Our results emphasized the influence of the land use on soil microbiota complexity (e.g., number of spores and soil nematodes’ abundance) during the three studied years. We must consider that land uses with high root growth (e.g., rootability) such as the agroforestry system and unassisted forest restoration, may promote the specific ecological patterns into the soil microbiota community that made them dissimilar to the natural ecosystem. It in turns increase the abundance of some AMF species and soil nematodes individuals (Terefe et al. 2021) and can create a disturbed plant-soil interaction (Tedersoo et al. 2018), by promoting some AMF species (e.g., Claroideoglomus and Funneliformis) and soil nematode groups (Fungivores, Bacterivores, Omnivores, and Carnivores). In our study, F. mosseae (Glomeraceae), and C. claroideum (Claroideoglomeraceae) showed the highest abundance in all land uses. Some studies have reported Claroideoglomus and Funneliformis (frequency of occurrence by 23.4 and 20.5%, respectively) as the most dominant AMF genera in different land uses in tropical, and subtropical ecosystems (Laurindo et al. 2021, Terefe et al. 2021, Lucena et al. 2018). These AMF species are considered as bioindicators of high human activity and soil degradation. These results agree with the host-specificity hypothesis (Souza and Freitas 2018), and it determines the ecological preference (e.g., more effective symbiosis) between the plant species within each studied land use, and the identified AMF species and soil nematode functional groups (Melo et al. 2020, Zhang et al. 2021). Thus, highlighting the role of land uses on structure of complex and dynamic microbial communities such as the AMF and soil nematode communities.
The soil nematode complexity is directly linked with the energy fluxes, soil organic carbon pools, and soil food web into the entire ecosystem at spatial scale (Kooch et al. 2020, Nielson et al. 2020). These soil organisms play important ecosystem services (e.g., nutrient cycling, soil carbon dynamic, net primary production, and herbivory control), through their food behaviour (Nisa et al. 2021). We found differences into the soil nematode ecological patterns among the studied ecosystems (e.g., agroforestry system, unassisted forest restoration, and natural ecosystem). It may show an important aspect linked to the land use and its capacity to provide feeding sources, and habitat to a wide range of soil nematode groups (Siebert et al. 2020, Yang et al. 2021). Bacterivores and Fungivores are soil nematode groups that can feed the organic matter decomposers (e.g., bacterial and fungi, respectively). Both functional-groups indirectly control the organic matter mineralization rate, nutrient cycling, and plant-soil interaction (Kou et al. 2020).
Our results showed that in the natural ecosystem, the high diversity of plant species plus high temperatures promote the leaf litter diversification on soil surface and SOC pools. Into this condition, the decomposers’ activity, and their abundance increase, thus promoting food sources for bacterivores and fungivores. It creates a positive plant-soil interaction into the soil nematode community structure (Silva et al. 2021). Omnivores and Carnivores are soil nematode groups that promotes the micro-regulation process by reducing herbivore nematodes and other protists’ abundance. They also play an important role into the organic matter decomposition rate by controlling other soil organisms (e.g., Bacteria, Fungi, and even other soil nematodes) (Timper et al. 2021). They are extremely influenced by changes into the soil ecosystem promoted by land use and climate type because they are dependent of a complex soil food web (e.g., presence of other nematodes, and microbiota groups), such as we have found in the natural ecosystem (Wu et al. 2021).
Agroforestry systems that present a habitat simplification, low soil carbon pools, low soil water content, and some previous anthropogenic actions may decrease the abundance of these groups, especially Carnivore soil nematodes (Le Provost et al. 2021). The herbivores play an important role in the ecosystems by promoting the net primary production, because they feed roots, thus stimulating belowground growth (e.g., fine roots), and improving nutrient uptake (Gilarte et al. 2020). However, in the agroforestry system at Tropical conditions, we found a high abundance of herbivores through the low abundance of functional groups that act promoting micro-regulation (e.g., Carnivore and Omnivores). Here, we can consider it as a negative bioindicator by showing a soil food web disruption (Peralta et al. 2020, Ye et al. 2020).
The differences in soil microbiota ecological indices among the studied ecosystems were revealed by the significance on both soil microbiota richness and diversity. In this study, we did not find significance differences for dominance. We observed that on agroforestry systems at tropical ecosystems there was the highest values of soil microbiota richness and diversity. It is related to the specific ecosystem conditions (e.g., temperature and precipitation), and soil properties (e.g., soil pH, water availability, Olsen’s P, and total nitrogen) from the Tropics (Nascimento et al. 2021). We must consider that tropical soils when compared to subtropical ones, can provide a better environment for a wide range of soil microbiota organisms (Silva et al. 2021). It also determines the composition and functioning of the entire soil food web (Chernov et al. 2021). On the other hand, we must consider that in the unassisted forest restoration we found the highest values of richness and diversity. According to studies from elsewhere (Laurindo et al. 2020) into this system we can found high rootability (e.g., root growth and activity) that increase the abundance and diversity of soil organisms, such as mycorrhizal fungi and soil nematodes. These soil organisms occur into the rhizosphere through biochemical signals (Souza 2015). On the other hand, we found the highest diversity in the agroforestry system. Here, we must consider that the agroforestry system promoted soil microbiota community structure through the rhizodeposition process (Lucena et al. 2021), by releasing C-rich compounds into the rhizosphere, thus promoting habitat provision for soil microbiota (Nascimento et al. 2021).
The differences in soil chemical properties between the studied ecosystems were modulated by plant diversity on different land uses (e.g., agroforestry system, unassisted forest restoration, and natural ecosystem). In our study, we observed that agroforestry system was useful to promote soil pH, and Olsen’s P, whereas natural ecosystem promoted higher soil organic carbon. Overall, two different mechanisms may be involved at the increasing these soil chemical properties into these two conditions: i) rootability by fine roots production, and ii) H+ extrusion in root zone (Melo et al. 2020, Gao et al. 2020). We cannot exclude that the increase in soil organic carbon is driven by rhizodeposition at high plant community diversity (Zarafshar et al. 2020, Zhang et al. 2021). Finally, the introduction of native tree species into an agroforestry system can cause changes in soil chemical properties as described by the island of fertility hypothesis (Nascimento et al. 2021). Furthermore, many tree species used in agroforestry systems are highly dependent on AMF species to adapt to soil phosphorus deficiencies (Muchane et al. 2020). Consequently, this changes the rhizobiome, and increases the phosphorus availability to plants (Dierks et al. 2021).
Overall, considering the PCA analysis the natural ecosystem was correlated to the highest abundance of Fungivores, Bacterivores, and soil organic carbon. Natural ecosystems usually present high plant diversity (Liu et al. 2020). It favours the habitat provision and source availability for the soil microbiota, thus increasing the functional-groups diversity (Chen et al. 2020). Changes into soil ecosystem may influence both habitat and the source availability, which can create a cascade of events thus creating a negative or positive plant-soil feedback (Singh et al. 2021). On the other hand, changes into habitat provision can promote the functional redundancy process (e.g., a negative plant-soil feedback). It can explain the AMF community and soil nematodes community changes in the studied ecosystems (Pyles et al. 2020). Different land uses with low plant diversity can promote soil quality loss and soil microbiota community disrupting (Wang et al. 2021). In turns, it reduces the AMF and soil nematode richness (Ossowicki et al. 2021). PCA analysis also showed that fungivore and bacterivores were the most representative soil nematode functional groups (Wilschut et al. 2020). Besides that, Gigasporaceae were the most representative AMF family. Gigasporaceae species (D. scutata and D. erythropus) predominates in soils with acid pH. Our results of soil organic carbon were inversely related to the soil pH, what explained the predominance of AMF species in tropical conditions. These results agree with the work done by Laurindo et al. (2021), that described the highest values of soil organic carbon, and Gigasporaceae abundance (e.g., R. coralloidea) in subtropical sites.
Our study revealed that the soil microbiota complexity and soil abiotic traits were influenced by the land use. Soil organic carbon, soil pH, Fungivores, Bacterivores, Racocetra coralloidea, Dentiscutata scutata, and D. erythrophus were the main factors contributing to the data variance. Our work increases the understanding of the soil microbiota complexity in the rhizosphere of agroforestry systems and unassisted forest restorations in tropical and subtropical ecosystems. We provided evidence that land uses strongly influence both AMF and soil nematode complexity at local scales. Also, our results demonstrated how agroforestry system can affect soil microbiota assemblage and the soil abiotic traits when compared to a natural ecosystem. Differences in soil microbiota ecological patterns were associated with (1) the land uses by promoting different habitat provision, as we found difference on soil microbiota abundance, richness, and diversity, (2) changes in soil properties such as, soil pH, soil organic carbon, and available P, and (3) rhizodeposition by differences on soil organic carbon content into the land uses as observed into the PCA analysis. The most abundant AMF species in all the soil samples were Claroideoglomus claroideum, Funneliformis caledonius, and F. mosseae. This study shows the importance to consider how land uses can affect soil abiotic traits, and how these traits may influence soil microbial ecological patterns at spatial scale.