphorus (P), and micronutrient (Micro) addition across different biomes (i.e, tropical/subtropical forest, savanna, temperate forest, grassland, boreal forest, and tundra) and explored whether the BNF responses were affected by fertilization regimes (nutrient-addition rates, duration, and total load) and environmental factors (mean annual temperature [MAT], mean annual precipitation [MAP], and N deposition). The results showed that N addition inhibited terrestrial BNF (by 19.0% (95% confidence interval [CI]: 17.7%-20.3%); hereafter), Micro addition stimulated terrestrial BNF (30.4% [25.7%-35.3%]), and P addition had an inconsistent effect on terrestrial BNF, i.e., inhibiting free-living N fixation (7.5% [4.4%-10.6%]) and stimulating symbiotic N fixation (85.5% [25.8%-158.7%]). Furthermore, the response ratios (i.e., effect sizes) of BNF to nutrient addition were smaller in low-latitude (<30°) biomes (8.5%-36.9%) than in mid-/high-latitude (≥30°) biomes (32.9%-61.3%), and the sensitivity (defined as the absolute value of response ratios) of BNF to nutrients in mid-/high-latitude biomes decreased with decreasing latitude (p ≤ 0.009; linear/logarithmic regression models). Fertilization regimes did not affect this phenomenon (p > 0.05), but environmental factors did affect it (p < 0.001) because MAT, MAP, and N deposition accounted for 5%-14%, 10%-32%, and 7%-18% of the variance in the BNF response ratios in cold (MAT < 15°C), low-rainfall (MAP < 2,500 mm), and low-N-deposition (<7 kg ha-1  year-1 ) biomes, respectively. Overall, our meta-analysis depicts a global pattern of nutrient impacts on terrestrial BNF and indicates that certain types of global change (i.e., warming, elevated precipitation and N deposition) may reduce the sensitivity of BNF in response to nutrient enrichment in mid-/high-latitude biomes.