Temperature changes affect multi-trophic interactions among pines, mycorrhizal fungi, and soil nematodes in a microcosm experiment
Introduction
Global climate warming can alter the community structures of various organisms (Tylianakis et al., 2008; van der Putten et al., 2010v), including those living below ground (Crowther et al., 2016). When soil organisms react to subtle climate changes (Bakonyi et al., 2007), it can lead to significant positive or negative feedback effects on plant growth and plant community structures (van der Stoel et al., 2002v; Kardol et al., 2010). The connection between belowground and aboveground biodiversity is more robust than formerly understood (Bardgett and van der Putten, 2014; de Vries and Wallenstein, 2017d), and the effects of environmental changes on aboveground vegetation compositions can indirectly affect soil biological communities (de Deyn et al., 2004d; Thakur et al., 2017).
Belowground, in the rhizosphere, root exudates and sloughing root cells provide resources supporting a hotspot of microbes and soil fauna (Bonkowski et al., 2009). In more than 85 % of land plants (Bundrett, 2017), intimate associations between mycorrhizal fungi and plant roots also create what is often referred to as the mycorrhizosphere (Garbaye, 1994). Ectomycorrhizal (ECM) fungi are key symbionts of woody plant roots, especially in boreal and temperate forests that include species in the Pinaceae, Betulaceae, and Fagaceae (Smith and Read, 2008). Extramatrical hyphae extending from ECM roots into the soil enhance the uptake of water and nutrients and provide fungal inocula for newly germinated seedlings (Leake et al., 2004). These hyphae are vulnerable to grazing by soil fauna (Fitter and Garbaye, 1994; Klironomos and Hart, 2001; Okada et al., 2005). Thus, ECM fungi interact with a wide range of other organisms in the rhizosphere.
Nematodes are a major group of soil microfauna because they are the most abundant animals on Earth (van den Hoogen et al., 2019). Bacterivorous and fungivorous nematodes can accelerate nitrogen and phosphorus flows by eating bacterial cells and fungal hyphae, respectively, contributing to nutrient cycling (Ingham et al., 1985). Nematodes are highly tolerant of even severe habitat conditions and thus occur in almost all habitats in freshwater, marine, and terrestrial ecosystems (Bongers, 1990). Nevertheless, soil-dwelling nematodes are affected by subtle environmental changes in both habitat conditions and biological interactions (Neher et al., 2005). For example, soil nematodes have been evaluated as possible bio-indicators of global warming (Bakonyi and Nagy, 2000; Bakonyi et al., 2007; Thakur et al., 2014; de Long et al., 2016d). As a proximate factor, soil temperature seems to be important in determining the assemblage pattern of nematode communities in the Antarctic (Freckman and Virginia, 1997), at alpine summits (Hoschitz and Kaufmann, 2004), in arid regions (Pen-Mouratov et al., 2004) and in a temperate forest (Thakur et al., 2014). However, the effect of biotic factors in the rhizosphere and mycorrhizosphere on nematode communities is not fully understood because of complex biological interactions in forest soils (Háněl, 2001; Matlack, 2001; Sun et al., 2013). Although nematodes and ECM fungi are known to have a predator–prey relationship (Ruess et al., 2000), the relative importance of ECM fungal hyphae as nematode food in forest soils remains to be clarified (Yeates, 2007).
To elucidate the corresponding effects of temperature on soil biota, a forest ecosystem with simple biota would be an ideal experimental system. Coastal sand systems are characterized by harsh, dry conditions with highly dynamic salinities, which lead to poor vegetation and low organic matter contents in the soil (Wilson and Sykes, 1999). Coastal sand systems are thus well suited to disentangling plant-nematode interactions (Brinkman et al., 2015). In eastern Asian coastal regions, monocultural Japanese black pine (Pinus thunbergii) stands have been established for protection against tidal intrusion and salt-bearing winds, for sand stabilization, and for recreational opportunities (Murai et al., 1992). The majority of P. thunbergii roots in a coastal forest are colonized by ECM fungi (Matsuda et al., 2009; Obase et al., 2009, 2011). ECM communities are affected by soil temperature — for example, warming led to an increase in the biomass of Cenococcum spp. (Fernandez et al., 2017) — and nematode communities may also be indirectly influenced by the extent of extramatrical hyphae of ECM fungi. Trophic structure of soil nematodes in cool to temperate pine forests has been characterized by the predominance of both bacterivorous and fungivorous nematodes (Háněl, 2001; Zhang et al., 2015; Kitagami et al., 2017, 2018), and those two trophic groups of nematodes play fundamental roles in nutrient cycling in the forests. Although forests with a single tree species characterized nematode communities, the mechanisms underlying their biological interactions remain to be clarified.
The aim of this study was to determine the effects of abiotic and biotic factors and their interactions on soil nematode communities. A pot experiment that simplifies the field environment was used to elucidate the relationships among (abiotic) temperature and (biotic) pines, fungi, and nematodes. We collected sandy soils from a coastal pine forest to simulate the tripartite (i.e., pines, fungi and nematodes) interactions. We added P. thunbergii seedlings in sterilized and unsterilized soils and observed nematodes after seedlings grew at different temperatures. We hypothesized that the richness at the genus level, abundance, trophic composition, and community structure of nematodes would be (1) directly affected by changing temperature and (2) indirectly facilitated by changing temperature via the stimulation of ECM hyphal production.
Section snippets
Experimental set-up
In February 2016, we collected approximately 15 L of sandy soils at 20-cm depth from an 18-year-old coastal P. thunbergii forest in Machiya, Mie prefecture, Japan (34°44′N, 136°31′E). The forest floor had few plants. The sandy soil was classified mainly as sand dune Regosol according to the Japanese soil classification (Forest Soil Division, 1976), which is equivalent to coarse sand (Soil Survey Staff, 2010). Soil pH at the collecting points was slightly acidic, 5.31 ± 0.09 (Kitagami et al.,
Plant biomass and mycorrhizal compositions
No significant interactions between soil and temperature treatments on either shoot or root biomass of pine seedlings were detected (Fig. 1, two-way ANOVA with treatment as between soil and temperature treatments, shoot; df = 2, F = 1.91, P = 0.17 and root; df = 2, F = 0.03, P = 0.96). Both biomasses significantly increased with temperature (Fig. 1, shoot; df = 2, F = 353.1, P < 0.001 and root; df = 2, F = 80.3, P < 0.001, Tukey HSD test, P < 0.05), but they did not differ significantly
Discussion
We examined the effects of temperature, pine seedlings, ECM fungi, and their interactions on the community structure of soil nematodes to determine the abiotic and biotic factors influencing nematode communities. Temperature significantly influenced not only plant biomass, ECM composition, and hyphal abundance (Fig. 1, Fig. 2), but also the abundance, trophic composition, and community structures of nematodes (Fig. 3, Fig. 4). In addition, structural equation modeling analysis revealed that
Conclusions
Our study revealed that above- and belowground plant biomass and rhizospheric biological interactions are controlled by abiotic and biotic factors that are also linked with the assemblage pattern of nematode communities. Our findings clarify that nematode community structures are regulated directly by temperature and indirectly via stimulation of pine seedling growth or ECM hyphal production. Because ECM fungi are found within nearly all pine root tips, ECM associations would create intimate
Declaration of Competing Interest
None.
Acknowledgements
We thank members of the laboratory of Forest Mycology at Mie University for their support in the experiments. This study was supported in part by the Grants-in-Aid for Scientific Research (B) 18H02237to YM and JSPS Research Fellow 18J13285 to YK from the Japan Society for the Promotion of Science.
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