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A recent epidemic of the mountain pine beetle (Dendroctonus ponderosae) has led to the deaths of billions of pine trees across western North America. Rapid warming has allowed the beetle to expand its elevational and latitudinal ranges. This photo shows trees that were attacked 100s of meters above the beetles’ historical elevational range limits in CO, USA. The trees with red needles were attacked during the previous growing season; recently attacked trees have not yet begun to fade (photo by Jeffry B. Mitton).
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Extensive tree mortality from insect epidemics has raised concern over possible effects on soil biogeochemical processes. Yet despite the importance of microbes in biogeochemical processes, how soil bacterial communities respond to insect-induced tree mortality is largely unknown. We examined soil bacterial community structure (via 16S rRNA pyroseq...
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... trees used in our study had uniquely numbered tags linking them to a forest demography study (see ) that established dates of bark beetle attack and subsequent tree mortality. Tree mortality from bark beetles occurs within a few weeks of mass attack and can be determined from notable changes in needle color (green fades to yellow and red), but does not cause substantial needle drop until the following year (Figure 1). We used trees from five temporal categories of bark beetle-induced mortality, which were considered as years 0, 1, 2, 3, and 4 of our 5 year chronosequence. ...
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... have long been known to influence species diver- sity and abundance patterns in macro-biological communities and the majority of microbial communities studied to date have been sensitive to a range of disturbance types, severities, and dura- tions ( Allison and Martiny, 2008;Shade et al., 2012). Nevertheless, the structure of bacterial communities in our study resisted bark beetle-induced tree mortality despite concurrent changes in soil N pools and cycling processes (Table 1; Figure 5). The stability of communities in response to perturbation relies on the ability of individual bacteria to tolerate, endure, or adapt to environ- mental change. ...
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Citations
... When trees appeared to die under different levels of disturbance due to the bark beetle, significant changes occurred mainly in bacteria, indicating that soil bacteria are highly sensitive to tree mortality. In contrast, Ferrenberg et al. [59] concluded that the soil bacterial community structure did not change when studying the tree mortality associated with bark beetle; the reason for the differing results may be due to the different locations of the study areas and the different number of years of recovery after tree death, suggesting that the response of the soil microbial community structure to changes in tree mortality is related to the host or ecosystem. In this study, it was found that the microbial community composition in the medium-intensity group was the most similar to that of the control group. ...
Forests are affected by a wide range of disturbances globally, resulting in the decline or death of large areas of them. There is a lack of comparative studies on how soil properties change in forests that die under the influence of disturbances, especially considering different levels of disturbance. For this study, we took Larix olgensis—a major plantation forest species in northeast China—as the research object, one in which a large outbreak of bark beetle led to large-scale forest death, and set up fixed sample plots characterized by different disturbance intensities. We investigated the responses of soil physicochemical properties and microbial community compositions to different disturbance intensities through the determination of soil nutrient indices and high-throughput sequencing. The results show that there were significant differences (p < 0.05) in the effects of different disturbance intensities on soil physicochemical properties, where the soil moisture content, total nitrogen, total carbon, and total phosphorus in the control group were significantly higher than those in the disturbed groups. The soil pH was highest under low-intensity disturbance and the soil total potassium content was highest under high-intensity disturbance. At different disturbance intensities, the highest soil moisture content was found in the high-intensity group. Proteobacteria, Actinobacteria, Verrucomicrobia, Acidobacteria, Candidatus_Rokubacteria, Chloroflexi, Gemmatimonadetes, and Thaumarchaeota were the dominant populations with higher abundances; meanwhile, the relative abundance of Bacteroidetes, Tenericutes, and a tentatively unclassified fungus differed significantly (p < 0.05) across disturbance intensities. Among the dominant microbial populations, Acidobacteria showed a significant negative correlation with soil pH and a significant positive correlation with total potassium content, Thaumarchaeota showed significant positive correlations with soil moisture content and total nitrogen content, and Firmicutes and Gemmatimonadetes showed significant negative correlations with total carbon content in the soil. Furthermore, soil total nitrogen content was the key factor driving changes in microbial communities. The results of this study provide a scientific basis for the study of the long-term effects of tree mortality caused by insect pests on soil microbial communities and their response mechanisms, which is of great theoretical value for the establishment of scientific and effective methods for woodland restoration.
... High tree mortality following pine beetle outbreaks leads to alterations in carbon storage (Kurz et al., 2008), nitrogen cycling (Griffin et al., 2011;Rhoades et al., 2017) and soil microbiomes (Ferrenberg et al., 2014;Treu et al., 2014;Mikkelson et al., 2016;Pec et al., 2017). Symbiotic ectomycorrhizal (ECM) fungi, which form obligate and diverse symbioses with P. contorta (Talbot et al., 2014) are particularly sensitive to tree mortality and their abundance and richness are reduced after beetle outbreaks (Treu et al., 2014;Pec et al., 2017). ...
... Symbiotic ectomycorrhizal (ECM) fungi, which form obligate and diverse symbioses with P. contorta (Talbot et al., 2014) are particularly sensitive to tree mortality and their abundance and richness are reduced after beetle outbreaks (Treu et al., 2014;Pec et al., 2017). While soil bacterial communities appear to be more resistant to beetle-induced tree mortality than fungi (Ferrenberg et al., 2014), heavily impacted forest (~85% tree mortality) have been shown to have an increased bacterial alpha diversity and significant compositional changes throughout the different infestation phases (Mikkelson et al., 2016). How these already stressed lodgepole pine forests and their associated soil microbiomes will recover after high severity wildfires over time remains an open question. ...
Lodgepole pine forests are under threat due to wildfires of increasing severity and frequency coupled with tree mortality from insect outbreaks. Soil microbial communities, which drive biogeochemical cycles and partner in mycorrhizal symbiosis with lodgepole pines, play critical roles in the ability of these forests to survive and regenerate in the face of simultaneous global change threats. How soil microbial communities are influenced by fire severity and soil depth and how they recover over time in lodgepole pine forests with existing insect-driven mortality remains an open question. Here, we sampled two soil depths (0-5 and 5-15 cm) and various burn severities across a ten-year wildfire chronosequence in the Southern Rocky Mountains. We used qPCR of 18S and 16S rRNA genes to assess changes in fungal and bacterial abundance and ITS2 and 16S amplicon sequencing to assess fungal and bacterial richness and composition. Our results show that: 1) higher severity fires led to larger reductions of both fungal and bacterial abundance and richness, 2) the impact of fire on fungal and bacterial communities was modulated by soil depth, with more severe impacts in shallower soils 3) both fungal and bacterial communities exhibit a partial recovery of abundance and species richness in older fires, 4) fire severity is the main driver of fungal and bacterial community structure but its effect varied across time, 5) pyrophilous "fire-loving" fungi and bacteria exhibit an increased abundance in burned plots, particularly in recent fires, and 6) symbiotic ectomycorrhizal fungi are particularly hard hit by the compound effect of the beetle-driven tree mortality and wildfires. They exhibit a consistently low abundance and richness in the high severity plots which did not recover over time, and unburned plots have a depauperated ectomycorrhizal community.
... High tree mortality following pine beetle outbreaks leads to alterations in carbon storage (Kurz et al., 2008), nitrogen cycling (Griffin et al., 2011;Rhoades et al., 2017) and soil microbiomes (Ferrenberg et al., 2014;Treu et al., 2014;Mikkelson et al., 2016;Pec et al., 2017). Symbiotic ectomycorrhizal (ECM) fungi, which form obligate and diverse symbioses with P. contorta (Talbot et al., 2014) are particularly sensitive to tree mortality and their abundance and richness are reduced after beetle outbreaks (Treu et al., 2014;Pec et al., 2017). ...
... Symbiotic ectomycorrhizal (ECM) fungi, which form obligate and diverse symbioses with P. contorta (Talbot et al., 2014) are particularly sensitive to tree mortality and their abundance and richness are reduced after beetle outbreaks (Treu et al., 2014;Pec et al., 2017). While soil bacterial communities appear to be more resistant to beetle-induced tree mortality than fungi (Ferrenberg et al., 2014), heavily impacted forest (~85% tree mortality) have been shown to have an increased bacterial alpha diversity and significant compositional changes throughout the different infestation phases (Mikkelson et al., 2016). How these already stressed lodgepole pine forests and their associated soil microbiomes will recover after high severity wildfires over time remains an open question. ...
... Despite its relevance, our understanding of tree mortality effects on soil microbial communities is still scarce and shows important knowledge gaps. For example, most studies have been conducted in conifer forests of Europe and North America affected by insect outbreaks (Ferrenberg et al., 2014;Š tursová et al., 2014;Saravesi et al., 2015;Mikkelson et al., 2016;Pec et al., 2017;Veselá et al., 2019;Custer et al., 2020). In these studies, insect outbreaks can cause major mortalities (e. g. > 75% of the trees) in very short time periods (e.g. ...
The loss of tree health is a global concern with many unknown cascading impacts on the diversity and function of forest ecosystems. Specifically, it is uncertain how the process of tree decline and mortality driven by exotic pathogens might alter the soil microbiome. Here we combined high-throughput sequencing, neighborhood models, and network analysis to explore the impacts of the decline of a Mediterranean tree species, Quercus suber, on the diversity, composition and network structure of soil fungal and bacterial communities in forests invaded by the exotic pathogen Phytophthora cinnamomi. The belowground footprint of pathogen-driven tree decline implied an increase in the taxonomic and phylogenetic diversity of both bacteria and fungi, but also a severe reduction of tree-symbiotic fungi and Proteobacteria known to have positive effects on plant growth and disease suppression. Moreover, we detected alterations of the topology of soil microbial networks in declining tree neighborhoods (lower connectivity, higher modularity), with implications for ecosystem function. Our findings reveal the large impacts that moderate levels of tree decline can have on the soil microbiome of invaded forests, and highlight the recovery of a functionally diverse and highly connected soil microbiome as a key target in the restoration of these disturbed systems.
... This suggests that active, rare taxa decrease in accordance with tree death, while active abundant taxa remain more stable, supporting the theory that rare taxa play a disproportionately large role in microbial community dynamics following bark beetle outbreaks (Mikkelson et al., 2016). Changes in soil bacterial communities may be short-term, however, as evidenced by a five-year chronosequence study after mountain pine beetle outbreak which revealed little change in bacterial community structure and assembly; this was also reflected in weak changes to soil nitrogen and carbon pools (Ferrenberg et al., 2014). ...
Bark beetle (Coleoptera: Curculionidae: Scolytinae) outbreaks can be spectacular, killing trees across hundreds to thousands of hectares or more of forest land. As bark beetles are a natural disturbance agent, it is hypothesized that ecosystems are adapted to such periodic disturbances. Under climate change, however, these beetle outbreaks have become more severe, persistent, and chronic on many landscapes, bringing into question the long-term resilience of these forests and the biota that depend on them. Our chapter objective is to review and generalize the effects of bark beetle outbreaks on flora, fauna, and soil microbiota across diverse landscapes worldwide. Through loss of canopy trees, there is an increase in forest gaps and dead organic material that alters resource availability for many organisms. As organisms respond to altered resources, they may create feedback loops to themselves and their environment. Tree regeneration dynamics may set the stage for dominance by the same or different canopy species, retriggering, advancing, or otherwise altering successional trajectories. Herbs and shrubs often become more abundant and diverse under postbark beetle outbreaks due to increased light, water, and nutrient availability. Faunal species that rely on open habitat conditions and greater availability of newly available resources (e.g., coarse woody debris, bark beetles as prey items, and understory plant release) tend to benefit from bark beetle outbreaks; vice versa for other species; and variable responses are indicated for other species. Both positive and negative impacts on red-listed or endangered species have been reported. Ectomycorrhizal and saprophytic fungi, respectively, tend to decrease and increase after bark beetle outbreaks. There may be an increase in soil bacteria with different bacterial species dominant in beetle-killed trees. Responses of biota are therefore species-specific, and there are winners and losers in systems based on habitat alterations and life-history requirements. Longer-term and comprehensive studies of cascading, interacting, and simultaneous ecological impacts for multitaxa are recommended for maintaining the resilience of these disturbed landscapes under climate change.
... The soil fungi's Shannon-Wiener index was calculated using QIIME 1.8.0 software based on a normalized database of OTUs [33]. At the same time, clustering analysis and analysis of similarities (ANOSIM) were used to test the differences in the composition of the soil fungi community among the four treatments. ...
Research Highlights: 1. Soil fungi have a higher influence on seedling density compared to soil environmental factors; 2. Host-specific pathogens and beneficial fungi affect seeding density via different influencing mechanisms. Background and Objectives: The growth and development of seedlings are the key processes that affect forest regeneration and maintain community dynamics. However, the influencing factors of seedling growth around their adult conspecifics are not clear in arid desert forests. Probing the intrinsic relations among soil fungi, soil environmental factors (pH, water content, salinity, and nutrition), and seedling density will improve our understanding of forest development and provide a theoretical basis for forest management and protection. Materials and Methods: Four experimental plot types, depending on the distance to adult conspecifics, were set in an arid desert forest. Soil environmental factors, the diversity and composition of the soil fungal community, and the seedlings’ density and height were measured in the four experimental plot types, and their mutual relations were analyzed. Results: Seedling density as well as the diversity and composition of the soil fungal community varied significantly among the four plot types (p < 0.05). Soil environmental factors, especially soil salinity, pH, and soil water content, had significant influences on the seedling density and diversity and composition of the soil fungal community. The contribution of soil fungi (72.61%) to the variation in seedling density was much higher than the soil environmental factors (27.39%). The contribution of detrimental fungi to the variation in seedling density was higher than the beneficial fungi. Conclusions: Soil fungi mostly affected the distribution of seedling density in the vicinity of adult conspecifics in an arid desert forest. The distribution of seedling density in the vicinity of adults was mainly influenced by the detrimental fungi, while the adults in the periphery area was mainly influenced by the beneficial fungi.
... For the temporal impact, bacterial alpha diversity and community structure showed significant changes with interannuality but not season, which did not support our second hypothesis. The nonsignificant variations of bacterial communities with seasons could be explained by several points: (1) Bacterial communities are relatively stable compared with their activities, which vary significantly with disturbances or shifts in environmental conditions (Ferrenberg et al. 2014); (2) High heterogeneity of bacterial communities within a sampling site may cover the low variations caused by seasons; and (3) The Illumina amplicon sequencing technique may fail to reveal low variations caused by the seasons. also reported that Illumina amplicon sequencing-based soil microbial community structure does not vary significantly among different seasons in alpine forest soils . ...
Seasonal dynamics of soil microbial communities may influence ecosystem functions and services. However, few observations have been conducted on the dynamics of a bacterial community assembly across seasons in different elevations in mountain forest ecosystems. In this study, the diversity, compositions, community assembly processes, and co-occurrence interactions of soil bacterial communities were investigated using Illumina sequencing of 16S rRNA genes across different seasons during two consecutive years (2016 and 2017) at two elevational sites in Mount Gongga, China. These two sites included an evergreen broad-leaved forest (EBF, 2100 m a.s.l.) and a dark coniferous forest (DCF, 3000 m a.s.l.). The results showed that bacterial diversity and structure varied considerably between the two elevational sites with only limited seasonal variations. Interannuality had a significant effect on the diversity and structure of soil bacterial communities. The bacterial alpha diversity was significantly higher at site EBF(e.g., OTUs richness, 2207 ± 276) than at site DCF(e.g., OTUs richness, 1826 ± 315). Soil pH, temperature, elevation, and water content were identified as important factors shaping soil bacterial communities in the mountain forests. Bacterial community assembly was primarily governed by deterministic processes regardless of elevation and season. Deterministic processes were stronger at site DCF than at EBF. The soil bacterial community at site EBF harbored a more complex and connected network with less resistance to environmental changes. Overall, this study showed that seasonal dynamics of bacterial communities were much weaker than those along elevations, implying that a single-season survey on a bacterial community along an elevational gradient can represent overall changes in the bacterial community.
Key points
• Seasonal dynamics of soil bacterial communities were studied in Mount Gongga.
• The bacterial community was mainly affected by elevation rather than season.
• Deterministic processes dominated bacterial community assembly.
• The bacterial network was more complex but less stable at EBF than at DCF.
... Some bacterial OTUs showed higher specificity towards disturbed plots, but their low general abundance in our limited data prevents any further interpretation. Soil bacterial community composition has previously been shown to be relatively little affected by storm and bark beetle disturbance (Ferrenberg et al., 2014;� Simonovi� cov� a et al., 2019) and the magnitude of changes relate to the proportion of remaining living trees (Mikkelson et al., 2017), which might have helped to stabilize the bacterial community in our disturbed plots. ...
Tree-killing forest disturbances such as storms and bark beetle outbreaks can lead to notable changes in the carbon (C) balance and functioning of forest ecosystems. In this study, the effects of a storm in 2010 followed by an outbreak of European spruce bark beetle (Ips typographus L.) on tree, litter and soil C stocks as well as humus layer C fractions and microbial community composition were examined in boreal Norway spruce (Picea abies L.) stands. Tree (aboveground), litter detritus (distinguishable twig, bark and cones) and soil (humus layer and 0–6 cm mineral soil) C stocks were quantified for undisturbed (living trees), storm disturbed and I. typographus disturbed plots in 2015–2016. Additional humus layer samples were collected in 2017 for determination of total microbial biomass C, ergosterol (fungal biomass indicator) and K2SO4 extractable (labile) C concentrations, as well as ectomycorrhizal (ECM) fungal mycelial abundance and microbial community composition (DNA sequencing). In spite of a differing development pace and intensity of the two disturbance types, they appeared to have a similar effect on humus layer C and microbiology, which may be due to the longer time since the storm than the I. typographus disturbance. The shift from tree biomass to necromass C stocks was not reflected in differences in SOC stocks or humus layer extractable C concentrations between undisturbed and disturbed plot types, but the amount of litter detritus on forest floor was similar (storm) or higher (beetle) in disturbed plots in comparison to undisturbed ones. Humus layer microbial biomass C and ergosterol concentrations and ECM fungal abundance were lower on disturbed plots in comparison to undisturbed plots. The disturbed plots were also indicated to have a slightly higher abundance of some saprotrophic fungi. Differences in the effects of the two disturbance types may occur when studied at differing spatial scales and at different times after disturbance. To understand the full impact of such disturbances on forest functioning and C balance, long-term monitoring studies will be required.
... Across the Northern Hemisphere, studies have examined microbial dynamics following bark beetle infestation revealing changes in microbial functioning (10) and community structure (10,(12)(13)(14), and specifically a decrease in symbiotic fungal taxa (10,12). However, conflicting results exist, for example, Ferrenberg et al. (15) found no changes in soil bacterial community structure in the first 5 years following mountain pine beetle-induced tree mortality in the southern Rocky Mountains. A shortcoming of these microbial studies is that they address changes to community structure in soil and/or litter following bark beetle infestation, neglecting to consider microbial dynamics in the bulk and rhizosphere soil compartments individually, and more often than not, only one kingdom is studied, and community data are not paired with microbial functional measurements. ...
... Though there was a trend of increased bacterial richness in the bulk soil of the infested clusters, it was not significant, and the rhizosphere soil had a stable number of taxa in all infestation stages. The lack of bark beetle-induced effects on soil bacterial alpha-diversity matches results from Mikkelson et al. (13) and Ferrenberg et al. (15). However, even though species richness was not affected, the bacterial community structure was significantly altered following bark beetle infestation, which is similar to results from the heavily impacted site in the study by Mikkelson et al. (13), but contrasts with the moderately impacted site of Mikkelson et al. (14), as well as the sites from Ferrenberg et al. (15). ...
... The lack of bark beetle-induced effects on soil bacterial alpha-diversity matches results from Mikkelson et al. (13) and Ferrenberg et al. (15). However, even though species richness was not affected, the bacterial community structure was significantly altered following bark beetle infestation, which is similar to results from the heavily impacted site in the study by Mikkelson et al. (13), but contrasts with the moderately impacted site of Mikkelson et al. (14), as well as the sites from Ferrenberg et al. (15). These contrasting results could be caused by differences in mortality levels and forest type, Pinus spp. ...
As the range of bark beetles expands into new forests and woodlands, the need to understand their effects on multiple trophic levels becomes increasingly important. To date, much attention has been paid to the aboveground processes affected by bark beetle infestation, with a focus on photoautotrophs and ecosystem level processes. However, indirect effects of bark beetle on belowground processes, especially the structure and function of soil microbiota remains largely a black box. Our study examined the impacts of bark beetle-induced tree mortality on soil microbial community structure and function using high throughput sequencing of the soil bacterial and fungal communities and measurements of extracellular enzyme activities. Results suggest bark beetle infestation affected edaphic conditions through increased soil water content, pH, EC and C:N ratio, and altered bulk and rhizosphere soil microbial community structure and function. Finally, increased enzymatic activity suggests heightened microbial decomposition following bark beetle infestation. With this increase in enzymatic activity, nutrients trapped in organic substrates may become accessible to seedlings and potentially alter the trajectory of forest regeneration. Our results indicate the need for incorporation of microbial processes into ecosystem level models.
Importance Belowground impacts of bark beetle infestation have not been explored as thoroughly as their aboveground counterparts. In order to accurately model impacts of bark beetle-induced tree mortality on carbon and nutrient cycling and forest regeneration, the intricacies of soil microbial communities must be examined. In this study, we investigated the structure and function of soil bacterial and fungal communities following bark beetle infestation. Our results show bark beetle infestation to impact soil conditions as well as soil microbial community structure and function.
... Such changes can also reflect to forest floor and soil microbial community composition and functioning. For example, abundance and/or diversity of tree-symbiotic ectomycorrhizal (ECM) (Štursová et al. 2014;Mayer et al. 2017;Pec et al. 2017) and saprotrophic decomposer fungi (Štursová et al. 2014;Pec et al. 2017) as well as bacteria (Ferrenberg et al. 2014;Mikkelson et al. 2017) have been indicated to be altered by storm or bark beetle disturbance. Similarly, changes in microbial biomass and DOC concentrations have been observed after bark beetle outbreaks (Štursová et al. 2014;Kaňa et al. 2015;Trahan et al. 2015). ...
... In studies I and II, the soil was sampled some 10 (I) and three years (II) after the initiation of the insect outbreaks and thus soil properties could have been influenced by the outbreak, contrary to what we were aiming to examine. Defoliator and bark beetle disturbance can have considerable temporary effects on the availability and cycling of N and C in forest floor and soil, lasting at least up to a few years after the events (Lovett and Ruesink 1995;Morehouse et al. 2008;Griffin and Turner 2012;Kaňa et al. 2013;Ferrenberg et al. 2014;Norton et al. 2015;Trahan et al. 2015). However, studies on the effects of defoliators and bark beetles on humus layer and/or mineral soil total C or N concentrations or C/N ratios in coniferous forests have mostly indicated no change during, a few years or decades after an outbreak (Streminska et al. 2006;Morehouse et al. 2008;le Mellec and Michalzik 2008;Griffin et al. 2011;Griffin and Turner 2012), with some exceptions (Kaňa et al. 2013;Mikkelson et al. 2017). ...
