Elsevier

Fungal Ecology

Volume 41, October 2019, Pages 198-208
Fungal Ecology

Effects of forest dieback on wood decay, saproxylic communities, and spruce seedling regeneration on coarse woody debris

https://doi.org/10.1016/j.funeco.2019.05.004Get rights and content

Highlights

  • The frequency of brown rot fungi increased with forest dieback intensity.

  • Brown rotted wood was negatively associated with bryophyte cover.

  • Bryophyte cover was positively associated with Picea seedling density on deadwood.

  • Forest dieback may indirectly affect Picea seedlings by altering fungal community.

Abstract

Picea is one of the most dominant conifer genera in the Northern Hemisphere and includes species which require coarse woody debris (CWD) as a seedbed for regeneration. To understand the future of forest distribution under global climate change, it is important to investigate regeneration mechanisms in Picea forests on the borders of its distribution. In the present study, we evaluated the biotic factors affecting the establishment of Picea jezoensis var. hondoensis seedlings on CWD in one of its southernmost populations in central Japan, where there is dieback of Picea forest. Amplicon sequencing of the fungal ITS1 region of rDNA obtained from wood samples showed that forest dieback increased the frequency of brown rot fungi in CWD. The frequency of brown-rotted wood, in which wood holocellulose is decayed, increased with dieback intensity. The domination of brown-rotted wood in dieback forests was negatively associated with bryophyte cover which was positively associated with Picea seedling density. Forest dieback itself also had other strong negative effects on bryophytes. Thus, linkages between dead wood and spruce seedlings via bryophytes had collapsed after the dieback event, which may partly be a reason that the spruce forest shifted to and is staying as open grassland.

Introduction

Picea is one of the most dominant conifer genera in boreal, montane and subalpine forests in the Northern Hemisphere and consists of 28–56 species, depending on the classification system: the highest species diversity is found in East Asia (Ran et al., 2006). Because of their dominance, Picea play key roles in ecosystems and are important for timber production and reducing the risks of avalanches, rockfall, and soil erosion in certain localities (Panayotov et al., 2011). Although shifts in the Picea distribution range under global warming are of major concern, studies to date have been restricted to the northern limits of the forests in Europe (Seppä et al., 2009), North America (Mimura and Aitken, 2007), and Russia (Kremenetski et al., 1998), with few having been conducted in the southern limits of the forests in East Asia (Aizawa et al., 2009). Investigating regeneration mechanisms in Picea forests along the southern border of their range is important for understanding the future dynamics and distribution of Picea forests under global climate change.

It is well known that some Picea species require coarse woody debris (CWD) as a seedbed for regeneration (Mori et al., 2004; Bače et al., 2012). Given that the physicochemical properties of CWD change constantly as it decomposes, the decay class (DC; decay stage) of CWD and differences in the decay types of fungi—the organisms primarily responsible for wood decay in forest ecosystems—are important for the regenerative success of Picea (Mori et al., 2004; Fukasawa, 2012; Fukasawa et al., 2017; Fukasawa and Ando, 2018a). Fungal wood decay type is traditionally grouped into one of three categories: white rot, brown rot, or soft rot, reflecting fungal preference for lignocellulose decomposition and wood moisture content (Eaton and Hale, 1993). Bače et al. (2012) reported that Picea abies seedlings preferentially regenerate on logs in which white rot rather than brown rot fungi dominate, possibly due to the nutrient-poor, acidic, and fragile nature of brown-rotted wood. Furthermore, Fukasawa (2015) found a clear increase in the frequency of brown-rotted wood in pine CWD from north to south. These results suggest that Picea may face more challenges in seedling regeneration on CWD in their southernmost localities.

The southernmost populations of Picea (Picea jezoensis var. hondoensis) exist on the main island of Japan, distributed as fragments among several subalpine areas as remnants of the vegetation of the last glacial period (Aizawa et al., 2009). In one of those populations, a serious decline in the forest was observed after severe blowdown disturbance caused by a large typhoon in 1959 (Akashi and Nakashizuka, 1999). Numerous studies have focused on the negative effects of grazing by increased deer and mouse populations on seedlings in the affected forest areas, and as a result, many fences have been put in place to prevent deer grazing (e.g. Akashi and Nakashizuka, 1999; Shibata et al., 2008; Kisanuki et al., 2009). However, successful colonisation of Picea seedlings on CWD has not yet been recorded in this area.

From a microbial point of view, forest disturbance should be a major factor affecting fungal communities in CWD and wood decay because canopy openness, which generally increases after forest disturbance, has been reported to be an important factor affecting fungal communities in CWD (Bässler et al., 2010, Bässler et al., 2016; Lehnert et al., 2013; Horak et al., 2016; Krah et al., 2018). Vogel et al. (2017) reported the marked dominance of a brown rot fungus Fomitopsis pinicola after severe dieback in a P. abies forest in central Europe. Because the CWD decay process of subalpine conifer tree species are known to take several decades (Yin, 1999), it is expected that the effects of forest disturbance on fungal communities and CWD decay as well as the knock-on effects on seedling establishment would be long-lasting. Furthermore, our previous study found that wood decay type affects not only tree seedlings but also bryophyte communities on CWD (Fukasawa et al., 2015), which have a pivotal role in Picea seedling establishment (Iijima and Shibuya, 2010; Ando et al., 2017; Fukasawa and Ando, 2018a). It has been reported that bryophyte communities were severely damaged after forest dieback in the focal area (Oishi and Doei, 2015), and thus this damage might also affect seedling establishment. In addition to the direct effects of the microclimatic changes after disturbance (Jonsson and Esseen, 1990), the effect of wood decay should also be considered when predicting bryophyte and seedling colonisation changes (Fukasawa et al., 2019). The effect of wood decay type on Picea seedling regeneration may be a complex phenomenon including interactions with bryophyte species.

In the present study, we aimed to evaluate the effect of forest dieback on Picea seedling establishment in one of its southernmost populations in central Japan, which was severely damaged by a large typhoon in 1959. We hypothesised that dieback intensity affects the fungal communities, wood decay type, and bryophyte and seedling communities of CWD. Potential links between variables associated with spruce seedling density were evaluated by structural equation modelling.

Section snippets

Study sites

This study was conducted in a subalpine coniferous forest (34˚ 11′ N, 136˚ 06′ E, 1550–1650 m a.s.l.) on Odaigahara Plateau, central Japan (Fig. S1). The mean annual temperature of the study area is 6.4 °C and the mean annual precipitation is over 4500 mm (Shibata et al., 2008). The bedrock is sandstone. The area was formerly dominated by P. jezoensis var. hondoensis, but the forest in this area experienced severe damage caused by a Category 5 typhoon, named Vera or the Isewan typhoon, in

Fungal communities in decay class II snags

The mean diameter at breast height of the investigated DC II snags was 18.9 cm, 23.7 cm, and 25.2 cm for the control, mid-level, and intensive dieback sites, respectively, and was significantly smaller at the control site than the two dieback sites (one-way ANOVA, F = 9.531, P < 0.001; Tukey's HSD, P < 0.05).

A total of 1,714,800 reads were obtained using Illumina MiSeq sequencing after filtering. The obtained 653 OTUs consisted of 413 Ascomycota, 231 Basidiomycota, 4 Chytridiomycota, 4

Discussion

The present study clearly shows that forest dieback intensity has a significant effect on fungal communities in dead wood. A noteworthy finding was the increase in the frequency of brown rot fungi in dieback sites as compared with the control site. The dominance of brown rot fungi in the disturbed forest was also reported in a previous study (Vogel et al., 2017). Even though there are various causes of dieback (e.g. blowdown, pests, clear-cutting, and forest fires), a common feature of forests

Conclusions

In the present study, forest dieback that began due to severe blowdown disturbance in 1959 had marked impacts on the current wood decay type, fungal communities in wood, bryophyte cover and Picea seedling establishment. No significant direct link between forest dieback intensity and Picea seedling density was detected in our SEM. This is likely because of the strong relationship between seedling density and bryophyte cover, which is strongly affected by dieback intensity. In addition to the

Acknowledgements

We wish to thank Kayo Honobe and Takashi Higuchi for providing vegetation data of the study site, and to Masakuni Kimura and Masaki Michimori for their help in bryophyte identification in the field. We are also grateful to Syuichi Shichimeki and Kosuke Kanno in Kinki branch office of Ministry of the Environment Japan for the permission for our fieldwork. This study was financially supported by Japan Society for the Promotion of Science KAKENHI Grant Number 26850093 to YF.

References (76)

  • L.W. Lehnert et al.

    Conservation value of forest attacked by bark beetles: highest number of indicator species is found in early successional stages

    J. Nat. Conserv.

    (2013)
  • A. Mori et al.

    Substrate-associated seedling recruitment and establishment of major conifer species in an old-growth subalpine forest in central Japan

    Ecol. Manag.

    (2004)
  • M. Panayotov et al.

    Wind disturbances shape old Norway spruce-dominated forest in Bulgaria

    Ecol. Manag.

    (2011)
  • V. Pouska et al.

    The relation of fungal communities to wood microclimate in a mountain spruce forest

    Fung. Ecol.

    (2016)
  • C. Pyle et al.

    Heterogeneity of wood decay classes within hardwood logs

    Ecol. Manag.

    (1999)
  • T. Rajala et al.

    RNA reveals a succession of active fungi during the decay of Norway spruce logs

    Fung. Ecol.

    (2011)
  • J.H. Ran et al.

    Molecular phylogeny and biogeography of Picea (Pinaceae): implications for phylogeographical studies using cytoplasmic haplotypes

    Mol. Phylogenetics Evol.

    (2006)
  • S. Seibold et al.

    Dead-wood addition promotes non-saproxylic epigeal arthropods but effects are mediated by canopy openness

    Biol. Conserv.

    (2016)
  • T. Shirouzu et al.

    Resource utilization of wood decomposers: mycelium nuclear phases and host tree species affect wood decomposition by Dacrymycetes

    Fung. Ecol.

    (2014)
  • S. Vogel et al.

    The red-belted bracket (Fomitopsis pinicola) colonizes spruce trees early after bark beetle attack and persists

    Fung. Ecol.

    (2017)
  • M. Aizawa et al.

    Range-wide genetic structure in a north-east Asian spruce (Picea jezoensis) determined using nuclear microsatellite markers

    J. Biogeogr.

    (2009)
  • M.J. Anderson

    A new method for non parametric multivariate analysis of variance

    Austral. Ecol.

    (2001)
  • Y. Ando et al.

    Interactive effects of wood decomposer fungal activities and bryophytes on spruce seedling regeneration on coarse woody debris

    Ecol. Res.

    (2017)
  • K. Araya

    Relationship between the decay types of dead wood and occurrence of Lucanid beetles (coleoptera: lucanidae)

    Appl. Entomol. Zool.

    (1993)
  • C. Bässler et al.

    Effects of resource availability and climate on the diversity of wood-decaying fungi

    J. Ecol.

    (2010)
  • D. Bates et al.

    lme4: Linear Mixed-Effects Models Using Eigen and S4

    (2014)
  • R.A. Eaton et al.

    Wood: Decay, Pests and Protection

    (1993)
  • E. Espejo et al.

    Production and degradation of oxalic acid by brown rot fungi

    Appl. Environ. Microbiol.

    (1991)
  • F. Faul et al.

    Statistical power analyses using GPower 3.1: tests for correlation and regression analyses

    Behav. Res. Methods

    (2009)
  • J. Fox et al.

    An R Companion to Applied Regression

    (2018)
  • J. Fox et al.

    Structural Equation Models. R Package Version 3.1-9

    (2017)
  • Y. Fukasawa

    Effects of wood decomposer fungi on tree seedling establishment on coarse woody debris

    Ecol. Manag.

    (2012)
  • Y. Fukasawa et al.

    Species effects of bryophyte colonies on tree seedling regeneration on coarse woody debris

    Ecol. Res.

    (2018)
  • Y. Fukasawa et al.

    The effects of wood decay type on the growth of bryophyte gametophytes

    J. Bryol.

    (2018)
  • Y. Fukasawa et al.

    Regeneration of Cryptomeria japonica seedlings on pine logs in a forest damaged by pine wilt disease: effects of wood decomposer fungi on seedling survival and growth

    J. Res.

    (2017)
  • Y. Fukasawa et al.

    Beech log decomposition by wood-inhabiting fungi in a cool temperate forest floor: a quantitative analysis focused on the decay activity of a dominant basidiomycete Omphalotus guepiniformis

    Ecol. Res.

    (2010)
  • Y. Fukasawa et al.

    Fungal wood decomposer activity induces niche separation between two dominant tree species seedlings regenerating on coarse woody materials

    Can. J. Res.

    (2017)
  • U. Hagemann et al.

    Accumulation and preservation of dead wood upon burial by bryophytes

    Ecosystems

    (2010)
  • Cited by (12)

    • Wood-decay type and fungal guild dominance across a North American log transplant experiment

      2022, Fungal Ecology
      Citation Excerpt :

      Finally, decomposition time is also an important factor explaining wood-rotting fungal dominance. BR fungi have been observed to be relatively abundant at the beginning of the decomposition process, and WR fungi to be relatively stable throughout wood decomposition (Rajala et al., 2012, 2015; Fukasawa et al., 2019). Few, if any studies have investigated the biotic and abiotic drivers of wood-rotting fungal guild balance using high-throughput amplicon sequencing (HTAS) technologies (WR, BR, and SR relative abundances and ratios) and their impacts on dead wood decay types.

    • Patterns of community composition and diversity in latent fungi of living Quercus serrata trunks across a range of oak wilt prevalence and climate variables in Japan

      2022, Fungal Ecology
      Citation Excerpt :

      Alternatively, they may accelerate decomposition if they enhance the establishment of later-arriving species or alter the wood substrate so that it can be more easily utilised by later-arriving species (e.g. by removing lignin; Fukasawa et al., 2011). Mass mortality of forest trees caused by infectious diseases provides an excellent opportunity to study the effects of tree diseases on latent fungal communities and fungal community development after tree death, which in turn influence long-term ecosystem processes such as decomposition (Fukasawa et al., 2019). Tree diseases caused by bark and ambrosia beetles, which bore into trunks and act as vectors of microbial pathogens, have been reported worldwide (Santini and Battisti, 2019).

    • Indirect biogeomorphic and soil evolutionary effects of spruce bark beetle

      2020, Global and Planetary Change
      Citation Excerpt :

      In the unmanaged response, dead trees are left with no interventions. Standing or broken lying dead trees protect the soil effectively against solar irradiation (Hais and Kucera, 2008), mass movement (Šamonil et al., 2018a), and make habitats available for regeneration (Fukasawa et al., 2019). Natural regeneration is frequently faster on such sites, likely reducing the biogeomorphic impacts and hastening recovery toward pre-outbreak hydrogeomorphic conditions.

    View all citing articles on Scopus
    View full text