Soil networks become more connected and take up more carbon as nature restoration progresses

Abstract

Soil organisms have an important role in aboveground community dynamics and ecosystem functioning in terrestrial ecosystems. However, most studies have considered soil biota as a black box or focussed on specific groups, whereas little is known about entire soil networks. Here we show that during the course of nature restoration on abandoned arable land a compositional shift in soil biota, preceded by tightening of the belowground networks, corresponds with enhanced efficiency of carbon uptake. In mid- and long-term abandoned field soil, carbon uptake by fungi increases without an increase in fungal biomass or shift in bacterial-to-fungal ratio. The implication of our findings is that during nature restoration the efficiency of nutrient cycling and carbon uptake can increase by a shift in fungal composition and/or fungal activity. Therefore, we propose that relationships between soil food web structure and carbon cycling in soils need to be reconsidered.

Figure 1. Network visualization of the interaction strengths.

Interaction strength between the species subgroups (a) and main species groups (b) in seminatural grasslands on recently, mid-term and long-term abandoned agricultural fields. Spearman's rank correlations of the relative abundances of all individual species combinations between two groups where calculated. The proportion of correlations >0.9 was divided by the total number of possible interactions to obtain the interaction strength between two groups of species. Line width is proportional to the absolute number of correlations >0.9. Line colour and transparency is proportional to the interaction strength, as indicated in the legend in the figure. The size of the circles is proportional to the number of species/taxa in that group. Red-filled circles are bacterial groups, blue-filled circles are fungal groups. Filled circles of other colours represent other taxa, with identities shown on the figure. B, bacterivorous; F, fungivorous; H, herbivorous; H.F, herbofungivorous; N, nematophagous; O, omnivorous; O.C., omni-carnivorous; P, predaceous; R.F., root-feeding; S., saprotrophic.

Figure 2. Plant species assemblage.

(a) Average H-values of recent, mid-term and long-term plant communities. (b) Principal coordinate analysis (PCO) on presence–absence data of the plant species in the field sites. Statistical summary on the difference between recent, mid-term and long-term sites is presented in Table 2 under analysis of similarities of the plant community in the field sites where the experimental cores were extracted.

Figure 3. Carbon flow in relation to biomass and abundance in the soil food web.

Labelled carbon derived from living components in the soil: roots (green), bacterial channel (red, orange and pink), fungal channel (blue, purple, magenta), and higher trophic levels (brown, yellow, orange). The groups indicated with +represent the amount of ¹³C excess in pmol per gram soil (bacteria, fungi, AMF) measured 1 day after pulse labelling. For all other groups, the ¹³C excess is the increase in δ¹³C values of the labelled compared with natural values, measured from non-labelled controls, in recently, mid-term and long-term abandoned agricultural fields. Labelled compounds in plant roots have been measured 1 day after pulse labelling. Labels in root-feeding nematodes, bacterivorous nematodes, enchytraeids, earthworms, collembolans, fungivorous cryptostigmatic mites and fungivorous nematodes have been determined 1 week after pulse labelling, and fungivorous non-cryptostigmatic mites, predaceous mites, spiders and omni-carnivorous nematodes were determined 2 weeks after pulse labelling.

Figure 4. Relative carbon amounts in trophic level along abandonment stage.

The carbon measured at the relevant time points for each group of soil biota. At day 1, the carbon is distributed among microbes. The microbe panel represents relative amounts of carbon exuded by the roots at day 1 after labelling. The total amount of labelled carbon in the roots decreases during succession (Supplementary Fig. 6).We have therefore presented the relative distribution of carbon scaled to the total amount of labelled carbon in the roots as excess ¹³C (the increase in atom% C values of the labelled compared with natural values measured from non-labelled controls) (bacteria, fungi, AMF). Bacteria (red), fungi (blue) and AMF (light blue) receive carbon from the plant roots. This carbon is distributed into the fungal channel and bacterial channel, where 1 week after labelling it is taken up by fungivorous mites, nematodes, collembola and bacterivorous nematodes and earthworms scaled to the total amount of labelled carbon in the roots as excess ¹³C. After 2 weeks after labeling, the carbon had reached the predators: spiders (brown), predaceous mites (orange), and omnivorous nematodes (yellow). Values of labels in the predators were also scaled to the total amount of labelled carbon in the roots as excess ¹³C. Absolute values for these groups are shown in Fig. 2. B, bacterivorous; F, fungivorous; O, omnivorous; P, predaceous.

Figure 5. Fungal-to-bacterial ratios in the three abandonment stages.

Left panel: fungal (F) to bacterial (B) ratio of excess C (labelled excess in contrast to unlabelled controls) in PLFA. Right panel: the total F–B ratios in PLFAs. Error bars represent s.d.