Soil physicochemical properties shape distinct nematode communities in serpentine ecosystems
Introduction
Serpentine soils, derived from ultramafic rocks, exhibit a low Ca/Mg ratio, high concentrations of certain heavy metals (e.g., Cr and Ni), low nutrient content, and low water availability (Proctor, 1999; Kazakou et al., 2008). These soils represent an extremely stressful environment and put the organisms under high selective pressure, leading to high levels of endemism. The vast majority of ecological and evolutional research on serpentine soils has focused on plants community structure and composition. Studies have also reported endemism as well as the mechanisms of physiological, morphological, and phenological adaptation to serpentine soils and their genetic bases (Proctor, 1999; Brady et al., 2005; Kazakou et al., 2008; Arnold et al., 2016; Kawai et al., 2019).
Soil chemical properties shape distinct microbial communities in serpentine and non-serpentine ecosystems (Schechter and Bruns, 2008; Igwe and Vannette, 2019). Moreover, microorganisms present in serpentine soils associated with plant roots enhance plant nutrient uptake and protect plants against toxic conditions (Abou-Shanab et al., 2006; Jourand et al., 2010; Doubková et al., 2012), thus greatly contributing to plant growth and fitness under harsh edaphic conditions. In contrast, literature regarding soil animal communities in serpentine soils is scarce (Visioli et al., 2019). Although soil fauna communities are known to be affected by high metal concentrations, e.g., Ni negatively affected the reproduction of a Collembola species (Visioli et al., 2013), or Cr affected the community compositions of nematodes (Šalamún et al., 2018). As soil organisms play key roles in the decomposition of organic matter and nutrient cycling, the clarification of their community structure will enhance our understanding of the ecosystem processes and functions in serpentine soils.
Nematodes are a major group of soil microfauna and are the most abundant animals on Earth (van den Hoogen et al., 2019). They play crucial roles in ecosystem processes, such as improving soil physical properties, participating in carbon and nitrogen cycling (Ingham et al., 1985), and maintaining ecosystem health by occupying key positions in the soil food cycle (Ferris, 2010; Zhang et al., 2017). On the other hand, soil nematode communities are affected by subtle changes in abiotic and biotic factors (Neher et al., 2005). For example, the abundance of bacterivorous nematodes is higher in soils with high nitrogen concentrations (Shaw et al., 2019), and the species richness of nematodes is positively correlated with the number of plant species (De Deyn et al., 2004; Thakur et al., 2017). Owing to such biological characteristics, community structures of nematode can be used to monitor changes in soil conditions and are expressed by several indices based on feeding guild and life strategies (defined by c-p values) (Bongers, 1990; Ferris et al., 2001; Griffiths et al., 2016). The maturity index (MI), channel index (CI), enrichment index (EI), and structure index (SI), aim to more accurately predict the disturbance of the soil environment, decomposition pathway, nutrient level, and soil food web development, respectively (Bongers, 1990; Ferris et al., 2001). In fact, these indices were applied for evaluating effects of nutrient inputs, conservation efforts of soil biodiversity and forest management practices on soil nematode communities (Zhao et al., 2014; Ciobanu et al., 2019; Kondratow et al., 2019).
Moreover, soil nematodes have been evaluated as possible bio-indicators of increased heavy metal content (Šalamún et al., 2014, 2018). Thus, the harsh environment of serpentine soils may shape unique nematode communities, in which stress-tolerant nematode taxa are prominent (Bongers, 1990). Previous studies have demonstrated more fungivorous nematodes in serpentine soils than in non-serpentine soils, suggesting a higher rate of energy flow through the fungal-based soil food web (Hungate et al., 2000; Monokrousos et al., 2014). In fact, microbial biomass and community are affected by changes in nutrients input (Frostegård et al., 1993; Bardgett and McAlister, 1999). Since nematodes are involved in nutrient cycling through feeding on bacteria and fungi (Ingham et al., 1985), nematode assemblages might be tightly connected with bacterial and fungal responses driven by nutrients input. However, there is a lack of knowledge regarding how abiotic and biotic factors affect nematode community structures in serpentine soil ecosystems. In the present study, we identified factors determining the structure of soil nematode communities by comparing the assemblage patterns of these organisms in serpentine and non-serpentine soils.
The aim of this study was to identify the nematode communities and their determinant proximate soil factors in serpentine and non-serpentine soil ecosystems in Mt. Oeyama, Japan. We hypothesised that (1) the abundance, taxonomic richness, and diversity indices of nematodes are higher in non-serpentine soils than in serpentine soils owing to harsh abiotic conditions in the latter; and (2) the community structures of soil nematodes in serpentine habitats are affected by low Ca/Mg ratio and water availability, high concentrations of certain heavy metals (e.g., Cr and Ni). Recalcitrant litters are often accumulated in serpentine ecosystems due to their high heavy metal concentration and lignin/N ratio from serpentine ecosystems (Nakamura et al., 2019). We expected that fungivorous nematodes are dominant in serpentine soils due to the accumulation of recalcitrant plant tissues which are preferably decomposed by fungi in serpentine ecosystems.
Section snippets
Site description
This study was conducted in cool-temperate broad-leaved forests on Mt. Oeyama (35° 27’ N, 135° 06’ E, 832 m a.s.l.) in Kyoto, Japan. The mean annual temperature and precipitation in the adjacent city of Miyazu are 14.7 °C and 1927 mm, respectively (data from the Japan Meteorological Agency, 2005–2015). Serpentine and non-serpentine sites were at a similar elevation (450–500 m a.s.l.) and situated 4 km apart. The both sites have a gentle slope and face south. The non-serpentine soil was a brown
Soil environmental conditions
Root biomass (4.6 ± 0.8 mg g–1 dry soil, W = 13, p < 0.001), soil pH (4.95 ± 0.16, W = 33, p < 0.001), Mg (938.3 ± 593.7 μg g–1 dry soil, W = 15, p < 0.01), and Ni (31.1 ± 11.6 μg g–1 dry soil, W = 15, p < 0.01) were significantly higher in serpentine habitats than non-serpentine ones (Table 1). In contrast, the soil water content (38.5 ± 2.0 %. W = 38, p = 0.03), NO3− (208.4 ± 63.1 μg g–1 dry soil, W = 39, p = 0.01), and Ca/Mg ratio (3.61 ± 0.20 μg g–1 dry soil, W = 40, p < 0.01) were
Nematode community indices show habitat features between serpentine and non-serpentine soil ecosystems
Our first hypothesis that (1) the abundance, taxonomic richness, and diversity indices of nematodes are higher in non-serpentine soils than in serpentine soils due to harsh abiotic conditions in serpentine soil was not supported. Serpentine soils do not limit nematode abundance and alpha diversities. Our sampling efforts were sufficient to depict nematode assemblages at the genus and family level from accumulation curves in both serpentine and non-serpentine habitats reached plateaus. The
Conclusion
Our study revealed that the physicochemical properties of serpentine soils shape nematode assemblage patterns. Even in nutritionally poor and high heavy metal contained serpentine soils, nematode abundance and diversity were comparable to those in non-serpentine soils, suggesting that some species adapt to serpentine soils. Since certain nematode taxa were affected by soil abiotic factors, these nematodes can be an indicator taxon to predict the effects of soil processes in harsh environments.
Declaration of Competing Interest
The authors report no declarations of interest.
Acknowledgments
We thank the landowners for their help and permission to access study sites. We also thank M. Mukai, A. Kataoka, M. Takagi, and M. Sasaki for the measurement of soil properties in study sites, members of the laboratory of Forest Mycology at Mie University for their support with laboratory experiments. We thank M. Ataka, R. Nakamura, and N. Okada, H. Kajino and R. Fujii for the maintenance of the study sites. We would like to thank Editage (www.editage.com) for English language editing. We also
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