Home‐field advantage of litter decomposition differs between leaves and fine roots

Litter decomposition is a fundamental process influencing carbon dynamics and nutrient cycling in terrestrial ecosystems. In the 20th century, it was commonly accepted that climate, litter quality and soil biota hierarchically influenced the decomposition process from the large to the local scale (Swift et al., 1979; Coûteaux et al., 1995). However, recent studies have suggested that decomposer communities are much more important in driving litter decomposition than previously thought, mainly because aggregate data at large spatial scales are falsely assumed to represent causative relationships at small spatial scales (Bradford et al., 2014, 2017). In particular, microbial functioning may depend on complex interactions between microbial decomposers and their substrates such as plant litter (Jackrel et al., 2019; Lin et al., 2019). The home-field advantage (HFA) hypothesis predicts that decomposers are more efficient with the plant litters they most frequently encounter (Gholz et al., 2000; Ayres et al., 2009b; Austin et al., 2014; Palozzi & Lindo, 2018). This hypothesis has been empirically tested in various ecosystems via reciprocal litter transplant experiments (Ayres et al., 2009a; Milcu & Manning, 2011; Fanin et al., 2016; Lu et al., 2017; Palozzi & Lindo, 2017; Veen et al., 2018; Jackrel et al., 2019; Lin et al., 2019), and HFA was shown to increase decomposition rates by 7.5% on average (Veen et al., 2015a). However, the vast majority of studies demonstrating HFA effects used leaf litter, and whether the results are consistent with root litter has seldom been tested. Fine roots account for a substantial amount of litter inputs in terrestrial ecosystems, and play a major role in carbon and nutrient cycling through their afterlife 'effects' (Jackson et al., 1997, 2017; Freschet et al., 2013). Because HFA may arise due to the specialization of microbial communities towards their substrates, especially when the substrate is recalcitrant (Milcu & Manning, 2011), root litter should generate important HFA effects because of the necessity to synthesize specific oxidative enzymes to breakdown complex organic compounds. Yet, the very limited empirical experiments evaluating HFA effects using roots have reported positive, neutral or negative effects (Freschet et al., 2012a; Jacobs et al., 2018; Minerovic et al., 2018), perhaps as a consequence of an important variability in litter chemistry between 'home' and 'away' sites (Veen et al., 2015a). Hence, it is difficult to generalize the specialization of microbial communities towards root litter decomposition. Furthermore, whether HFA effects are coherent between different plant organs originating from the same species (e.g. leaves and roots), has never been evaluated in the same experiment. Because leaves and roots of the same species commonly differ substantially in their chemical compositions (Freschet et al., 2012b; Ma et al., 2016; Sun et al., 2018), different substrate qualities may stimulate contrasting microbial communities characterized by varying metabolic requirements and catabolic capacities (Sauvadet et al., 2019). Therefore, we hypothesize that the concordance in HFA effects between aboveground and belowground plant parts depends on the (dis)similarity in litter chemistry between leaves and roots, that is, plant species having a greater similarity in their chemical traits between leaves and roots should present relatively similar HFA effects (hypothesis 1). Furthermore, because litter recalcitrance is thought to be one of the main drivers controlling HFA due to a higher degree of specialization of microbial communities (Milcu & Manning, 2011), we hypothesize that root litters should display greater HFA effects than leaf litters because they are often more recalcitrant (hypothesis 2). We performed an 1132-d reciprocal litter transplant experiment among three forest sites using litters collected from the dominant tree species in each site: broadleaf (Castanopsis eyrei), coniferous (Cunninghamia lanceolata) and bamboo (Phyllostachys heterocycla cv Pubescens) (see Supporting Information Methods S1 for more details of the study sites). Freshly fallen leaf litters were collected using litter traps to prevent infection by soil biota of the 'home' site. Roots were extracted from the soil and washed on a sieve under running water. Fresh fine roots (Ф < 2 mm) were picked out and sterilized using chloroform vapour. Litter quality was characterized by 14 chemical traits related to element concentration, stoichiometry and carbon quality (Table S1; details about trait measurements are in Methods S1). In each site, six randomized blocks, with a distance of at least 10 m between each block, were selected for litterbag incubation. Each litterbag (15 cm × 10 cm with a mesh size of 25-μm, which allows microbial decomposers to enter the litterbags), was filled with c. 3.0 g litters, and labelled with a plastic tag. Although soil fauna may also significantly affect the magnitude of the HFA effects in some ecosystems (Milcu & Manning, 2011), previous results in our study sites showed that soil fauna did not substantially contribute to driving the HFA (Lin et al., 2019). In total, we placed six litterbags per litter type in each block for six successive harvests during the first year (94 and 222 d), second year (392 and 583 d) and third year (827 and 1132 d) after the start of the incubation, resulting in a total of 648 litterbags used in this study (three sites × six blocks × six litter types × six harvest times). Leaf litterbags were anchored on the forest floor and root litterbags were buried in the soil. Following harvest, the litter samples were cleaned under tap water, oven-dried at 60°C for 48 h and weighed. Litter mass loss (%) was calculated as (Mi − Mf)/Mi × 100, where Mi and Mf are initial and final litter dry mass, respectively. We ran nonmetric multidimensional scaling (NMDS) on the 14 chemical litter traits to visualize the variation in litter quality among the different litter types, and then performed a permutational multivariate analysis of variance (PERMANOVA) to test the significant effects of species, organ type and their interaction on litter chemical traits. We also calculated dissimilarity among the different litter types using the Euclidean distance. The effects of litter species, incubation site, harvest time and their interactions on mass loss of leaves or fine roots, respectively, were analysed using linear mixed effects models with a first-order auto-regressive variance structure to account for temporal pseudo-replication. To improve the reliability of our statistical inference, we selected the most parsimonious models based on the lowest AICc (Akaike's information criterion corrected for small sample sizes). In addition, the HFA index was estimated at each harvest time by running the regression model proposed by Keiser et al. (2014) (see Methods S1 for detailed description of the statistical analyses). The NMDS ordination separated relatively well the six litter types along the two first NMDS axes (Fig. 1), which were associated to chemical traits known to directly affect litter decomposition rates such as nutrients (i.e. nitrogen (N), phosphorus (P), potassium (K), manganese (Mn)), carbon forms (i.e. total phenols, lignin, tannins) and stoichiometric ratios (N : P, C : P, lignin : N) (Swift et al., 1979; Melillo et al., 1982; Keiluweit et al., 2015; Chomel et al., 2016; Sun et al., 2018). Litter chemistry differed significantly between different species (P < 0.001; Table S2). Litter chemical traits also differed significantly between plant organs (P < 0.001; Table S2), especially for the bamboo and coniferous species (Fig. 1). Specifically, bamboo litters were the most labile among the six litter types (Table S1), and both leaves and roots were generally located at the high quality end of the NMDS axes (Fig. 1). By contrast, broadleaf litters were more recalcitrant in comparison to bamboo litters and were generally located at the low quality end of the NMDS axes (Fig. 1), especially for the fine root litter (Table S1). In line with our expectations, bamboo and broadleaf litters generally exhibited higher and lower litter mass loss, respectively (Fig. 2). Coniferous was intermediate between bamboo and broadleaf litters. Overall, coniferous fine root litter was more recalcitrant than leaf litter, mainly because of higher concentrations in total phenols and tannins (Table S1), which may explain the lower mass loss of fine root litter compared with leaf litter over the course of the experiment (Fig. 2). We found a significant tree species × incubation site interaction effect on leaf litter mass loss (F4,40 = 13.23, P < 0.001; Table 1), suggesting that leaf litter decomposition depends on the environment in which it decomposes (Ayres et al., 2009a; Milcu & Manning, 2011; Lu et al., 2017; Veen et al., 2018; Lin et al., 2019). This is mainly the result of lower leaf litter mass loss of broadleaf species in its 'away' site, especially in the bamboo forest (Fig. 2). By contrast, there is no significant tree species × incubation site interaction effect on fine root litter mass loss (F4,40 = 0.78, P = 0.546; Table 1). Accordingly, we found that HFA effects were generally inconsistent between leaves and fine roots over 1132 d of decomposition (Fig. 2). In addition, although the similarity in litter chemistry between leaves and roots varied in the order broadleaf > bamboo > coniferous (Table S3), the broadleaf species showed the highest degree of difference in HFA effects between leaves and roots, that is leaf litter exhibited significant HFA effects throughout the 1132-d of decomposition, but fine root litter did not (Fig. 2). The only case for which both leaf and root litters displayed significant HFA effects was for the bamboo litter after 222-d of decomposition (Fig. 2). Yet, this species showed a relatively low degree of similarity in litter chemistry between leaves and roots (Table S3). Therefore, these results contradict our first hypothesis predicting that plant species having a greater similarity in their chemical traits between leaves and roots should present a greater similarity in HFA effects, and suggest that the interactions between microbes and their substrates depend on the plant organ considered. Interestingly, we found that root litter rarely showed significant HFA effects compared with leaf litter (Fig. 2). Contrary to our second hypothesis, these findings highlight that HFA effects are not higher for low litter quality compared with relatively high quality litter (Veen et al., 2015b; Palozzi & Lindo, 2017; Lin et al., 2019). In line with these results, previous microcosm incubation and field studies have also reported that root litter decomposition did not exhibit significant HFA effects (Jacobs et al., 2018; Minerovic et al., 2018). One potential explanation could be due to the differences in microhabitats along the soil profile. Leaf litter decomposes on the forest floor that is covered by freshly fallen litter, which is relatively rich in nutrients and labile carbon compounds, whereas root litter decomposes within the soil, in which the organic matter is heavily decomposed and more recalcitrant (Adl, 2003). These different resource conditions may generate significant differences in the composition and activity of microbial communities along the litter–soil continuum (Sterkenburg et al., 2018). In particular, the microbial communities from recalcitrant environments may have a wider functional capacity than those originating from richer environments, meaning that they more efficiently decompose root litters that vary widely in their chemical characteristics (functional breadth hypothesis; Keiser et al., 2011, 2014; Fanin et al., 2016), thereby decreasing their specialization toward the litters they most frequently encounter. Alternatively, although we buried fine root litter in the soil close to the adult trees of targeted species, the soil environment is likely more heterogeneous than the forest floor because it includes fine root litters from many other coexisting tree species. Therefore, the adaptation of specialist decomposers to individual species might be less important in an environment in which the resources are highly diverse and mixed. Furthermore, we cannot exclude that the difference in microclimatic conditions along the soil profile, with notably higher water content in the soil, may also affect decomposer communities and reduce the differences in decomposition rates for root litter (Fanin et al., 2019a). Additional studies simultaneously manipulating leaves and roots on the forest floor and in the soil will be necessary to disentangle the effects of microclimatic conditions from those of resource environment on HFA effects. By using a long-term reciprocal litter transplant experiment, we sought to test whether HFA patterns were consistent between leaves and fine roots. We found that HFA effects were generally inconsistent between plant organs, either across or within species, thereby underlining that leaf and root litters need to be considered separately when evaluating the adaptation of decomposers to their substrates. These results have several implications. First, they emphasize that HFA is not more pronounced for recalcitrant (i.e. roots) than labile litter (i.e. leaves) (Veen et al., 2015b; Palozzi & Lindo, 2017), and they demonstrate that HFA may also occur when litters are relatively rich in nutrients and labile carbon compounds (Lin et al., 2019). Second, the results highlight that there is often some decoupling between the aboveground and belowground subsystems in terrestrial ecosystems (Cameron et al., 2019; Delgado-Baquerizo et al., 2019; Fanin et al., 2019b), and this finding begs the question of whether the position at which soil communities perform decomposition is important to understand the local adaption of microbes to their sustrates. Finally, our results over a thousand days of incubation demonstrate an important temporal variability in HFA effects (Ayres et al., 2009a; Fanin et al., 2016; Veen et al., 2018), indicating that the succession in microbial communities may be also an important factor to predict the variability in plant–soil interactions over time. We conclude that plant–microbe interactions contribute significantly to nutrient and carbon cycling, but these interactions may strongly depend on the plant organ considered and the environmental conditions at the local scale. This research was funded by the National Natural Science Foundation of China (31500356). The authors thank Mei Pan, Fang Wang, Yan Liu, Pei Wang for the laboratory and field assistance. The authors thank Tania Maxwell for her help with English and useful remarks. Three anonymous reviewers provided helpful suggestions to improve the manuscript. DL designed the research. DL, PD, GY and HW performed the experiments with input from SQ, LZ, YY, XM and KM. DL carried out all of the statistical analyses with input from NF. DL and NF wrote the first draft of the manuscript. All authors contributed to manuscript completion and revision. Methods S1 Descriptions of the study site, litter traits measurements and statistical analyses. Table S1 Initial litter chemical traits of leaf and fine root litters for each of the three species used in this study. Table S2 PERMANOVA statistics for the effects of species, organs and their interaction on litter chemical traits. Table S3 Dissimilarity of chemical traits between leaf and root litters calculated with the Euclidean distance index among different litter types. Table S4 Results of the model selection procedure of the linear mixed effects models used to test for the effects of species, incubation site, harvest time and their interactions on mass loss of leaf and fine root litter, respectively. Please note: Wiley Blackwell are not responsible for the content or functionality of any Supporting Information supplied by the authors. Any queries (other than missing material) should be directed to the New Phytologist Central Office. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.