Ecosystem functioning in urban grasslands: The role of biodiversity, plant invasions and urbanization
Authors:
Gabriela Onandia aff001; Conrad Schittko aff002; Masahiro Ryo aff002; Maud Bernard-Verdier aff002; Tina Heger aff002; Jasmin Joshi aff002; Ingo Kowarik aff002; Arthur Gessler aff002
Authors place of work:
Research Platform “Data”, Leibniz Centre for Agricultural Landscape Research (ZALF), Müncheberg, Germany
aff001; Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), Berlin, Germany
aff002; Biodiversity Research and Systematic Botany, University of Potsdam, Potsdam, Germany
aff003; Institute of Biology, Freie Universität Berlin, Berlin, Germany
aff004; Division of Zoology, Freie Universität Berlin, Berlin, Germany
aff005; Restoration Ecology, Technical University of Munich, Freising, Germany
aff006; Institute for Landscape and Open Space, HSR Hochschule für Technik, Rapperswil, Switzerland
aff007; Department of Ecology, Ecosystem Science and Plant Ecology, Technische Universität Berlin, Berlin, Germany
aff008; Department of Forest Dynamics, Swiss Federal Research Institute for Forest, Snow and Landscape Research WSL, Birmensdorf, Switzerland
aff009; Department of Environmental Systems Science, ETH Zurich, Zurich, Switzerland
aff010
Published in the journal:
PLoS ONE 14(11)
Category:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0225438
Summary
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.
Keywords:
Species diversity – Biodiversity – Urban ecosystems – Urban ecology – Grasslands – Invasive species – Urban environments – Ecosystem functioning
Introduction
Increasing human population and urban sprawl are driving the fast transformation of natural and rural environments into urban ecosystems worldwide [1]. Over the past six decades, 25% of the global population has moved from rural into urban settlements and this trend is expected to continue [2]. Urbanization encompasses significant changes in all components of urban ecosystems and their functioning [3], such as the so-called urban heat island effect [4], higher concentrations of heavy metals in the soil and soil compaction [5–7] increased atmospheric nitrogen deposition [8], habitat fragmentation and isolation [9] as well as the development of transportation networks that favor the dispersal of alien plants [10, 11]. Urbanization is also a powerful driver of change to biodiversity patterns, associated with filtering species according to their pre-adaptation to urban environments [12–14]. While alien plant species are frequently found in different urban settings, particularly in novel urban ecosystems [15], cities can also harbor a considerable richness of native plant species [12, 16]. However, urbanization has been also linked to a loss of biodiversity, ecological homogenization and changes in community composition, including a higher proportion of alien species pre-adapted to novel habitats [17–20] and species compositions that cannot be found in near-natural environments.
Consequently, species in urbanized settings face situations to which they have not been exposed during their evolutionary history. Urbanization leads to the transformation of (near-)natural into novel urban ecosystems that prevail in many cities and can be characterized by both novel habitat configurations and novel species assemblages without analogues to natural landscapes [18]. These conditions thus can be characterized as ‘ecologically novel’ [21], and ‘ecological novelty’ in this sense can be seen as an overarching conceptual framework to address the complex eco-evolutionary consequences of anthropogenically induced changes for organisms and ecosystems. In the following, we use the term ‘abiotic novelty’ to characterize environmental conditions that differ from near-natural grassland conditions typical for a particular area. ‘Biotic novelty’ refers to the presence of species, and thus interaction partners, that have not been present in the area in historic times (i.e. alien species).
Grasslands in rural settings provide a wide variety of relevant ecosystem services such as microclimate regulation, water flow regulation and nutrient cycling [22]. Grassland vegetation supports the sequestration of carbon dioxide and soil formation through primary production and modulates hydrological flows by fluctuations in its water use. Moreover, through the acquisition and storage of nitrogen (N), grassland vegetation plays a major role in terrestrial nitrogen cycling. Worldwide, grasslands make up a considerable area in cities. In Berlin, for instance, they cover as much as 5% of the city area [23]. Urban grasslands encompass meadows and lawns in domestic gardens, parks, vacant land, remnants of rural landscapes, and areas along transportation corridors [23–28]. The role of urban grasslands for biodiversity conservation has gained increasing attention in the last decade [23, 24, 29, 30]. Yet in urban grasslands, the role of plant diversity in modulating ecosystem functioning, including proxies such as aboveground biomass (AGB) production or resource use has received little attention [24, 31].
A positive relationship between biodiversity and ecosystem functioning (often exemplified by AGB and less frequently by plant water or N use) has been widely described in non-urban experimental grasslands resembling natural or agricultural grassland communities [22, 32–39]. This relationship has been also found in experimental urban grassland assemblages resembling North America turfgrass communities [40] and experimental grassland assemblages resembling the soil and vegetation on abandoned urban sites in Berlin [41]. However, it remains unknown whether the positive link between biodiversity and ecosystem functioning prevails in urban grasslands where biodiversity and other environmental factors are not manipulated (i.e. non-experimental grasslands)[42]. Ecosystem functioning in urban grasslands is critically understudied, with only a few studies focusing on urban lawns as a subgroup of urban grasslands (e.g. [20, 40, 43, 44]). Furthermore, studies comparing ecosystem functions of urban vs non-urban grasslands are rare (but see [43, 44]). One of these few studies has shown that in the Front Range of Colorado (USA), lawns were more productive than native grasslands, likely as a result of increased irrigation or fertilization associated to management [44].
Along with biodiversity, both biotic novelty (the presence of alien species) and abiotic novelty (altered environmental conditions) can be expected to ultimately affect ecosystem services by modifying ecosystem functioning. For example, strongly altered urban soils may be less productive than rural soils; and a high abundance of alien plants may modulate biomass production or nutrient cycling–with negative effects on ecosystem services [45]. Plant invasions have been often associated with negative effects on native plant and animal species, ecological functions and ecosystem services [45–47]. For instance, a global meta-analysis of field studies assessing the impact of alien plants revealed that overall species diversity declined but primary production increased, probably due to a sampling effect [47]. Yet, invasion effects on ecological functions are clearly understudied in urban environments (e.g., [31, 46]). Given the high abundance of alien plants in urban environments, and particularly in novel urban ecosystems [15], enhanced insights into biodiversity-ecosystem functioning relationships in cities are important for urban planning and biodiversity conservation, and ultimately for human well-being.
Nonetheless, the available information on the role of ecological novelty in influencing ecosystem functioning proxies such as AGB production, intrinsic water-use efficiency (iWUE) and N cycling in urban grasslands is limited. Furthermore, the relative role of biotic versus abiotic factors, and their significance in comparison to biodiversity as a driver of ecosystem functioning is unclear. Evidence on the key drivers of various ecosystem properties compiled for a wide range of aquatic and terrestrial ecosystems is diverse ([36] and references therein): biotic changes were generally found to have an equally important effect on ecosystem properties than abiotic changes [48]. For instance, in boreal forests, changes in microclimate (i.e. decreased heat flux into the soil) induced by moss cover may modulate permafrost stability in a comparable way to environmental change. Conversely, abiotic conditions may sometimes offset the effects of species richness on ecosystem processes, as shown for instance by a theoretical modelling study revealing that abiotic conditions mask the effect of plant species richness on plant productivity [49]. Such ambiguity may be due to different mechanisms acting upon different groups of plant species, such as functional groups or native versus alien species, or different mechanisms acting during different periods of the growing season.
Despite the fact that the performance of individual species, or functional groups of species, might ultimately determine ecosystem level functioning (e.g. [50, 51]), current knowledge on species-specific responses to biodiversity and ecological novelty [52] and on seasonal variations in such response is scarce, especially in the context of urban grassland research. In this regard, the combined estimation of multiple photosynthetic parameters as well as leaf stable isotope composition can provide insights into the physiological mechanisms controlling plant individual´s performance and AGB production, especially when measured over the course of the growing season [53]. Chlorophyll fluorescence, for instance, reflects the plant ability to put up with abiotic stress factors and indicates the damage level of the photosynthetic apparatus [54], while leaf C isotope composition reflects the average intrinsic water use efficiency throughout the time period during which the organic matter assessed was formed [55].
Based on the positive relationship between diversity and ecosystem functioning found in numerous experimental grasslands and semi-natural grasslands, namely between diversity and AGB production [22, 33, 37, 40], diversity and water use [50, 56] as well as diversity and N cycling [57], we hypothesize that species richness is the main controlling factor for plant community AGB, iWUE and N use in urban grasslands, overriding both abiotic and biotic novelty effects. In this study we aim to improve the understanding of the relative importance of biodiversity, abiotic and biotic novelty for the functioning of urban grasslands. To our knowledge, this is the first study to do so based on in situ measurements in non-manipulated urban grasslands. Indeed, previous results based on experimental urban grasslands pointed to the importance of such field assessments [40]. In particular, we aim to:
identify the main factors (i.e. parameters related to biodiversity, abiotic and biotic novelty) driving the variability in AGB, iWUE and N cycling of whole plant communities, plant functional groups and plants with different biogeographic status (native vs alien) across 20 urban grasslands located in Berlin;
assess the biodiversity-ecosystem functioning relationship in the studied urban grasslands and compare it with that found in natural and agricultural grasslands;
test if parameters related to AGB production, iWUE and N use at the species level significantly differ between the mid- and peak growing season and assess the relationship between those parameters and biodiversity, abiotic and biotic novelty in both time periods.
Material and methods
Study area and study system
The study was carried out in Berlin, Germany. Berlin has an area of 891.1 km2 and a population of ≈ 3.6 mio. inhabitants [58]. Mean annual precipitation amounted to 576 mm and mean annual air temperature was 9.9°C for the period from 1981 to 2010 at the central city location of Tempelhof [59]. Our study system is dry grasslands according to the classification of the “Catalogue of Natural Habitats and Species of Appendices I and II of the Habitats Directive in Brandenburg” [60]. Dry grasslands are a vegetation type that spans a range of near-natural to strongly human-influenced sites throughout the city. For this reason, urban dry grasslands had been selected as a model ecosystem within the CityScapeLabs, an experimental platform established by the Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB) with a network of permanent plots for the investigation of biodiversity and ecosystem functioning in urban environments [61]. For this study, we selected a subset of 20 dry grassland plots of 16 m2 that were relatively evenly distributed across the city (Fig 1) and whose surroundings were subject to different levels of urbanization, indicated, e.g. by human population density or percentage of impervious (sealed) surface. These plots comprised several land use types (e.g. parks, cemeteries, forest clearings), but were selected to minimize human management inputs such as fertilization, irrigation and mowing. The parameters related to biodiversity and abiotic novelty at the study sites (with the exception of air temperature and air relative humidity) were provided by the CityScapeLabs, and the degree of biotic novelty of the study sites was calculated based on the CityScapeLabs biodiversity data (see Table 1 for more information).
Biodiversity
Vascular plant diversity was characterized both by taxonomic and functional diversity, estimated as species richness and Rao’s quadratic entropy (Rao´s Q, [62]), respectively. To assess species richness, vegetation surveys were carried out in a 4 x 4 m plot delimited within each of the 20 grasslands between April 18th and May 19th 2017. Based on expert knowledge and region-specific literature [63–65], plant species were classified according to their biogeographic status into native or alien. Species introduced after 1492 (neophytes) were considered ‘alien’, while species introduced before 1492 (archeophytes) and native species were merged into the category ‘native’. Thereafter, the proportion of alien species at each grassland plot was estimated. Rao's quadratic entropy was calculated using Gower distances between species pairs based on twelve plant functional traits: plant height, specific leaf area, life form, flower color, flower class, clonal growth organs, length of dispersal unit, seed mass, leaf area, leaf nitrogen content, nitrogen fixation and mycorrhizal infection [66]. Trait data were extracted from the TRY database [67] and the BiolFlor database [68]. Additionally, the percentage of plot surface covered by moss (moss cover) and litter (litter cover) was visually estimated.
Abiotic novelty
A total number of 22 environmental variables related to abiotic novelty were assessed in the 20 selected dry grasslands plots within the CityScapeLabs (Table 1). Abiotic novelty-related parameters included urban parameters (i.e. human population density, impervious surface, floor area ratio, etc.), climate and soil parameters assumed to be linked to urbanization (i.e. heavy metals in the soil, long-term average air temperature, etc.) as well as habitat continuity (age) and size of dry grassland biotope patch.
The age of the grasslands was assessed by digitizing and georeferencing historical land use maps (i.e. Preußische Uraufnahme (1831–71) and Preußische Neuaufnahme (1927–40)) and intersecting them with the current biotope mapping of Berlin and Brandenburg. Data on size of dry grassland biotope patch, share of grassland, impervious surface, FAR, PopD, RoadD, RailwD, RDist, RailwDist, long-term air T and UrbClim (see Table 1 for parameter description) were extracted from the Geoportal Berlin of the Senate Department for Urban Development and Housing [69]. A mean value for buffer areas of multiple sizes around the biotope patch was calculated for share of grassland, impervious surface, FAR, PopD, RoadD and RailwD using QGIS 2.18.0 [70]. RDist and RailwDist were also calculated using QGIS 2.18.0 as the shortest distance from the grassland plot midpoint to the nearest road or railway, respectively.
To analyze soil parameters (Table 1), 15 subsamples of 30 cm depth were taken with a 1.4 cm stainless steel soil corer in the aforementioned delimited 4 x 4 m plot within each grassland in June 2017, air-dried, sieved (2 mm) and then mixed and homogenized into a single sample. Total soil N (TN) was analyzed by adsorption chromatography [71], whereas soil Cu, Zn, Cd, Pb and Ni were analyzed by inductively coupled plasma optical emission spectrometry (iCAP 6000 Spectrometer, Thermo Fisher Scientific, Dreieich, Germany) following soil extraction using ammonium nitrate solution [72]. Gravimetric soil water content (WC) was determined as % of the soil dry weight by oven drying the samples at 105°C until constant weight.
At each grassland plot, air temperature (AirT) and relative humidity (AirRH) were recorded every 30 minutes at a 20 cm height throughout the growing season (between April 21th and 26th November 26th, 2017) with a data logger (OMEGA, OM-EL-USB-2). Subsequently, the mean AirT and AirRH for the whole growing season was calculated. Due to logger misappropriation, it was not possible to record AirT and AirRH either partly or entirely in 6 plots, where 50–100% of the data were missing. Therefore, we collected missing data from meteorological stations located within 0.36 to 5 km to the plots [73]. At the plots where only part of the data was missing, we confirmed that AirT and AirRH from Weather Underground differed less than 5% and 12%, respectively, from the data recorded with microclimate logger data. Sky view factor (SVF) is a parameter related to the urban heat island phenomenon, with higher values indicating lower long-wave radiation emissions of built surfaces to the sky during the night [74]. SVF was estimated as the share of open sky based on the analyses of images taken using a Canon EOS 700D camera coupled to a circular fisheye (4.5 mm F2.8 EX DC HSM, Sigma) at ≈ 1.5 m height on the plots. Namely, SVF was calculated using the subversion SOLWEIG1D of the SOLWEIG model (version 2015a) [75, 76].
Biotic novelty
The degree of biotic novelty of individual plots was estimated by a biotic novelty index (BNI). The BNI is a compound measure based on a modified version of Rao´s quadratic entropy and designed to quantify the functional ecological novelty of communities [66]. The index captures the functional diversity contributed by novel species recently arrived in the community, weighted by their relative abundance. It is based on two components: the pairwise functional distance between species, see [62, 77]) and a temporal coexistence component that weighs the functional differences between pairs of species based on how long both species have been present in the region. For example, if a given species pair consists of one native and one recently arrived alien species, the trait distance between both will receive a higher weight than the distance between a pair consisting of one native and one earlier arrived alien species. This idea is based on the finding that alien species will gradually become familiar with their interaction partner(s) over time [78–81] which may lead to a decrease of novelty in the community. The temporal coexistence component of the index was calculated from species’ residence times in the Berlin area. For the calculation of the functional diversity component after Rao, we used the same method and traits as described above. More information can be found in the S1 Appendix.
Plant community aboveground biomass and soil collection for isotope analyses
Total standing aboveground biomass (AGB) of the plant community was sampled between July 24th and August 9th 2017 in the 20 selected dry grasslands in Berlin. As grasslands are regularly managed by the local authorities, protective bands were placed around the 4 x 4 m plot in early spring 2017 to prevent mowing prior to sampling. Since the plots had been last mowed in autumn 2016, the AGB collected in late summer 2017 biomass integrated the biomass production throughout the 2017 growing season, including both alive and dead plant parts. Replicate samples (n = 3) were collected by clipping the vegetation to the ground in 20 x 50 cm quadrats randomly selected within each plot [82]. After identification to the genus or species level, the collected plants were classified into three functional groups: legumes (N-fixing dicots), forbs (non-N-fixing dicots) and graminoids (grasses, sedges and rushes). Next, they were separated into biogeographic status classes (native vs alien). Samples were transported to the lab within 6 hours, oven dried at 70°C to constant weight and weighed thereafter (Kern EW 620, Kern & Sohn GmbH, Balingen, Germany). For each plot, the AGB of different plant groups (i.e. graminoids (AGBG), forbs (AGBF) and legumes (AGBL), natives (AGBN) aliens (AGBN), native graminoids (AGBNG), alien graminoids (AGBAG), native forbs (AGBNF), alien forbs (AGBAF), native legumes (AGBNL), alien legumes (AGBAL)) as well as the whole community AGB (AGBC) was calculated as the average of the three replicates within the plot. Following aboveground biomass collection, a soil core of 30 cm depth was extracted with a 5 cm diameter soil core sampler (Wurzelbohrer V2A, Umwelt-Geräte-Technik GmbH, Müncheberg, Germany) at every quadrat replicate (n = 3) within each grassland plot. The upper 10 cm of the soil cores were homogenized, sieved (2 mm mesh size) and oven-dried at 105°C prior to isotope analyses.
Species level gas-exchange and chlorophyll-a fluorescence measurements
In order to assess the effects of biodiversity, abiotic novelty and biotic novelty on AGB production at the species level, we selected two plant species that were relatively common in the study area and belonged to the two dominant functional groups in terms of biomass: the grass Calamagrostis epigejos (L.) Roth and the forb Plantago lanceolata L.. Ecophysiological parameters were measured during two time periods: in spring (mid-growing season), between May 8th and May 19th 2017, and in summer (peak of the growing season), between July 27th and August 9th 2017, simultaneously to the collection of AGB and soil. Whereas in spring we selected individuals that were exclusively present in the 4 x 4 m plot delimited within each grassland, in summer we selected individuals that were also outside the plot in order to obtain a minimum number of replicates. These individuals were located within a distance of 10 m from the plot, in comparable vegetation and soil conditions and thus we do not expect them to be experiencing different conditions from the ones inside the plot. Therefore, the number of plots in which the species were present varied between months, with C. epigejos being present in 13 and 17, respectively, out of the 20 selected grassland plots in spring and summer, respectively, and P. lanceolata occurring in 9 and 12 plots, in spring and summer, respectively. In total, C. epigejos and P. lanceolta co-occurred in 40–55% of the study plots, which covered a comparable gradient of plant species richness, abiotic, and biotic novelty (S1 Table).
The ecophysiological parameters were measured with a portable gas exchange fluorescence system (Walz GFS-3000, Heinz Walz GmbH, Effeltrich, Germany) equipped with a clamp-on leaf chamber of 8 cm2. Gas exchange measurements were carried out mostly on clear sunny days between 09:00 and 16:30 on unshaded, fully expanded mature and healthy leaves from three individuals per species in each plot/grassland. The leaf chamber conditions were set constant to 20°C leaf temperature, 60% relative humidity, 400 ppm CO2 concentration and saturating photosynthetic photon flux density (PPFDsat, 1500 μmol m-2 s-1). Gas exchange parameters were logged after the leaves reached steady-state conditions at saturating PPFD and comprised photosynthetic rate (A, μmol CO2 m-2 s-1), transpiration rate (E, mmol H2O m-2 s-1), stomatal conductance (gs, mol air m-2 s-1) and ratio of the intercellular to ambient CO2 concentration (ci/ca, μmol CO2 μmol-1 CO2). Instantaneous water-use efficiency (instant-WUE, μmol CO2 μmol-1 H2O) was calculated as A/E. Chlorophyll-a fluorescence parameters were measured with a fluorescence Module (LED-Array/PAM-Fluorometer 3055-FL, Heinz Walz GmbH, Effeltrich, Germany) integrated in the leaf chamber. These parameters included steady-state fluorescence of the light-adapted leave (F), steady-state fluorescence of the dark-adapted leave (F0), fluorescence of the dark-adapted leaf during a saturating light pulse (Fm), fluorescence of the illuminated leaf when a saturating light pulse is superimposed on the prevailing environmental light levels (Fm´, [83]). The maximum potential quantum yield of photosystem II was calculated as Fv/Fm, where Fv = Fm—F0. The effective quantum yield of electron transport through photosystem II was calculated as ΔF/Fm′ = (Fm´ - F)/Fm´ [84]. Photosynthetic light-response curves of ΔF/Fm′ and apparent electron transport rate (ETR) were obtained by increasing PPFD intensity (i.e. 0, 100, 300, 600, 900, 1200, 1500 and 2000 μmol m-2 s-1) after 30 to 120 s (i.e. instant light curves, [85]). ETR was estimated as:
Carbon and nitrogen isotope composition
The oven dried leaves and AGB samples were finely ground with a Vibrator Disc Mill RS 200 and a Mixer Mill MM 200 (Retsch GmbH Haan, Germany). About 1.5 mg of the powdered material from each sample was placed into a tin (Sn) capsule (IVA Analysentechnik, Meerbusch, Germany) for analysis of carbon isotope composition (δ13C, ‰) nitrogen isotope composition (δ15N, ‰), total nitrogen content (N%, %) and total carbon content (C%, %). The analyses were performed at the ZALF Stable Isotope Facility, Müncheberg, Germany. C%, N%, δ13C and δ15N were determined using a Flash 2000 HT Elemental Analyzer (Thermo Fisher Scientific, Bremen, Germany) coupled to a Delta V isotope ratio mass spectrometer (IRMS) via a ConFlo IV interface (both Thermo Fisher Scientific, Bremen, Germany). In the case of the soil samples extracted following AGB collection, 20 mg were placed into a tin (Sn) capsule (Säntis Analytical AG, Teufel, Switzerland). The analyses were performed at the WSL Stable Isotope Research Centre (SIRC), Birmensdorf, Switzerland. C%, N%, δ13C and δ15N were determined using an EA1110 Elemental Analyzer (CE Instruments, Milan, Italy) coupled to a Delta Plus XL ratio mass spectrometer via a ConFlo II interface (both Thermo Fisher Scientific, Bremen, Germany).
Reported isotope ratios were calculated as:
The average δ13C and δ15N of each plant group in a given plot (δ13CFGi and δ15NFGi by functional group, biogeographic status or by their combination) was calculated as the C-weighted and N-weighted average of every replicate in the plot, respectively. In order to estimate the average δ13C and δ15N at the community level (δ13CC and δ15NC) we applied a stable isotope mixing model were δ13C and δ15N of each plant group was scaled by the group specific contribution to the total C and N pool. We thus assumed that the contribution of each plant group to δ13CC and δ15NC was proportional to the relative contribution of that particular group to the total community C pool and N pool, respectively, as described by [87]. That is, average δ13CC and δ15NC were calculated as the C-weighted and N-weighted average, respectively, of all the plant groups present in a plot:
As a next step, carbon isotope discrimination, which is the carbon isotopic ratio in plant tissue relative to that of the atmosphere, was calculated at the plant group, community and species level as:
To correct δ15N values for site-specific differences in background bulk soil δ15N, we estimated the 15N enrichment factor of biomass compared to soil background values [94] at the community (Δδ15NC), plant group (Δδ15NFGi) and species level (Δδ15NSpi) as:
Data analysis
The relationship between species richness and AGB, iWUE or Δδ15N was assessed by regression analysis. To test if the relationship between biodiversity and AGB in Berlin grasslands was comparable to that found in multiple experimental grasslands across Europe, we extracted numerical data from plots in Fig 3 in [36] using Web Plot Digitizer v4.1 (https://apps.automeris.io/wpd/). To ensure that differences in the biodiversity-AGB relationship were not stemming from environmental differences among grassland locations, the extracted data were min-max normalized. The slopes from the corresponding biodiversity-AGB significant regression or ANOVA models were then synthesized.
Random forest (RF) analyses was used to identify the main factors driving the variability in AGB, iWUE and Δδ15N across the studied urban grasslands in Berlin at the plant group (i.e. concerning functional group or biogeographic status) and community level and to thereby assess the relative contribution of biodiversity, biotic and abiotic novelty in controlling urban grassland functioning. These factors included functional and taxonomic diversity, the BNI, environmental variables related to abiotic novelty but also moss and litter cover in the grasslands. We used a conditional inference random forest algorithm [96, 97] to deal with missing values, nonlinear associations among variables, and a number of predictors larger than the number of samples. RF was applied for each response variable to estimate the relative importance of the predictors, measured as the contribution to model fitting accuracy of R2 with variable selection [98]. RF can robustly estimate the relative importance among highly correlated predictors (e.g. land use cover proportion at different buffer radii; [99–101]. As small sample size can result in instable estimates [102], we took the following strategies. Firstly, we determined the number of tree hyper-parameter (ntree = 2000) after confirming its performance stability compared with lower numbers (10, 100, and 1000). Secondly, we estimated variable importance 100 times with changing random seed for randomization and then took an average. Finally, we estimated statistical significance for each predictor, i.e. the probability that the averaged importance score is obtained just by chance (999 permutation; alpha = 0.05) [102, 103]. Thereby, significant predictors were selected and their explanatory power (R2) was estimated for each response variable. For non-significant predictors, variable importance was set to 0 [103]. Modeled association patterns between significant predictors and each response variable were visualized using partial dependence plot (PDP) approach, which averages out the other predictors’ effects to confirm the direction of the effects but not the effect size [104]. All procedures were done in R v3.5.1 [105], with ‘party’ and ‘mlr’ packages [106, 107]. The R script including the other hyperparameter values is available at [108].
It was not possible to obtain a RF model for every plant group (an overview of the RF models developed is provided in S2 Table). This was partly due to the sparse presence of some functional groups at the plots (i.e. alien graminoids and alien legumes), but also due to a relatively limited sample size and the lack of explanatory power of the predictors; we emphasize, however, that the sample size (i.e. the number of sites) was relatively large for such a field study, where all plots had to be sampled and measured within a short time frame for comparability. Likewise, the available data was not sufficient to identify the main factors driving the variability in photosynthetic parameters, iWUE and Δδ15N at the species level by using RF model analysis. Therefore, we opted for analyzing the correlation (Spearman´s rho, rs) between AGB, iWUE or Δδ15N at the species level and species richness, SVF or BNI as representative parameters for biodiversity, abiotic and biotic novelty, respectively. Mann-Whitney or Kruskal-Wallis with pairwise multiple comparison tests were used to analyze significant differences (p < 0.05) in iWUE and Δδ15N among plants with different biogeographic status (i.e. native vs alien) or plant from different functional groups. The Mann-Whitney test was also used to analyze seasonal differences in photosynthetic parameters, iWUE and Δδ15N at the species level. The aforementioned analyses were performed with IBM® SPSS® Statistics 22.0.0.0 Software.
Results
Variability in aboveground biomass, intrinsic water use efficiency and 15N enrichment factor
The 20 urban grasslands studied in Berlin covered a wide range of plant species richness and functional diversity as well as biotic and abiotic novelty (Table 1). Plant species richness varied more than threefold among grasslands and the BNI (biotic novelty index) showed a tenfold variation. Likewise, soil parameters, climate and urban parameters showed wide value ranges across sites. Total plant community aboveground biomass (AGBC) varied threefold across the studied urban grasslands in late summer 2017 (Fig 2A). Important variations were also found between replicates within plots in AGBC (CV = 5–66%, mean 30%). Overall, native species dominated AGBC, contributing more than 60% in 18 out of 20 plots (Fig 2B). Graminoids and forbs made up for most of AGBC (on average >90%) and their share was similar, whereas legumes contribution was relatively small (Fig 2B). All legume and graminoid species present in the sampled quadrats were native to Berlin with the exception of Medicago x varia T. Martyn and Eragrostis minor Host, which were found in one and two plots, respectively. Indeed, the average contribution of alien legumes and graminoids to AGBC across the 20 studied urban grasslands was 1.4% and 0.9%, respectively. However, approximately one third of the forb species were alien to Berlin, and these were present in most plots, contributing on average 13.1% to AGBC in the study sites. An overview of the species present in the sampled quadrats is provided in S3 Table. Both iWUEC and Δδ15NC varied markedly among urban grasslands, having an average value of 50.84 μmol mol-1 (SE = 0.44) and -3.43 ‰ (SE = 0.37), respectively. Plants with different biogeographic status did not significantly differ in their iWUE or Δδ15N (Mann-Whitney, p > 0.05; Fig 3A and 3B). However, iWUEG was significantly higher than iWUEF and iWUEL (Kruskall-Wallis, p < 0.05; Fig 3C) and Δδ15NG was significantly lower than Δδ15NF and Δδ15NL (Kruskall-Wallis, p < 0.05; Fig 3D).
With regard to the seasonal differences at the species level, in C. epigejos A increased significantly from spring to summer, whereas instant-WUE decreased (Mann-Whitney, p > 0.05; Fig 4A and 4C). In P. lanceolata, both instant-WUE, Fv/Fm and ΔF/Fm′ significantly decreased from spring to summer (Mann-Whitney, p > 0.05; Fig 4C, 4E and 4F). Whereas iWUEC.ep significantly increased from spring to summer, iWUEP.la significantly decreased over the growing season but no seasonal differences were found for Δδ15NC.ep or Δδ15NP.la (Fig 4H and 4I). Intrinsic photosynthetic capacity, as indicated by the light-response curves and their associated cardinal points, did not show important seasonal variations in the case of C.epigejos but decreased from spring to summer in P.lanceolata (Fig 5).
Key predictors for the functioning of urban grasslands
In the following, we report the RF models´ results obtained for AGB, iWUE and Δδ15N. For each ecosystem functioning proxy, we first described the RF models´ results for the whole plant community, followed by those for plant biogeographic status classes, plant functional groups and finally for the combination of the latter two. As mentioned above, it was not possible to obtain a RF model for every plant group. Therefore, the RF model description is not consistent among ecosystem functioning proxies and plant groups and we decided to only include results of those plant groups that were more consistently modelled in Fig 6. The results for all the plant groups are provided in the S1 File, S2 File and S3 File.
Aboveground biomass
The explanatory power (R2) of the AGBC, AGBN and AGBA random forest models were 0.87, 0.83 and 0.76, respectively, with a corresponding validation accuracy (R2) of 0.36, 0.41 and 0.17. Out of 27 explanatory variables, six were selected for the AGBC RF model. Species richness was the most important predictor (R2contribution: 41%), followed by size of dry grassland biotope patch (16%), moss cover (12%), functional diversity (8%), SVF (7%) and litter cover (3%). While AGBC was predicted to markedly increase above 25 plant species and a dry grassland biotope patch size of 3500 m2, AGBC diminished with increasing moss cover, being this trend especially strong at moss cover < 10% (Fig 6A; Figure A in S1 File). The five variables selected for the AGBN RF model partially overlapped with those selected for the AGBC and included in descending order of importance: size patch, litter cover, relative humidity, species richness and N soil content. As for the AGBC RF model, the AGBN RF model predicted a monotonic increase with species richness (8%), size of dry grassland biotope patch (40%) and litter cover (22%; Fig 6B; Figure B in S1 File). In the case of AGBA, most predictors selected for the RF model were related to abiotic novelty and specifically to urban parameters. In general terms, AGBA increased monotonically with both PopD and FAR in buffer areas of multiple sizes around the biotope patch (R2: 59% and 11%, respectively; Fig 6C; Figure C in S1 File). Functional diversity influenced AGBA positively as well (Figure C in S1 File), but its explanatory power was low (6%).
The explanatory power (R2) of the AGBG and AGBF RF models was 0.57 and 0.72, with a corresponding validation accuracy of 0.17 and 0.30. AGBG decreased with increasing moss cover, which was the only predictor selected for the AGBG RF model (R2 contribution: 57%; Fig 6D). Species richness was the main predictor for AGBF (53%), followed by functional diversity (17%) and litter cover (3%). For the two strongest predictors, the RF model revealed a hump-shaped relationship (Fig 6E; Figure D in S1 File). AGBNG, AGBNF and AGBAF revealed a similar pattern to that observed for the overall plant groups with different biogeographic status (Figures E-F in S1 File). AGBNG showed a strong monotonic negative dependence on moss cover (61%; Figure E in S1 File). Whereas the size of dry grassland biotope patch and species richness were the main predictors for AGBNF (55% and 10%, respectively), abiotic novelty-related variables explained the variance observed in AGBAF (Figures F-G in S1 File). Specifically, AGBAF increased monotonically with PopD in buffer areas of multiple sizes around the biotope patch (39%) but declined at low Pb (11%).
Intrinsic water use efficiency
The explanatory power (R2) of the iWUEC, iWUEN and iWUEA RF models was 0.84, 0.85 and 0.88, respectively, with a corresponding validation accuracy of 0.50, 0.56 and 0.45. A total of 4 variables were selected for the iWUEC RF model. SVF was the most important predictor (R2 contribution: 62%), followed by Wc, share of grassland and Cu (8%, 7% and 6%, respectively). Community iWUE increased monotonically above a SVF of 0.8 and showed a rapid increase when the share of grassland was very low, reaching a maximum at ≈ 5% (Fig 6A; Figure A in S2 File). Likewise, iWUEC varied markedly at the lower Cu and Wc ranges, but in this case its response was negative (Figure A in S2 File). The four predictors selected for the iWUEN mostly overlapped with those selected for iWUEC, with SVF being also the strongest predictor for iWUEN (53%) and having a positive effect (Fig 6B; Figure B in S2 File). Additional parameters such as Wc, TN and Cu content accounted for 30% of R2 and showed a negative e relation with iWUEN (Figure B in S2 File). RailwD_5000 (47%) was the main predictor for iWUEA, although SVF and AirT were also relevant for (26% and 15%, respectively). iWUEA decreased monotonically with increasing RailwD_5000 but showed a positive response to SVF and AirT (Fig 6C; Figure C in S2 File). The explanatory power (R2) of the iWUEG RF model was 0.83, with a validation accuracy of 0.49. iWUEG increased with increasing SVF (49%), but decreased with Zn, WC and Cu (14%, 13% and 8%, respectively; Fig 6; Figure D in S2 File). The iWUENG and iWUEAF RF models revealed a similar pattern to that observed for the overall plant groups with different biogeographic status (Figures E-F in S2 File). iWUENG increased monotonically with SVF (39%) but decreased with WC and N (14% and 10%, respectively. iWUEAF decrease with increasing RailwD_5000 (53%) and showed significantly lower values in new plots (10%) (Figures E-F in S2 File).
15N enrichment factor
The explanatory power (R2) of the Δδ15NC, Δδ15NN and Δδ15NA RF models was 0.71, 0.7 and 0.75, respectively, with a corresponding validation accuracy of 0.2, 0.22 and 0.3. The 8 predictors selected for the Δδ15NC RF model in descending order of importance when summing up the explanatory power of the predictors for buffer areas of multiple sizes around the biotope patch were FAR (R2 = 0.17), RailwD (14%), PopD (14%), impervious surface (12%) and share of grassland (7%), followed by UrbClim (3%), RoadD_100 (2%) and AirRH (2%) (Fig 6A; Figure A in S3 File). Note that when considering separately the explanatory power of the predictors for different buffer areas sizes around the biotope patch, impervious surface_100 was the main predictor selected by the model. The predictors selected for Δδ15NN and Δδ15NA mostly overlapped with those selected for Δδ15NC, though their explanatory power differed (Figures A-C in S3 File). The main predictor for Δδ15NN was RailwD in buffer areas of multiple sizes (34%), followed by impervious surface_100 (14%), share of grassland_5000 (9%), FAR in buffer areas of multiple sizes (8%), PopD_500 (3%) and AirRH (3%) (Fig 6B; Figure B in S3 File). However, PopD and FAR in buffer areas of multiple sizes (32% and 22%) were the strongest predictors for Δδ15NA, followed by impervious surface, AirT_long term, UrbClim and share of grassland 500 (8%, 8%, 3% and 2%, Fig 6C; Figure C in S3 File)). All the aforementioned predictors showed a positive monotonic relationship with Δδ15NC, Δδ15NN and Δδ15NA except for share of grassland, AirRH and UrbClim, which showed an overall negative relationship with the response variables (Fig 6A–6C; Figures A-C in S3 File). The explanatory power (R2) of the Δδ15NG and Δδ15NF RF models was 0.45 and 0.21, with a corresponding validation accuracy of 0.14 and 0.17. Δδ15NG increased monotonically with RailwD in buffer areas of multiple sizes around the biotope patch and impervious surface_100 (45% and 14%) but decreased with share of grassland_5000 (13%) and similarly, Δδ15NF RF increased with FAR, PopD, impervious surfaceand RailwD when summing up the explanatory power of the predictors for buffer areas of multiple sizes around the biotope patch (21%, 17%, 16% and 13%; Figures D-E in S3 File). Note that when considering separately the explanatory power of the predictors for different buffer areas sizes around the biotope patch, impervious surface_100 was the main predictor selected for Δδ15NF RF model. The Δδ15NNG, Δδ15NNF and Δδ15NAF RF models reflected the pattern observed for the overall plant groups with different biogeographic status, with RailwD, FAR, impervious surface and PopD in buffer areas of multiple sizes around the biotope patch being the main predictors (Figures F-H in S3 File).
Biodiversity-ecosystem functioning in urban grasslands
AGBC increased significantly with species richness in urban grasslands (Fig 7A). Namely, AGBC increased up to a saturating value of 350 g m-2 at 30 species. The relationship between species richness and AGBC was not influenced by the proportion of alien species (Fig 7A). The positive biodiversity-aboveground biomass relationship in non-manipulated urban grasslands was similar to that found in experimental non-urban grasslands across Europe, in other words, the regression slope in our study fell within the slope range reported by [36], Fig 7C. Unlike in the case of AGBC, species richness was not significantly correlated to iWUEC or Δδ15NC (Fig 7B and 7D).
Species level AGB, iWUE or Δδ15N
Species richness was not significantly correlated with photosynthetic parameters, iWUE or Δδ15N at the species level. The BNI did not affect photosynthetic parameters of C. epigejos and P. lanceolata, iWUEC.ep or iWUEP.la but it was negatively correlated to Δδ15NC.ep in summer. In C. epigejos, both A (rs = 0.59, p = 0.036, n = 13) and gs (rs = 0.61, p = 0.028, n = 13) increased with SVF in spring. No significant correlation was found between SVF and photosynthetic parameters in C.epigejos in spring or in P.lanceolata in spring and summer. iWUEC.ep increased significantly with SVF in both spring and summer (rs = 0.8, p = 0.001, n = 13; rs = 0.53, p = 0.029, n = 17). No effect of SVF on Δδ15NC.ep or Δδ15NP.la was found.
Discussion
The relationship between biodiversity and ecosystem function has received much attention during the last decades in ecological research (e.g. [34, 36, 39, 109]). At present, accelerated urban sprawl poses the question whether urban ecosystems are able to provide services in a comparable way to their non-urban counterparts. We focused on aboveground biomass, intrinsic water use efficiency and 15N enrichment factor (AGB, iWUE and Δδ15N) as proxies for biomass production, water and N cycling, respectively, which have been acknowledged as relevant processes for ecosystem integrity [110]. As a major insight we found that biodiversity, abiotic, and biotic novelty were related differently to these ecosystem functions. Community aboveground biomass (AGBC) was mainly explained by species richness. In contrast, community intrinsic water use efficiency (iWUEC) and community 15N enrichment factor (Δδ15NC) were mostly determined by light availability (depicted by the SVF) and urban parameters, respectively, which overrode biodiversity effects. In addition, our results indicate that abiotic novelty potentially favors alien plants in Berlin, mainly by enhancing their dispersal and fitness (via increased iWUE) under low water availability conditions. We found that abiotic novelty, exemplified by urban parameters, specifically affected aboveground biomass and intrinsic water use efficiency of aliens (AGBA and iWUEA), but this effect did not translate into effects on the community level. However, abiotic novelty did affect both 15N enrichment factor of natives and aliens (Δδ15NN and Δδ15NA), suggesting a broader impact of urbanization on N cycling compared to C and water cycling. At the species level, abiotic novelty, and specifically sky view factor (SVF), appeared to be the prevailing driver of photosynthetic performance and resource use efficiency over both species richness and biotic novelty.
Key predictors for the functioning of urban grasslands
Aboveground biomass
Plant invasions have been linked to declines in species diversity and increases in primary production, often attributed to the presence of highly productive alien species [47]. In the studied urban grasslands in Berlin, the relationship between species richness and AGBC was not influenced by the proportion of alien species, that is, lower species richness was not necessarily associated to a higher share of aliens. We found that AGBC increased significantly with plant species richness and more importantly, according to the RF models, species richness was the strongest predictor for AGBC. Although we did not explicitly assess complementarity and selection effects [111] in our study, the fact that the increase in AGBC was associated with increasing Rao´s Q suggests that complementarity was the main mechanisms driving the observed diversity-ecosystem functioning relationship. Functional diversity quantifies trait variability in a given community, and it has been suggested to foster niche complementarity by reducing niche overlap among species pools comprising higher trait ranges [110]. The positive effect of size of dry grassland biotope patch on AGBC further suggests that biomass is boosted by complementarity effects, since biotope space strengthens the biodiversity-AGB relationship by enabling higher niche complementarity among species [112].
Our results additionally indicate that light availability (depicted by the SVF) limits primary production in urban grasslands in Berlin. Moss cover was also associated to reduced AGBC, mainly via a decrease in the aboveground biomass of graminoids (AGBG). Numerous studies have described a negative relationship (mostly attributed to competition) between bryophyte and vascular plant biomass [113]. For instance, in the arctic tundra, moss cover was associated to lower graminoids productivity via reduced soil temperature and N availability [114]. However, our results do not provide enough information to elucidate the mechanisms behind this relationship and reduced vascular plant aboveground biomass production might have also relieved light competition for bryophytes.
Our study points to differing controlling factors for the AGB of plants with different biogeographic status. Whereas aboveground biomass of natives (AGBN) was mainly affected by plant diversity and size of dry grassland biotope patch, aboveground biomass of aliens (AGBA) was mainly explained by abiotic novelty-related parameters, specifically PopD (population density). We hypothesize that this discrepancy stems from different predominant dispersal mechanisms of the alien and native species most frequently found in our plots. The most common aliens were Berteroa incana (L.) DC. and Conyza canadensis (L.) Cronquist, found in 9 and 4 plots, respectively (the geographic location of these plots is provided in S4 Table). Despite the fact that these species are predominantly wind-dispersed, dispersal via footwear and mowing machines have been reported as potential dispersal mechanisms for B. incana [115]. Unintended human-mediated dispersal by vehicles [116] or clothing attachment [117] was found to effectively disperse C. canadensis, which also has highly volatile seeds to the extent that may even reach the planetary boundary layer of the atmosphere [118]. Human-mediated dispersal is known to increase with PopD due to higher density of transport networks integrated by roads or walking routes [119]. By contrast, the most common native species in our plots were the perennial grasses C. epigejos and Festuca trachyphylla (Hack.) Hack (present in 9 and 11 plots, respectively). These clonal species seem to prioritize vegetative over seed reproduction once they are established [120] which reduces the probability of human-mediated dispersal. These results are in line with those from previous studies showing that alien species diversity increased with settlement connectivity and number of inhabitants along an urban-rural gradient in the vicinity of Frankfurt (Germany), which suggests that dispersal mechanisms of alien species are associated with human mobility patterns [121].
Intrinsic water use efficiency
Unlike in the case of AGBC, species richness was not significantly correlated to iWUEC in the studied urban grasslands. In our study, environmental factors related to resource availability and urbanization seemed to override biodiversity effects. In particular, SVF was the strongest predictor for iWUEC followed by soil gravimetric water content (WC). A higher SVF implies higher incoming solar radiation, which very likely boosted non-light-saturated photosynthesis, resulting in increased iWUEC in grasslands with a higher share of open sky. The increasing trend in iWUEC observed with decreasing WC most likely reflected lowered stomatal conductance to avoid water loss associated to increasing water stress [122]. While a positive biodiversity-aboveground biomass relationship seems to be relatively general across ecosystems and studies, and even robust to nutrient enrichment and drought [33], the contrasting patterns how biodiversity relates to water use reported in the literature point to a more variable relationship. For instance, species mixtures were found to be more efficient in water use (estimated via water balance) in comparison with monocultures in experimental grasslands and this was attributed to complementary [50]. By means of a soil water balance modelling approach, a more complete exploitation of soil water, ascribed to higher root density, was linked to higher diversity in experimental grasslands [56]. In contrast, stable water isotopologue labeling revealed no positive effects of species richness on water uptake by plant communities in the temperate experimental grasslands of the Jena Experiment [123].
The differences in iWUE among functional groups is consistent with previous observations in natural grasslands, in which δ13CG was lowest, followed by δ13CF and δ13CL ley [124, 125]. Higher stomatal conductance—which might be a reason for lower iWUE—in forbs compared to grasses was observed in soil-plant monoliths from the Jena experiment and attributed to water uptake from deeper and thus moister soil layers [126]. Even though plants with distinct biogeographic status did not significantly differ with regard to their iWUE, different dominant drivers were identified for natives and aliens. Intrinsic water use efficiency of natives (iWUEN) was mainly controlled by light and to a lesser extent by water availability (i.e. SVF and WC). However, urbanization, and specifically railway density (RailwD) in a buffer area of 5 km, was the main factor modulating iWUEA. Railway embankments functioned as active water sources to nearby ecosystems in a Mediterranean watershed by increasing runoff [127]. This increased water supply could be one reason for aliens spreading along railways [128] and increased iWUEA with decreasing RailwD might point to lower stomatal conductance associated with increasing water stress in areas with less dense railway networks. [129] indicated that aliens often have competitive physiological traits that increase their fitness in unfavorable environments, including the capacity to increase WUE in water-poor environments. This might at least partly explain the alien-specific response observed in urban grasslands in Berlin, where overall, WC was fairly low.
15N enrichment factor
As in the case of iWUEC, no effect of species richness on Δδ15NC was observed in the studied urban grasslands. This result contrasts with findings in central European semi-natural grasslands, where increasing plant diversity was associated to lower Δδ15N at the community and species level, indicating a more closed N cycle that was attributed to efficient N uptake via complementarity [57]. In our study, urban parameters were consistently identified as the main controlling factors for Δδ15N at the community, biogeographic status class and functional group level, which illustrates the predominant role of abiotic novelty over biodiversity or biotic novelty in regulating N cycling in urban grasslands in Berlin. Even though the relative importance of different urban parameters for different levels varied, all predictors were associated to an increasing trend in Δδ15N, that is, they favored a more open N cycle. Very likely, this common trend reflects the association of PopD, RailwD, FAR and impervious surface with urban N emissions. Increased anthropogenic N inputs stimulate N transformations (i.e. mineralization and nitrification), ultimately favoring N mobilization and loss in the form of leachable nitrate or nitrogenous gas [130], which might have led to a more N open cycle.
Biodiversity-ecosystem functioning in urban grasslands
Our results on the positive relationship between total species richness and biomass illustrate the ability of urban grasslands to provide services in a comparable way to their non-urban counterparts. Previous studies have revealed the importance of urban grasslands for biodiversity conservation [24, 131] and cultural ecosystem services [132, 133]. Our findings highlight the relevance of biodiverse urban grasslands to ensure the provision of certain supporting and provisioning ecosystem services (i.e. primary production, carbon sequestration). In particular, we found that the positive relationship between species richness and AGBC extensively described for European experimental grasslands [36] is maintained in the urban grasslands in Berlin even though they are intensively influenced by biotic and abiotic novelty (e.g. urbanization-related parameters) (Table 1). Our results agree with previous studies which reported a positive relationship ranging from linear to log linear with regression slopes that did not significantly differ from zero ([37] and references therein).
Species level AGB, iWUE or Δδ15N
At the species level, we found no effect of species richness on photosynthetic performance, iWUE or Δδ15N, which suggests that the diversity of the surrounding vegetation did neither enhance nor hamper AGB production, water and N use of C. epigejos or P. lanceolata in the studied urban grasslands. Similar to our study, plant species richness did not affect 13C abundances in AGB of individual species in experimental grasslands, where photosynthetic assimilation seemed to be rather determined by the species position (i.e. height) in the plant canopy and the associated availability of light, air humidity and CO2 concentrations [134]. In accordance with the latter study, iWUE significantly increased with light availability (depicted by the SVF) in C. epigejos both in spring and summer, and at least in spring, this increase seemed to be driven by enhanced A and gs. The lack of SVF effects on P. lanceolata might be due to its comparably limited access to direct sunlight due to the lower position of this rosette species in the canopy. Height most likely also determined the contrasting seasonal variations observed in iWUE for the two studied species. iWUEC.ep increased over the growing season, possibly due to increasing height and therefore greater access to light, which boosted A. However, in P. lanceolata, increasing height of the grassland canopy probably resulted in stronger shading of the rosette leaves, which increased gs leading to a reduction in iWUE throughout the season. The significant decrease in Fv/Fm and ΔF/Fm′ in P. lanceolata from spring to summer suggests a decline in photosynthetic capacity, in agreement with our above proposed explanation that the rate of AGB production decreased over the growing season due to increased shading. This is further supported by the results of the instant light-curves, which indicated an important decrease in intrinsic photosynthetic capacity (ETRmax, ΔF/Fm′ and ΔF/Fm′ at PPDFsat) in P. lanceolata over the growing season but minimal seasonal variations in C. epigejos. The latter results, along with the lack of consistent effects of the degree of biotic novelty of the plots on photosynthetic parameters, iWUE or Δδ15N, suggest that abiotic novelty is the prevailing driver of photosynthetic performance and resource use efficiency of the selected individual species.
Conclusions
While the biodiversity-ecosystem functioning relationship is critically understudied for urban grasslands, this study untangles a range of relationships between plant species richness, abiotic and biotic novelty and three important proxies of ecosystem functioning, namely aboveground biomass, intrinsic water use efficiency and 15N enrichment factor. Even though we identified a significant impact of abiotic novelty on AGB, iWUE and Δδ15N for various plant groups, the species richness-AGBC relationship found in the studied urban grasslands in Berlin was comparable to that described in non-urban experimental grasslands in Europe. Our results support previous evidence that conserving and enhancing biodiversity in urban ecosystems is essential to warrant certain functions and ultimately their associated services (i.e. AGB production and primary production or carbon sequestration) and stress that management of urban grasslands in Berlin and other large cities should aim at preserving plant species richness. However, our results also suggest that preserving species richness is insufficient to ensure the provision of ecosystem services associated to other functions such as water and N use, which highlights the need for further studies addressing urban ecosystem functioning and exploring potential additional management measures directed to modify urban abiotic parameters.
Supporting information
S1 Appendix [docx]
Calculation of the Biotic Novelty Index (BNI).
S2 Table [docx]
Overview of the random forests run for aboveground biomass (AGB), intrinsic water use efficiency (iWUE) and N enrichment factor (ΔδN) at the community, plant group (either biogeographic status, functional or combined) and species level in Berlin grasslands in 2017.
S3 Table [docx]
Species present in the sampled quadrats in the grassland plots in Berlin in late summer 2017 along with the number and percentage of plots in which they were present.
S4 Table [docx]
Geographic location of the grassland plots in Berlin in which and were present in late summer 2017.
S1 File [pdf]
Partial dependence plots for the predictors selected by random forest models for aboveground biomass.
S2 File [pdf]
Partial dependence plots for the predictors selected by random forest models for intrinsic water use efficiency.
S3 File [pdf]
Partial dependence plots for the predictors selected by random forest models for N enrichment factor.
S1 Dataset [xlsx]
Digitized data extracted from Fig 3 in [].
Zdroje
1. Ellis EC. Ecology in an anthropogenic biosphere. Ecol Monogr. 2015;85(3):287–331.
2. United Nations. World urbanization prospects: The 2014 revision, highlights. department of economic and social affairs. Population Division, United Nations. 2014;32.
3. Grimm NB, Faeth SH, Golubiewski NE, Redman CL, Wu J, Bai X, et al. Global change and the ecology of cities. Science. 2008;319(5864):756–60. doi: 10.1126/science.1150195 18258902
4. Oke T. The heat island of the urban boundary layer: characteristics, causes and effects. Wind climate in cities: Springer; 1995. p. 81–107.
5. Madrid L, Díaz-Barrientos E, Madrid F. Distribution of heavy metal contents of urban soils in parks of Seville. Chemosphere. 2002;49(10):1301–8. doi: 10.1016/s0045-6535(02)00530-1 12489727
6. Wang M, Liu R, Chen W, Peng C, Markert B. Effects of urbanization on heavy metal accumulation in surface soils, Beijing. J Environ Sci. 2018;64:328–34.
7. Jeffery S, Gardi C. Soil biodiversity under threat—a review. Acta Soc Zool Bohem. 2010;74(1–2):7–12.
8. Rao P, Hutyra LR, Raciti SM, Templer PH. Atmospheric nitrogen inputs and losses along an urbanization gradient from Boston to Harvard Forest, MA. Biogeochemistry. 2014;121(1):229–45.
9. Scolozzi R, Geneletti D. A multi-scale qualitative approach to assess the impact of urbanization on natural habitats and their connectivity. Environ Impact Assess Rev. 2012;36:9–22.
10. Antrop M. Landscape change and the urbanization process in Europe. Landscape Urban Plann. 2004;67(1–4):9–26.
11. Kowarik I, von der Lippe M. Pathways in plant invasions. Biol Invasions: Springer; 2008. p. 29–47.
12. Aronson MF, La Sorte FA, Nilon CH, Katti M, Goddard MA, Lepczyk CA, et al. A global analysis of the impacts of urbanization on bird and plant diversity reveals key anthropogenic drivers. Proceedings of the Royal Society B: Biological Sciences. 2014;281(1780):20133330. doi: 10.1098/rspb.2013.3330 24523278
13. Duncan RP, Clemants SE, Corlett RT, Hahs AK, McCarthy MA, McDonnell MJ, et al. Plant traits and extinction in urban areas: a meta‐analysis of 11 cities. Global Ecol Biogeogr. 2011;20(4):509–19.
14. McDonnell MJ, Hahs AK. Adaptation and adaptedness of organisms to urban environments. Annu Rev Ecol Evol S. 2015;46:261–80.
15. Kowarik I, von der Lippe M. Plant population success across urban ecosystems: A framework to inform biodiversity conservation in cities. J Appl Ecol. 2018;55(5):2354–61.
16. Kühn I, Brandl R, Klotz S. The flora of German cities is naturally species rich. Evol Ecol Res. 2004;6(5):749–64.
17. Hahs AK, McDonnell MJ, McCarthy MA, Vesk PA, Corlett RT, Norton BA, et al. A global synthesis of plant extinction rates in urban areas. Ecol Lett. 2009;12(11):1165–73. doi: 10.1111/j.1461-0248.2009.01372.x 19723284
18. Kowarik I. Novel urban ecosystems, biodiversity, and conservation. Environ Pollut. 2011;159(8–9):1974–83. doi: 10.1016/j.envpol.2011.02.022 21435761
19. Wania A, Kühn I, Klotz S. Plant richness patterns in agricultural and urban landscapes in Central Germany—spatial gradients of species richness. Landscape Urban Plann. 2006;75(1–2):97–110.
20. Groffman PM, Cavender-Bares J, Bettez ND, Grove JM, Hall SJ, Heffernan JB, et al. Ecological homogenization of urban USA. Front Ecol Environ. 2014;12(1):74–81.
21. Heger T, Bernard-Verdier M, Gessler A, Greenwood AD, Grossart H-P, Hilker M, et al. Towards an integrative, eco-evolutionary understanding of ecological novelty: Studying and communicating interlinked effects of global change. Bioscience. 2019: doi: 10.1093/biosci/biz095 31719711
22. Weigelt A, Weisser W, Buchmann N, Scherer-Lorenzen M. Biodiversity for multifunctional grasslands: equal productivity in high-diversity low-input and low-diversity high-input systems. Biogeosciences. 2009;6(8):1695–706.
23. Fischer LK, von der Lippe M, Kowarik I. Urban land use types contribute to grassland conservation: The example of Berlin. Urban For Urban Gree. 2013;12(3):263–72.
24. Klaus VH. Urban grassland restoration: a neglected opportunity for biodiversity conservation. Restor Ecol. 2013;21(6):665–9.
25. Sikorski P, Wińska-Krysiak M, Chormański J, Krauze K, Kubacka K, Sikorska D. Low-maintenance green tram tracks as a socially acceptable solution to greening a city. Urban For Urban Gree. 2018;35:148–64.
26. Thompson K, Hodgson JG, Smith RM, Warren PH, Gaston KJ. Urban domestic gardens (III): composition and diversity of lawn floras. J Veg Sci. 2004;15(3):373–8.
27. Van der Walt L, Cilliers S, Du Toit M, Kellner K. Conservation of fragmented grasslands as part of the urban green infrastructure: how important are species diversity, functional diversity and landscape functionality? Urban Ecosyst. 2015;18(1):87–113.
28. Zeeman BJ, McDonnell MJ, Kendal D, Morgan JW. Biotic homogenization in an increasingly urbanized temperate grassland ecosystem. J Veg Sci. 2017;28(3):550–61.
29. Chollet S, Brabant C, Tessier S, Jung V. From urban lawns to urban meadows: Reduction of mowing frequency increases plant taxonomic, functional and phylogenetic diversity. Landscape Urban Plann. 2018;180:121–4.
30. Rudolph M, Velbert F, Schwenzfeier S, Kleinebecker T, Klaus VH. Patterns and potentials of plant species richness in high‐and low‐maintenance urban grasslands. Appl Veg Sci. 2017;20(1):18–27.
31. Niemelä J, Saarela S-R, Söderman T, Kopperoinen L, Yli-Pelkonen V, Väre S, et al. Using the ecosystem services approach for better planning and conservation of urban green spaces: a Finland case study. Biodivers Conserv. 2010;19(11):3225–43.
32. Caldeira MC, Ryel RJ, Lawton JH, Pereira JS. Mechanisms of positive biodiversity–production relationships: insights provided by δ13C analysis in experimental Mediterranean grassland plots. Ecol Lett. 2001;4(5):439–43.
33. Craven D, Isbell F, Manning P, Connolly J, Bruelheide H, Ebeling A, et al. Plant diversity effects on grassland productivity are robust to both nutrient enrichment and drought. Philosophical Transactions of the Royal Society B: Biological Sciences. 2016;371(1694):20150277.
34. Guerrero-Ramírez NR, Craven D, Reich PB, Ewel JJ, Isbell F, Koricheva J, et al. Diversity-dependent temporal divergence of ecosystem functioning in experimental ecosystems. Nat Ecol Evol. 2017;1(11):1639. doi: 10.1038/s41559-017-0325-1 28970481
35. Hector A, Schmid B, Beierkuhnlein C, Caldeira M, Diemer M, Dimitrakopoulos P, et al. Plant diversity and productivity experiments in European grasslands. Science. 1999;286(5442):1123–7. doi: 10.1126/science.286.5442.1123 10550043
36. Hooper DU, Chapin F, Ewel J, Hector A, Inchausti P, Lavorel S, et al. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr. 2005;75(1):3–35.
37. Spehn E, Hector A, Joshi J, Scherer-Lorenzen M, Schmid B, Bazeley-White E, et al. Ecosystem effects of biodiversity manipulations in European grasslands. Ecol Monogr. 2005;75(1):37–63.
38. Tilman D, Downing JA. Biodiversity and stability in grasslands. Nature. 1994;367(6461):363.
39. Weisser WW, Roscher C, Meyer ST, Ebeling A, Luo G, Allan E, et al. Biodiversity effects on ecosystem functioning in a 15-year grassland experiment: Patterns, mechanisms, and open questions. Basic Appl Ecol. 2017;23:1–73.
40. Thompson GL, Kao-Kniffin J. Diversity enhances NPP, N retention, and soil microbial diversity in experimental urban grassland assemblages. PloS one. 2016;11(5):e0155986. doi: 10.1371/journal.pone.0155986 27243768
41. Schittko C, Hawa M, Wurst S. Using a multi-trait approach to manipulate plant functional diversity in a biodiversity-ecosystem function experiment. PloS one. 2014;9(6):e99065. doi: 10.1371/journal.pone.0099065 24897501
42. Thompson GL, Kao-Kniffin J. Applying Biodiversity and Ecosystem Function Theory to Turfgrass Management. Crop Sci. 2017;57(supplement1):S-238–S-48.
43. Kaye JP, McCulley R, Burke I. Carbon fluxes, nitrogen cycling, and soil microbial communities in adjacent urban, native and agricultural ecosystems. Global Change Biol. 2005;11(4):575–87.
44. Golubiewski NE. Urbanization increases grassland carbon pools: Effects of landscaping in Colorado's front range. Ecol Appl. 2006;16(2):555–71. doi: 10.1890/1051-0761(2006)016[0555:uigcpe]2.0.co;2 16711044
45. Vilà M, Hulme PE. Impact of biological invasions on ecosystem services: Springer; 2017.
46. Schirmel J, Bundschuh M, Entling MH, Kowarik I, Buchholz S. Impacts of invasive plants on resident animals across ecosystems, taxa, and feeding types: a global assessment. Global Change Biol. 2016;22(2):594–603.
47. Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošík V, Maron JL, et al. Ecological impacts of invasive alien plants: a meta‐analysis of their effects on species, communities and ecosystems. Ecol Lett. 2011;14(7):702–8. doi: 10.1111/j.1461-0248.2011.01628.x 21592274
48. Chapin Iii FS, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, Reynolds HL, et al. Consequences of changing biodiversity. Nature. 2000;405(6783):234. doi: 10.1038/35012241 10821284
49. Loreau M. Biodiversity and ecosystem functioning: A mechanistic model. Proc Natl Acad Sci USA. 1998;95:632–5636. doi: 10.1073/pnas.95.2.632
50. De Boeck HJ, Lemmens CM, Bossuyt H, Malchair S, Carnol M, Merckx R, et al. How do climate warming and plant species richness affect water use in experimental grasslands? Plant Soil. 2006;288(1–2):249–61.
51. Spehn E, Scherer‐Lorenzen M, Schmid B, Hector A, Caldeira M, Dimitrakopoulos P, et al. The role of legumes as a component of biodiversity in a cross‐European study of grassland biomass nitrogen. Oikos. 2002;98(2):205–18.
52. Scherling C, Roscher C, Giavalisco P, Schulze E-D, Weckwerth W. Metabolomics unravel contrasting effects of biodiversity on the performance of individual plant species. PLoS One. 2010;5(9):e12569. doi: 10.1371/journal.pone.0012569 20830202
53. Zavalloni C, Gielen B, De Boeck HJ, Lemmens CM, Ceulemans R, Nijs I. Greater impact of extreme drought on photosynthesis of grasslands exposed to a warmer climate in spite of acclimation. Physiol Plant. 2009;136(1):57–72. doi: 10.1111/j.1399-3054.2009.01214.x 19374719
54. Maxwell K, Johnson GN. Chlorophyll fluorescence—a practical guide. J Exp Bot. 2000;51(345):659–68. doi: 10.1093/jxb/51.345.659 10938857
55. Weiwei L, Xinxiao Y, Guodong J, Hanzhi L, Ziqiang L. Responses of Intrinsic Water-use Efficiency and Tree Growth to Climate Change in Semi-Arid Areas of North China. Sci Rep-UK. 2018;8(1):308.
56. Verheyen K, Bulteel H, Palmborg C, Olivié B, Nijs I, Raes D, et al. Can complementarity in water use help to explain diversity–productivity relationships in experimental grassland plots? Oecologia. 2008;156(2):351–61. doi: 10.1007/s00442-008-0998-x 18305961
57. Kleinebecker T, Hölzel N, Prati D, Schmitt B, Fischer M, Klaus VH. Evidence from the real world: 15N natural abundances reveal enhanced nitrogen use at high plant diversity in Central European grasslands. J Ecol. 2014;102(2):456–65.
58. Amt für Statistik, Berlin-Brandenburg. 2017. [Available from: https://www.statistik-berlin-brandenburg.de/home.asp.
59. Quanz J, Ulrich S, Fenner D, Holtmann A, Eimermacher J. Micro-scale variability of air temperature within a local climate zone in Berlin, Germany, during summer. Climate. 2018;6(1):5.
60. LUA. Brandenburg State Environmental Office. Catalogue of Natural Habitats and Species of Appendices I and II of the Habitats Directive in Brandenburg: German Institute for Standardization, Beuth Verlag, GmbH, Berlin; 2002.
61. ScapeLabs Experimental Platform. 2019. [Available from: https://www.bbib.org/scapelabs.html.
62. Rao CR. Diversity and dissimilarity coefficients: a unified approach. Theor Popul Biol. 1982;21(1):24–43.
63. Jäger EJ, Werner K. Rothmaler-Exkursionsflora von Deutschland: Springer; 2011.
64. Prasse R, Ristow M, Klemm G, Machatzi B, Raus T, Scholz H, et al. Liste der wildwachsenden Gefäßpflanzen des Landes Berlin: mit Roter Liste. 2001.
65. Seitz B, Ristow M, Meißner J, Machatzi B, Sukopp H. Rote Liste und Gesamtartenliste der etablierten Farn-und Blütenpflanzen von Berlin: Universitätsverlag der TU Berlin; 2018.
66. Schittko C, Bernard-Verdier M, Heger T, Buchholz S, Kowarik I, von der Lippe M, et al. A multidimensional framework for measuring biotic novelty: How novel is a community? bioRxiv. 2019:824045. Cited 31 October 2019.
67. Kattge J, Diaz S, Lavorel S, Prentice IC, Leadley P, Bönisch G, et al. TRY–a global database of plant traits. Global Change Biol. 2011;17(9):2905–35.
68. Klotz S, Kühn I, Durka W. Biolflor: Eine Datenbank zu biologisch-ökologischen Merkmalen der Gefäßpflanzen in Deutschland–Schriftenreihe für Vegetationskunde 38. Bonn, Bundesamt für Naturschutz–http://wwwufzde/biolflor/indexjsp. 2002.
69. Geoportal Berlin of the Senate Department for Urban Development and Housing. 2019. [Available from: www.stadtentwicklung.berlin.de/geoinformation/fis-broker/.
70. QGIS Development Team, 2016. QGIS geographic information system. Open Source Geospatial Foundation Project. 2016 [Available from: http://qgis.osgeo.org.
71. DIN ISO 13878: 1998. Soil quality—Determination of total nitrogen by dry combustion: German Institute for Standardization, Beuth Verlag, GmbH, Berlin.
72. DIN ISO 19730: 2008. Soil quality–Extraction of trace elements from soil using ammonium nitrate solution: German Institute for Standardization, Beuth Verlag, GmbH, Berlin.
73. Weather Uderground. 2019. [Available from: http://www.weatherunderground.com.
74. Bernard J, Bocher E, Petit G, Palominos S. Sky view factor calculation in urban context: computational performance and accuracy analysis of two open and free GIS tools. Climate. 2018;6(3):60.
75. Lindberg F, Holmer B, Thorsson S. SOLWEIG 1.0–Modelling spatial variations of 3D radiant fluxes and mean radiant temperature in complex urban settings. Int J Biometeorol. 2008;52(7):697–713. doi: 10.1007/s00484-008-0162-7 18523814
76. Lindberg F, Grimmond C. Nature of vegetation and building morphology characteristics across a city: influence on shadow patterns and mean radiant temperatures in London. Urban Ecosyst. 2011;14(4):617–34.
77. Botta‐Dukát Z. Rao's quadratic entropy as a measure of functional diversity based on multiple traits. J Veg Sci. 2005;16(5):533–40.
78. Carthey AJ, Banks PB. When does an alien become a native species? A vulnerable native mammal recognizes and responds to its long-term alien predator. PloS one. 2012;7(2):e31804. doi: 10.1371/journal.pone.0031804 22355396
79. Pearse IS, Harris DJ, Karban R, Sih A. Predicting novel herbivore–plant interactions. Oikos. 2013;122(11):1554–64.
80. Strauss SY, Lau JA, Carroll SP. Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecol Lett. 2006;9(3):357–74. doi: 10.1111/j.1461-0248.2005.00874.x 16958902
81. Verhoeven KJ, Biere A, Harvey JA, Van Der Putten WH. Plant invaders and their novel natural enemies: who is naive? Ecol Lett. 2009;12(2):107–17. doi: 10.1111/j.1461-0248.2008.01248.x 19143824
82. Scurlock JM, Johnson K, Olson RJ. Estimating net primary productivity from grassland biomass dynamics measurements. Global Change Biol. 2002;8(8):736–53.
83. Schreiber U, Bilger W. Progress in chlorophyll fluorescence research: major developments during the past years in retrospect. Progress in Botany/Fortschritte der Botanik: Springer; 1993. p. 151–73.
84. Genty B, Briantais J-M, Baker NR. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. BBA-Gen Subjects. 1989;990(1):87–92.
85. Rascher U, Liebig M, Lüttge U. Evaluation of instant light‐response curves of chlorophyll fluorescence parameters obtained with a portable chlorophyll fluorometer on site in the field. Plant, Cell Environ. 2000;23(12):1397–405.
86. Coplen TB. Guidelines and recommended terms for expression of stable‐isotope‐ratio and gas‐ratio measurement results. Rapid Commun Mass SP. 2011;25(17):2538–60.
87. Grossiord C, Granier A, Gessler A, Scherer‐Lorenzen M, Pollastrini M, Bonal D. Application of Loreau & Hector's (2001) partitioning method to complex functional traits. Methods Ecol Evol. 2013;4(10):954–60.
88. Farquhar GD, Ehleringer JR, Hubick KT. Carbon isotope discrimination and photosynthesis. Annu Rev Plant Biol. 1989;40(1):503–37.
89. Ehleringer JR, Hall AE, Farquhar GD. Stable isotopes and plant carbon-water relations: Academic Press San Diego; 1993.
90. Farquhar GD, O'Leary MH, Berry JA. On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Funct Plant Biol. 1982;9(2):121–37.
91. Betts RA, Jones CD, Knight JR, Keeling RF, Kennedy JJ. El Niño and a record CO2 rise. Nat Clim Change. 2016;6:806.
92. O'Leary MH. Carbon isotope fractionation in plants. Phytochemistry. 1981;20(4):553–67.
93. Farquhar G, Richards R. Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Funct Plant Biol. 1984;11(6):539–52.
94. Craine JM, Brookshire E, Cramer MD, Hasselquist NJ, Koba K, Marin-Spiotta E, et al. Ecological interpretations of nitrogen isotope ratios of terrestrial plants and soils. Plant Soil. 2015;396(1–2):1–26.
95. Malone ET, Abbott BW, Klaar MJ, Kidd C, Sebilo M, Milner AM, et al. Decline in ecosystem δ 13 C and mid-successional nitrogen loss in a two-century postglacial chronosequence. Ecosystems. 2018;21(8):1659–75.
96. Breiman L. Random forests. Mach Learn. 2001;45(1):5–32.
97. Strobl C, Boulesteix A-L, Zeileis A, Hothorn T. Bias in random forest variable importance measures: Illustrations, sources and a solution. BMC Bioinformatics. 2007;8(1):25.
98. Hapfelmeier A, Hothorn T, Ulm K, Strobl C. A new variable importance measure for random forests with missing data. Stat Comput. 2014;24(1):21–34.
99. Bradter U, Kunin WE, Altringham JD, Thom TJ, Benton TG. Identifying appropriate spatial scales of predictors in species distribution models with the random forest algorithm. Methods Ecol Evol. 2013;4(2):167–74.
100. Nicodemus KK, Malley JD, Strobl C, Ziegler A. The behaviour of random forest permutation-based variable importance measures under predictor correlation. BMC Bioinformatics. 2010;11(1):110.
101. Strobl C, Boulesteix A-L, Kneib T, Augustin T, Zeileis A. Conditional variable importance for random forests. BMC Bioinformatics. 2008;9(1):307.
102. Ryo M, Rillig MC. Statistically reinforced machine learning for nonlinear patterns and variable interactions. Ecosphere. 2017;8(11). doi: 10.1002/ecs2.2002
103. Hapfelmeier A, Ulm K. A new variable selection approach using random forests. Comput Stat Data Anal. 2013;60:50–69.
104. Hastie T, Tibshirani R, Friedman J. The elements of statistical learning: prediction, inference and data mining. Springer-Verlag, New York. 2009.
105. R Core Team. A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria 2018 [Available from: https://www.R-project.org.
106. Bischl B, Lang M, Kotthoff L, Schiffner J, Richter J, Studerus E, et al. mlr: Machine Learning in R. J Mach Learn Res. 2016;17(1):5938–42.
107. Strobl C, Hothorn T, Zeileis A. Party on! A new, conditional variable importance measure for random forests available in the party package. Technical Report Number 050, 2009, Department of Statistics, University of Munich. 2009:1–5.
108. Onandia G, Acame CM, Schittko C, Kowarik I, Gessler A, Seitz B, et al. 2019. Ecosystem functioning in urban grasslands: the role of biodiversity, abiotic and biotic novelty. Database: Open Research Data ZALF. Available from: https://www.doi.org/10.4228/ZALF.DK.111.
109. Leimer S, Bischoff S, Boch S, Busch V, Escher P, Fischer M, et al. Does plant diversity affect the water balance of established grassland systems? Ecohydrology. 2018;11(4):e1945.
110. Díaz S, Lavorel S, Chapin FS, Tecco PA, Gurvich DE, Grigulis K. Functional diversity—at the crossroads between ecosystem functioning and environmental filters. Terrestrial ecosystems in a changing world: Springer; 2007. p. 81–91.
111. Loreau M, Hector A. Partitioning selection and complementarity in biodiversity experiments. Nature. 2001;412(6842):72. doi: 10.1038/35083573 11452308
112. Dimitrakopoulos PG, Schmid B. Biodiversity effects increase linearly with biotope space. Ecol Lett. 2004;7(7):574–83.
113. Ingerpuu N, Liira J, Pärtel M. Vascular plants facilitated bryophytes in a grassland experiment. Plant Ecol. 2005;180(1):69–75.
114. Gornall JL, Woodin SJ, Jónsdóttir IS, van der Wal R. Balancing positive and negative plant interactions: how mosses structure vascular plant communities. Oecologia. 2011;166(3):769–82. doi: 10.1007/s00442-011-1911-6 21279654
115. Warwick S, Francis A. The biology of invasive alien plants in Canada. 6. Berteroa incana (L.) DC. Can J Plant Sci. 2006;86(4):1297–309.
116. von der Lippe M, Kowarik I. Long‐distance dispersal of plants by vehicles as a driver of plant invasions. Conserv Biol. 2007;21(4):986–96. doi: 10.1111/j.1523-1739.2007.00722.x 17650249
117. Ansong M, Pickering C, Arthur JM. Modelling seed retention curves for eight weed species on clothing. Austral Ecol. 2015;40(7):765–74.
118. Shields EJ, Dauer JT, VanGessel MJ, Neumann G. Horseweed (Conyza canadensis) seed collected in the planetary boundary layer. Weed Sci. 2006;54(6):1063–7.
119. Bullock JM, Bonte D, Pufal G, da Silva Carvalho C, Chapman DS, García C, et al. Human-mediated dispersal and the rewiring of spatial networks. Trends Ecol Evol. 2018.
120. Rebele F, Lehmann C. Biological flora of central Europe: Calamagrostis epigejos (L.) Roth. Flora. 2001;196(5):325–44.
121. Brunzel S, Fischer SF, Schneider J, Jetzkowitz J, Brandl R. Neo‐and archaeophytes respond more strongly than natives to socio‐economic mobility and disturbance patterns along an urban–rural gradient. J Biogeogr. 2009;36(5):835–44.
122. Farquhar GD, Lloyd J. Carbon and oxygen isotope effects in the exchange of carbon dioxide between terrestrial plants and the atmosphere. Stable isotopes and plant carbon-water relations: Elsevier; 1993. p. 47–70.
123. Bachmann D, Gockele A, Ravenek JM, Roscher C, Strecker T, Weigelt A, et al. No evidence of complementary water use along a plant species richness gradient in temperate experimental grasslands. PloS one. 2015;10(1):e0116367. doi: 10.1371/journal.pone.0116367 25587998
124. Smedley MP, Dawson TE, Comstock JP, Donovan LA, Sherrill DE, Cook CS, et al. Seasonal carbon isotope discrimination in a grassland community. Oecologia. 1991;85(3):314–20. doi: 10.1007/BF00320605 28312034
125. Tsialtas J, Handley L, Kassioumi M, Veresoglou D, Gagianas A. Interspecific variation in potential water‐use efficiency and its relation to plant species abundance in a water‐limited grassland. Funct Ecol. 2001;15(5):605–14.
126. Guderle M, Bachmann D, Milcu A, Gockele A, Bechmann M, Fischer C, et al. Dynamic niche partitioning in root water uptake facilitates efficient water use in more diverse grassland plant communities. Funct Ecol. 2018;32(1):214–27.
127. Pereira P, Gimeìnez-Morera A, Novara A, Keesstra S, Jordán A, Masto R, et al. The impact of road and railway embankments on runoff and soil erosion in eastern Spain. Hydrol Earth Syst Sci. 2015;12(12).
128. Walter J, Essl F, Englisch T, Kiehn M. Neophytes in Austria: habitat preferences and ecological effects. Neobiota. 2005;6:13–25.
129. Quinet M, Descamps C, Coster Q, Lutts S, Jacquemart A-L. Tolerance to water stress and shade in the invasive Impatiens parviflora. Int J Plant Sci. 2015;176(9):848–58.
130. Fenn ME, Poth MA, Terry JD, Blubaugh TJ. Nitrogen mineralization and nitrification in a mixed-conifer forest in southern California: controlling factors, fluxes, and nitrogen fertilization response at a high and low nitrogen deposition site. Can J Forest Res. 2005;35(6):1464–86.
131. Planchuelo G, von Der Lippe M, Kowarik I. Untangling the role of urban ecosystems as habitats for endangered plant species. Landscape Urban Plann. 2019;189:320–34.
132. Fischer LK, Honold J, Cvejić R, Delshammar T, Hilbert S, Lafortezza R, et al. Beyond green: Broad support for biodiversity in multicultural European cities. Global Environ Change. 2018;49:35–45.
133. Southon GE, Jorgensen A, Dunnett N, Hoyle H, Evans KL. Biodiverse perennial meadows have aesthetic value and increase residents’ perceptions of site quality in urban green-space. Landscape Urban Plann. 2017;158:105–18.
134. Roscher C, Karlowsky S, Milcu A, Gessler A, Bachmann D, Jesch A, et al. Functional composition has stronger impact than species richness on carbon gain and allocation in experimental grasslands. PloS one. 2019;14(1):e0204715. doi: 10.1371/journal.pone.0204715 30703101
Článek vyšel v časopise
PLOS One
2019 Číslo 11
- Řekněte mi, co jíte, a já vám řeknu, jaká je úroveň vaší kognice
- Duševní onemocnění se u teenagerů přenáší v rámci školní třídy
- Od kostiček k lidské kůži. Jak si postavit 3D biotiskárnu?
- Pomohou nám s detekcí karcinomu plic i včely?
- Původní český test ALBA pro odhalení mírných kognitivních deficitů získal certifikaci MZ ČR
Nejčtenější v tomto čísle
- A daily diary study on maladaptive daydreaming, mind wandering, and sleep disturbances: Examining within-person and between-persons relations
- A 3’ UTR SNP rs885863, a cis-eQTL for the circadian gene VIPR2 and lincRNA 689, is associated with opioid addiction
- A substitution mutation in a conserved domain of mammalian acetate-dependent acetyl CoA synthetase 2 results in destabilized protein and impaired HIF-2 signaling
- Molecular validation of clinical Pantoea isolates identified by MALDI-TOF