Ecosystem functioning in urban grasslands: The role of biodiversity, plant invasions and urbanization

Abstract

Urbanization is driving the transformation of natural and rural ecosystems worldwide by affecting both the abiotic environment and the biota. This raises the question whether urban ecosystems are able to provide services in a comparable way to their non-urban counterparts. In urban grasslands, the effects of urbanization-driven ecological novelty and the role of plant diversity in modulating ecosystem functioning have received little attention. In this study, we assessed the influence of biodiversity, abiotic and biotic novelty on ecosystem functioning based on in situ measurements in non-manipulated grasslands along an urbanization gradient in Berlin (Germany). We focused on plant aboveground biomass (AGB), intrinsic water-use efficiency (iWUE) and 15N enrichment factor (Δδ15N) as proxies for biomass production, water and N cycling, respectively, within grassland communities, and tested how they change with plant biogeographic status (native vs alien), functional group and species identity. Approximately one third of the forb species were alien to Berlin and they were responsible for 13.1% of community AGB. Community AGB was positively correlated with plant-species richness. In contrast, iWUE and Δδ15N were mostly determined by light availability (depicted by sky view factor) and urban parameters like the percentage of impervious surface or human population density. We found that abiotic novelty potentially favors aliens in Berlin, mainly by enhancing their dispersal and fitness under drought. Mainly urban parameters indicating abiotic novelty were significantly correlated to both alien and native Δδ15N, but to AGB and iWUE of alien plants only, pointing to a stronger impact of abiotic novelty on N cycling compared to C and water cycling. At the species level, sky view factor appeared to be the prevailing driver of photosynthetic performance and resource-use efficiency. Although we identified a significant impact of abiotic novelty on AGB, iWUE and Δδ15N at different levels, the relationship between species richness and community AGB found in the urban grasslands studied in Berlin was comparable to that described in non-urban experimental grasslands in Europe. Hence, our results indicate that conserving and enhancing biodiversity in urban ecosystems is essential to preserve ecosystem services related to AGB production. For ensuring the provision of ecosystem services associated to water and N use, however, changes in urban abiotic parameters seem necessary.

Fig 1. Geographical location of the 20 grasslands studied in Berlin (Germany) in 2017.

Fig 2. Contribution of plant groups to grassland community above ground biomass.

(A) Average contribution of plant functional groups with different biogeographic status to community aboveground biomass in the 20 studied grasslands (AGB_C), where grasslands are ordered from left to right according to increasing species richness and (B) average percentage contribution of plant functional groups and plants with different biogeographic (i.e. graminoids (AGB_G), forbs (AGB_F) and legumes (AGB_L), natives (AGB_N), aliens (AGB_A), native graminoids (AGB_NG), alien graminoids (AGB_AG), native forbs (AGB_NF), alien forbs (AGB_AF), native legumes (AGB_NL), alien legumes (AGB_AL)) to AGB_C across the studied grasslands in Berlin in summer 2017.

Fig 3. Intrinsic water use efficiency and ¹⁵N enrichment factor of different plant groups.

(A) Average intrinsic water use efficiency (iWUE) of plants with different biogeographic status and (B) plants belonging to different functional groups; (C) average ¹⁵N enrichment factor (Δδ¹⁵N) of plants with different biogeographic status and (D) plants belonging to different functional groups across the studied grasslands in Berlin in summer 2017. Box plots indicate interquartile ranges (areas within a box), medians (horizontal line within the box), 25th and 75th percentiles (lower and upper box boundaries), and 5th and 95th percentiles (whiskers above and below the box); outliers are shown as solid circles. Significant differences between plant with different biogeographic status (p < 0.05, Mann-Whitney test) or functional groups (p < 0.05, Kruskal-Wallis test with pairwise multiple comparisons) are indicated by letters.

Fig 4. Seasonal difference in ecophysiological parameters at the species level.

(A) Photosynthetic rate (A), (B) transpiration rate (E), (C) instantaneous water-use efficiency (instant-WUE), (D) stomatal conductance (g_s), (E) effective quantum yield of electron transport through photosystem II (ΔF/F_m′), (F) maximum potential quantum yield of electron transport through photosystem II (F_v/F_m), (G) ratio of the intercellular to ambient CO₂ concentration (c_i/c_a), (H) Intrinsic water use efficiency (iWUE) and (I) ¹⁵N enrichment factor (Δδ¹⁵N) in spring (grey) and summer (white) 2017. Box plots indicate interquartile ranges (areas within a box), medians (horizontal line within the box), 25th and 75th percentiles (lower and upper box boundaries), and 5th and 95th percentiles (whiskers above and below the box). Significant differences between seasons (p < 0.05, Mann-Whitney test) are indicated by asterisks: ** p<0.01 and *** p<0.001).

Fig 5. Photosynthetic light response curves.

(A) Effective quantum yield of electron transport through photosystem II, ΔF/F_m′ in Calamagrostis epigejos and (B) Plantago lanceolata; (C) apparent photosynthetic electron transport rate, ETR in C. epigejos and (D) Pl. lanceolata. Shown data are single values from chlorophyll fluorescence measurements on 3 to 9 individuals in spring (solid lines) and summer (dotted lines) in Berlin grasslands in 2017. Regression lines were fitted with an exponential decay function for ΔF/F_m′ (y = a (1- e^(-bx)) (A, B) and with an exponential rise to max function for ETR: y = ae ^(-bx) (C, D). The numbers at the horizontal and vertical lines in the lower panels indicate apparent maximal electron transport rate (ETR_max) and PPDF at saturation of photosynthesis (PPDF_sat), respectively. Numbers at the horizontal lines in the upper panels indicate ΔF/F_m′ at PPDF_sat.

Fig 6. Partial dependence plots for the strongest predictor selected by random forest models for aboveground biomass, intrinsic water use efficiency and ¹⁵N enrichment factor.

(A) for the whole plant community (AGB_C, iWUE_C, Δδ¹⁵N_C), (B) natives (AGB_N, iWUE_N, Δδ¹⁵N_N), (C) aliens (AGB_A, iWUE_A, Δδ¹⁵N_A), (D) graminoids (AGB_G, iWUE_G, Δδ¹⁵N_G) and (E) forbs (AGB_F, iWUE_F, Δδ¹⁵N_F) in the studied grasslands in Berlin in summer 2017. The full description of variables is given in Table 1. Note that a partial dependency plot is used not to confirm the effect size but the association pattern including effect direction, since due to normalization, the ranges of y-axes do not directly correspond to the range of the variable. Plots for AGB_G and iWUE_F were not computed either because only one predictor was selected or because of lack of explanatory power (see text for more information).

Fig 7. Biodiversity-ecosystem functioning in urban grasslands.

Relationship between species richness and (A) community aboveground biomass (AGBC), where color scale indicates the percentage of aliens in each plot, (B) community intrinsic water use efficiency (iWUEC) and (D) community ¹⁵N enrichment factor (Δδ¹⁵N_C) in Berlin grasslands in summer 2017. Given values are the average at each grassland. (C) Slopes of significant regression models reflecting the relationship between min-max normalized species richness and min-max normalized AGBC in Berlin novel grasslands in summer 2017 and in multiple European experimental grasslands (extracted from (36), S1 Dataset).