Succession of litter-decomposing microbial organisms in deciduous birch and oak forests, northern Japan

Highlights

• Litter decomposition was experimentally monitored in birch and oak forests.

• The litter mass remaining was 50% for three years in a cool-temperate region.

• C/N ratios in the litter decreased in the first year and became stable thereafter.

• The forest types affected the litter decomposition.

• The microbial succession occurred from fungi to (gram-positive) bacteria.

Abstract

Biological litter decomposition and the litter-associated microbial organisms were monitored for three years to characterize litter decomposition in early and late successional stages. Two forests were used for the investigation: pioneer a forest dominated by birch (Betula platyphylla var. japonica) and a climax forest by oak (Quercus mongolica var. grosseserrata) in the cool-temperate region of northern Japan. Three types of litter were used: birch, oak and mixed litter. The litter decomposition was effective during the first year but 50% of the original litter remained even after three years. Carbon-to-nitrogen ratios in the litter decreased largely in the first year and became stable thereafter. The litter decomposition rates were not different among the litter types and between the forests. The temporal changes in phospholipid fatty acids (PLFAs) showed that fungal biomass reached its peak in the first year and the bacterial biomass increased steadily until the end of the experiment. The concentrations of fungal PLFAs in the litter did not differ between the litter types but were lower in the oak forest. The litter decomposition was performed mostly by fungi, in particular in the early stages, while bacterial decomposition depended on the litter types and/or the forest types. Gram-negative bacteria reached their peak of PLFAs in the second year while gram-positive bacteria PLFAs increased gradually during the three years. Therefore, the succession of microorganisms in the litter occurred from fungi to bacteria and from gram-negative bacteria to gram-positive bacteria in the two forests. Unlike in the case of coniferous or monotonic forests, the effects of forests and litter types on litter decomposition for the first year were weak. The forest types on litter decomposition appeared only for the long-term litter decomposition. The successional changes of microorganisms occurred from fungi to bacteria for long-term litter decomposition processes with increasing N concentration in the litter.

Introduction

Litter decomposition determines N and C dynamics in terrestrial ecosystems and is promoted by three processes, physical, chemical and biological degradation (Wardle et al., 2004; Hobbie, 1992). Of these processes, the biological decomposition, conducted mostly by bacteria and fungi, affects C/N flux between forest floor and trees (Lladó et al., 2017) and controls the fertility of forest ecosystems (Osono, 2007; Møller et al., 1999).

The litter decomposition by bacteria and fungi is regulated by the micro-climate, influenced by temperature, precipitation, vegetation and litter type (Parton et al., 2007). In addition, forest structures affect the composition of fungal and bacterial communities in the soils (Prescott and Grayston, 2013) and in the litter (Urbanová et al., 2015). Litter decomposers regulate C and N consumption in the early litter decomposition stages, while moisture and legacy in the soils play a major role in the later stages (García-Palacios et al., 2016). Since litter decomposition is slow in cool-temperate region, to investigate the microbial activities in the litter, long-term monitoring is required. However, few studies have been conducted for long term in this study area so far.

The composition of microorganisms involved in litter decomposition varies depending on the stage of decomposition. The fungi/bacteria ratio decreases greatly in the first eight months in the oak forests of Czech Republic (Voříšková et al., 2013). The diversities of bacteria and fungi change with succession (Tláskal et al., 2016; Purahong et al., 2016), although the relationships between bacteria and fungi are unclear. In the cool temperate regions of Japan, the dominant species along a successional sere change from birch to oak. This implies that litter mixed with birch and oak are often developed. During vegetation succession in temperate and cool-temperate regions, including Japan, birches (Betula) often develop pioneer forests and oaks (Quercus) form later and/or climax forests (Ishikawa and Ito, 1988). These two forest types are broadly distributed in Japan (Krestov et al., 2015). Therefore, the comparisons of these forests are invaluable to understand successional changes in litter decomposition and microbial composition. Furthermore, the conservation of these forests provides diverse ecosystem services, such as forestry, recreation and education, including learning succession (Mölder et al., 2019; Yokoyama and Tsuyuzaki, 2015). When the succession of microorganisms is observed in relation to litter decomposition as well as vegetation succession, these changes are applied to the evaluation of ecosystem health.

The home-field advantage (HFA) hypothesis suggests that litter decomposition is encouraged by litter mixed from only a few species. This hypothesis is examined well by litter mixed with broad-and needle-leaved leaves (Gartner and Cardon, 2004; Asplund et al., 2018; Ayres et al., 2009). However, this hypothesis has not been examined well in broad-leaved forests where the litter should be made of various broad-leaved plants (Gao et al., 2016). Since the litter components are different between broad-leaved and mixed forests, the different HFA effects are expected in broad-leaved forests. Also, the succession of microorganisms in these forests has not been investigated well. Therefore, the decomposition of litter consisting of birch, oak and their mixture were monitored.

Litterbag experiments are often used to investigate litter decomposition and its related factors (Wieder and Lang, 1982; Kazakou et al., 2006). In addition, biological litter decomposition is commonly estimated by indicators of biomass and composition of microorganisms, represented by quality and quantity of phospholipid fatty acids (PLFAs) (Chapman and Newman, 2010; Šnajdr et al., 2011). The concentrations of carbon (C) and nitrogen (N) in litter show the litter quality and N/C fluxes (Berg and McClaugherty, 2008). The present study provides new insights into microbial succession by using these techniques with considering differences in litter quality in cool-temperate regions. We monitored the successional changes in the biomass of each microbial taxon and litter decomposition at two forest sites of mixed forest examining birch and oak litter to investigate how the litter decomposition and the microbial succession develops and changes over time. Using these surveys, two hypotheses were examined: (1) HFA effects were weak to decompose litter in broad-leaved forests, as compared with mixture of broad-and needle-leaved litter, because of the similarity of litter species. (2) Microbial succession occurred during the litter decomposition for a few years with changes in nitrogen and carbon concentrations in the litter.