Plant removal disturbance and replant mitigation effects on the abundance and diversity of low-arctic soil biota

Applied Soil Ecology 82 (2014) 82–92

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Applied Soil Ecology journal homepage: www.elsevier.com/locate/apsoil

Plant removal disturbance and replant mitigation effects on the abundance and diversity of low-arctic soil biota Juha Mikola a, *, Louise Ilum Sørensen b , Minna-Maarit Kytöviita c a

Department of Environmental Sciences, University of Helsinki, Niemenkatu 73, FIN-15140 Lahti, Finland Department of Biology, University of Oulu, FIN-90014 Oulu, Finland c Department of Biological and Environmental Science, University of Jyväskylä, P.O. Box 35 (YAC), FIN-40014, Finland b

A R T I C L E I N F O

A B S T R A C T

Article history: Received 20 December 2013 Received in revised form 6 May 2014 Accepted 11 May 2014 Available online xxx

Due to the dependence of soil organisms on plant derived carbon, disturbances in plant cover are thought to be detrimental for the persistence of soil biota. In this work, we studied the disturbance effects of plant removal and soil mixing and the mitigation effects of replanting on soil biota in a low-arctic meadow ecosystem. We set up altogether six replicate blocks, each including three randomized treatment plots, at two distinct fells at Kilpisjärvi, northern Finland. Vegetation was removed in two thirds of the plots: one third was then kept barren (the plant-removal treatment), while the other third was replanted with a local herb Solidago virgaurea. The remaining plots of intact vegetation were used as treatment comparisons. The responses of soil microbes and fauna were examined six years later in the early and late growing season. The biomass of bacteria, non-mycorrhizal fungi and mycorrhizal fungi (estimated using PLFA markers) were on average 74%, 89% and 84% lower in the plant-removal and 64%, 74% and 71% lower in the Solidago replant plots than in the intact meadow. The positive effect of replanting was statistically significant for fungi, but not for bacteria. The PCA of relative PLFA concentrations further showed that the structure of the microbial community differed significantly among all three treatments. The abundance of nematodes and collembolans was on average 82 and 95% lower, but the total number of nematode genera and collembolan taxa only 27 and 7% lower in the plant-removal plots than in the intact meadow soil. Few disturbance effects on soil fauna were significantly mitigated by the Solidago replant (the plant parasitic nematodes being a notable exception) and in the case of the collembolans, the Solidago replant plots had even fewer animals than the plant-removal plots. The response of soil biota also varied with locality: the effects on fungivorous nematodes were found at one site only and the replant effects on the number and diversity of collembolan taxa varied with site. Our results suggest that despite drastic reductions in the abundance of soil biota, the majority of animal taxa can persist for years in disturbed arctic soils in the absence of vegetation. In contrast, the alleviating replant effects on the abundance of soil biota appear weak and may only partially reverse the negative effects of vegetation removal and soil disturbance. ã 2014 Elsevier B.V. All rights reserved.

Keywords: Microbes Nematodes Collembolans Diversity Community Solidago virgaurea

1. Introduction Due to their short growing seasons and low productivity, the arctic and sub-arctic ecosystems can be particularly sensitive to both anthropogenic and natural disturbances. Industry (Kashulina et al., 1997; Walker et al., 1987), reindeer grazing and trampling (Kashulina et al., 1997; Moen and Danell, 2003; Van der Wal et al.,

* Corresponding author. Tel.: +358 2 94120335. E-mail address: juha.mikola@helsinki.fi (J. Mikola). http://dx.doi.org/10.1016/j.apsoil.2014.05.013 0929-1393/ ã 2014 Elsevier B.V. All rights reserved.

2001) as well as off-road vehicles and tourist activities (Babb and Bliss, 1974) all have impacts on the arctic vegetation and soil. Cryoturbation and landslides further disturb the soil in the arctic ecosystems, and while these disturbances are natural, landslides can also be influenced by human activities and the climate change (Restrepo et al., 2009). Besides affecting the soil structure, disturbances typically reduce the coverage of plants and both of these effects are likely to have an impact on soil communities. It can take fifty years to restore the species composition of the arctic vegetation after a landslide and the recovery of the full plant cover can take even longer (Cannone et al., 2010). How arctic soil

J. Mikola et al. / Applied Soil Ecology 82 (2014) 82–92

communities respond to such disturbances, persist in areas with no plant cover and recover along with newly establishing vegetation is poorly known. Plant biomass not consumed by the herbivores enters the soil as plant litter. Fresh litter is mostly easily decomposable and fuels the microbial and animal activities (Kandeler et al., 1999; Rønn et al., 1996), but the litter also forms the soil organic matter, which is important for soil water retention, formation of three dimensional space and maintenance of soil fertility through absorbing and releasing nutrients (Ehrenfeld et al., 2005; Sturm et al., 2005). Plants also lose a significant proportion of their fixed carbon to soil as root exudates, and in mycorrhizal plants, this carbon is further channeled to the soil community as the exudates and litter of the mycorrhizosphere (Jones et al., 2009). Due to the carbon supply, the activity and abundance of soil organisms are usually several magnitudes higher in the vicinity of roots than in the bulk soil (Cheng et al., 1996; Griffiths et al., 1992; Hamilton and Frank, 2001). It is therefore clear that the abundance of soil biota will decline after plant removal but the effects on the diversity may not be as straightforward (Hirsch et al., 2009) and there are remarkably few field studies of the consequences of long-term plant absence on soil communities. In the arctic soils, microbes act as a strong nutrient sink (Jonasson et al., 1996; Michelsen et al., 1999) and the ability of soil fauna to release nutrients from microbial biomass (Bardgett and Chan, 1999; Setälä et al., 1990) is likely to be particularly important for plant nutrient uptake. As earthworms are few or non-existing in these soils, the relative role of other animal groups, such as nematodes and collembolans, is emphasized (Rusek, 1998). Of these, collembolans are generally considered as fungivores (De Ruiter et al., 1993; Hunt et al., 1987) while nematodes represent several trophic groups (Yeates et al., 1993). To forecast the ecosystem trajectory after a disturbance, as well as to plan the possible remediation actions such as replanting, it is therefore essential to understand the time course of the changes not only in the vegetation, but also in the abundance and diversity of these soil biota. Here we present results from a study designed for monitoring the response of soil microbes and animals to soil disturbance and long-term vegetation removal. We removed the plant cover and disturbed the soil at several field plots in a low-arctic meadow and kept half of these plots non-vegetated for six years. To examine whether such disturbance could be mitigated by replanting, we planted the other half of the plots with a common local herb, Solidago virgaurea. Intact meadow plots were used as references for these two treatments. We chose S. virgaurea as the replant species due to its intensive arbuscular mycorrhizal association (Kytöviita et al., 2011), commonness in the meadows and tundra heaths of the northern Fennoscandia and because it is one of the few plant species capable of growing in the early as well as late successional communities. Earlier studies have shown that even rudimentary vegetation, such as plant monoculture, can greatly benefit soil organisms (Johnson et al., 2003). We therefore hypothesized that while the soil disturbance and the absence of plant cover would decrease the abundance, richness and diversity of the soil community, Solidago replanting would significantly alleviate this effect through the supply of root exudates and shoot and root litter to soil organisms. 2. Materials and methods 2.1. Study site and experimental design Two low-arctic meadows, approximately 2.5 km apart and 600 m above sea level, situating on south facing slopes of two fells, Saana (69
030 N, 20
500 E) and Jehkas (69
050 N, 20
470 E), were selected at Kilpisjärvi, northern Finland. The two sites were

83

selected relatively far from each other to have higher level replication of experimental sites and better ground for generalizations. Vegetation is at both sites dominated by the grass Deschampsia flexuosa and includes sedges and herbs like Solidago virgaurea, Trollius europaeus, Potentilla crantzii and Bistorta vivipara. Few species of dwarf shrubs, such as Betula nana, Juniperus communis and Vaccinium myrtillus also occur at the sites. In the area, the long-term mean annual temperature is 2.6
C and the mean precipitation 422 mm (1961–1985), as measured at the Kilpisjärvi meteorological station, 483 m above the sea level (Järvinen and Partanen, 2008). The experiment was established at the end of June 1999 and consisted of control, plant-removal and replant plots (each 3.5 m in diameter). The plots were randomly placed 1–10 m apart within three replicate blocks at each site (giving altogether six replicate plots for each treatment) and each plot (including the control plots) was ditched to prevent clonal plant growth and soil animal movement from the surrounding meadow. All vegetation was first removed from the plant-removal and replant plots. Plant roots were pulled out of the soil and at this point, the soil was disturbed by mixing the topsoil with the deeper layers. In August 1999, the replant plots were re-vegetated by planting one hundred mature S. virgaurea individuals into each plot. S. virgaurea is a very common, herbaceous perennial plant in the low-arctic meadows. It has a broad distribution in the northern hemisphere (Hultén and Fries, 1986) and can occur in many habitats, ranging from early successional sand dunes to late successional forests. It also sustains an intensive (typically 80–90% of root length colonized) and stable mycorrhizal colonization (Kytöviita et al., 2011). The plant material for replanting was collected from the surrounding undisturbed meadow. Seed rain on the plots was prevented by covering the plots (including the control plots) with a thin transparent cloth from mid-August to early June. The cloths were laid at the onset of the seed rain and remained in place until the soil was defrosted enough to remove them. To know whether this covering per se had effects on soil organisms, additional control samples were taken for microbes and nematodes at each replicate block from non-manipulated non-covered areas using the same procedures as for other samples. These plots are hereafter called as ‘additional controls’. The plant-removal and monoculture plots were weeded at every growing season (few seedlings emerged after the first season) and the plots were fenced to exclude reindeer. During the warmest summer months, July and August, the average (2000–2005) soil temperature at 3–5 cm depth was 10.6
C, 10.6
C, 11.9
C and 12.0
C in the control, additional control, monoculture and plant-removal plots, respectively. 2.2. Sampling and analyses For evaluating the response of soil microbes, nematodes and collembolans to the treatments, the plots were sampled twice in 2005: at early growing season after the snow melt (middle June) and at late season (middle August). Six soil cores (diameter 3 cm, depth 6 cm) were first taken to estimate the biomass and community structure of microbes. The soil cores were sieved (4 mm) within 24 h, pooled and stored frozen until the phospholipid fatty acid (PLFA) analysis. For the analysis, 3.0 g sub-samples (fresh weight) of soil were first extracted with one-phase mixture of chloroform, methanol and phosphate-buffer (0.05 M K2HPO4, pH 4.0, 1:2:0.8 v/v/v). The phases were separated using water and chloroform, and the lower phase was collected and fractionated in silic acid columns (Bond Elut Extraction Cartridges, Varian US). Neutral lipids were extracted with 5 ml chloroform, glycolipids with 10 ml acetone and phospholipids with 5 ml methanol. The phospholipid fraction was collected and methyl nonadecanoate was added to the fraction as an internal standard. The fraction was

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then transesterified by mild alkaline methanolysis according to Dowling et al. (1986). The resulting methylated esters were analyzed using an Agilent 6890N GC equipped with 7683 series injector, flame ionization detector and a HP-5 capillary column (30 m  0.32 mm). Of the identified PLFAs i15:0, a15:0, 15:0, i16:0, 16:1v9, i17:0, a17:0, cy17:0, 18:1v7 and cy19:0 were used to represent bacterial biomass, while the biomass of non-mycorrhizal fungi was estimated using 18:2v6 (Frostegård and Bååth, 1996.) Both Basidiomycota and Ascomycota contain 18:2v6 and both also include ectomycorrhizal symbionts, but since the ectomycorrhizal associations are few in our meadow, we assume that 18:2v6 mainly represents the non-mycorrhizal fungi. The PLFA16:1v5 was used to estimate the biomass of arbuscular mycorrhizal (AM) fungi (Olsson et al., 1995), but these estimates should be taken with caution since there is evidence that 16:1v5 can also be produced by bacteria (Hedlund, 2002). The soil organic matter (SOM) concentration was measured as loss on ignition (475
C, 4 h). Nematode abundance was estimated using another six soil cores (diameter 3 cm, depth 6 cm) per plot. These were kept in 4
C until the animals were extracted up to two weeks later. In the laboratory, the soil cores were pooled, gently mixed and the nematodes were extracted from 20 g sub-samples using a wet funnel device (Sohlenius, 1979). To get a sufficient number of nematodes for identification, one to five additional 20 g subsamples were extracted of the soil collected from the Solidago replant and plant-removal plots. The total number of nematodes was counted live and later, using preserved samples, 50–150 nematodes per sample (all individuals if the sample had less or equal to 150 individuals, a sub-sample of 150 individuals for more numerous samples) were identified to genus and allocated into trophic groups according to Yeates et al. (1993). Plant-feeding genera were further sorted into plant parasites (Paratylenchus, Pratylenchus and Tylenchorhynchus) and more generalist feeders of root epidermal cells, root hairs, algal, lichen and moss (Aglenchus, Filenchus, Lelenchus, Malenchus and Tylenchus) (Yeates et al., 1993). The proportion of parasites of all plant feeders was then calculated using this grouping. Collembolan abundance was estimated in August using two soil cores (diameter 6 cm, depth 6 cm) per plot. Due to fewer samples, the treatment effect estimates for collembolans may be less accurate than those for the nematodes. The cores were kept in 4
C until extracted up to three weeks later using a modified high-gradient-extractor (Macfadyen, 1961). Collembolans were then stored in ethanol, counted and all individuals were identified to species or higher taxa according to Fjellberg (1998, 2007),). 2.3. Statistics

component analysis (PCA) was first performed using PLFA concentrations and the score values of the first two PCA axes were then analysed using the repeated measures ANOVA. To test whether the seed rain cover had effects on the tested variables, only the two control treatments were included in the ANOVA. The homogeneity of variance was tested using Levene’s test and the normality using model residuals and the Kolmogorov–Smirnov test. To satisfy the assumptions of ANOVA, variables were log or square root transformed when necessary. Even after transformations, however, homogeneity of variances could not be reached for bacterivorous nematodes at the June sampling, neither for plantfeeding nematodes, number of collembolan taxa and the fungal marker 18:2v6 at the August sampling. When ANOVA indicated a significant treatment effect, Tukey’s post-hoc test or Tamhane test (in the case of heterogeneous variances) was employed to find the statistically significant differences between the treatment means. 3. Results 3.1. Soil organic matter and microbial PLFA Soil OM concentration was on average 50% lower in the plantremoval and Solidago replant plots than in the control plots (Fig. 1). The biomass of bacteria (the sum of ten PLFAs), non-mycorrhizal fungi (18:2v6) and AM fungi (16:1v5) were on average 74%, 89% and 84% lower, respectively, in the plant-removal and 64%, 74% and 71% lower in the Solidago replant plots than in the control plots, and for both groups of fungi, the biomass in the Solidago plots was significantly higher than the biomass in the plant-removal plots (Fig. 2). The ratio of the bacterial PLFAs to 18:2v6 was highest in the plant-removal, intermediate in the Solidago and lowest in the control plots (Fig. 2). The structure of the microbial community (estimated using PLFA marker concentrations) differed significantly among all three treatments along the PCA Axis 1, with the Solidago replant plots having intermediate score values (Fig. 3a, Table 1). Plant removal increased the relative abundance of the bacterial markers i15:0, a15:0, 15:0, i17:0, a17:0 and cy17:0 and decreased the relative abundance of the fungal markers 18:2v6 and 16:1v5 and the bacterial marker 18:1v7 (Table 1, Fig. 3a). The sampling month interacted with the treatment on the Axis 2, although not highly significantly (P = 0.066), which was due to the communities differing between the June and August samplings in the plantremoval plots, but not in the other plots (Fig. 3a). In the plantremoval plots, both fungal markers and the bacterial i16:0 were relatively more abundant and the bacterial cy19:0 less abundant in the August than June sampling (Fig. 3a, Table 1). The month  site interaction was significant along both PCA axes, which was due to a

The diversity of nematodes and collembolans was estimated using the Shannon–Wiener diversity index: s X pi lnpi i¼1

where pi is the proportion of a nematode genus/collembolan group of the total abundance of identified nematodes/collembolans. The richness (S) of taxa was defined as the number of identified nematode genera or collembolan species/groups. The statistical tests were accomplished using plot mean values and the SPSS statistical package (version 16.0). The effects of the treatment (undisturbed meadow vs. plant removal vs. Solidago replanting), site (Jehkas vs. Saana) and sampling time (June vs. August) on the abundance of soil organisms, structure of the microbial community and richness and diversity of the animal groups were analysed using a repeated measures ANOVA with the replicate block nested within the site. For the PLFA data, a principal

12

Loss on ignition (% of soil dry mass)

H0 ¼ 

T: F=10.6, P=0.006

9 6 3 0 Saana

Jehkas

Fig. 1. Loss on ignition of the soil (mean + SE, n = 6, the two samplings combined) in plant removal (black bars), Solidago replant (grey) and control (white) plots of the Saana and Jehkas low-arctic meadows. F and P values are given for statistically significant effects; T = treatment.

J. Mikola et al. / Applied Soil Ecology 82 (2014) 82–92

35

T: F=48, P<0.001

250 200 150 100 50

25 20 15 10 5

0

0 Saana

30

Saana

Jehkas 35

T: F=84, P<0.001

20 15 10

Jehkas

T: F=24, P<0.001

30

Bacterial to fungal PLFA ratio

25

AM fungal PLFA 16:1ω5 (nmol/g dry soil)

T: F=106, P<0.001

30

Fungal PLFA 18:2ω6 (nmol/g dry soil)

Bacterial PLFAs (nmol/g dry soil)

300

85

25 20 15 10

5

5

0

0 Saana

Jehkas

Saana

Jehkas

Fig. 2. Biomass of bacteria (estimated using ten PLFA markers), non-mycorrhizal fungi (estimated using the PLFA 18:2v6), arbuscular mycorrhizal fungi (16:1v5) and the ratio of bacteria to non-mycorrhizal fungi (mean + SE, n = 6, the two samplings combined) in plant removal (black bars), Solidago replant (grey) and control (white) plots of the Saana and Jehkas low-arctic meadows. Statistics are as in Fig. 1.

plots was also found for bacterivores, fungivores and plant feeders, while for omnivores and predators the number of genera was more equal among the treatments (Table 2). The bacterivorous Acrobeloides and Plectus, omnivorous Eudorylaimus and Aporcelaimellus, fungivorous Aphelenchoides and plant-feeding Filenchus were found in almost all samples, regardless of the plot treatment (Table 2). In other genera, individuals were typically less frequently found in the samples collected from the plant-removal and Solidago replant plots than in the samples collected from the control plots, but there were also many genera (such as the

difference found between June and August communities in Jehkas, but not in Saana (Fig. 3b, Table 1). 3.2. Nematodes A total of 53 nematode genera were observed in the study plots during the two samplings, and the number of genera was 17 and 27% lower in the Solidago replant and plant-removal plots than in the intact meadow soil (Table 2). A similar trend of decreasing richness from the control to Solidago replant and plant-removal

2

1

A

1 0.5 0

0 -0.5 -1

-0.5 -1

B

0.5 Axis 2 (14%)

Axis 2 (14%)

1.5

-1.5

-1

-0.5

0 0.5 1 Axis 1 (54%)

1.5

2

-1.5

-1

-0.5

0 Axis 1 (54%)

0.5

1

Fig. 3. PCA graphs of the microbial PLFA data (the twelve PLFAs as concentrations of total PLFA) in Axis 1  Axis 2 ordination planes with (A) treatment means (SE, n = 6, the two sites combined) and (B) site means (SE, n = 9, the three treatments combined) as overlays. In both graphs the circles and squares denote June and August samplings, respectively. In (A) white, gray and black signify control, Solidago replant and plant-removal plots, respectively; in (B) white and black denote samples from Saana and Jehkas, respectively.

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J. Mikola et al. / Applied Soil Ecology 82 (2014) 82–92

Table 1 Variable loadings from a PCA of the microbial PLFA data of the 36 field samples (the twelve PLFAs as concentrations of total microbial PLFA), and the effect of treatment, site and sampling month on the score values of the samples along the two PCA axis (the P values are from repeated measures ANOVA). The variable loadings are directly proportional to the correlations between the variables and the PCA axes, and values near and above |0.5|, shown in bold type, indicate a significant contribution of the variable to the respective PCA axis. PLFA

Microbial group

Axis 1

Axis 2

i15:0 a15:0 15:0 i16:0 16:1v9 16:1v5 i17:0 a17:0 cy17:0 18:2v6 18:1v7 cy19:0

Bacteria Bacteria Bacteria Bacteria Bacteria AM fungi Bacteria Bacteria Bacteria Non-mycorrhizal fungi Bacteria Bacteria

893 0.806 0.779 0.424 0.459 0.712 0.962 0.943 0.923 0.497 0.773 0.104

0.032 0.208 0.369 0.596 0.045 0.489 0.140 0.057 0.125 0.540 0.083 0.708

P <0.001 0.130 0.100 0.743 0.002 0.008

P

Effect Treatment (T) Site (S) Month (M) TS TM SM

bacterivorous Prismatolaimus, omnivorous Epidorylaimus and fungivorous Tylencholaimus) that were equally found in all treatments (Table 2). As a contrast to other genera, the predatory Pseudodiplogasteroides was almost exclusively confined to the plant-removal and Solidago replant plots and the fungivorous Diphtherophora to the Solidago plots. Total nematode abundance was on average 82 and 69% lower in the plant-removal and Solidago replant plots than in the intact meadow soil. The abundances of all trophic groups, except for the predators, were also lower in the plant-removal and Solidago replant plots than in the control plots, but for plant feeders the difference between the control and Solidago plots was not statistically significant (at both sites due to an insignificant treatment  site interaction although the graph suggests that this pattern was only observed at Saana) and fungivore abundance differed significantly at Jehkas only (Fig. 4). The proportion of parasites of all plant feeders was on average higher at Saana than Jehkas (Fig. 5). The proportion was also considerably lower in the plant-removal (on average 0.17) than control (0.70) plots, whereas the proportion in the Solidago replant plots did not statistically significantly differ from the proportion in the other two treatments (Fig. 5). Although predators were not affected by the treatments, their abundance differed between the sites and was higher at Jehkas than Saana (Fig. 4). The mean number of genera was significantly lower in the treated than control plots and the plantremoval and Solidago replant plots did not differ from each other (Fig. 6). The mean diversity of nematode genera was lower in the plant-removal than control plots, but the diversity in the Solidago plots did not significantly differ from the diversity in the other two treatments (Fig. 6). 3.3. Collembolans The total number of collembolan taxa found in the plantremoval and Solidago replant plots was 7 and 40% lower than in the control plots (Table 3). The most abundant taxa were Isotomiella minor (41% of the total number of animals), Mesaphorura/Willemia sensu lato (24%), Folsomia quadrioculata (10%), Folsomia palaearctica (7%) and Onychiurus spp. sensu lato (6%). Mesaphorura/ Willemia was found in all samples regardless of the plot treatment and I. minor was lacking in only one sample taken from the plant-

0.115 0.418 0.066 0.917 0.017 0.034

removal treatment (Table 3). Of the other taxa, Isotoma spp. sensu lato was equally frequent in all treatments, while the others were typically less frequent in the plant-removal and Solidago samples than in the control samples (Table 3). The abundance of collembolans was 95 and 99% lower in the plant-removal and Solidago replant plots than in the control plots, and marginally higher (P = 0.069) in the plant-removal than Solidago plots (Fig. 4). Treatment effects on the mean number of taxa varied with site: at Saana, the Solidago replant plots had significantly fewer taxa than the plant-removal plots, while at Jehkas the plant-removal and Solidago plots did not differ from each other (Fig. 6). Similarly, the effects on collembolan diversity varied with locality: at Saana, the diversity was lower in the plantremoval and Solidago replant plots than in control plots but at Jehkas there was no difference between the Solidago and control plots, which exceeded both the plant-removal plots (Fig. 6). 3.4. Additional control plots In the additional control plots, which were established to determine the influence of plot covering, the concentration of the fungal PLFA marker 18:2v6 was on average lower (20.3 nmol/g dry soil) and the bacterial to fungal ratio higher (11.2) than in the control plots (P = 0.030 and P = 0.006, respectively), but the other PLFA markers and the nematodes were not affected. 4. Discussion 4.1. Plant removal and soil disturbance In the present day world, where the human activities increasingly disturb the plant cover of the earth, it is important to understand the link between the plant-derived carbon and soil biodiversity. In our study, the absence of vegetation and the accompanying soil disturbance caused a drastic reduction in the abundance of soil biota. The abundances of nematodes and collembolans were on average 82 and 95% lower, respectively, and the biomass of microbial groups 74–89% lower in the plantremoval plots than in the intact meadow soil. However, despite these large reductions in the abundance of soil biota, the total number of nematode genera and collembolan taxa found in the

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Table 2 The number of samples that contained individuals from different nematode genera in the three treatments (twelve samples collected for each treatment) and the number of genera found for each trophic group in each treatment. The genera are listed in decreasing frequency of occupied samples for each trophic group and B, F, O, PF, PP and P mean bacterivorous, fungivorous, omnivorous, plant-feeding, plant parasite and predatory genera, respectively. Genus

Trophic group

Plant removal

Solidago replant

Control

Acrobeloides Plectus Teratocephalus Prismatolaimus Alaimus Heterocephalobus Cervidellus Wilsonema Rhabdolaimus Metateratocephalus Panagrolaimus Rhabditis Eumonhystera Tylocephalus Cephalobus Anaplectus Ceratoplectus Eucephalobus Geomonhystera Achromadora Bastiania Bunonema Chiloplacus Leptolaimus Mesorhabditis Protorhabditis Number of genera

B B B B B B B B B B B B B B B B B B B B B B B B B B

12 12 11 8 5 7 7 7 5 2 1 2 1 1 0 0 0 1 1 0 0 0 0 0 0 0 16

12 12 6 8 7 4 7 4 5 4 3 4 1 0 1 0 0 0 1 0 1 0 1 0 1 0 18

12 12 11 7 9 9 5 7 7 10 6 2 4 3 2 2 2 1 0 1 0 1 0 1 0 1 22

Aphelenchoides Tylencholaimus Ditylenchus Diphtherophora Dorylaimoides Belodiridae Deladenus Funaria Number of genera

F F F F F F F F

10 7 6 0 1 0 0 0 4

12 6 2 10 1 1 0 0 6

11 7 10 2 1 1 1 1 8

Filenchus Paratylenchus Tylenchus Pratylenchus Aglenchus Lelenchus Malenchus Tylenchorhynchus Number of genera

PF + F PP PF PP PF PF PF PP

11 5 2 3 1 0 0 0 5

8 8 4 0 4 3 0 1 6

12 12 7 8 3 2 4 3 8

Eudorylaimus Aporcelaimellus Epidorylaimus Enchodelus Takamangai Aporcelaimus Mesodorylaimus Number of genera

O O O O O O O

12 10 7 6 4 0 0 5

12 11 9 3 6 0 1 6

12 10 7 11 8 1 0 6

Pseudodiplogasteroides Clarkus Prionchulus Diplogasteriana Number of genera

P P P P

11 4 2 1 4

8 3 2 0 3

1 9 5 0 3

34

39

47

Total number of genera found

88

J. Mikola et al. / Applied Soil Ecology 82 (2014) 82–92

T: F=31, P<0.001

8 6 4 2

10 Fungivorous nematodes (ind./g dry soil)

Bacterivorous nematodes (ind./g dry soil)

10

0

4 2

T: F=18, P<0.001

8

Saana

Jehkas

6 4 2

10 Omnivorous nematodes (ind./g dry soil)

Plant-feeding nematodes (ind./g dry soil)

10

0 Saana

Jehkas

T: F=25, P<0.001

8 6 4 2 0 18

Jehkas

Saana

Jehkas

T: F=60, P<0.001

S: F=7.6, P=0.024 15

8

Collembolans (ind./g dry soil)

Predatory nematodes (ind./g dry soil)

6

0 Saana

10

8

T: F=59, P<0.001 T×S: F=8.8, P=0.010

6 4 2

12 9 6 3

0

0 Saana

Jehkas

Saana

Jehkas

Fig. 4. Abundance of nematode trophic groups (mean + SE, n = 6, the two samplings combined) and collembolans (mean + SE, n = 3) in plant removal (black bars), Solidago replant (grey) and control (white) plots of the Saana and Jehkas low-arctic meadows. Statistics are as in Fig. 1, S = site.

Proportion of parasites of plant feeders

1.0

T: F=6.6, P=0.025 S: F=6.5, P=0.038

0.8 0.6 0.4 0.2 0.0 Saana

Jehkas

Fig. 5. Proportion of plant parasites of all plant-feeding nematodes (mean + SE, n = 6, the two samplings combined) in plant removal (black bars), Solidago replant (grey) and control (white) plots of the Saana and Jehkas low-arctic meadows. Statistics are as in Fig. 1, S = site.

plant-removal plots were only 27 and 7% lower, respectively, than the number of taxa found in the intact meadow soil. Consistent with these results, the abundance of nematodes, but not their species richness, was significantly reduced in the bare soil in comparison to the vegetated soil in Antarctica (Convey and WynnWilliams, 2002). In a unique field set-up including plots of 50 years of bare soil, Hirsch et al. (2009) further found that while the microbial and animal numbers and the mite diversity had significantly declined in the long-term absence of plants, the diversity of the bacterial community was comparable to that found under a grass sward. Together these findings suggest that major parts of the soil biodiversity can persist for years in the absence of plant cover. In our study, the soil structure was perturbed in the plantremoval and Solidago replant plots and it is possible that six years after plot establishment, the abundance and diversity of soil biota were still controlled by this initial disturbance. Microarthropods, such as collembolans, are sensitive to changes in soil structure and their abundance and diversity have been suggested as bioindicators for disturbance in the arctic (Niwranski et al., 2002)

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3

T: F=7.5, P=0.015

25

Diversity of nematode genera

Number of nematode genera

30

20 15 10 5 Saana

2

1

Saana

Jehkas 3

T: F=66, P<0.001 T×S: F=9.1, P=0.009 Diversity of collembola taxa

Number of collembola taxa

T: F=6.5, P=0.021

0

0 16

89

12 8 4 0

Jehkas

T: F=23, P<0.001 T×S: F=9.9, P=0.007

2

1

0 Saana

Jehkas

Saana

Jehkas

Fig. 6. Number and Shannon–Wiener diversity of nematode genera (mean + SE, n = 6, the two samplings combined) and collembolan taxa (mean + SE, n = 3) in plant removal (black bars), Solidago replant (grey) and control (white) plots of the Saana and Jehkas low-arctic meadows. Statistics are as in Fig. 1, S = site.

and other environments (Ponge et al., 2003). Nematodes are also often used as disturbance bio-indicators (Yeates and Bongers, 1999; Zhao and Neher, 2013) but in our study the vegetation removal and soil mixing were clearly more detrimental for the abundance of collembolans than nematodes. Another explanation for the reduced abundance and diversity of soil biota is that SOM concentration was 50% lower in the plant-removal plots than in the intact meadow, both due to the initial soil disturbance and due to lack of plant production in these plots during the experiment. Plant litter provides easily utilizable resources for soil animals and is an important physical structure of their habitat, particularly for Table 3 The number of samples in the three treatments (six samples collected for each treatment) that contained individuals from different collembolan taxa (listed in decreasing frequency of occupied samples). Taxon

Plant removal

Solidago replant

Control

Mesaphorura/Willemia sensu lato Isotomiella minor Folsomia quadrioculata Isotoma spp. sensu lato Micranurida pygmaea Onychiurus spp. sensu lato Folsomia spp. Folsomia palaearctica Parisotoma notabilis Sminthuridae Friesea mirabilis Isotoma ekmani Micranurida forsslundi Lepidocyrtus lignorum Pseudanurophorus binoculatus Megalothorax minimus Total number of taxa found

6 5 2 4 3 3 2 1 1 1 1 1 1 0 0 1 14

6 6 4 4 3 1 1 0 1 1 0 0 0 0 0 0 9

6 6 6 4 5 6 5 6 5 5 6 5 3 2 1 0 15

collembolans (Sayer, 2006). In another study in the same lowarctic meadow, reindeer grazing reduced the number of enchytraeids and some collembolans although it simultaneously increased the SOM content (Francini et al., 2014). This finding seems to suggest that disturbances (such as reindeer trampling) rather than resource availability are in the key role in determining soil animal abundances in these habitats. The primary decomposers, bacteria and non-mycorrhizal fungi, were greatly reduced in the plant removal and Solidago replant plots (relatively much more than the SOM concentration), which supports the theory that their abundances are bottom-up, or resource controlled in the soil (Mikola and Setälä, 1998). The abundance of the second trophic level, the microbial feeding nematodes, was also reduced but the third level, the predatory nematodes, was not. These findings suggest that while the abundance of microbial feeders is controlled by microbial production, other factors than prey availability control the predatory nematodes. In a temperate grassland, preventing reestablishment of vegetation reduced the abundance of microbes and fauna, including the predatory nematodes (Wardle et al., 1999) but in our case, the predatory nematodes were not adversely affected and one of the genera, Pseudodiplogasteroides, was exclusively restricted to the disturbed plots. It is likely that predators benefited of the decreased SOM concentration in the plant-removal plots although the abundance of their prey was reduced. The predatory nematode Prionchulus punctatus prefers sand as a habitat to a humus–litter mixture and P. punctatus populations grow larger when the sand and SOM form separate patches (Mikola and Sulkava, 2001). This can happen despite opposite trends in their prey populations (Mikola and Sulkava, 2001) because predation is easier in coarse-grained soil, where the

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prey cannot escape into pores inaccessible to the predator (Elliott et al., 1980). In general, our meadow habitat sustained a diverse nematode community; the 53 nematode genera recorded in this study are above the average species richness earlier reported from high latitude ecosystems (Boag and Yeates, 1998). 4.2. Replanting In our study, Solidago replanting could not significantly mitigate the adverse effects of plant removal and soil disturbance on the abundance of soil biota. The few clear signs of mitigation were on soil microbes, while the effects on soil fauna were weak and varied between the two sites of the meadow. For some reason, although Solidago replanting increased the abundance of mycorrhizal and non-mycorrhizal fungi, the abundance of fungal-feeding collembolans and nematodes did not increase. Rather, the collembolans seemed to be adversely affected by the Solidago replanting. Considering that the presence of plants increases SOM content (Johnson et al., 2003) and that soil microbial biomass typically correlates with the SOM content (Bardgett et al., 1997), replanting had unexpectedly few positive effects on soil biota in our study. This may be because plant production is low in the sub-arctic climate and our Solidago plantations could not produce a measurable increase (or a measurable mitigation of decrease) in SOM concentration within the six years of the study. The SOM concentration was reduced by half by plant removal and soil disturbance but the abundance of most soil organisms was reduced by more than 50%. This could be taken as an evidence that the release of recently fixed carbon by plant roots, rather than the accumulated SOM, is the primary factor that controls microbial communities and biological processes in the soil (Högberg and Read, 2006; Johnson et al., 2003; Paterson et al., 2007). On the other hand, the weak Solidago replant effects on soil organisms are incompatible with this idea. The nonmycorrhizal fungi seemed to respond more readily to the rootderived carbon than bacteria. This contrasts earlier microcosm studies, where bacteria and fungi were found to respond uniformly to an increase in their basal resources (Mikola and Setälä, 1998). Also, in contrast to the microcosm results, the increased abundance of fungi under the Solidago replant did not seem to propagate up the trophic levels; the abundance of fungal-feeding nematodes and collembolans did not increase along with increasing fungal biomass. Similar lack of responses at the upper trophic levels was observed in a sub-arctic heath, where the response of nematodes did not mirror the response of microbial biomass to fertilization and carbon addition (Ruess et al., 2002). The other groups of soil biota that showed a positive response to Solidago replanting – the plant-feeding nematodes and the symbiotic AM fungi – both derive resources directly from live plants. It further appeared that the negative response of plant feeders to plant removal and their positive response to Solidago replanting were mainly driven by the response of plant parasites; the parasites comprised over two thirds of all plant feeders in the intact meadow but only 17 and 46% in the plant-removal and Solidago replant plots. The non-parasitic genera feed on root epidermal cells and root hairs but also the algae and mosses (Yeates et al., 1993) and some can also feed on fungal hyphae (Okada et al., 2005) which apparently makes them less sensitive to the absence of vascular plants. The increased abundance of AM fungi shows that AM hyphal networks were reconstructed in a measurable extent in the Solidago replant plots and indicates that resources for fungalfeeders were indeed higher in these than plant-removal plots. That collembolans did not respond to the increased AM densities might result from collembolans preferably feeding on non-mycorrhizal fungi (Gange, 2000). However, the lack of response to the increased biomass of non-mycorrhizal fungi as well indicates that the effects of habitat destruction prevailed over those of enhanced resource

availability. It is good to note, though, that had we used another species of plant instead of S. virgaurea, the results of replanting might have been different as microbial community structure and the abundance of nematodes and collembolans often depend on plant species identity (De Deyn et al., 2004; Salamon et al., 2011; Wardle et al., 1999). On the other hand, in a greenhouse study, in which the soil and plant species (including S. virgaurea) originated from the same meadow as in the present study, plant species composition had no influence on the abundance of nematode trophic groups or genera despite the plant species differing in root and shoot production (Sørensen et al., 2008). 4.3. Between-site variation and plot covering We have earlier shown that low-arctic soil communities are heterogeneous at the scale of the landscape (Sørensen et al., 2009) and that microbial and animal communities can differ among closely located sites that have the same overall vegetation but differ in soil chemistry and the relative abundance of plant species (Kytöviita et al., 2011; Sørensen et al., 2009). Our present results suggest that such variation can also influence the seasonal variation of the communities as well as their responses to disturbances. The structure of the microbial community differed between the June and August sampling at Jehkas but not at Saana. Similarly, the fungivorous nematodes were significantly affected by plant removal and Solidago replanting at Jehkas only and the effects of Solidago replanting on the number and diversity of collembolan taxa were more positive at Jehkas than Saana. These differences in soil community responses are hard to explain and likely originate from various reasons but they might be related to the fact that Jehkas has more nutrient-rich soil with higher plant and arbuscular mycorrhizal diversity than Saana (Kytöviita et al., 2011; Pietikäinen et al., 2007), although the vegetation of the two sites is otherwise similar (Francini et al., 2014). In our study, the treatment and control plots were covered most part of the year to avoid seed rain. As the covering probably alters the microclimate, such as temperature and humidity, and this can affect soil communities (Coulson et al., 1996; Harte et al., 1996), we sampled adjacent un-manipulated non-covered meadow soil to check that the control plots gave a realistic picture of the soil communities. The concentration of bacterial PLFA markers and the abundance of nematodes were not affected by the covering and the only organisms responding were the non-mycorrhizal fungi, which increased under the cover. In a longer-term data set from the same experiment (PLFA samples from 2000 to 2006) this difference in fungal biomass was, however, not found (M.-M. Kytöviita, unpublished observation), suggesting that even this difference was coincidental. The covering was conducted nearly completely outside the growing season, which probably explains the lack of effects. 5. Conclusions Our results show that soil disturbance and absence of vegetation can severely reduce the abundance of soil biota in low-arctic ecosystems without large effects on soil biodiversity. This challenges the dogma of the importance of root exudates and fresh carbon input in maintaining soil biodiversity and suggests that a major part of the soil biodiversity may remain in disturbed sites in the absence of plant cover until the sites are revegetated by the nature or humans. Unlike we expected, however, replanting Solidago to the disturbed plots enhanced the growth of the nonmycorrhizal fungi, AM fungi and plant parasitic nematodes only and the abundance of bacteria and other soil fauna were not affected. This suggests that although a significant part of biodiversity may remain in the disturbed soil, natural abundances

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