Long-term effects of tree harvesting on ectomycorrhizal fungal communities in boreal Scots pine forests
Introduction
Industrialized forest management has led to transformation of forests into homogenous managed stands, which have impacted biodiversity negatively (Secretariat of the Convention on Biological Diversity, 2010). Clear-cutting followed by soil scarification and planting is the most widespread forest harvesting method being applied in Fennoscandian countries for more than half a century (Framstad et al., 2013, Lundmark et al., 2013, Ratnam et al., 2014).
One group of organisms directly and negatively affected by clear-cutting is ectomycorrhizal fungi (EMF) (Jones et al., 2003). They depend on their symbiosis with trees and largely disappear after clear-cutting as a consequence of the ceased transport of carbon from the cut trees (Harvey et al., 1980, Jones et al., 2003, Luoma et al., 2004). Observations within a few years after clear-cutting indicate that the composition of the surviving and re-establishing EMF community may differ from that of older stands (Byrd et al., 2000, Durall et al., 2006, Hartmann et al., 2012, Jones et al., 2003, Rao et al., 1997). The difference is mainly attributed to the strong reduction of living EMF mycelia, as a consequence of the harvested trees, but other contributing factors could be changes in the biological and chemical environment selecting for certain species as well as variation between different EMF species in their ability to re-establish (Jones et al., 2003). The EMF community in boreal forests is species rich (Jonsson et al., 1999b, Taylor, 2002) with relatively few common species and many rare ones (Koide et al., 2005, Sterkenburg et al., 2015). As a regenerating stand develops and more belowground root biomass is created, the potential EMF species richness and activities of EMF increase, following the classical species richness vs. area relationship (Peay et al., 2007). Thus, it is essential to study disturbance responses of EMF communities in appropriate spatial and temporal scales. Studies of EMF communities done 30 years or more after harvest, using sporocarp surveys, mycorrhizal morphotyping or RFLP, show that EMF communities partly differ between previously clear-cut forest stands of different ages (Kranabetter et al., 2005, Palfner et al., 2005, Smith et al., 2002). However, the difference seems to be largest between young and older stands and less between older stands (Kranabetter et al., 2005). Wallander et al. (2010) studied long-term succession following clear-cutting using high throughput sequencing of EMF communities, based on extra radical mycelium, and reported Tylospora fibrillosa to totally dominate up to 30 years old stands of Scots pine but that species richness increased in 30–90-year-old stands.
Trees and other mycorrhizal host plants left at harvest enable EMF mycelia to survive into the new, regenerating forest (Amaranthus and Perry, 1987, Rosenvald and Lõhmus, 2008). An interesting question is whether the choice of forest regeneration method affects the survival of EMF after forest harvest. At present, the majority (78%) of the Swedish forests are clear-cut and planted or seeded compared to 20% that are naturally regenerated using seed trees (Skogsstyrelsen, 2014). In seed tree regeneration 50–150 seed trees per hectare are temporarily retained at harvest and cut when the seedlings are naturally established, around 10 years later (Karlsson and Örlander, 2004). By then, a portion of the naturally regenerated seedlings may potentially be colonized by EMF mycelia that were life-boated by the seed trees. Seedlings planted on clear-cut areas instead introduce a subset of EMF naturally established in the nurseries (Menkis et al., 2016). In theory, the use of seed trees should thus be more favorable for maintaining the EMF community in a harvested forest than clear-cutting and planting. A natural regeneration method similar to regeneration with seed trees is shelterwood regeneration, in which more trees are left (Karlsson and Örlander, 2004) and gradually harvested over a longer period of time aiming to increase regeneration success by reinforcing the effects of seed trees. This method is, however, not used in Sweden, but chosen since it is more contrasting to clear-cutting than seed tree regeneration.
The objective of this study was to investigate long-term effects on EMF communities by forest management using soil DNA sequencing in 50-year-old forest regeneration field experiments. We hypothesized (1) that effects of forest harvesting on the community composition and species richness of EMF to last for at least 50 years and, (2) that shelterwood regeneration has smaller effects than clear-cutting, due to differing levels of biological legacies of EMF during the early tree regeneration phase. We emphasize the community composition since a shift in community composition could potentially have functional effects on the ecosystem but also investigate species richness. We examined three stands that had been clear-cut and planted and three stands that were self-regenerated under shelterwood trees as part of experiments on regeneration methods initiated around 1960 and compared these with nearby natural stands. We also hypothesized (3) that EMF communities 2013 would be similar to those recorded at the same sites 18 years earlier. Finally, we examined (4) the potential of soil DNA sequencing to detect, not only widespread and frequent EMF, but also more rare species. The latter two questions were addressed by comparing the sequence data from the present study with previous results from an RFLP analysis of root tips and a sporocarp survey performed 18 years earlier in the same stands (Kårén, 1997).
Section snippets
Study site and sampling design
The study was conducted in Siljansfors Experimental Forest (1500 ha), located in west central Sweden, in a Scots pine dominated area within the boreal zone at an elevation of 210–425 m above sea level (N 60°54′, E 14°23′) (Fig. 1). Mean annual temperature is +3 °C and mean annual precipitation 674 mm. The annual deposition of atmospheric nitrogen was in the range of 2–4 kg N/ha (data from 1995 to 2014, Swedish Environmental Protection Agency, 2016). Management and production of the stands are well
Common EMF SHs
A total of 4,095,630 sequences were obtained from the IonTorrent sequencing, of which 2,685,934 passed quality filtering (Table A2). After trimming the data for observations with few sequence reads, 212 samples with in total 2,141,558 sequence reads remained, with the total number of reads per sample ranging from 1983 to 28,108. Ninety-eight out of the total 914 SHs (Table A2) were classified as EMF (4 Ascomycota and 94 Basidiomycota, in total 843,745 reads), representing 39.4% of the total
Discussion
Clear-cutting has immediate radical and inevitable effects on the community of EMF, causing death of mycelia and local extirpation of species (Jones et al., 2003). Our study addressed potential long-term effects on individual frequencies of the most common EMF, and on the overall composition of EMF.
Conclusion
Our results indicate that forest harvesting may affect the frequencies of some common EMF in Scots pine forests even after 50 years, while other common EMF appear to attain similar frequencies as in natural forests. Regeneration by shelterwood instead of clear-cutting and planting has little effect on the development of the common EMF after harvest. However, rare species were not well covered in the current study design and will probably require conservation efforts. Increased knowledge of
Acknowledgements
We thank Maria Jonsson for field and laboratory assistance in 1995 and 2013. We gratefully acknowledge Christer Karlsson at Siljansfors Experimental Forest for data of the experimental stands and logistic support. Dan Broström skilfully conducted the sporocarp inventories at Siljansfors. The study in 2013 was supported by Formas and Consul Faxe’s foundation. The work in the 1990s was supported by the Swedish Environmental Protection Agency.
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