Effects of nature restoration on soil nematode community
We found that the basal resources favored the soil nematode community, as well as the all trophic groups, both of which showed increasing patterns with forest ages during forest secondary succession. These findings agree well with previous reports (Keith et al., 2009; Morrien et al., 2017), which demonstrated that soil nematode populations peaked in the oldest age classes, mainly due to the increased root activity and ample food sources for soil nematode. For example, van Eekeren et al. (2009) observed that the abundance of herbivorous nematode was positively associated with fine root mass. Indeed, vegetation biomass accumulates substantially with forest stand ages, providing greater amounts of resources (leaves and litter) to soil nematode community. Consistent with previous studies (Banning et al., 2008; Orozco-Aceves et al., 2017), we found that soil microbial biomass carbon and the abundance of soil bacteria tended to increase with stand ages. Furthermore, litter accumulation and decomposition may improve the microclimates and soil properties (e.g. bulk density, soil moisture and pH), thereby potentially increasing the population of nematode trophic groups (Qin et al., 2019). These findings indicated that the abundance of soil nematode in secondary succession may eventually reach a level similar to that of primary forest soils in subtropical forests.
Contrary to our expectations, soil nematode diversity did not increase with forest stand age (Fig. 1b). This might be attributed to external disturbances which greatly alter the resource availability for soil nematode, consequently homogenizing these taxa across forest age classes (Francini et al. 2018). There are several possible reasons to explain this phenomenon. Firstly, in the same experimental site, Su et al. (2021) found that natural secondary forests had similar species diversities of shrub and bryophyte across all age classes. Secondly, soil biota in the higher trophic level require a longer time to adapt to changes in habitats than that in the lower trophic level (Valladares et al., 2012). Another possible explanation may be the distinct linkages among guilds in the soil food webs, because different trophic levels participated in differential interactions, including competition, predation, and mutualistic symbiosis (Yang et al., 2018). In this regard, soil nematodes may recover quickly after soil disturbances (Holtkamp et al., 2008) and are unaffected by forest stand age, despite an increase in plant biomass with time.
Our NMDS analysis of soil and plant communities separated intermediate age classes from primary forests. This suggested that the soil nematode and microbial communities showed an unstable structure during natural forest succession (Francini et al., 2018). We also observed that the community composition of soil nematode in the oldest stand age clustered together with the primary forests, although nematode abundance was lower in the T35-40 than primary forests. Soil nematode abundances and MBC were substantially higher in primary forests than in other forests, which is likely due to frequent disturbances in the young forests (Pickett et al., 2009).
Another important finding was that the value of plant parasite index decreased with forest stand ages. The plant parasite index, which denotes the proportion of plant parasites and free nematode, could reflect the health of soil and plant in the ecosystem (Bongers, 1990). These results suggest that natural ecosystem disturbance would shift the soil nematode community in a forest ecosystem and may threaten its ecosystem services.
Contributions of environmental factors to the soil nematode under nature restoration
In the present study, soil nutrient availability and vegetation growth were improved markedly during forest secondary succession. Soil nematode community composition was generally correlated with changes in abiotic soil parameters, such as pH, C and N availability, and soil moisture (Liu et al., 2016; Wang et al., 2021). The structure and composition of soil nematode communities might be associated with soil nutrients and biochemical factors, and their interactions with other factors (e.g., vegetation, soil, climate) (Chen et al., 2015; Wilschut and Geisen, 2020). This suggests that soil nematodes are sensitive indicators of temporal changes in soil characteristics and plant communities under disturbances (Williamson et al., 2005). Soil NH4+-N concentration likely increased with time, in response to increased plant biomass and organic matter turnover, (Banning et al., 2008), as we observed in primary forests. This will benefit the expansion of the soil nematode community in the older forest age classes (Chen et al., 2013).
We found that soil NH4+-N and available P concentrations were key factors influencing soil nematode abundance during forest secondary succession, and soil available P and NO3−-N concentrations for soil nematode diversity. These results agree with the observation that changes in soil nutrient due to forest secondary succession could shape soil nematode density and diversity (Betts et al., 2017; Frouz et al., 2013). Future studies should devote more efforts to soil food web communities for a better understanding of the potential effects of artificial or natural disturbance on ecosystem function and health in forest soils.
The soil nematode community across six forest stand ages highlighted the overarching importance of microbe and vegetation in indirectly regulating the bottom-up control of food webs, relative to soil environment. The establishment of vegetation exerted a direct effect on soil nematode community by changing the quantity and quality of resource inputs (Cortois et al., 2017; De Deyn et al., 2007) and an indirect effect through their influence on soil microbes and habitat conditions (Liu et al., 2016). Soil physico-chemical properties are often correlated with plant growth; such interaction affects soil organisms directly and/or indirectly through changes in microclimates, the quality and quantity of litter and root exudates, as well as the interactions among components of soil food webs (Paul et al., 2010). Previous studies have reported that changes in the abundance and diversity of soil nematode can be attributed to alteration of the vegetation community during succession (Scherber et al., 2010; Thornton and Matlack, 2002). Changes in quantity and quality of vegetation with time strongly affected soil nematode communities through bottom–up (resource control) effect (Cesarz et al., 2013; Eisenhauer et al., 2013). The bottom-up forces mediated by soil microbial and plant communities can control soil nematode community structure (Eisenhauer et al., 2013; Scharroba et al., 2012), and the trajectories of soil nematode communities probably mirror the distribution of tree species (Cesarz et al., 2013; Zhang et al., 2015). Therefore, among the driving forces of soil nematode community, bottom-up effects mediated by plants and soil microbes could be important under forest secondary succession in subtropical forests.
At the whole system level, the responses of the soil nematode communities to forest secondary succession were much stronger than those of soil microbial community, plant community and soil environment (Fig. 6). Additionally, the responses of soil nematode and microbial communities were more sensitive to environment changes than that of soil properties and plant communities (Wang et al., 2021; Chen et al., 2015; Wilschut and Geisen, 2020). Expanding the knowledge on soil nematode in forest ecosystems would provide insights into sustainable forest management.