OPEN

Direct and indirect efects of urban gardening on aboveground and belowground diversity infuencing soil multifunctionality

Received: 21 March 2019

Accepted: 18 June 2019

Published: xx xx xxxx

Simon Tresch   1,2,3, David Frey2,4, Renée-Claire Le Bayon3, Paul Mäder   1, Bernhard Stehle1,5, Andreas Fliessbach   1 & Marco Moretti2

Urban gardens are popular green spaces that have the potential to provide essential ecosystem services, support human well-being, and at the same time foster biodiversity in cities. We investigated the impact of gardening activities on fve soil functions and the relationship between plant (600 spp.) and soil fauna (earthworms: 18 spp., springtails: 39 spp.) in 85 urban gardens (170 sites) across the city of Zurich (Switzerland). Our results suggest that high plant diversity in gardens had a positive efect on soil fauna and soil multifunctionality, and that garden management intensity decreased plant diversity. Indices of biological activity in soil, such as organic and microbial carbon and bacterial abundance, showed a direct positive efect on soil multifunctionality. Soil moisture and disturbance, driven by watering and tilling, were the driving forces structuring plant and soil fauna communities. Plant indicator values proved useful to assess soil fauna community structure, even in anthropogenic plant assemblages. We conclude that to enhance soil functions, gardeners should increase plant diversity, and lower management intensity. Soil protective management practices, such as applying compost, mulch or avoiding soil tilling, should be included in urban green space planning to improve urban biodiversity and nature’s contribution to people.

Maintaining functional and biodiverse urban green spaces is fundamental for liveable cities (cf. SDG 111). Urban gardens are a major component of urban green spaces in many countries2,3. Tey are heterogeneous in structure, but despite their relatively small size they provide critical habitat resources and increase the connectivity of urban landscapes4. Garden management creates diverse garden land-use types including perennially vegetated habitats such as lawns or annually vegetated habitats such as vegetable beds2. Tese diverse microhabitats support urban biodiversity and have the ability to provide nature’s contributions to people5,6. Te worldwide increase in human population is expected to take place mainly in urban areas7, while growing cities ofen expand onto fertile agricul tural soils, thus challenging the supply of fresh food in the future8. Tere is a great potential for producing food in urban gardens and at the same time to provide other ecosystem services (ES) in densely populated cities9. It is estimated that urban farming delivers food for approximately 800 million people10, although the current global scale is difcult to assess11. However, hundreds of millions of citizens rely on urban agriculture for part of their nourishment12. Nonetheless, urban garden soils are also important for regulating soil functions such as water storage (food control13), C and N storage14, pollination15, soil formation16, pest control17, or to decrease urban heat island intensity18 and provide habitats for many species even in densely urbanised areas6. From a sociological perspective, urban gardens are important for recreation, well-being, and social interaction19.

Urban gardening has a long tradition in many countries around the world20. As a consequence of decades of benefcial soil management practices, such as the application of compost21, urban garden soils may not always

1Research Institute of Organic Agriculture (FiBL), Department of Soil Sciences, Ackerstrasse 113, 5070, Frick, CH,Switzerland. 2Swiss Federal Research Institute WSL, Biodiversity and Conservation Biology, Zürcherstrasse 111,8903, Birmensdorf, CH, Switzerland. 3University of Neuchâtel, Institute of Biology, Functional Ecology Laboratory,Rue Emile-Argand 11, 2000, Neuchâtel, CH, Switzerland. 4ETHZ, Department of Environmental System Science,Institute of Terrestrial Ecosystems, Universitaetstrasse 16, 8092, Zurich, CH, Switzerland. 5University of Konstanz,Department of Biology, Ecology, Universitätstrasse 10, 78464, Konstanz, DE, Germany. Correspondence and requests for materials should be addressed to S.T. (email: )

Table 1.  Soil characteristics describing the soil quality of urban garden sites used as explanatory variables in the SEM. Te frst four PCA axes scores (PC1–PC4; Fig. S4) were used (Kaiser-Guttman criteria) as explanatory variables in the SEM (Fig. 2), explaining 64.2% of the total variation.

Figure 1.  A priori SEM model with hypothesised direct and indirect efects of urban gardening on soil multifunctionality. Expected positive relationships are given in black and negative ones in red, grey arrows represent both positive and negative efects. We expected that annual vegetables (arrows 1a) will negatively infuence plant and soil fauna as well as soil multifunctionality compared to perennial grass sites, while perennial fowers (arrows 1b) will show positive efects. Management intensity (arrows 2) is expected to negatively afect plant diversity and soil fauna as well as soil multifunctionality. Higher plant diversity (arrows 3) is hypothesised to have a positive efect on soil fauna and soil multifunctionality. Soil fauna diversity and biomass (arrows 4a & 4b) are also expected to have a positive efect on soil multifunctionality. Urbanisation (arrows 5) might have a positive or negative efect on soil fauna and soil multifunctionality. Expected efects of soil characteristics (arrows 6) can be found in Fig. S9.

be as poor in quality and potentially polluted as other urban soils3,22. Despite the importance of gardens for urban biodiversity6, information on the ecological importance of allotment and domestic gardens is still scarce compared to public green spaces2,23. However, there is a large body of evidence that biodiversity drives ecosystem processes and related services in aboveground communities24, but the functioning of belowground biodiversity is much less understood25. Although it has been shown that soil biodiversity is linked in multiple ways with aboveground biodiversity26,27, further investigation is needed to better understand these relationships. Garden soils are strongly infuenced by human activities3,22,28, but they are also afected by the past land-use, the degree of disturbance or climate related drivers such as the urban heat island efect29. Soil functions are provided and controlled by a large variety of soil organisms30, also in urban soils28, where the frequency of soil disturbance is ofen high29. Changes in community composition of soil fauna in both alpha and beta diversity31, for instance due to soil disturbance, can impair soil functions such as organic matter decomposition or nutrient retention32. Te interactions of aboveground and belowground species, driving ecosystem functions, at least at the local scale33, are mainly linked via plants34. However, still very little is known about this relationship between aboveground and belowground diversity and associated soil functions35, especially for garden soils36.

Te ability of an ecosystem to provide multiple functions, so-called multifunctionality24, can be calculated as indices based on the functions of interest37. Such measures of multifunctionality (i.e. the averaging approach), have been used to analyse a wide range of ecosystem drivers38, such as soil characteristics39, habitat diversity40, cli mate41, or management practices in agriculture42 and even in constructed ecosystems such as green roofs43. Here, we focus on fve independent measurements for calculating soil multifunctionality ranging from aboveground44 and belowground27 litter decomposition, to nutrient supply for plant growth45 and water regulation, such as water storage capability46.

Research on urban garden soils has recently received increased attention3,17,28,47,48, especially with regard to human health and well-being29. However, our understanding of the complex interactions between management practices, soil biodiversity and soil functioning is still scarce49. In this study, we focus on gardening activities in the two most dominant garden types of Zurich (CH), allotment and domestic gardens, and assess the interactions between aboveground diversity of plants and belowground diversity of soil fauna. We investigated earthworms (Oligochaeta: Lumbricidae), representing soil macrofauna species and springtails (Hexapoda: Collembola), rep resenting soil mesofauna species, as indicators for soil functioning50 and assessed the impacts of urban gardening on soil multifunctionality. Earthworms are generally described as ecosystem engineers50, due to their impact on soil structure and quality, at least in temperate soils51. Tey are important indicator organisms for soil functions52, soil disturbance, and management practices50. It has been shown that also in urban ecosystems such as parks or urban gardens, they are sensitive indicators of anthropogenic management intensity47. Springtails are a key group of microarthropods50 and can be used as indicators of sustainable land-use, soil quality27, or the use of pes ticides53. Moreover, they are used to assess soil functionality54 and the impact of environmental factors55 on soil biodiversity. In addition, we assessed soil microfauna by biological soil measurements, such as basal respiration, microbial biomass and gene copy numbers of bacteria and fungi (Table 1).

Te overall objective of our study was to investigate impacts of garden management practices (management intensity index, garden land-use types) on aboveground plant diversity and belowground diversity of soil fauna, and their direct and indirect efects on soil multifunctionality. We hypothesised (cf. a priori structural equation model (SEM) Fig. 1) that (i) intensive soil management will reduce the diversity of both plant and soil fauna and negatively afect soil multifunctionality (arrows 1 & 2). We assumed that (ii) aboveground and belowground diversity are also linked in urban garden ecosystems and therefore expected that a higher diversity of plants will have a positive efect on both soil fauna and soil multifunctionality (arrows 3). Furthermore, we expected that (iii) soil fauna diversity (arrow 4a) and biomass (arrow 4b) will have a direct positive efect on soil multifunctionality. Additionally, we assumed an infuence of (iv) soil characteristics and (v) urbanisation on soil multifunctionality (arrows 5 & 6).

In a second step, we analysed soil fauna community structure. We expected that frequently disturbed soils would have the lowest species diversity within (alpha diversity) and among (beta diversity) garden sites, includ ing a high community evenness and beta diversity mainly driven by species loss (nestedness) rather than species replacement (turnover). For the plant community, we expected highest alpha and beta diversity for garden sites with high planting activities, including a high species turnover component for beta diversity. Furthermore, we investigated impacts of management practices on soil fauna community composition and on soil fauna distur bance indices.

Results

Urban gardening efects on soil fauna and soil multifunctionality. Te SEM based on our a priori expectations (Fig. 1) of urban gardening efects on aboveground and belowground diversity and soil multifunc tionality met the criteria of Fisher’s C statistic56 (Fisher’s C = 30.7; p = 0.80; AICc = 286.8). Te model included one signifcant missing path57 between PC1 and soil fauna diversity (SEM; 0.18;p=0.03). With the inclusion of this path the overall model ft of the SEM improved (Fisher’sC=24.3;p=0..93;AICC=288.3), with marginal diferences in the AICc (1.5). Overall, the strongest relationships in the SEM originated from garden land-use types, infuencing plant diversity, fauna biomass and soil characteristics (PC2) and soil multifunctionality both in indirect and direct ways (Figs 2 and S10). Te strongest efects on soil multifunctionality came from soil PC1 (SEM; −0.61;p=<0.001), represented by lower loads of$C _ { m i c } C _ { o r g ^ { prime } }$ bacteria, Fe and K, but higher soil bulk density values (Fig. S4). Soils with increased$C _ { min } C _ { o r g ^ { 3 } }$bacteria, Fe and K, but lower bulk density values thus covaried with higher soil multifunctionality. Annual vegetable sites showed lower soil multifunctionality values (SEM; −0.40;p=0..03)compared to perennial grass sites. Moreover, we found positive efects of plant diversity (SEM; 0.17;p=0.01),and fauna biomass (SEM; 0.17; p = 0.02) on soil multifunctionality. Taken together, both signif icant and non-signifcant efects explained 74% of the total variation of soil multifunctionality. In addition, we

Figure 2.  Final most parsimonious SEM connecting garden management (land-use types, management intensity), urbanisation, plant and soil fauna diversity with soil multifunctionality (AICc = 288.3, Fisher’s C=24.3,P = 0.93). Arrows represent unidirectional relationships among variables. Black arrows denote signifcantly (p<0.05)positive and red arrows signifcantly negative relationships (Table 3). Dashed grey arrows represent non signifcant relationships (p > 0.05). Te thickness of paths has been scaled based on the magnitude of the standardised regression coefcient. Conditional R2s, based on the variance of both the fxed and random efects, as well as marginal R2s, based on the fxed efect parts for each component models are given in the boxes of the response variables. Soil multifunctionality consists of fve measurements related to important soil functions. Soil characteristics are included in Fig. S10.

also identifed several indirect efects on soil multifunctionality (Fig. 2 and S10, Table S6). We found that plant diversity had a positive indirect efect on soil multifunctionality mediated by increased fauna diversity and fauna biomass. Plant diversity itself was positively afected by fower & berry sites (SEM; 0.37;p=0.04)and negatively by management intensity (SEM; −0.22; p = 0.01), explaining 39% of the variation in plant diversity. A similar pattern was found in high beta diversity values (Table S5) for the plants (0.94 ± 0.001), dominated by a high turnover component (0.92 ± 0.001) and low nestedness component (0.02 ± 0.001), indicating the high variability between garden plots. Moreover, the management intensity indirectly negatively afected soil multifunctionality by decreasing fauna biomass and plant diversity (Fig. 2, Table S6). Plant and soil fauna beta diversity and fauna phylogenetic diversity were not included in the fnal SEM (cf. Table S10, Fig. S7) due to a large increase in the AICc (588.5) and because it explained only 3% more variance in soil multifunctionality (Fig. S8).

Urban gardening efects on soil fauna community composition. We investigated the efects of man agement practices, plant ecological indicators (Table 2), soil characteristics (Table 1), garden land-use types, and urbanisation on the community composition of both earthworms and springtails (Table 4). Both soil fauna groups were strongly afected by the plant ecological indicator nutrients (PERMANOVAEW;F=5.9;P=<0.001, COL; F=5.4; p =< 0.001), that represented the requirements of nutrient-rich soils for plants that are predominantly found in vegetable sites (Fig. 3). Earthworm communities were further afected by the penetration resistance of the soil (PERMANOVA EW;F=5.3;p=<0.001), favouring anecic species such as L. terrestris. Furthermore, plants indicating humus rich soils (PERMANOVAEW;F=3.0;P=0.01) favoured the two most abundant earth worm species (Table S1, Fig.3) A. chlorotica and A. caliginosa. Tose soils were further associated with higher contents of Mg (PERMANOVA EW; F=2.1;p = 0.04) and K (PERMANOVA EW; F=2.7;p=0.01), resulting from higher soil disturbance (PERMANOVA EW; F=2.4;p=0.02) predominantly in vegetable sites. In sum mary, the NMDS ordination was driven by endogeic species A. chlorotica (NMDS; $R ^ { 2 } = 0 . 3 0 ;$p=<0.001)and A. caliginosa (NMDS; $R ^ { 2 } = 0 . 1 3 ;$p=<0.001), anecic species L. terrestris (NMDS;$R ^ { 2 } = 0 . 1 7 ; P = < 0 . 0 0 1 ) , a n d$ both endogeic (NMDS;$R ^ { 2 } = 0 . 2 0 ;$p =< 0.001) and anecic (NMDS;$R ^ { 2 } = 0 . 1 9 ;$p =< 0.001) juveniles. Although the garden land-use type was not a signifcant factor afecting the earthworm community composition, the most abundant species can be allocated to specifc land-use types (Fig. 3, Table S1). In vegetable sites we primarily found endogeic species such as A. chlorotica (64.5%), which is tolerant to disturbances28 and a pioneer species58, endogeic juveniles (41.9%) and A. caliginosa (45.1%). Perennial grass sites were dominated by anecic species such as L. terrestris (52.5%) and anecic juveniles (47.6%), probably due to deeper and more compacted soils. As

Table 2.  Garden management practices based on the gardener survey (Table S3) and plant ecological indicator values refecting the plant environmental requirements81. Plant ecological indicator values are calculated as community weighted means of plant species found on each sampling plot.

expected, we found the lowest earthworm diversity (DSimpson) in vegetable sites (1.85 ± 0.2) and the highest in grass sites (2.57 ± 0.2). Te earthworm diversity was driven by endogeic and anecic species but not by epigeic species (Table 4). Additionally, we found the lowest beta diversity$( beta _ { 1 A C } )$for earthworms in vegetables and the highest in grass sites (Fig. S5, Table S5). However, evenness $( E _ { sin t }$pson) was not highest in vegetable sites but in grass sites and fower & berry sites, where we also observed higher nestedness components$( beta _ { 1 N E } ) .$

Springtails were affected by the plant ecological indicators moisture (PERMANOVA COL; F=3.7; p =< 0.001) and moisture variability (PERMANOVA COL; F=3.7;p=<0.001). Tese indicate moist soil or alternating soil moisture conditions, favouring species that were more abundant in grass sites such as S. aureus (81.1%) or P. alba (67.3%) on soils with high penetration resistance (PERMANOVA COL;F=2.3;;p=0.01)and $C _ { min }$(PERMANOVACOL;F=2.1;p=0.02). All three life forms of springtails were present in the species that had the biggest efect on the community composition (Table S4). B. hortensis showed the largest efect (NMDS; $R ^ { 2 } = 0 . 2 9 ; P = < 0 .$001), and was most ofen found in vegetable sites (75.5%), where also C. thermophilus (NMDS; R2 = 0.13; p =< 0.001) was ofen present (56.7%), correlating with potassium loads (PERMANOVA COL;F=2.5; p=<0.001). Other species driving the community composition of springtails were mostly found in grass sites, such as P. notabilis (85.4%), representing the most abundant (22.9%) springtail species (13,435 individuals) in this survey. Moreover, we found eight springtails (marked with stars in Table S1) which were not included yet in the Fauna Europaea species list, with two new records for Switzerland (I. balteatus and I. graminis) according to the available literature and expert opinion (c.f. Table S1). Te separation of fower & berry sites in the NMDS was mainly driven by C. denticulata (NMDS;$R ^ { 2 } = 0 . 0 8 ;$p =< 0.001). Moreover, we found a clear efect of garden land-use type (PERMANOVA COL;F=2.8;p =< 0.001), but also two signifcant efects of specifc garden man agement practices: applying water (PERMANOVA COL;F=2.5;P=<0.001) and weeding (PERMANOVA COL; F=1.8;p=0.04).. Weeding was more attributed to vegetable sites and applying water to grass sites in the NMDS ordination, whereas fower & berry sites were associated with a higher degree of urbanisation (PERMANOVA COL;F=1.8;P=0.04) and with more alkaline soils (basifcation; PERMANOVA COL;F=2.0;p=0..02). As expected, we found lower mean values for the springtail diversity$( D _ { S i m }$Pdon, Table S2) in vegetable sites (3.3±0.2) compared to grass sites (3.8 ± 0.1). Beta diversity (βJAC) was highest for fower & berry sites with a high turnover in comparison to the nestedness component (Fig. S5, Table S5). Springtail evenness (ESimpson) was highest in fower & berry sites, where we also found the highest nestedness component $( beta _ { 1 N E } )$, probably due to hemiedaphic and euedaphic species being more similar in fower & berry sites.

Additionally, we found diferences between garden land-use types in soil fauna disturbance indices. Te col lembolan ecomorphological index and the earthworm anecic to endogeic ratio were lowest in vegetable sites (Table S2). Te acari to collembola ratio was lowest in grass sites and the fungal to bacterial ratio was highest in vegetable sites.

Discussion

Worldwide, there is a growing interest of city administrations in the socio-economic and ecological benefts of urban gardens6,11,12,17,23,29,59. We investigated impacts of garden management practices on aboveground and belowground diversity and interlinked soil functions. Te SEM (Fig. 2, Table 3) revealed direct efects on soil multifunctionality and indirect efects mediated by soil fauna. Overall, our results showed that the largest efects on soil multifunctionality were caused by specifc soil characteristics. Soils showing high biological soil quality indices such as organic and microbial carbon and bacteria increased the potential for soil multifunctionality. Tis probably originates from organic gardening practices such as the application of compost, due to the correlation with increased potassium loads and with decreased bulk density values (Table 3, Table 1), also infuencing soil

Table 3.  Final most parsimonious structural equation model (SEM;$A I C = 1 5 6 . 3 , F i s h e r ^ { prime } s$C=24.3, P=0.93) indicating direct and indirect efects on soil multifunctionality from garden land-use types, garden management, plant and soil fauna diversity, soil fauna biomass, soil characteristics and urbanisation.$R ^ { 2 } _ { M } i s$ based on fxed efects and R2C on fxed and random (garden ID) efects. Total estimates of indirect pathways are given in Table S6.

quality22. Te second strongest efect on soil multifunctionality was caused by the cultivation of vegetables and legumes in annual vegetable sites (hypothesis (i), Fig. 1 arrows 1a), probably due to the frequent soil disturbance and the unprotected open soils in comparison to perennial grass sites. Te cultivation of fowers and berries increased plant diversity (Fig. 1 arrows 1b), but decreased soil fauna biomass compared to grass sites. Urban gar dens with higher plant diversity (hypothesis (ii), Fig. 1 arrows 3) increased soil multifunctionality directly, and indirectly through increasing fauna diversity and thus fauna biomass. Te general pattern of enhanced soil mul tifunctionality with increased plant diversity is in line with results found in other ecosystems such as croplands, shrublands, grasslands, and forests, where plant diversity increased ES such as pollination, C storage, pest control, and productivity60,61. Contrary to our expectations, we found no signifcant direct efect of management intensity on soil multifunctionality, but more intensively managed sites decreased plant diversity and fauna biomass. A

Table 4.  PERMANOVA of earthworms (PERMANOVA EW; lef) and springtails (PERMANOVA COL; right) and management practices, plant ecological indicators, soil characteristics and garden characteristics as explanatory variables. SA: Soil stable aggregates, BD: Soil bulk density, PR: Penetration resistance.

similar relationship of management intensity and decreased diversity has been observed in urban lawns. Lerman et al.62 showed that mowing only every three weeks instead of every week increased the numbers of fowers by 2.5 times and thus the abundance and diversity of bee populations. Although Tresch et al. showed that aboveground63 and belowground22 organic matter decomposition increased with urbanisation, there was no signifcant efect of urbanisation (hypothesis (v), Fig. 1 arrow 5), on soil multifunctionality.

Te structure of earthworm and springtail communities were infuenced by plant ecological indicators (Fig. 3, Table 3), representing the living conditions of plants. Interestingly, springtails were more afected by plant eco logical indicators than earthworms, highlighting the dominant infuence of plants on springtails50. As expected, we found a lower alpha diversity of earthworms and springtails in vegetable sites, likely due to the high soil distur bance. Beta diversity was constantly high in both soil fauna and plant communities, driven by high turnover and low nestedness components. Te plant community composition was shaped by the high species turnover between the garden sites, with highest dissimilarities for fower & berry sites. As expected, these signifcant diferences originated most likely from planting and other garden management practices leading to site specifc community compositions. Te beta diversity values for both fauna communities were lowest in vegetable sites and peaked for earthworms in grass sites and for springtails in fower & berry sites, refecting the diferent ecological strategies of earthworms and springtails.

Earthworms are important indicators for soil functioning51,52. Functional groups of earthworms have been used to detect impacts of cultivation in diferent soils such as pastures, orchards or forest soils, while the ratio of anecic to endogeic species was used as an indicator of contaminated soils64, or soil disturbance65. In the frequently

Figure 3.  Soil fauna community structure analysis of earthworms (a,b) and springtails (c,d). Soil fauna species are coloured in grey, corresponding to three ecological categories (Table S1). Only species with a signifcant (p < 0.001) efect (Table S4) and only signifcant explanatory variables (p < 0.05) from the PERMANOVA model (Table 1) were ftted. Garden land-use types include standard deviation bars.

disturbed vegetable sites we found the lowest values for the earthworm anecic to endogeic ratio and the collem bolan ecomorphological index, indicating a decreased soil biological quality due to soil disturbance48. Other stud ies have reported the highest value of the collembolan ecomorphological index in urban vegetable gardens and forest sites48. However, the highest value found in forest sites (2.3) was still considerably lower than the average we found in urban gardens of Zurich (5.8 ± 0.1), with a high number of euedaphic springtails such as P. pulvinata, F. quadriculata, and I. minor. Springtail abundance ofen increases from agricultural to forest sites66. Here they increased form vegetable to grass sites by a factor of 4.3. Besides soil disturbance, the increased abundance in grass sites could be explained by the higher plant cover of the perennially vegetated sites66 and because grass strips ofer a variety of microhabitats for soil mesofauna species48. In contrast, Joimel et al.48 found higher mean densities in vegetable beds than forest or grassland sites, underlining the quality of urban gardens for soil fauna biodiversity and soil quality. In addition, the increased organic matter content in urban garden soils3 can be an important factor for the high soil fauna diversity, since the input of organic matter in garden soils can be higher than in agri cultural felds67. Moreover, high management intensity is known to decrease soil mesofauna diversity68. We found a lower acari to collembola ratio in grass compared to fower & berry sites, which is in line with the dominance of acari in frequently disturbed arable or vineyard soils48. Additionally, we found a higher springtail biomass for grass sites, while earthworm biomass was at a similar and comparably high level in all urban garden land-use types. For instance, earthworm abundance (227.4 ± 15.5) was considerably higher than mean reference values for biological soil quality indicators found in grass or cropland soils69. Referring to all microorganisms68, $C _ { m i c }$ peaked for grass sites, while the mean value (780.9 ± 21.3) was higher than in cropland soils (341 mg kg−1), but lower than in grassland soils (1249 mg kg−1) found in Belgium69 or Switzerland70 (2077 mg kg−1). Tis pattern of $C _ { min }$ refected management practices such as fertilisation or tillage68. Additionally, the composition of soil micro organism communities is an important driver for soil functioning35. For instance, a shif in fungal composition or activity can increase carbon uptake and nutrient cycling35. Both soil disturbance71 or lower plant diversity72

can result in decreased fungal to bacterial ratios. While increasing fungal to bacterial ratios can be expected from desert to temperate grassland and forest soils, assuming that grassland soils are more bacteria dominated than forest soils26. Here, we found an increased fungal to bacterial ratio for vegetable sites, due to the increased fungal and decreased bacterial gene copy numbers in those sites (cf. Table S9, Fig. S13). Tis might be related to the input of compost on the vegetable sites or the increased plant diversity compared to grass sites.

Te intuitive and rather simple concept of multifunctionality24 and its reduction to one single metric, such as the averaging approach37, needs to be examined critically. For example, the functions and methods to measure them must be carefully selected42. Te strength of the biodiversity ecosystem multifunctionality relationships depends on the number of included functions, which was generally stronger when more functions were con sidered73. Another point is that the aggregation of multiple functions into one single metric can obscure infor mation about potentially contrasting single functions74. Te highest correlations among the soil functions (cf. Fig. S14) were found between $C _ { min }$and$N _ { min }$(r=0.45,p =< 0.001), both used to calculate soil nutrient supply, and between $C _ { min }$ and WHC(r=0..43,p =< 0.001). All other correlations(r<0.27) claimed a certain independence of the selected soil functions. Te moderately positive correlation of all components to soil multifunctionality is required, because negative correlations among functions can be a limitation for multifunctionality assessments73. However, this multifunctionality assessment framework could also be used in future studies to assess the impact of managed urban green spaces on nature’s contributions to people in cities.

With this city-wide assessment of the efect of urban gardening practices on aboveground and belowground diversity of plants and soil fauna, we demonstrated the potential impacts of gardeners’ decisions on the quality and functioning of the soil and implications on the biodiversity of a city. In conclusion, our study suggests that a higher plant diversity can directly or indirectly increase soil multifunctionality by enhancing soil fauna diversity and biomass. In a previous study, intensive garden management decreased soil quality indices22. Here we demon strated that a high garden management intensity indeed also declined plant diversity and soil fauna biomass, with negative impacts on soil multifunctionality. In addition, we analysed drivers shaping soil fauna community structure of earthworm and springtail species. We showed that both were afected by plant ecological indicators, soil characteristics, and management practices such as the frequency of soil disturbance or applying water. We conclude that increasing plant diversity together with soil protective management practices have the potential to increase soil functions as well as foster biodiversity, and to create more biophilic59 urban gardens, supporting human well-being and the ecological value of urban green spaces. Even though soil is a key resource in cities, it has not been integrated in most urban green space plans75, thus we recommend that urban gardens including ecological management practices should be integrated in future green city strategies.

Methods

Study design and gradients. Tis study took place in 85 urban gardens of the city of Zurich, Switzerland (Fig. S1). We selected gardens based on three independent criteria22,76: (i) the type of garden (domestic N=43vs. allotment;N=42Fig. S2), (ii) the management intensity (such as intensively managed vegetable or fower beds or extensively managed meadows), and (iii) the degree of urbanisation, ranging from densely built-up to peripheral areas within the city boundaries. In each garden two sampling plots (2 m × 2 m) with diferent land-use management were selected (Table S12), belonging to one of the following three categories: annual vegetable beds (vegetables;N=47), perennial fowers and berries (fowers & berries;N=52) or perennial lawn and meadows (grass;N=71), refecting the most dominant garden land-use types in Zurich and in many other cities.

Garden management practices were assessed using a questionnaire with 26 management questions, specifc for each land-use type, ranging from the frequency of lawn cutting to fertiliser application or weeding (Table S3). Garden management intensity was assessed as the sum of 26 management questions. In addition, fve common management practices (disturbance, fertiliser, pesticides, water, weeding; Table 2) were used in the commu nity composition analysis. Urban warming was used as a proxy for urbanisation due to the correlation with the amount of built-up and paved area for diferent radii (30–500 m) around the gardens63. It has been assessed as the deviation in local mean air temperatures at night near the surface based on a local climate model77, showing temperatures increased of up to 5 °C for urbanised gardens.

Aboveground diversity. Plant diversity was assessed by a foristic inventory78 of cultivated and spontane ously growing plants on each sampling plot (N = 170). Based on this inventory of 600 plant species, we calculated plant alpha diversity as the total number of plant species per sampling plot and plant beta diversity as the mean of the pairwise Jaccard dissimilarity comparisons between each focal plot and all other plots79. Additionally, we used a six-point ordinal scale78 to calculate community weighted mean values of seven plant ecological indicator values80 (Table 2), refecting the plant environmental requirements81.

Belowground diversity. Earthworms were collected in a smaller subplot of 0.3 m × 0.3 m within the 2m×2m sampling plots by a combined hand sorting and mustard extraction method22. Earthworms were stored in 70% ethanol58, identifed to the species level, and classifed into three ecological categories (Table S1): epigeic species (living in the litter layer, with little burrowing activity), endogeic species (living in the soil, with horizontal burrows) and anecic species (living in large and deep vertical burrows).

Springtails and mites were sampled with six undisturbed soil cores (5 cm diameter, 8 cm length, Eijkelkamp, NL) randomly taken in the 2 m × 2 m sampling plots63. Springtails were identifed to the species level including life forms according to ecological and functional traits (Table S1): epedaphic species (living in the upper litter layer), hemiedaphic species (living at the interface between litter and soil) and euedaphic species (soil-dwelling species).

We defned soil fauna diversity as the average proportional species richness across soil macrofauna (earth worms) and mesofauna (springtails) species following Allan et al.82. Soil fauna beta diversity was calculated as the average proportional species beta diversity of earthworms and springtails, while the individual measures of beta diversity per soil fauna group were computed as mean pairwise Jaccard dissimilarities, similarly to the plant beta diversity. Soil fauna biomass was calculated as the average proportion of biomass per m2 of soil, with measured earthworm biomass [gm−2] on an individual basis (including gut contents) and estimated springtail biomass (conversion factor of 5 g for each springtail83).

Soil fauna disturbance indices. Te adaptation of soil fauna to management practices was assessed with four soil fauna disturbance indices: the collembolan ecomorphological index48, the acari to collembola ratio84, the fungal to bacterial ratio26, and the earthworm anecic to endogeic ratio64.

Soil characteristics. Soil characteristics were assessed with a combination of three physical, six chemical and four biological soil measurements (Table 1), representing the most commonly used soil quality indicator measurements85. Te microbial community information of bacterial (16S) and fungal (18S) gene copy numbers were used to calculate the fungal to bacterial ratio. Measurement details can be found in Table S13 and Tresch et al.86.

Soil multifunctionality. Similar to other studies87 we used the averaging approach37 to calculate soil multi functionality. It calculates the mean value across standardised soil functions for each sampling plot. In total, we used fve measurements (Table S11), which are related to important soil functions, for the computation of soil multifunctionality. Te three assessed key soil functions are (i) aboveground and belowground litter decompo sition, (ii) soil nutrient supply, and (iii) soil water storage and regulation. Te soil function litter decomposition aboveground was measured by standardised leaf litter mass loss (Zea mays L.) in 4 mm mesh sized litter bags63, while belowground litter decomposition was measured by the net mass loss of green tea bags, buried in 8 cm soil depth22. Te supply of nutrients in the soil was assessed by the mineralisation rates of N$( N _ { min } )$ and C$( C _ { min } )$, and the capacity of the soil for water regulation, was measured by the water holding capacity (WHC).

Data analysis. Soil fauna diversity and biomass were calculated by taking species richness per taxonomic group, applying a standardisation for each taxonomic group scaled to a range from 0 to 1$( f ( x ) = ( x _ { i } - x _ { min } )$ $/ ( x _ { max } - x _ { min } ) )$ and then averaging the values for each plot82. Aboveground and belowground beta diversity were calculated as mean pairwise Jaccard dissimilarities comparing each focal plot to all other sampling plots79 using the R package ‘betapart’88. Soil multifunctionality was computed by scaling each of the fve measurements of soil functions to a range from 0 to 187 and deriving mean values across the standardised soil functions according to the averaging approach37. Community weighted means of plant ecological indicators were calculated with the R pack age ‘FD’89.

We ftted a piecewise structural equation model (SEM), with the ‘piecewiseSEM’ package57, to infer relative importance of direct and indirect efects of urban gardening, plant diversity, urbanisation and soil characteristics on soil fauna and soil multifunctionality. To address multicollinearity and reduce the amount of variables we applied a PCA for the soil characteristics and used the frst four PCA axes, explaining 64.2% (Table 1; Fig. S4) of the variation (Kaiser-Guttman criteria). We used Shipley’s d-separation test to identify missing paths in the SEM and the AICC for model comparison. We used linear mixed efect models (LMEM; lme(nlme;90) with the garden as random efect for each SEM component and reported standardised (scaled by mean and variance) path coefcients, as well as marginal R2 and conditional R2 based on fxed and random efects57 (Table 3). Model assumptions were tested (Fig. S11) and potential spatial autocorrelation patterns were calculated with Moran’s I autocorrelation indices and the spatial structure in the model residuals using semivariograms (Fig. S12).

We applied individual LMEM with garden identity as random efect and land-use types as response varia bles to assess changes in fauna and plant diversity and soil fauna disturbance indices. We checked for normal distribution, autocorrelation, and heteroscedasticity of the model residuals and applied a transformation (log(x+1)) in the cases of: earthworm biomass, anecic to endogeic ratio, acari to collembola ratio and spring tail biomass. We reported means and 95% credible intervals of the Bayesian inference posterior distribution based on 10,000 independent simulations91. Soil fauna community structure was further analysed using a per mutational multivariate analysis of variance (PERMANOVA, 10,000 permutations) with a Hellinger trans formed Euclidean distance species matrix of earthworms (EW) and springtails (COL) and a non-metric multidimensional scaling (NMDS) using the ‘vegan’ package92. For the NMDS only signifcant variables from the PERMANOVA were ftted. Data management and statistical analyses are provided as an R project using R 3.4.2 (R Core Team, 2017).

References

1. United Nations. Transforming our world: Te 2030 agenda for sustainable development. Tech. Rep. (2015).
   1. Loram, A., Warren, P. H. & Gaston, K. J. Urban Domestic Gardens (XIV): Te Characteristics of Gardens in Five Cities. Environ.Manag. 42, 361–376, https://doi.org/10.1007/s00267-008-9097-3 (2008).
2. Edmondson, J. L., Davies, Z. G., Gaston, K. J. & Leake, J. R. Urban cultivation in allotments maintains soil qualities adversely afected by conventional agriculture. J. Appl. Ecol. 51, 880–889, https://doi.org/10.1111/1365-2664.12254 (2014).
   1. Soanes, K. et al. Correcting common misconceptions to inspire conservation action in urban environments. Conserv. Biol. 33, 300–306, https://doi.org/10.1111/cobi.13193 (2019).

   2. Owen, J. Te Ecology of a Garden: Te First Fifeen Years. (Cambridge University Press, Cambridge, 1991).

   3. Goddard, M. A., Dougill, A. J. & Benton, T. G. Scaling up from gardens: biodiversity conservation in urban environments. Trends Ecol. Evol. 25, 90–98, https://doi.org/10.1016/j.tree.2009.07.016 (2010).

   4. Martellozzo, F. Forecasting High Correlation Transition of Agricultural Landscapes into Urban Areas. Int. J. Agric. Environ. Inf. Syst.3, 22–34, https://doi.org/10.4018/jaeis.2012070102 (2012).

   5. Tan, P. Y. & Jim, C. Y. Greening Cities. Advances in 21st Century Human Settlements (Springer Singapore, Singapore, 2017).

   6. Endreny, T. A. Strategically growing the urban forest will improve our world. Nat. Commun. 9, 1160, https://doi.org/10.1038/s41467018-03622-0 (2018).

   7. Lee-Smith, D. Cities feeding people: an update on urban agriculture in equatorial Africa. Environ. Urban. 22, 483–499, https://doi.org/10.1177/0956247810377383 (2010).

   8. Siegner, A., Sowerwine, J. & Acey, C. Does Urban Agriculture Improve Food Security? Examining the Nexus of Food Access and Distribution of Urban Produced Foods in the United States: A Systematic Review. Sustainability 10, 2988, https://doi.org/10.3390/su10092988 (2018).

   9. Redwood, M. Agriculture in urban planning: generating livelihoods and food security (Routledge, 2009).

   10. Bolund, P. & Hunhammar, S. Ecosystem services in urban areas. Ecol. Econ. 29, 293–301, https://doi.org/10.1016/S09218009(99)00013-0 (1999).

   11. Edmondson, J. L., Davies, Z. G., McHugh, N., Gaston, K. J. & Leake, J. R. Organic carbon hidden in urban ecosystems. Sci. Rep. 2,963, https://doi.org/10.1038/srep00963 (2012).

   12. Samnegård, U., Persson, A. S. & Smith, H. G. Gardens beneft bees and enhance pollination in intensively managed farmland. Biol.Conserv. 144, 2602–2606, https://doi.org/10.1016/j.biocon.2011.07.008 (2011).

   13. Levin, M. J. et al. Soils within Cities. (2017).

   14. Frey, D. et al. Predation risk shaped by habitat and landscape complexity in urban environments. J. Appl. Ecol. 55, 2343–2353, https://doi.org/10.1111/1365-2664.13189 (2018).

   15. Susca, T., Gafn, S. & Dell’Osso, G. Positive efects of vegetation: Urban heat island and green roofs. Environ. Pollut. 159, 2119–2126, https://doi.org/10.1016/j.envpol.2011.03.007 (2011).

   16. Hofmann, M., Young, C., Binz, T. M., Baumgartner, M. R. & Bauer, N. Contact to nature benefts health: Mixed efectiveness of diferent mechanisms. Int. J. Environ. Res. Public Heal. 15, https://doi.org/10.3390/ijerph15010031 (2018).

   17. Bardgett, R. D. Earth Matters: How soil underlies civilization. (Oxford University Press, Oxford, 2016).

   18. Cogger, C. G. Potential Compost Benefts for Restoration Of Soils Disturbed by Urban Development. Compost. Sci. Util. 13, 243–251, https://doi.org/10.1080/1065657X.2005.10702248 (2005).

   19. Tresch, S. et al. A Gardener’s Infuence on Urban Soil Quality. Front. Environ. Sci. 6, https://doi.org/10.3389/fenvs.2018.00025 (2018).

   20. Cabral, I. et al. Ecosystem services of allotment and community gardens: A Leipzig, Germany case study. Urban For. Urban Green.23, 44–53, https://doi.org/10.1016/j.ufug.2017.02.008 (2017).

   21. Hector, A. & Bagchi, R. Biodiversity and ecosystem multifunctionality. Nature 448, 188–190, https://doi.org/10.1038/nature05947 (2007).

   22. Wall, D. H., Bardgett, R. D. & Kelly, E. Biodiversity in the dark. Nat. Geosci. 3, 297–298, https://doi.org/10.1038/ngeo860 (2010).

   23. Fierer, N., Strickland, M. S., Liptzin, D., Bradford, M. A. & Cleveland, C. C. Global patterns in belowground communities. Ecol. Lett.12, 1238–1249, https://doi.org/10.1111/j.1461-0248.2009.01360.x (2009).

   24. Buchholz, J. et al. Soil biota in vineyards are more infuenced by plants and soil quality than by tillage intensity or the surrounding landscape. Sci. Rep. 7, 1–12, https://doi.org/10.1038/s41598-017-17601-w (2017).

   25. Amossé, J. et al. Patterns of earthworm, enchytraeid and nematode diversity and community structure in urban soils of diferent ages. Eur. J. Soil Biol. 73, 46–58, https://doi.org/10.1016/j.ejsobi.2016.01.004 (2016).

   26. Lorenz, K. Managing Urban Soils for Food Production. In Steward, T. A. & Lal, R. (eds) Urban Soils (Boca Raton: CRC Press., 2017). 30. Bardgett, R. & Van Der Putten, W. Belowground biodiversity and ecosystem functioning. Nature 515, 505–511, https://doi.org/10.1038/nature13855 (2014).

   27. Mori, A. S., Isbell, F. & Seidl, R. β-Diversity, Community Assembly, and Ecosystem Functioning. Trends Ecol. Evol. 33, 549–564, https://doi.org/10.1016/j.tree.2018.04.012 (2018).

   28. Wagg, C., Bender, S. F., Widmer, F. & van der Heijden, M. G. A. Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc. Natl. Acad. Sci. 111, 5266–5270, https://doi.org/10.1073/pnas.1320054111, arXiv:1604.05974v2 (2014).

   29. Dedeyn, G. & van der Putten, W. H. Linking aboveground and belowground diversity. Trends Ecol. Evol. 20, 625–633, https://doi.org/10.1016/j.tree.2005.08.009 (2005).

   30. Wardle, D. A. Communities and Ecosystems Linking the Aboveground and Belowground Components. No. Vol. 34 in Monographs in Population Biology (Princeton University Press, 2002).

   31. Morriën, E. et al. Soil networks become more connected and take up more carbon as nature restoration progresses. Nat. Commun.8, 14349, https://doi.org/10.1038/ncomms14349 (2017).

   32. Vauramo, S. & Setälä, H. Decomposition of labile and recalcitrant litter types under diferent plant communities in urban soils.Urban Ecosyst. 14, 59–70, https://doi.org/10.1007/s11252-010-0140-9 (2011).

   33. Byrnes, J. E. K. et al. Investigating the relationship between biodiversity and ecosystem multifunctionality: Challenges and solutions.Methods Ecol. Evol. 5, 111–124, https://doi.org/10.1111/2041-210X.12143, arXiv:1011.1669v3 (2014).

   34. Manning, P. et al. Redefning ecosystem multifunctionality. Nat. Ecol. Evol. 2, 427–436, https://doi.org/10.1038/s41559-017-0461-7 (2018).

   35. Mori, A. S. et al. Low multifunctional redundancy of soil fungal diversity at multiple scales. Ecol. Lett. 19, 249–259, https://doi.org/10.1111/ele.12560 (2016).

   36. Alsterberg, C. et al. Habitat diversity and ecosystem multifunctionality—Te importance of direct and indirect efects. Sci. Adv. 3, https://doi.org/10.1126/sciadv.1601475 (2017).

   37. Delgado-Baquerizo, M. et al. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat. Commun. 7, 10541, https://doi.org/10.1038/ncomms10541 (2016).

   38. Allan, E. et al. Land use intensifcation alters ecosystem multifunctionality via loss of biodiversity and changes to functional composition. Ecol. Lett. 18, 834–843, https://doi.org/10.1111/ele.12469 (2015).

   39. Lundholm, J. T. Green roof plant species diversity improves ecosystem multifunctionality. J. Appl. Ecol. 52, 726–734, https://doi.org/10.1111/1365-2664.12425, arXiv:1011.1669v3 (2015).

   40. Wall, D. H. et al. Global decomposition experiment shows soil animal impacts on decomposition are climate-dependent. Glob.Chang. Biol. 14, 2661–2677, https://doi.org/10.1111/j.1365-2486.2008.01672.x (2008).

   41. Van Eekeren, N. et al. Ecosystem services in grassland associated with biotic and abiotic soil parameters. Soil Biol. Biochem. 42, 1491–1504, https://doi.org/10.1016/j.soilbio.2010.05.016 (2010).

   42. Egerer, M. H. et al. Herbivore regulation in urban agroecosystems: Direct and indirect efects. Basic Appl. Ecol. 29, 44–54, https://doi.org/10.1016/j.baae.2018.02.006 (2018).

   43. Smetak, K. M., Johnson-Maynard, J. L. & Lloyd, J. E. Earthworm population density and diversity in diferent-aged urban systems.Appl. Soil Ecol. 37, 161–168, https://doi.org/10.1016/j.apsoil.2007.06.004 (2007).

   44. Joimel, S. et al. Urban and industrial land uses have a higher soil biological quality than expected from physicochemical quality. Sci.Total. Environ. 584–585, 614–621, https://doi.org/10.1016/j.scitotenv.2017.01.086 (2017).

   45. Setälä, H. M. et al. Vegetation Type and Age Drive Changes in Soil Properties, Nitrogen, and Carbon Sequestration in Urban Parks under Cold Climate. Front. Ecol. Evol. 4, 1–14, https://doi.org/10.3389/fevo.2016.00093 (2016).

   46. Gobat, J. M., Aragno, M. & Matthey, W. Te Living Soil, Fundamentals of Soil Science and Soil Biology. (Science Publishers, Enfeld, NS, Canada, 2004).

   47. Blouin, M. et al. A review of earthworm impact on soil function and ecosystem services. Eur. J. Soil Sci. 64, 161–182, https://doi.org/10.1111/ejss.12025, 0000-0002-8166-1526 (2013).

   48. Le Bayon, R.-C. et al. Earthworms as ecosystem engineers: A review (Nova Science Publishers, Inc., 2017).

   49. de Lima e Silva, C. et al. Comparative toxicity of imidacloprid and thiacloprid to diferent species of soil invertebrates. Ecotoxicology 26, 555–564, 10.1007Vs10646-017-1790-7, arXiv:1408.1149 (2017).

   50. dos Santos, M. A. B. et al. Morphological Diversity of Springtails in Land Use Systems. Rev. Bras. Ciência do Solo 42, 1–19, https://doi.org/10.1590/18069657rbcs20170277 (2018).

   51. Hopkin, S. P. Biology of the springtails:(Insecta: Collembola) (OUP Oxford, 1997).

   52. Shipley, B. A New Inferential Test for Path Models Based on Directed Acyclic Graphs. Struct. Equ. Model. A Multidiscip. J. 7, 206–218, https://doi.org/10.1207/S15328007SEM0702_4 (2000).

   53. Lefcheck, J. S. piecewiseSEM: Piecewise structural equation modelling in r for ecology, evolution, and systematics. Methods Ecol.Evol. 7, 573–579, https://doi.org/10.1111/2041-210X.12512, 1509.01845 (2016).

   54. Schomburg, A. et al. Topsoil structure stability in a restored foodplain: Impacts of fuctuating water levels, soil parameters and ecosystem engineers. Sci. Total. Environ. 639, 1610–1622, https://doi.org/10.1016/j.scitotenv.2018.05.120 (2018).

   55. Lin, B. B., Egerer, M. H. & Ossola, A. Urban Gardens as a Space to Engender Biophilia: Evidence and Ways Forward. Front. Built Environ. 4, 1–10, https://doi.org/10.3389/fuil.2018.00079 (2018).

   56. Isbell, F. et al. Benefts of increasing plant diversity in sustainable agroecosystems. J. Ecol. 105, 871–879, https://doi.org/10.1111/13652745.12789 (2017).

   57. Chen, S. et al. Plant diversity enhances productivity and soil carbon storage. Proc. Natl. Acad. Sci. 115, 4027–4032, https://doi.org/10.1073/pnas.1700298114 (2018).

   58. Lerman, S. B., Contosta, A. R., Milam, J. & Bang, C. To mow or to mow less: Lawn mowing frequency afects bee abundance and diversity in suburban yards. Biol. Conserv. 221, 160–174, https://doi.org/10.1016/j.biocon.2018.01.025 (2018).

   59. Tresch, S. et al. Litter decomposition driven by soil fauna, plant diversity and soil management in urban gardens. Sci. Total. Environ.658, 1614–1629, https://doi.org/10.1016/j.scitotenv.2018.12.235 (2019).

   60. Pérès, G. et al. Earthworm indicators as tools for soil monitoring, characterization and risk assessment. An example from the national Bioindicator programme (France). Pedobiologia (Jena). 54, https://doi.org/10.1016/j.pedobi.2011.09.015 (2011).

   61. Fournier, B., Samaritani, E., Shrestha, J., Mitchell, E. A. & Le Bayon, R. C. Patterns of earthworm communities and species traits in relation to the perturbation gradient of a restored foodplain. Appl. Soil Ecol. 59, 87–95, https://doi.org/10.1016/j.apsoil.2012.03.015 (2012).

   62. Sousa, J. P. et al. Changes in Collembola richness and diversity along a gradient of land-use intensity: A pan European study.Pedobiologia (Jena). 50, 147–156, https://doi.org/10.1016/j.pedobi.2005.10.005 (2006).

   63. Joimel, S. et al. Physico-chemical characteristics of topsoil for contrasted forest, agricultural, urban and industrial land uses in France. Sci. Total. Environ. 545–546, 40–47, https://doi.org/10.1016/j.scitotenv.2015.12.035 (2016).

   64. Cluzeau, D. et al. Integration of biodiversity in soil quality monitoring: Baselines for microbial and soil fauna parameters for diferent land-use types. Eur. J. Soil Biol. 49, 63–72, https://doi.org/10.1016/j.ejsobi.2011.11.003 (2012).

   65. Krüger, I., Chartin, C., van Wesemael, B. & Carnol, M. Defning a reference system for biological indicators of agricultural soil quality in Wallonia, Belgium. Ecol. Indic. 95, 568–578, https://doi.org/10.1016/j.ecolind.2018.08.010 (2018).

   66. Oberholzer, H. R. & Scheid, S. Bodenmikrobiologische Kennwerte. Erfassung des Zustands landwirtschaflicher Böden im NABO Referenzmessnetz anhand biologischer Parameter (NABObio). Umwelt-Wissen (2007).

   67. Parftt, R. L. et al. Efect of fertilizer, herbicide and grazing management of pastures on plant and soil communities. Appl. Soil Ecol.45, 175–186, https://doi.org/10.1016/j.apsoil.2010.03.010 (2010).

   68. Eisenhauer, N. et al. Root biomass and exudates link plant diversity with soil bacterial and fungal biomass. Sci. Rep. 7, 1–8, https://doi.org/10.1038/srep44641, NIHMS150003 (2017).

   69. Meyer, S. T. et al. Biodiversity–multifunctionality relationships depend on identity and number of measured functions. Nat. Ecol.Evol. 2, 44–49, https://doi.org/10.1038/s41559-017-0391-4 (2018).

   70. Bradford, M. A. et al. Discontinuity in the responses of ecosystem processes and multifunctionality to altered soil community composition. Proc. Natl. Acad. Sci. 111, 14478–14483, https://doi.org/10.1073/pnas.1413707111 (2014).

   71. Teixeira da Silva, R., Fleskens, L., van Delden, H. & van der Ploeg, M. Incorporating soil ecosystem services into urban planning: status, challenges and opportunities. Landsc. Ecol. 33, 1087–1102, https://doi.org/10.1007/s10980-018-0652-x (2018).

   72. Young, C., Frey, D., Moretti, M. & Bauer, N. Research Note: Garden-owner reported habitat heterogeneity predicts plant species richness in urban gardens. Landsc. Urban Plan. 185, 222–227, https://doi.org/10.1016/j.landurbplan.2019.01.013 (2019).

   73. Parlow, E., Scherer, D. & Fehrenbach, U. Klimaanalyse der Stadt Zürich (KLAZ) - Wissenschaflicher Bericht. Tech. Rep. (2010).

   74. Frey, D. & Moretti, M. A comprehensive dataset on cultivated and spontaneously growing vascular plants in urban gardens. Data Br. in press, 103982, https://doi.org/10.1016/j.dib.2019.103982 (2019).

   75. Villéger, S., Grenouillet, G. & Brosse, S. Decomposing functional b-diversity reveals that low functional b-diversity is driven by low functional turnover in European fsh assemblages. Glob. Ecol. Biogeogr. 22, 671–681, https://doi.org/10.1111/geb.12021, 1106.4388 (2013).

   76. Landolt, E. et al. Flora indicativa. Ecological indicators values and biological attributes of the fora of Switzerland and the Alps. 2nd edn.(Haupt Verlag, Bern, 2010).

   77. Wildi, O. Why mean indicator values are not biased. J. Veg. Sci. 27, 40–49, https://doi.org/10.1111/jvs.12336 (2016).

   78. Allan, E. et al. Interannual variation in land-use intensity enhances grassland multidiversity. Proc. Natl. Acad. Sci. 111, 308–313, https://doi.org/10.1073/pnas.1312213111 (2014).

   79. Petersen, H. & Luxton, M. A Comparative Analysis of Soil Fauna Populations and Teir Role in Decomposition Processes. Oikos 39, 288, https://doi.org/10.2307/3544689 (1982).

   80. Parisi, V., Menta, C., Gardi, C., Jacomini, C. & Mozzanica, E. Microarthropod communities as a tool to assess soil quality and biodiversity: A new approach in Italy. Agric. Ecosyst. Environ. 105, 323–333, https://doi.org/10.1016/j.agee.2004.02.002 (2005).

   81. Bünemann, E. K. et al. Soil quality – A critical review. Soil Biol. Biochem. 120, 105–125, https://doi.org/10.1016/j.soilbio.2018.01.030, arXiv:1011.1669v3 (2018).

   82. Tresch, S. et al. Urban Soil Quality Assessment—A Comprehensive Case Study Dataset of Urban Garden Soils. Front. Environ. Sci.6, 1–5, https://doi.org/10.3389/fenvs.2018.00136 (2018).

   83. Schuldt, A. et al. Biodiversity across trophic levels drives multifunctionality in highly diverse forests. Nat. Commun. 9, 2989, https://doi.org/10.1038/s41467-018-05421-z (2018).

   84. Baselga, A. & Orme, C. D. L. Betapart: An R package for the study of beta diversity. Methods Ecol. Evol. 3, 808–812, https://doi.org/10.1111/j.2041-210X.2012.00224.x (2012).

   85. Laliberté, E. & Legendre, P. A distance-based framework for measuring functional diversity from multiple traits. Ecology 91, 299–305, https://doi.org/10.1890/08-2244.1 (2010).

   86. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & R Core Team. {nlme}: Linear and Nonlinear Mixed Efects Models (2018).

   87. Korner-Nievergelt, F. et al. Bayesian data analysis in ecology using linear models with R, BUGS, and Stan (Academic Press, 2015).

   88. Oksanen, J. et al. vegan: Community Ecology Package (2017).

Acknowledgements

We are grateful to Adolphe Munyangabe and Anton Kuhn (soil measurements), Lena Fischer (tea bag index and earthworm extraction), Stefan Grubelnig and Reto Henzmann (soil and soil fauna sampling), Dr. Lukas Pffner (earthworm identifcation), Dr. Daniel Haefelfnger (litter bag decomposition), and Dr. Joerg Salamon (collembola identifcation) for their extraordinary support and help in the feld or laboratory. In particular, we thank Dr. Robert Home for his support in fnalising the manuscript and the 85 participating gardeners of this study for granting access to their gardens and their interest in promoting biodiversity in cities. We gratefully acknowledge the fnancial support for this interdisciplinary project BetterGardens provided by the Swiss National Science Foundation in frame of the Sinergia program (CRSII1_154416).

Author Contributions

A.F., M.M., R.L., P.M., D.F. and S.T. conceived and designed the research, S.T. performed both feld and laboratory work with the help of B.S. and D.F. S.T. analysed the data. All authors reviewed the manuscript.

Additional Information

Supplementary information accompanies this paper at https://doi.org/10.1038/s41598-019-46024-y.

Competing Interests: Te authors declare no competing interests.

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional afliations.

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Cre ative Commons license, and indicate if changes were made. Te images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not per mitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

Image from https://pxhere.com/en/photo/991732