Nutrient enrichment, biodiversity loss, and consequent declines in ecosystem productivity

Abstract

Anthropogenic drivers of environmental change often have multiple effects, including changes in biodiversity, species composition, and ecosystem functioning. It remains unknown whether such shifts in biodiversity and species composition may, themselves, be major contributors to the total, long-term impacts of anthropogenic drivers on ecosystem functioning. Moreover, although numerous experiments have shown that random losses of species impact the functioning of ecosystems, human-caused losses of biodiversity are rarely random. Here we use results from long-term grassland field experiments to test for direct effects of chronic nutrient enrichment on ecosystem productivity, and for indirect effects of enrichment on productivity mediated by resultant species losses. We found that ecosystem productivity decreased through time most in plots that lost the most species. Chronic nitrogen addition also led to the nonrandom loss of initially dominant native perennial C4 grasses. This loss of dominant plant species was associated with twice as great a loss of productivity per lost species than occurred with random species loss in a nearby biodiversity experiment. Thus, although chronic nitrogen enrichment initially increased productivity, it also led to loss of plant species, including initially dominant species, which then caused substantial diminishing returns from nitrogen fertilization. In contrast, elevated CO2 did not decrease grassland plant diversity, and it consistently promoted productivity over time. Our results support the hypothesis that the long-term impacts of anthropogenic drivers of environmental change on ecosystem functioning can strongly depend on how such drivers gradually decrease biodiversity and restructure communities.

Keywords: biogeochemistry; community ecology.

Fig. 1.

Effects of N addition on productivity and plant diversity in natural grasslands. (A) Nutrient enrichment promoted productivity (F_7,176 = 54.5, P < 2.2 × 10⁻¹⁶), but this effect substantially diminished over time (F_1,176 = 36.9, P = 7.48 × 10⁻⁹), especially in the plots that received the most fertilizer (N × Year: F_7,176 = 2.8, P = 0.0096). (B) Nutrient enrichment also decreased the number of species (F_7,176 = 72.4, P < 2.2 × 10⁻¹⁶), and this effect became increasingly negative over time (F_1,176 = 92.1, P < 2.2 × 10⁻¹⁶) at all rates of N addition (N × Year: F_7,176 = 1.6, P = 0.13). (C and D) Declines in the number of species were positively associated with declines in productivity. That is, productivity decreased most in plots that lost the most species over time (F_1,7 = 42.9, P = 0.00032, R² = 0.86) (D). Differences in biomass (A) or number of species (B) were quantified between enriched and control plots, with positive biomass differences indicating that enriched plots were more productive, and with negative species differences indicating that enriched plots had fewer species, than control plots. Arrows in C point from values observed during 1982, the first year of N addition, toward values observed during 2008, the most recent year that all fields were sampled. Changes in D were quantified over the same time interval. In D, for comparison, we also show the relationship between planted species richness and productivity in a nearby biodiversity experiment during 2008 (gray triangles and dashed line). Both lines in D are linear fits of the response on the ln-transformed predictor. Treatments C (control) and 0 differ in that non-N nutrients were added to the latter but not the former.

Fig. 2.

(A) Global environmental changes may indirectly influence ecosystem functioning by changing biodiversity. (B–F) Results from the BioCON experiment. Net effects on grassland plant productivity (B), which can be split into direct (C) and indirect (D) components, which can subsequently be split into effects of N and CO₂ on observed diversity (E) and the effect of planted diversity on productivity (F). The positive effect of N enrichment on productivity diminished over time (P = 0.0188) (B), partly because N enrichment slightly decreased observed plant species diversity (P < 0.0001) (E) (Table S1). In contrast, there was no significant temporal trend in the positive effect of elevated CO₂ on productivity (P = 0.77) (B), partly because elevated CO₂ did not significantly influence observed plant species diversity (P = 0.49) (E) (Table S1). Effects in B, E, and F were estimated by linear mixed effects models (Table S1); effects in C and D were estimated by a structural equation model. Differences in biomass (B) or number of grassland plant species (E) were quantified between enriched and ambient plots, with positive biomass differences indicating that enriched plots were more productive, and with negative species differences indicating that enriched plots had fewer species, than ambient plots. Biomass differences for diversity effects (F) were quantified between plots planted with 16 and 4 grassland plant species, with positive values indicating that diverse plots were most productive.

Fig. 3.

(A and B) BioCON plots planted with the most grassland plant species exhibited the largest declines in the net effect of N enrichment on productivity (N × Year × Diversity: F_{1, 2056} = 20.52, P < 0.0001; Table S1) (A), and the largest negative effects of N enrichment on observed diversity (N × Year × Diversity: F_{1, 2056} = 7.79, P = 0.0053; Table S1) (B). Linear mixed effects models were used to estimate effects (Table S1). Differences in biomass (A) or number of species (B) were quantified between enriched and ambient plots, with positive biomass differences indicating that enriched plots were more productive, and with negative species differences indicating that enriched plots had fewer species, than ambient plots.