Corresponding author: Juha Pöyry (
Academic editor: I. Steffan-Dewenter
A landfill site in southern Finland was converted into urban green space by covering it with a layer of fresh forest humus transferred from nearby construction sites. The aim was to develop the 70 m high artificial hill into a recreational area with high biodiversity of flora and fauna. Forest humus was used as a source of organic matter, plant roots, seeds, soil fauna and microorganisms in order to enable rapid regeneration of diverse vegetation and soil biological functions. In this study we report the results of three years of monitoring of soil enzyme activity and plant species compositional patterns. Monthly soil samples were taken each year between June and September from four sites on the hill and from two standing reference forests using three replicate plots. Activities of 10 different enzymes, soil organic matter (SOM) content, moisture, pH and temperature of the surface layer were monitored. Abundances of vascular plant species were surveyed on the same four hill sites between late May and early September, three times a season in 2004 and 2005. Although the addition of organic soil considerably increased soil enzyme activities (per dw), the activities at the covered hill sites were far lower than in the reference forests. Temporal changes and differences between sites were analysed in more detail per soil organic matter (SOM) in order to reveal differences in the quality of SOM. All the sites had a characteristic enzyme activity pattern and two hill sites showed clear temporal changes. The enzyme activities in uncovered topsoil increased, whereas the activities at the covered Middle site decreased, when compared with other sites at the same time. The different trend between Middle and North sites in enzyme activities may reflect differences in humus material transferred to these sites, but difference in the succession of vegetation affects enzyme activities strongly. Middle yielded higher β-sitosterol content in 2004, as an indication of more intense plant impact. All reclaimed sites had characteristic plant species assemblages and parallel temporal changes, reflecting vegetation succession, occurred across all the sites. Rapid growth of vegetation on the covered sites restored the rhizosphere and contributed to the persistence of microbial activity. We suggest that transferring the surface soil humus layer is a useful approach for ensuring the outcome of habitat restoration and complementary habitat creation especially in situations where the source soil areas would otherwise be lost.
Niemi RM, Pöyry J, Heiskanen I, Uotinen V, Nieminen M, Erkomaa K, Wallenius K (2014) Variability of soil enzyme activities and vegetation succession following boreal forest surface soil transfer to an artificial hill. Nature Conservation 8: 1–25. doi:
Land and soil use is drastically altered in a growing city, where new territory is needed for housing and for the infrastructure (
Plant root and leaf litter is the primary source of soil organic matter and it affects the quality and quantity of carbon substrates and nutrients available to free-living fungi and bacteria. Helsinki City had constructed an artificial hill using mainly mineral soil removed from construction sites. As a novel approach to the various needs of landscaping, building of recreation areas and restoring biological diversity and functions through utilisation of surface soils removed from discontinued forest sites under constructional development, it was decided to collect the organic surface layer of forest separately and to use this biologically diverse material to cover a barren artificial hill. Fresh forest soil humus was distributed as a layer of a few tens of centimetres on a hill area, excluding steep slopes. The intention was to enhance the development of vegetation on the hill, to improve its recreational value and to restore biological functionality and ecosystem services through the increase in biodiversity (e.g.
Habitat creation is potentially a very efficient tool for enhancing biodiversity in highly disturbed or completely artificial sites. The habitats being created are typically novel ones with plant and animal communities characteristically different from naturally occurring communities (
The aim of our study was to monitor temporal changes in the enzyme activity and developing vegetation, and to compare the enzyme activity patterns in surface soil and plant species composition in order to reveal changes due to alteration in vegetation, as well as in litter quality and quantity and in physical conditions important to soil biota (moisture, temperature, pH). Regards to vegetation composition we hypothesize that vegetation succession should in the early phases be faster in moist depression (e.g. Grove) than in more exposed experimental sites (e.g. Top). On enzyme activities we hypothesize that (1) surface soil transfer decreases enzyme activities, (2) increase in vegetation supports enzyme activities in transferred soil and (3) plant species composition affects enzyme activity patterns. The enzyme activity pattern measured consisted of fundamental reactions in macromolecule degradation: arylsulphatase releases inorganic S, phosphomonoestarase and phosphodiesterase release inorganic P from organic molecules, and alanine and leucine aminopeptidases hydrolyze the amino-terminal from amino acids of peptides and some proteins. β-N-Acetyl hexosaminidase degrades chitin. Cellobiohydrolase and β-glucosidase are active in the degradation of cellulose into sugar monomers and β-xylosidase in the hydrolysis of xylo-oligosaccharides produced in the degradation of xylan. α-Glucosidase degrades starch. Soil ergosterol content is widely used as a measure of fungal biomass (
The study area is a former landfill site situated in Helsinki City, in the proximity of the Gulf of Finland. A total of about 5*106 m3 of mineral soil and non-biodegradable construction waste was transferred to the artificial hill site area of 38 hectares between 1990 and 2002. The organic surface layer of forest soil was distributed to the hill sites, excluding steep slopes and the hill top, in spring 2003. Heavy machinery (typical to mine industry and construction) was used for the collection, transportation and distribution on the soil cover. Due to the large-scale operation, characteristics of the humus material collected over large forest areas and level of mixing with mineral soil may have varied. Soil cover depth varied also, when organic material was spread over an uneven terrain. Middle and North sites were covered with surface soil from clear cut spruce forest and Grove was covered with clay and surface soil from an alder grove. Later Grove was planted with siblings of ash (
Three replicate 10 m × 10 m plots of four hill sites (Middle, North, Grove and Top) and of two reference sites were selected for soil microbial activity studies (Fig.
Map of the study area. The study area is situated in Helsinki City (
Characteristics of the sites monitored (see Fig.
Site | Characteristics |
---|---|
Top | The top of the hill consisted of moraine. Vegetation was sparse but increased slightly during the monitoring. |
Grove | Indentation on the southwest side of the hill. The bottom was covered with clay to prevent water infiltration and the clay layer was covered with surface soil from a black alder ( |
Middle | Ridge site in the middle of the hill. Sandy moraine was covered with surface layer of old |
North | Ridge site in the north side of the hill. Sandy moraine was covered with surface layer of old |
Alder | Old |
Spruce | About 60 years old |
For studies of vegetation composition, the abundance of all vascular plant species was surveyed in the same hill site (Middle, North, Grove and Top) replicate plots as in the microbial activity study three times (late May, early July and early September) in 2004 and 2005. Plant abundance was estimated using a frequency method in which the number of positive records across sampling plots is summed and used to describe the commonness of a species. Here we applied this method so that each replicate plot was further divided into nine subplots and the number of subplots with positive records of a species was then used as the measure of abundance of vascular plants in plots (
The sieved samples were stored at +5 °C for 1 to 7 d before measuring dry weight, loss on ignition and pHKCl in duplicate. For the measurement of soil dry weight and water content, fresh samples were dried at 105 °C overnight. Soil organic matter content (SOM) was determined by loss on ignition at 550 °C. For the pH measurement, 10 g of soil was weighed to 50 ml of 1 mol l-1 KCl solution in a screw cap bottle. After 10 min shaking at 200 rpm and settling for 2 h, pH was measured from the liquid phase using an Orion 550A electrode. Soil moisture and temperature were measured in the field at 5 cm depth on all the sampling dates from each plot at 20 random points using an HH2 Moisture Meter- instrument with a WET-sensor (Delta-T Devices Ltd). The means of 60 measurements for each site were calculated.
Samples were stored at +5 °C for 3 d and then, depending on the SOM content, 0.9 to 5.5 g aliquots were weighed into distillation flasks and 50 ml methanol (Rathburn, HPLC quality) was added and the suspensions were stored well capped at –20 °C until analysed for ergosterol and β-sitosterol. The slightly modified method of
Enzyme activities were measured from 4 g samples stored in small plastic bags at –20 °C for 6 to 38 d (
Multivariate ordination methods with non-metric multidimensional scaling (NMDS; see (
We performed two NMDS runs with both the enzyme activity and plant species data, one with all the replicate samples handled separately and the other using monthly site means in the analysis but using otherwise similar settings. After performing the first NMDS run, Pearson correlations between axis scores for sites and environmental variables were calculated. Next, multiresponse permutation procedures (MRPP), a method designed for testing group-wise differences (
Cluster analysis using Gower's coefficient and Ward's method was applied for enzyme activity data calculated per loss on ignition (SOM) using home tailored programs (ZymProfiler).
The surface soils of the reference forests, with rather even terrain and trees providing shadow, were more moist, contained more organic matter and had lower temperatures than the hill sites (Table
Ranges and medians for each site and year for the physical and chemical characteristics.
Water content % | SOM % | Temperature | pHKCl | ||||||
---|---|---|---|---|---|---|---|---|---|
Site | Year | Range | Median | Range | Median | Range | Median | Range | Median |
Spruce | 2003 | 33–48 | 43 | 37–46 | 40 | 10 -25 | 14 | 3.2 | 3.2 |
2004 | 36–58 | 50 | 31–40 | 38 | 11–18 | 17 | 3.3–3.7 | 3.5 | |
2005 | 36–49 | 38 | 38–41 | 39 | 13–19 | 15 | 3.6–3.7 | 3.7 | |
Alder | 2003 | 39–54 | 43 | 34–39 | 37 | 10–24 | 14 | 3.8–4.0 | 3.8 |
2004 | 51–64 | 58 | 39–47 | 42 | 11–18 | 16 | 4.1–4.3 | 4.2 | |
2005 | 45–61 | 52 | 41–49 | 44 | 14–20 | 15 | 4.3–4.6 | 4.4 | |
Middle | 2003 | 23–32 | 30 | 18–20 | 19 | 9.6–29 | 14 | 3.4–3.6 | 3.5 |
2004 | 25–42 | 35 | 18–26 | 22 | 9.7–22 | 19 | 3.5–3.7 | 3.6 | |
2005 | 25–37 | 26 | 24–25 | 25 | 12–22 | 15 | 3.6–3.7 | 3.6 | |
North | 2003 | 11–20 | 16 | 6.5–7.9 | 7.0 | 11–30 | 15 | 3.9–4.0 | 3.9 |
2004 | 10–25 | 19 | 7.0–12 | 7.4 | 11–23 | 19 | 3.9–4.1 | 4.0 | |
2005 | 12–20 | 16 | 6.4–8.0 | 7.4 | 12–19 | 15 | 4.1–4.2 | 4.1 | |
Grove | 2003 | 13–22 | 19 | 4.4–8.5 | 6.7 | 9.1–30 | 15 | 5.3–5.6 | 5.4 |
2004 | 19–29 | 23 | 3.8–7.0 | 5.6 | 10–26 | 22 | 5.4–5.6 | 5.5 | |
2005 | 20–27 | 21 | 5.7–7.2 | 6.4 | 14–23 | 15 | 5.6–5.7 | 5.7 | |
Top | 2003 | 4.2–13 | 10 | 1.3–1.5 | 1.4 | 9.5–30 | 15 | 4.7–4.8 | 4.7 |
2004 | 5.4–15 | 13 | 1.5–1.8 | 1.6 | 10–25 | 22 | 4.6–4.8 | 4.8 | |
2005 | 7.1–12 | 8.7 | 1.3–1.8 | 1.6 | 14–23 | 16 | 4.7–4.8 | 4.8 |
The samples were analyzed for sterols at the end of July and September in 2004 (Table
Ergosterol and β-sitosterol (µg/g) in soil in 2004. Standard deviations in parentheses.
Per dw | Per SOM | ||||
---|---|---|---|---|---|
Site | Date | Ergosterol | β-sitosterol | Ergosterol | β-sitosterol |
Spruce | July 27th | 38 (±7) | 139 (±27) | 127 (±26) | 468 (±102) |
Sept 27th | 75 (±22) | 236 (±74) | 199 (±52) | 605 (±84) | |
Alder | July 27th | 37 (±14) | 203 (±159) | 99 (±12) | 472 (±149) |
Sept 27th | 49 (±32) | 275 (± 222) | 100 (±37) | 518 (±183) | |
Middle | July 27th | 14 (±7) | 138 (±95) | 54 (±6) | 487 (±96) |
Sept 27th | 15 (±8) | 130 (±76) | 68 (±5) | 551 (±140) | |
North | July 27th | 3.6 (±1.0) | 20 (±6) | 48 (±5) | 262 (±38) |
Sept 27th | 4.0 (±2.2) | 27 (±10) | 56 (±26) | 382 (±98) | |
Grove | July 27th | 1.6 (±0.5) | 8.4 (±1.2) | 30 (±5) | 163 (±22) |
Sept 27th | 1.4 (±0.3) | 6.1 (±2.3) | 38 (±10) | 162 (±68) | |
Top | Sept 27th | 0.3 (±0.2) | 3.0 (±3.0) | 18 (±5) | 145 (±89) |
Enzyme activities per dry soil were clearly highest in the reference forest and lowest in Top not covered with forest soil organic layer (Fig.
A two-dimensional solution was achieved with NMDS ordination for the enzyme activity data calculated per SOM (final value of the stress function = 9.50). A joint plot of the ordination for experimental sites is presented in Fig.
A two-dimensional solution was also achieved with NMDS ordination including monthly means of within-site replicate plots of enzyme activities (final value of the stress function = 8.75). Successional vectors joining monthly samples of different sites (i.e. experimental treatments) showed directional changes in two sites, with Top site moving closer to Grove and North and Middle gradually diverging from the other areas (Fig.
A three-dimensional solution was achieved with NMDS ordination for the plant species composition data (final value of the stress function = 10.52). A joint plot of the ordination for experimental sites is presented in Fig.
A three-dimensional solution was also achieved with NMDS ordination including monthly means of within-site replicate plots of plant composition data (final value of the stress function = 5.09). Successional vectors joining monthly samples of experimental treatments showed parallel directional changes in all four areas (Fig.
The cluster analysis on the basis of enzyme activities was applied separately for the data for the years 2003 and 2005. The pattern was characteristic to each site at the onset of the study in 2003 and, with one exception, all the samples from different dates formed a site specific sub-cluster (Fig.
The relative enzyme activities per SOM between sites from 2003 to 2005 (Figs
Sums of different enzyme activities in different sites per soil. Medians in three replicate plots calculated per dw from June to September in 2003, 2004 and 2005.
The joint plot of NMDS ordination for enzyme activity per SOM. All replicate plots of each study site with samples taken in June, July, August and September in 2003, 2004 and 2005. The vectors of environmental variables with strongest correlation to ordination axes (r > |0.5|) are shown.
The NMDS plot showing temporal change in enzyme activity per SOM. Successional vectors joining the monthly means of replicate samples of each study site (i.e. experimental treatment) taken in June, July, August and September in 2003, 2004 and 2005. Point labels show two initials of the site, sampling month and year (e.g. Gr0603 = Grove June 2003).
The joint plot of NMDS ordination for plant species composition. All replicate plots of each study site with vegetation surveys done in late May, July and early September in 2004 and 2005. The vectors of environmental variables with strongest correlation to ordination axes (r > |0.5|) are shown. The upper panel (
The NMDS plot showing temporal change in plant species composition. Successional vectors joining the monthly means of replicate surveys of each study site (i.e. experimental treatment) done in late May, July and early September in 2004 and 2005. The upper panel (
The dendrogram obtained by using means of enzyme activities per SOM in 2003. Triplicate samples of each site in June–September, lg transformed data (µmol MUF or AMC/g SOM in 3 h), standardised data, Gower's similarity coefficient and Ward's method. The original enzyme activity data is arranged according to the dendrogram to reveal differences between clusters. Sampling month (mm) is given for each sample. For each activity, the lower quartile is shown in
The dendrogram obtained by using means of enzyme activities per SOM in 2005. Explanations as in Fig.
β-Sitosterol present in plant membranes indicates phytobiomass in soil and it has been shown that in early stages of decomposition it is degraded at about the same rate as bulk litter (
Enzyme activity levels in soil per dw were clearly different between sites, true forests yielding the highest activities, followed by sites covered with old coniferous forest organic layer, of which Middle displayed higher activities than North, still lower activities in a site covered with alder forest soil with less organic matter and the lowest activities in hill top covered with mineral soil. The measurement of catabolic respiration patterns (
NMDS ordination revealed that the different study sites had characteristic enzyme activity and plant species compositional patterns. The enzyme activity patterns, normalized by calculation per SOM, were clearly dependent on pH, SOM content and mineral matter content (loi revealing organic matter and dw reflecting mineral contents). This observation is in accordance with the results of previous studies (
The study sites were clearly different in pH but each hill site exhibited a rather stable pH. The importance of pH for enzyme activity patterns plausibly reflected compositions of microbial consortia (
In accordance with
One of the main aims was to study how enzyme activities persist in soil transferred from forest to the open hill. Activities calculated per dry soil (Fig.
Both NMDS ordination and cluster analysis revealed a temporal successional change in enzyme activity patterns calculated per SOM between years. The hill top consisting primarily of mineral soil became more fertile, and in photographs taken in 2013, ten years after starting the experiment this change is also reflected by increasing cover of vegetation (Suppl. Figs
NMDS ordination also showed changes in plant species composition that occurred in all study areas towards the same direction during the first two years of monitoring that covered early phases of the vegetation succession. These changes clearly indicate the early phases of plant succession (Suppl. Table
The exact reason that would explain the parallel directional change across all experimental treatments remains unclear as none of the explanatory variables measured from the soil samples was correlated with the observed changes in plant composition, but one potential explanation is the increasing vegetation height caused by the same dominant species during early succession. Unfortunately, as with enzyme activities, we do not have data for plant occurrences for the period of ten years after the onset of the experiment (Fig. S4), and thus quantitative comparisons between the early phases of vegetation succession and the later time period were not possible. Grove site has developed to a true grove, but North and Middle sites still look like pastures after a decade.
A landfill site covered with forest soil top layer developed rapidly to urban green space. Soil enzyme activities increased markedly due to the forest soil cover, but remained lower than in the true forests. Soil enzyme patterns were characteristic to each site. They changed during a 3 year monitoring period reflecting differences in developing vegetation.
The value of integration of soil ecological knowledge with other successional patterns, such as changes in vegetation, in restoration management has been emphasised by several authors (
The study was financed by the City of Helsinki and we thank its personnel for help and for excellent cooperation. The laboratory work and sampling were carried out by personnel of the Finnish Environment Institute and our special thanks are due to Kaisa Heinonen, Tuula Ollinkangas, Minna Rännäli, Susanna Vähäkuopus, Anuliina Putkinen and Niina Lehtonen. Field work on plants was carried out by Thomas Kuusela, Tapio Rintanen and Irmeli Vuorinen. Michael Bailey is acknowledged for correction of the language of the manuscript.
Table S1
occurrence data
Vegetation data used in the ordination analyses.
Figure S1
photograph
The studied sites at the onset of the study in June 2003:
Figure S2
photograph
The studied sites in August 2003:
Figure S3
photograph
The studied
Figure S4
photograph
The studied