nature reviews microbiology https://doi.org/10.

1038/s41579-023-00876-4

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Forest microbiome and global change

Petr Baldrian 1
, Rubén López-Mondéjar 1,2
& Petr Kohout 1,3

Abstract Sections

Forests influence climate and mitigate global change through the Introduction

storage of carbon in soils. In turn, these complex ecosystems face Forests under global change
important challenges, including increases in carbon dioxide, warming, Boreal, temperate and tropical
drought and fire, pest outbreaks and nitrogen deposition. The response forests under global change
of forests to these changes is largely mediated by microorganisms, Microbiome response
especially fungi and bacteria. The effects of global change differ among to global change

boreal, temperate and tropical forests. The future of forests depends Conclusions and outlook
mostly on the performance and balance of fungal symbiotic guilds,
saprotrophic fungi and bacteria, and fungal plant pathogens. Drought
severely weakens forest resilience, as it triggers adverse processes
such as pathogen outbreaks and fires that impact the microbial and
forest performance for carbon storage and nutrient turnover. Nitrogen
deposition also substantially affects forest microbial processes,
with a pronounced effect in the temperate zone. Considering plant–
microorganism interactions would help predict the future of forests
and identify management strategies to increase ecosystem stability and
alleviate climate change effects. In this Review, we describe the impact
of global change on the forest ecosystem and its microbiome across
different climatic zones. We propose potential approaches to control
the adverse effects of global change on forest stability, and present
future research directions to understand the changes ahead.

Laboratory of Environmental Microbiology, Institute of Microbiology of the Czech Academy of Sciences, Prague,
1

Czech Republic. 2Department of Soil and Water Conservation and Waste Management, CEBAS-CSIC, Campus
Universitario de Espinardo, Murcia, Spain. 3Faculty of Science, Charles University, Prague, Czech Republic.
e-mail: [email protected]

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Introduction multiple microbiome components, as is also the case for the cycling of
Forest ecosystems cover approximately 30% of Earth’s land surface nitrogen, phosphorus and other nutrients (Fig. 2).
— 42 million km2 — and store 45% of the carbon found in terrestrial In this Review, we explore the varied effects of global change on
ecosystems (Fig. 1), being responsible for 50% of terrestrial net primary forest microbiomes, including changes in microbial abundance and
production1. They also act as an important carbon sink that captures microbiome composition, as well as the impact on the performance
7.6 Gt of carbon dioxide (CO2) per year2. Trees are the dominant primary of root-symbiotic fungi and microbial pathogens in soils and other
producers in forests, and provide a multitude of habitats for microor- habitats that are tightly linked to the forest ecosystem properties
ganisms and other biota, such as the rhizosphere (soil surrounding and processes (decomposition, nutrient cycling, carbon storage or
plant roots) and phyllosphere (surface and interior of leaves). Trees also greenhouse gas emissions). By combining observations of past devel-
substantially influence the remaining parts of the ecosystem, mainly opment, experimental approaches simulating global change factors
because they supply the bulk of the carbon that enters the forests. Some and observations on the realized niches of microorganisms and bio-
of this carbon is deposited in the soil by trees through roots or through geochemistry, we discuss the ongoing and future changes in forest
the mycelia of root-symbiotic fungi in the form of simple organic mole­ ecosystems across climatic zones. Finally, we provide an example of
cules, whereas another fraction, represented by the dead biomass forest management strategies to mitigate adverse effects of global
of wood, litter or roots, provides a pool of recalcitrant biopolymers3. change on forest microbiomes and ecosystem performance and stabil-
Structured by trees, forest ecosystems are complex and consist ity, and suggest forthcoming research directions needed to understand
of multiple habitats of specific features and specific microbiomes4. the future of global forests.
The activity of these microbiomes, which comprise fungi, bacteria,
archaea, protists and viruses, will determine the functioning of the Forests under global change
forest. The role of microorganisms is especially important in the topsoil Human activity has transformed the surface of the planet over millennia,
(composed of a litter layer, soil and roots of trees), where they mediate having a major impact on land use and land cover worldwide. The defor-
the cycling of nutrients. The litter layer, dominated by fungal activity, estation and land-cover change associated with agriculture together
is a hot spot of recycling nutrients from plant biomass. Soil consists with industrial activities induced a global change, which encompasses
of more recalcitrant organic matter and the microbiomes are rich in several phenomena and processes and has been intensified in the last
bacteria and mycorrhizal fungi that transport carbon from roots to soil centuries. Fossil fuel burning has locally increased the deposition of
and nutrients from soil to trees5. Roots and rhizospheres are enriched nitrogen and increased the concentrations of CO2 in the atmosphere, a
on these plant-symbiotic fungi. Microbiomes of deadwood consist heat-trapping gas responsible for climate change through the warming
of microorganisms adapted to efficient decomposition and nitrogen of the atmosphere, ocean and land (global warming)13. The increase in
limitation, that is decomposer fungi and nitrogen-fixing bacteria6. temperature on the planet involves altered atmospheric circulation
Specific, yet less abundant, are the microbiomes of tree phyllospheres patterns and changes in precipitation regimes across the globe, caus-
and rock surfaces4. Fungi are the most studied forest microbes due to ing heatwaves and drought events that are more intense and recurrent.
their important ecosystem functions. Mycorrhizal fungi are key to the Reduced precipitation and warmer weather increase the frequency and
mobilization and sequestration of nitrogen and phosphorus in forest intensity of fires and induce the outbreaks of many pests14.
soils, and in the transport of carbon from tree roots into soil. There are Similar to other biomes, forests both contribute to and are affected
two major types of mycorrhizal symbioses: ectomycorrhizal, which can by these global change processes15–17 (Fig. 3). Because of their complex
decompose organic matter and access organic nitrogen7 and are more nature, the response of forest ecosystems to global change is both
efficient under nutrient limitation, and arbuscular mycorrhizal, which complex and context-dependent, but the decreased rates of global
cannot decompose soil organic matter and are restricted to the use of forest carbon storage appear to be one of the consequences of global
mineral forms of nitrogen and phosphorus. Saprotrophic fungi are change18. The carbon sink saturation and the increase in carbon losses in
important decomposers in forest litter and soils due to their wide range forests are the linked result of CO2 fertilization, rising air temperatures
of extracellular enzymes that break down recalcitrant biopolymers, or drought impact and tree mortality. The understanding of forests
whereas plant pathogenic fungi may substantially affect ecosystem under future environmental conditions, their functioning and the
productivity through predation and reductions in host fitness and functioning of their microbiomes is still insufficient, but of critical
growth4. Bacteria represent another integral part of forest ecosystems, importance for modelling, management and conservation purposes.
although they are less explored. In addition to their contribution to Elevated CO2 concentration (eCO2), warming and changes in pre-
the decomposition of plant and microbial biomass8, bacteria substan- cipitation and nitrogen deposition are the most important global
tially contribute to multiple nitrogen cycling processes, including the change factors affecting forests, independent of land management
fixation of atmospheric N2, nitrification and denitrification6,9. Both decisions such as deforestation or transformation of natural forests
bacteria and fungi contribute to nutrient mobilization by mineral into plantation forests (Fig. 3). Each factor has specific consequences,
weathering4. Protists, on the other hand, often act as predators on but they also act in combination. Among other consequences, climate-
fungal or bacterial cells10. The role of archaea in forests is typically driven risks may compromise the capacity of forests to act as carbon
constrained to specific microhabitats, and their importance varies, sinks across large spatial scales14.
contributing to, among other processes, methane (CH4) and nitrogen Increasing CO2 concentrations were predicted to boost the net pri-
cycling11. Although viruses are common in forest soils12, the extent mary production of forests, but free-air CO2 enrichment experiments
of their contribution to ecosystem processes remains unclear. The show that the net primary production increase diminishes over time19.
functions of the microbiome components should not be seen as sepa- The higher belowground carbon input under eCO2 is compensated by
rate. Decomposition and cross-feeding on decomposition products, faster carbon turnover due to accelerated microbial growth, metab­
mycorrhizal establishment, and predation on and decomposition of olism and respiration, higher enzymatic activities and priming of soil
microbial biomass can be viewed as examples of processes integrating carbon, nitrogen and phosphorus pools under warming20. Warming

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Tropical forest in Nouragues, Temperate forest in Divoká Šárka, Boreal forest in Karstula, Finland
French Guiana Czechia

Boreal forests
Temperate forests
Tropical forests

Boreal forests Temperate forests Tropical forests

Abiotic environment Abiotic environment Abiotic environment
• Face low temperatures with cold winter lasting more • Temperature ranges between –30 and 30 °C, • Do not show temperature seasonality, all year with average
than 6 months and average summer temperatures of with hot summers and cold winters daily temperatures higher than 20 °C
10 °C • 750–1,300 mm of precipitation per year • Rainforests receive the most rain (2,000–10,000 mm), but
• Limited precipitation (300–900 mm of rain per year) Distribution drier tropical forests (above 800 mm) are also common.
but moist due to reduced evaporation • Largely found at mid-latitudes in the northern Precipitation can vary during the year with distinct wet and
Distribution hemisphere with smaller areas in South America dry seasons
• Largest terrestrial biomes, including mountainous and Australia Distribution
forest in temperate zone Productivity and biodiversity • Occur around the world close to equator
Productivity and biodiversity • Less diverse and productive than tropical Productivity and biodiversity:
• Low productivity allows the most extensive soil forests but more so than boreal forests • Well known for their immense tree species diversity,
organic matter pool to develop, being a significant • Most trees form ectomycorrhizal symbiosis, containing the largest carbon pools in aboveground
global carbon stock but in certain areas trees forming arbuscular plant biomass
• Low diversity of tree species, the vast majority mycorrhizal symbiosis either dominate or • Relatively warm and moist climates lead to rapid
associated with ectomycorrhizal fungi coexist with ectomycorrhizal trees decomposition and lower soil organic matter stocks
• Understorey vegetation represented by dwarf ericoid compared with higher latitude forests
shrubs contributes to half of the net • Dominated by tree species with arbuscular mycorrhizal root
primary production symbioses, although ectomycorrhizal trees occur as well

Fig. 1 | Global distribution and features of forest ecosystems. Natural areas The diversity of tree vegetation at the plot scale increases from boreal to
and properties of boreal, temperate and tropical forests are constrained by tropical forests. The temperate forest zone is the one most affected by forest
climatic factors: temperature, precipitation and length of the growing season. management.

was the main driver of the global soil microbial biomass decrease of net primary production, soil carbon and microbial biomass, among
3.4% observed between 1992 and 2013, especially at high latitudes with other effects24.
high soil microbial carbon stocks21. Although precipitation may both Unlike other global change factors, atmospheric nitrogen depo-
increase and decrease with changing climate, the latter phenomenon, sition is spatially associated with human activity and, thus, is highly
leading to temporary or permanent drought, has a much stronger spatially variable25. As available nitrogen is often limiting in forests,
effect on ecosystems than the former. The combination of warming nitrogen deposition may positively affect net primary production
and drought may lead to the extinction of tree species22 and, ultimately, in such environments26, but it also increases phosphorus limitation in
the replacement of tree cover by shrubs or grasses23. Drought affects phosphorus-limited soils that are globally more common27. Nutri-
a wide range of ecosystem properties, leading to the reduction in ent limitation affects carbon storage as nutrient-rich forests show

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Fungi
Protists
Ectomycorrhizal fungi and arbuscular fungi
• Carbon allocation from roots to soil Photosynthesis
• Nutrient mobilization and provision to plants Predation (certain taxa)
Saprotrophs
• Decomposition of litter and soil organic matter
• Nutrient redistribution
Plant pathogens
• Reduction of performance of vegetation/tree dieback

Decomposition Decomposition
of dead biomass of dead biomass

Bacteria
• Decomposition of organic matter
• Fixation of atmospheric N2 Viruses
• Nitrification
• Denitrification
Infection and lysis
• Methylotrophy
• Mycorrhizal establishment — helper bacteria
• Nutrient mobilization through mineral weathering

Archaea
• Methanogenesis
• Denitrification

Fig. 2 | Roles of the members of forest microbiomes. Fungi, bacteria, archaea, as forested peatlands. Protists and viruses are ubiquitous in forests and are
protists and viruses compose the forest microbiome. Although the roles of known to affect the other members of the microbiome through predation and
fungi and bacteria are widely studied and known, there is much less information cell lysis, yet the extent of their importance is unclear. The biomass of dead
about the other microbiome members. The abundance of archaea in forest microorganisms — fungi and bacteria — is largely recycled by the same two
soils appears rather limited and may be associated with specific habitats, such groups, with bacteria probably being more important in the process.

higher carbon use efficiency and, thus, sequester more carbon than major roles. More than 20% of intact undisturbed forests have already
nutrient-limited forests28. Similar to the change of CO2 concentrations, supposedly reached a critical threshold of resilience beyond which
it is expected that atmospheric nitrogen deposition will increase in they experience further degradation36 and adaptation is less likely.
upcoming decades25.
The negative effects of global change, such as the combination Boreal, temperate and tropical forests under
of drought induced by warming and precipitation reduction, weaken global change
forests. Dieback of suffering trees, triggered by dry and hot climatic Although some aspects of global change appear to have universal con-
conditions, has been documented on all continents29–31. Climate change sequences, their effects are largely modulated by the specific features
led to an increased incidence of biotic pests in weakened trees but also of boreal, temperate and tropical forests and their microbiomes. This
in healthy trees, as the winter survival of insect pathogens is higher in is because climatic and edaphic factors make these forests distinct in
warmer climates14. In positive feedback, forests weakened by insect multiple aspects: the climate selects local tree species pools, and the
or fungal pathogens are more sensitive to adverse climatic conditions diversity of dominant trees determines the turnover rate of organic
and more prone to dieback29. Increased tree mortality combined with matter and affects the composition of tree–fungal symbioses involved
warmer and drier climatic conditions results in the observed increase in nutrient cycling (Fig. 1). Globally, the gross primary production of for-
in forest fire frequency, exposing larger areas of forest to fire risk across ests benefits from higher temperatures and precipitation, whereas net
longer fire weather seasons32. Altogether, pest and fire incidence are primary production saturates above a threshold of either 10 °C mean
significantly correlated with tree mortality and stress33. Climate models annual temperature or 1,500 mm precipitation37. In the past 20 years,
thus predict that tree mortality and connected disturbances, including boreal forests showed, on average, an increasing trend in resilience,
forest fires, will further increase in the future33,34. probably benefiting from warming and fertilization through eCO2,
The future challenges to forest ecosystems may be partly offset which might have outweighed the adverse effects of climate change
by their ability to adapt. Tree mortality is taxonomically biased and on tropical and temperate forests. With temperatures above the limit,
changes species composition31, where trees and their mycorrhizal temperate and tropical forests experienced a significant decline in
symbionts may, in the long term, adapt by migration through seedling resilience, probably related to increased water limitations and climate
establishment in places with more favourable conditions22. The change variability36. The future of forests and their microbiomes should thus
in vegetation is already visible in most global change experiments, be explored separately by forest type (Fig. 1).
especially when multiple factors are combined35. The potential of
forest adaptation is, however, limited by the fact that forest resilience Boreal forests
has already declined in the past decade due to a multitude of global Because of slow decomposition limited by low temperatures and low
change factors, in which water limitation and climate variability played nutrient contents, boreal forests (and analogous mountainous forests

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at higher altitudes in the temperate zone) represent a large stock of car- temperature sensitivity of respiration42. Thus, carbon storage rates
bon in their upland and peatland soils, including soils with permafrost38. are likely to decline in the future.
They also represent an important carbon sink driven by the production Although there is a large gradient in water availability in the
of roots and mycelia of root-associated fungi forming ectomycorrhizal boreal zone, drought-induced mortality has been reported in several
and ericoid mycorrhizal fungi symbioses39. regions and is predicted to increase further, amplifying the extent, fre-
The productivity of boreal forests has been on the rise due to quency and severity of biotic and abiotic disturbances, including fires16.
rapidly increasing temperatures and longer growing seasons16; the Forest fires represent an important phenomenon in the boreal zone,
warming, predicted to be faster than that in other forest biomes in with 1% of boreal forest areas burnt annually. The frequency of intense
the future40, may also tend to support this trend. However, the decom- fires that burn much of the organic matter will likely increase because of
position potential of fungal communities in boreal forest soil has also climate change removing high amounts of carbon, decreasing carbon
increased due to warming41, and could increase further due to the and nitrogen availability and retarding ecosystem development43.

Increase of CO2 Warming

• Boost of forest net primary production and higher • Decrease of soil microbial biomass
belowground carbon input • Stimulation of the microbial decomposition of soil
• Fast carbon turnover due to accelerated microbial organic matter, reducing the carbon storage
growth, metabolism and respiration • Shifts towards a more diverse, oligotrophic microbial
• Acceleration of the nitrogen cycle (e.g. nitrification) community (fungi and Actinobacteria decrease and
• Reduction of the methane uptake by microorganisms Alphaproteobacteria and Acidobacteria increase)
and the ability of soil to act as a sink of methane

Fires Drought
• Remove high amounts of carbon and decrease carbon • Reduction of net primary production, soil carbon and
and nitrogen availability microbial biomass
• Lack of nutrients reduces microbial abundance and • Persistent water limitation changes the microbial
biomass community composition (increase of fungi and
• Development of fungal communities with high Actinomycetales but reduced ectomycorrhizal fungi)
capacity for decomposition, preventing soil carbon • Reduces the rates of multiple ecosystem processes
sequestration (e.g. nitrification, decomposition, microbial activity)

Nitrogen deposition Pest outbreaks

• Increase of net primary production in nitrogen-limited • Weakened trees that suffer dry and hot climatic
forest and phosphorus limitation in phosphorus-limited conditions are more vulnerable to pest
soils • Higher survival of insect pathogens in warmer
• Suppression of decomposition and accumulation of climates
soil carbon • Abundance of fungal pathogens is predicted to
• Weakens ECM symbiosis and decrease of fungal to increase in future
bacterial biomass ratio

Boreal forest Temperate forest Tropical forest

Fig. 3 | Global change factors affecting forest ecosystems and their factors, and nitrogen deposition derived from local anthropogenic pressure
microbiomes. The most important processes that affect forest ecosystems (industrial activity and transportation). Forest fires and pest outbreaks are local
independently from management decisions (such as conversion of forests to factors largely triggered by other global change processes that can make forest
croplands) comprise globally occurring ones, such as elevated carbon dioxide ecosystems susceptible to these disturbances. Although locally one of the global
concentration (eCO2) and warming, and those that vary in intensity across change factors may dominate in importance, forest ecosystems are always
space, such as reduced precipitation and drought resulting from climatic affected by their combination.

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Furthermore, in areas with permafrost, fire exposes frozen organic microbial turnover of root-derived carbon under elevated CO2 is suf-
matter to microbial decomposition, causing positive feedback to ficient in magnitude to offset increased belowground inputs63. Carbon
global warming44. Fire has multiple effects on the soil microbiome. The losses are associated with accelerated nitrogen cycling, including
lack of nutrients decreases microbial abundance45, including fungal nitrification, suggesting that trees exposed to elevated CO2 not only
biomass and, consequently, enzyme activity46. The overall diversity enhance nitrogen availability by stimulating microbial decomposition
of fungi and ectomycorrhizal tree symbionts decreases47, resulting of soil organic matter via priming but also increase the rate at which
in an increased ericoid mycorrhizal to ectomycorrhizal fungal ratio nitrogen cycles through microbial pools63,64. Despite accelerated car-
and the development of soil fungal communities with a high capacity bon and nitrogen cycling, microbial abundance is not substantially
for organic matter decomposition, which may prevent soil carbon affected by elevated CO2 (ref. 65). CH4 uptake by soil microorganisms
sequestration39,48. Compared with fungi, bacterial communities are less is substantially decreased under elevated CO2 (ref. 66). The globally
affected by forest fires in boreal ecosystems49. Although, for a certain important sink of CH4 in temperate forest soils resulting from the
time, specific post-fire microbial communities can develop49,50, the activity of methylotrophic bacteria67 may thus decrease in the future.
recovery to pre-fire conditions often takes up to several decades44. The longest forest warming manipulation has been run in the
Boreal forests are typically nitrogen-limited51, and atmospheric Harvard Forest for almost 30 years68. The experiment indicated that
nitrogen deposition can thus offset the limitations of plant productiv- ecosystem responses changed over time. Rapid carbon loss through
ity52 and carbon storage53. Nitrogen addition to boreal soils increases respiration was followed by increased degradation of more recalcitrant
the share of bacteria, and available ammonia promotes nitrification, carbon compounds68. The microbial community underwent reorgani-
leading to leaching of nitrate and losses of nitrogen oxides through zation with a shift towards a more diverse, oligotrophic community
denitrification. High nitrogen content also weakens ectomycorrhizal with decreased abundance of fungi and Actinobacteria, increased
symbiosis and decreases the share of ectomycorrhizal fungi that liberate abundance of Alphaproteobacteria and Acidobacteria69, and poten-
nitrogen from soil organic matter51,54. However, the future development tially higher involvement of bacteria in decomposition70. Long-term
of nitrogen deposition in boreal zones is uncertain as even across all warming ultimately results in the depletion of soil organic carbon
the highly populated regions of Sweden, the deposition of nitrogen has with corresponding reductions in microbial biomass68. Because tem-
decreased in the last decade55. Nitrogen deposition in less populated perate forests show weather seasonality, it is expected that warming
boreal areas is, nevertheless, of very low intensity56. should increase decomposition in winter months when soils are not
The permafrost thaw in boreal forests substantially changes drought-limited71.
local hydrology57 and increases the area of inundated land58. As water- This is important as rising global temperatures with limited precip-
logged soils developing after thaw are an important source of CH4, it itation increase drought frequency and severity in temperate forests14.
is projected that CH4 emissions will increase substantially, although Although short droughts have limited effects, persistent water limita-
the extent of such an increase is unclear58. In areas where permafrost tion changes the microbial community composition72, increasing the
thawed, the relative abundance of mycorrhizal fungal taxa as well as proportion of fungi and filamentous bacteria of the Actinomycetales73
mycorrhizal plant productivity decreased whereas the relative abun- and reducing the abundance and diversity of ectomycorrhizal fungi74.
dance of putative fungal pathogens increased57, but it is uncertain Furthermore, as many specialized bacteria, including ammonia oxidiz-
whether this is a common trend. ers, sulfur oxidizers and CH4 oxidizers, are drought-sensitive75, drought
Along with permafrost thaw, warming shifts climatic zones on reduces the rates of multiple ecosystem processes. For example, the
the forest ecotone, which is the border zone between the forest and persistent decline in ammonia-oxidizing bacteria as a consequence
non-forest ecosystems. Although treeline shift develops through the of drought led to massive reductions in gross nitrification rates and
establishment of seedlings and their root symbionts, the speed of forest nitrate availability in a mountainous forest, ultimately resulting in
advance is one order of magnitude slower than the speed of warming16. reduced nitrogen uptake by Fagus sylvatica seedlings76. Drought can
Additionally, in high mountains, the treeline shift to higher elevations reduce microbial abundance and enzyme activity in litter and soil72,77
lags behind climate warming59, and ectomycorrhizal fungal advance is and alter fungal community composition in deadwood78, thus decreas-
delayed even further, likely due to dispersal limitation60, setting limits ing their decomposition. Enhanced carbon storage due to a decrease
to climate-driven tree expansion. As a consequence, potential forest in decomposition can, however, hardly compensate for the loss of tree
expansion into so far unforested areas of tundra lags behind warming, net primary production under drought. At a long timescale, sustained
which limits the extent of carbon storage that forest expansion may pressure of drought and warming promotes the shift of tree species
potentially bring. composition, as occurred in the ‘Mediterranization’ of forests in South
Europe79, and may lead to changes in their associated microbiomes.
Temperate forests As in boreal forests, drought combined with warming will
Temperate forests, especially those in North America and Europe, are increase the frequency and severity of wildfires in temperate
the subject of intensive research comprising experiments with CO2 forests50,80. Although decomposition may be slowed down shortly after
enrichment, simulated warming and nitrogen addition that run suf- fire, temperate forests recover to pre-fire states much more rapidly than
ficiently long and allow to understand the effect of global change in boreal forests81, reflecting the development of vegetation82,83. Moreover,
these ecosystems at a deeper and more detailed level than in other wildfires leave behind biological legacies, such as fire-adapted fungi,
forest biomes. which may promote ecosystem recovery after subsequent fires80,81. Fire
frequency increases the relative abundance of ectomycorrhizal trees,
Temperate forest microbiomes under climate change. Free-air which are better able to cope with nutrient limitation following fire
CO2 enrichment experiments in temperate forests indicate that eCO2 losses because symbiosis with ectomycorrhizal fungi is more efficient
increases the production of fine roots and litter but has a limited effect in nitrogen acquisition84. Drought was also a direct or indirect trigger
on carbon storage due to their rapid turnover61,62. Indeed, accelerated of past outbreaks of insects and pathogens that resulted in millions of

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hectares of forest defoliation, canopy dieback, declines in forest growth United States will likely show accelerated nutrient turnover with critical
and forest mortality in North America and Europe in recent decades. Not consequences for forest productivity, ecosystem carbon and nutrient
surprisingly, there is positive feedback on fire frequency and severity17,85. retention, and feedback to climate change106. Indeed, gene expression
studies reveal a 3.5 times greater transcription of nitrogen-cycle genes
Nitrogen deposition effects in temperate forests. Due to the intensity in arbuscular mycorrhiza-dominated soils than in ectomycorrhiza-
of human activity, nitrogen deposition is particularly pronounced in dominated soils and a linear increase in volatile reactive nitrogen gases
the temperate zone. In the absence of disturbance, nitrogen deposition with an increasing share of arbuscular mycorrhizal trees108. Therefore,
enhances the growth of most of the dominant tree species in the United shifts from ectomycorrhizal to arbuscular mycorrhizal tree species
States, potentially leading to increased tree carbon storage86. Across associated with global change have predictable consequences for
several experiments, simulated nitrogen deposition resulted in soil nitrogen cycling, which include a faster nitrogen turnover in the future
acidification, accumulation of soil organic matter and changes in its and an increase in losses in the volatile form108.
composition, including higher lignin accumulation. Soil carbon accu-
mulation in response to long-term nitrogen enrichment was largely Tropical forests
due to the suppression of organic matter decomposition rather than Despite threats of deforestation, degradation and disturbance109 that
enhanced carbon inputs to soil via litter fall and root production87. call for attention, tropical forests are heavily understudied with respect
The response of the bacterial community to simulated nitrogen to their response to global change110. The structural complexity, tree
deposition is moderate compared with that of fungi88. A decrease in species diversity and inaccessibility of tropical forests make experimen-
the fungal to bacterial biomass ratio was frequently observed87,89,90, but tation and predictions difficult. Experimental 2-year warming of a soil
this response was context-dependent. Although fungal biomass and profile in a Panama rainforest increased CO2 emissions by 55% compared
richness increased with simulated nitrogen deposition at sites with low with soil at ambient temperature, which was considerably higher than
ambient deposition, they were reduced at sites where ambient nitrogen model predictions. The additional CO2 originated from heterotrophic
deposition was high91,92. The fungal community undergoes profound sources, indicating faster decomposition111. However, considering the
restructuring that particularly affects ectomycorrhizal fungi supply- complex response of temperate forests to warming, it is unclear what
ing their tree hosts with nitrogen93. A large survey of ectomycorrhizal would happen at longer timescales in tropical forests. Because nutri-
fungi associated with forest trees in Europe shows that, as those ecto- ent limitation is widespread in tropical forests112, the potential positive
mycorrhizal fungi that decompose organic matter to obtain nitrogen effects of elevated CO2 fertilization are probably limited.
are associated with low nitrogen deposition, nitrophilic fungi that use Drought is probably the major factor affecting tropical forests.
inorganic nitrogen are associated with high nitrogen deposition94. Water availability has a strong positive effect on biomass stocks and
Whereas nitrophilic fungi increase under simulated nitrogen deposi- tree growth, and a predicted increase in drought intensity might, poten-
tion92,95, the diversity and mycelial production of ectomycorrhizal fungi tially, reduce carbon storage113. The increase in atmospheric water
both decline as their activity is less important for their tree hosts95,96. stress driven by climate warming was probably also the main factor
Decomposition is generally suppressed by nitrogen addition89,97 responsible for the doubling of tree mortality risk in tropical forests
through the reduction in the activity of extracellular enzymes medi- of Australia over the past 35 years114. Prolonged, severe droughts can
ating plant cell wall decay89,98. Not surprisingly, nitrogen addition have profound effects on global carbon storage: it has been speculated
also shifts the bacterial and archaeal potential for nitrogen fixation, that the Amazon drought caused the exceptional increase in atmos-
ammonification, denitrification and nitrate reduction as a reflection of pheric CO2 concentrations in 2005 (ref. 115). The impact of drought
increased availability of inorganic nitrogen99. When deposition results on the microbiome of tropical forests is unclear. It was assumed that
in nitrogen saturation of soils, bacterial and archaeal nitrification tropical soils have a low adaptive capacity to perturbations due to lower
and denitrification increase and may result in the efflux of nitrogen seasonality, yet the first experiments indicate that the diversity and
compounds (nitrate, N2 or nitrous oxide gas) from the ecosystem97,100,101. composition of soil microbial communities in tropical forests are sensi-
tive to small changes in soil water content116. Modest changes in water
Temperate forest adaptation to global change. Climatic factors are potential also altered the functional potential and activity of the micro-
already changing the composition of temperate forests. Northwards biome. Drought resulted in an increase in hydrolytic enzyme activity
tree species migration is observed in the United States, although the and oxidation of complex carbon compounds, such as cellulose, chitin,
speed is species-specific102. Because the survival of tree seedlings under lignin and pectin116.
modest warming and drought differs widely among tree species103, it Because of the high tree species diversity, natural tropical forests
is apparent that future forests will be different from the present ones, weakened by drought are likely less vulnerable to insect pests and plant
possibly with higher tree diversity104. pathogen effects than temperate and boreal forests. Drought waves,
The present distribution of trees forming arbuscular mycorrhizal however, induce severe fires with multiple consequences30. Current cli-
and ectomycorrhizal symbioses is primarily driven by climate and matic scenarios predict that fire intensity, recurrence and burned area
anthropogenic influences, for example nitrogen deposition105. The size will all increase in several areas of Brazil. An increase in fire impact is
latter, in concert with warming, have already increased arbuscular myc- predicted for 97% of the Amazon area117. Moreover, frequent recurrence
orrhizal tree dominance during the past three decades in the eastern of fires can create positive feedback as areas that burn repeatedly are
United States106. Because trees associated with arbuscular mycorrhizal more susceptible to new fires. The vegetation in these locations does
fungi (AM) promote soil microbial communities with higher nitrogen not recover fully after fires and is not able to restore productivity117,
cycling potential and activity relative to those in soils under trees with which has consequences for the plant-dependent microbiome.
ectomycorrhizal fungi107, the ongoing shift of ectomycorrhizal to arbus- The extent of nitrogen deposition is likely of limited importance
cular mycorrhizal forests will have important functional consequences. in most tropical systems56. Although it might locally increase produc-
The future arbuscular mycorrhiza-dominated forests in the eastern tivity in nitrogen-limited soils, nitrogen deposition would increase

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Boreal forest

Reduced precipitation Warming Nitrogen deposition Increase of CO2

Ectomycorrhizal fungi Fire severity Nitrogen

Permafrost thaw Drought
and frequency limitation

Environmental conditions
Ecosystem processes Ecosystem level
CH4 emissions Decomposition Carbon storage
nitrogen losses
Vegetation
Microorganisms
Dead trees Forest expansion

Root-symbiotic fungi Fungi/bacteria Biotic pests Microbial biomass

Temperate forest

Reduced precipitation Warming Nitrogen deposition Increase of CO2

Ectomycorrhizal AM
fungi Fire severity Nitrogen
Drought
and frequency limitation

Ecosystem level Carbon Nitrogen Carbon

Decomposition CH4 sink
nitrogen losses storage turnover turnover

Arbuscular mycorrhizal
fungi trees/ectomycorrhizal Dead trees
fungi trees

Biotic pests Microbial biomass Fungi/bacteria Root-symbiotic fungi

Tropical forest

Reduced precipitation Warming Nitrogen deposition Increase of CO2

Fire severity Phosphorus

Drought
and frequency limitation

Ectomycorrhizal AM
fungi
Carbon storage Decomposition

Dead trees

Microbial biomass Fungi/bacteria Root-symbiotic fungi

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Fig. 4 | Effects of global change in boreal, temperate and tropical forest (blue). Although boreal forests may benefit from higher productivity under a
ecosystems. Climatic factors (reduced precipitation, warming, nitrogen warmer climate and higher CO2 concentrations, they will be under danger of
deposition and increase of CO2) have complex direct and indirect effects on drought, fire and pathogens. Temperate forests are expected to mostly suffer
environmental conditions, ecosystem processes, vegetation and the microbiome from drought-increased mortality and its consequences, and the microbiome
of forests. Whereas certain effects of global change are universal, such as the will reflect changes in the relative share of ectomycorrhizal and arbuscular
combination of warming and reduced precipitation inducing drought that mycorrhizal trees. For tropical forests, the largest challenge will likely be the
itself brings a multitude of consequences. The importance of global change consequences of droughts. Nitrogen deposition may relieve nitrogen limitation
factors varies among forest biomes because climate, tree species diversity (low in boreal forests whereas it may induce phosphorus limitation in tropical
in boreal forests, high in tropics) and dominant mycorrhizal symbioses differ, forests; in the temperate forests, nitrogen deposition may lead to saturation
the proportion of trees forming arbuscular mycorrhiza increasing from high and induce ecosystem-level nutrient losses. AM, arbuscular mycorrhizal fungi;
latitudes to the tropics. Arrows indicate positive effects (red) and negative effects CH4, methane; eCO2, elevated carbon dioxide concentration.

phosphorus deficiency in soils where this element is limited, which are availability, acidification by nitrogen deposition generally increases the
more common across the tropics112. Nitrogen additions in the tropics share of acidotolerant bacterial phyla such as Acidobacteria and Alphapro-
had similar consequences to those in temperate forests, decreasing teobacteria at the expense of Bacteroidetes and Actinobacteria8. As in the
ectomycorrhizal fungi colonization, changing community composition case of drought, shifts in bacterial community due to nitrogen deposition
and reducing the activity of several enzymes118. suggest a change in soil bacterial lifestyle from copiotrophy to oligotrophy,
which may affect carbon cycling processes involving bacteria, such as the
Microbiome response to global change decomposition of soil organic matter, impacting the forest functioning8.
General trends
Although the responses of forests to global change partly reflect spe- Species-level responses to global change
cific conditions, some responses of the forest microbiome are general Microbial communities are composed of individual taxa, and the eco-
and can act across biomes. One example is the limited effect of eCO2 on system response can be seen as the sum of species-specific responses.
microbial communities. Elevated CO2 is likely to have a limited effect Species are constrained to their realized niches that define the condi-
because soil CO2 concentrations are normally higher than those in the tions under which they can survive and reproduce in the presence of
atmosphere65. Any community changes that occur under elevated CO2, biotic interactions. The realized niche can be derived from the observed
such as the increase in copiotrophic microorganisms and the decrease species distribution and abundance across habitat properties, includ-
in oligotrophic microorganisms such as Acidobacteria, reflect elevated ing climatic factors122, offering the possibility to predict the suitability
rhizodeposition (trafficking of carbon by tree roots into soil)8. Soil of the present and future conditions for individual microbial taxa.
respiration generally increases with temperature to a maximum at According to a global meta-analysis, climate is the main driver
approximately 25 °C and decreases at higher temperatures. As no of the distribution of individual fungal taxa and the composition of
alteration of this pattern due to warming was observed119, ecosystem fungal communities123. Climatic niches — ranges of mean annual pre-
responses will depend on actual climatic conditions, that is, an increase cipitation and mean annual temperature — of fungal species differ
in cold biomes and a decrease in the tropics. among fungal guilds. There is considerably less information on the
The effects of drought are also similar across biomes. Based on climatic niche space in bacteria, although temperature and moisture
a meta-analysis, net primary production, aboveground net primary content both contribute to shaping bacterial communities124,125. Con-
production, belowground net primary production, total biomass, sidering the sensitivity of bacteria to the nitrogen content and pH in
aboveground biomass, root biomass, gross ecosystem productivity soils124, nitrogen deposition is expected to have a profound effect on
and net ecosystem productivity are all decreased by drought, and the bacterial community composition. In a laboratory experiment, fungi
responses are more pronounced with drought intensity and duration. and bacteria exhibited a wide range of respiration responses to water
These effects, along with decreased soil moisture and increased soil pH, potential126. Water potential preferences had coarse taxonomic-level
result in a consistent decrease in soil microbial biomass and an increase signals, suggesting that the moisture niche of soil microorganisms is
in fungal to bacterial biomass ratios24. Fungi are better adapted to highly conserved. In particular, strains that were capable of producing
drought than bacteria due to their filamentous growth, which gives them biofilms had drier moisture optima and wider niche breadths126.
the possibility to redistribute water to the actively growing parts of the As vegetation composition is expected to change in response to
mycelia75. Additionally, among bacteria, filamentous taxa increase in dry global change, its future development will influence microbial com-
conditions, whereas unicellular, flagellate bacteria are more abundant in munities' composition. The impact is expected to be larger in fungi
wetter conditions and decrease with increasing water deficit73. Drought than in bacteria because of their closer association with plants as hosts
effects on the bacterial community are consistent: whereas the share of or dead plant biomass as a nutrition source127. Although plant host
Actinobacteria (including filamentous taxa) and Firmicutes increases, shifts in fungi appear to be a consequence of ongoing global change128,
that of Proteobacteria, Verrucomicrobia and Bacteroidetes decreases8. it is unlikely that such shifts will be frequent and rapid.
Not surprisingly, global change-driven disturbances of forests tend If global change factors cause the disappearance of certain micro-
to reduce microbial abundance in soils due to reduced tree activity, more bial taxa, these losses are unlikely to be rapidly compensated by the
in the case of abiotic (fire, windthrow) than biotic (insects or pathogenic colonization of adapted microbes60. However, the microbiomes of
fungi) disturbances120. Due to the dependence of mycorrhizal fungi on forest habitats are complex, with a high level of species diversity129 and
tree roots, disturbances decrease the share of mycorrhizal taxa, over- functional redundancy, where several functions are performed by hun-
all fungal biomass and the fungal to bacterial biomass ratio in soils121. dreds of microbial species5. We may speculate that the negative effects
Although microbial responses to nitrogen deposition reflect soil nitrogen of global change on certain taxa may be functionally compensated

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Glossary of nutrients to trees as well as the transfer of recently photosyntheti-

cally fixed carbon into soil. The global distribution of each of these
groups of trees is climatically constrained: ectomycorrhizal symbiosis
Arbuscular mycorrhizal fungi phyla. Some ectomycorrhizal fungi dominates in forests where seasonally cold and dry climates inhibit
(AM). Fungi that form a mycorrhizal are involved in organic matter decomposition and is predominant at high latitudes and elevations. In
symbiosis with a plant host. This is decomposition. contrast, arbuscular mycorrhizal trees dominate in unseasonal, warm
typical for certain trees and most non- tropical forests and occur with ectomycorrhizal trees in temperate
woody plants and is characterized by Ericoid mycorrhizal fungi biomes in which seasonally warm and wet climates enhance decom-
fungal hyphae that penetrate plant cell Fungi in a mycorrhizal symbiosis with position133. As stated above, global warming and nitrogen deposition
walls, where they form highly branched certain members of the plant family shift the dominance in favour of arbuscular mycorrhizal trees with
structures known as arbuscules. AM Ericaceae that are characterized consequences for fungal symbioses. Changes in the relative share of
belong to a single monopyhyletic by the penetration of hair root cells ectomycorrhizal fungi and AM then affect bacterial communities. This
lineage of Glomeromycota. They are and the formation of hyphal coils. is because the mycorrhizosphere and mycosphere of ectomycorrhizal
not able to decompose biopolymers. Ericoid mycorrhizal fungi include fungi have large absorptive areas where fungal hyphae exude labile
diverse species from the Basidiomycota compounds. This gives these soil compartments distinct features
Biopolymers and Ascomycota phyla, and can that select for specific bacterial communities134. The lower mycelial
Polymeric molecules consisting of efficiently decompose biopolymers. stock of AM does not strongly affect bacterial communities8. With
organic building blocks, typically the ectomycorrhizal to arbuscular mycorrhizal tree shift, we can thus
forming cell walls of plant biomass Free-air CO2 enrichment expect a decrease in the spatial diversity of soil bacterial communi-
(for example, cellulose, hemicelluloses, An experimental approach that raises ties with unclear consequences for ecosystem functioning. From a
lignin, pectin), bacterial biomass (for the concentration of carbon dioxide functional viewpoint, arbuscular mycorrhizal symbiosis will lead to
example, peptidoglycan) or fungal (CO2) in a specified experimental faster nitrogen cycling and potential nitrogen losses108 but may also
biomass (for example, chitin). system, such as a forest stand, and alleviate phosphorus limitation at higher nitrogen levels due to the
allows the response of the ecosystem specialization of AM in phosphorus acquisition135.
Copiotrophic microorganisms to be analysed. Global change also affects the species composition within ectomy-
Microorganisms found in environments corrhizal and arbuscular mycorrhizal guilds. Importantly, ectomycor-
or microhabitats rich in nutrients, Oligotrophic microorganisms rhizal fungal species inhabit narrow ranges of mean annual temperature
particularly carbon. Microorganisms found in environments and mean annual precipitation with generally lower temperature
or microhabitats poor in nutrients, optima123. With the projection of future warming and reduced precipi-
Ectomycorrhizal fungi particularly carbon, or those habitats tation, the ecological constraints of the distribution of these fungi may
Fungi engaged in a mycorrhizal where carbon is contained in complex lead to their relative reduction. Future climate models indeed locally
symbiosis that is characterized macromolecules that are difficult predict a decrease in ectomycorrhizal fungal diversity136. This is in line
anatomically by fungal hyphae that to utilize. with the observed decrease in their diversity with increasing mean
wholly enclose the fine roots of the annual temperature across Japan137. In AM, temperature and pH are the
tree host. Ectomycorrhizal fungi Resilience main determinants of niche space122. Acidification, as a result of nitro-
include diverse species from the The capacity of an ecosystem gen deposition and warming, can thus potentially change arbuscular
Basidiomycota and Ascomycota to recover from perturbations. mycorrhizal communities. Because the carbon to nitrogen ratio and pH
are also important drivers of community composition on non-AM123,138,
atmospheric nitrogen deposition likely adds further constraints to the
by the activity of other unaffected community members. Even when stress on fungi under the influence of warming or changed precipitation.
global change factors may not cause a clear compositional shift in the The realized niche of ectomycorrhizal fungi is significantly
active microbial community, they might affect transcription of genes narrower than that of fungal plant pathogens, with optima at lower
involved in key biochemical processes in these ecosystems130. For exam- temperatures and intermediate levels of precipitation123. Global warm-
ple, anthropogenic nitrogen deposition downregulates the expression ing and droughts may thus disproportionally affect ectomycorrhizal
of fungal genes involved in organic matter decomposition and increases fungi and open a window of opportunity for fungal pathogens. A recent
the abundance of bacterial ones, thus altering the interactions between global model of the future distribution of plant pathogens predicts
soil and bacteria in charge of degrading organic matter in forest soil131. increases in pathogen abundance, with increasing mean annual tem-
Global change affects not only species distribution and gene perature being its major driver139,140. Forest ecosystem stability might
expression but also physiology. One example is the increased length be at risk if trees struggle in recruiting ectomycorrhizal symbionts
of the fruiting season of saprotrophic and ectomycorrhizal fungi in and are simultaneously challenged by an increase in pathogen abun-
Europe paralleling the extension of the vegetation season, as a con- dance. Such an increase in the share of plant pathogens as a response
sequence of warming. The ectomycorrhizal fruiting season is more to experimental warming was occasionally observed141, as was the
constrained, probably due to the necessary cues from the host132. The potential effect of climate on fungal pathogen that likely contributed
ecological implications may be diverse, but their effect on ecosystem to a decline of a specific tree species142.
processes remains yet unclear.
Conclusions and outlook
The future of microbial tree root symbionts and pathogens Global change will undoubtedly affect the functioning of forest eco-
Microbial symbionts — especially tree root-symbiotic ectomycorrhizal systems, including their microbiomes, in a profound and complex way.
fungi and AM — are essential for forest functioning due to the provision Although boreal forests may benefit from higher productivity, they

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will be threatened by drought, fire and pathogens. Temperate forests The applicability and efficiency of each management type is largely
are expected to mostly suffer from drought-increased mortality and context-dependent, and the evaluation of management outcomes is
reflect changes in nitrogen saturation. For tropical forests, the largest essential for the development of smart forestry approaches.
challenge will likely be the consequences of droughts (Fig. 4). Forest The present level of understanding of the future development of
management will have decisive effects on the health of forest ecosys- forest ecosystems clearly has its limitations. One of the constraints is
tems and their ability to store carbon. Although natural shifts in tree geographical. There is far less information from tropical ecosystems
species composition are a lengthy process, planting tree species suit- and their microbiomes. The same is true for forests on permafrost and
able for future climate or assisted migration143 may be a rapid alternative in other remote areas110,146,147. These gaps in knowledge should be filled
applicable in managed forests. As forest trees are long-lived organisms, by targeted exploration of microbiomes of undersampled locations148.
forest management needs to consider future climatic conditions when Clearly, experimental manipulations such as free-air CO2 enrich-
establishing future forests. Shifts from monocultures to mixed stands ment, warming or simulated nitrogen deposition are important sources
should increase resilience, as observed when comparing monocultures of information on the potential future trajectories of ecosystem devel-
and mixed stands in Central Europe144. The increased resilience may opment. Their establishment in underexplored areas is thus an urgent
be due to a multitude of factors including the limited response to out- need. Furthermore, the changes in the ecosystem response to manipu-
breaks of tree species-specific insects or pathogens, or due to better lation over time make it clear that the running experiments should be
resource sharing in mixed stands145. There are a wide range of silvicul- maintained across sufficiently long time intervals to cover the whole
tural measures that come into consideration to mitigate the effects of duration of ecosystem transition. Because global change is an ongo-
global change and to promote carbon storage in forest soils (Box 1). ing process, the establishment of a time series of forest microbiome

Box 1

Forest management strategies to mitigate the effects of global

change
Promotion of carbon storage through tree species selection further increased by selecting tree species tolerant to dieback
The carbon storage potential of forest soils is tree species- under stress.
dependent160, and tree species selection is thus one of the possibilities
affecting the rate of carbon storage at any certain condition. Planting of forests on peatlands
Especially in the boreal zone, peatlands are an important source
Continuous-cover silviculture of methane (CH4) emissions produced by soil anaerobes. CH4
The maintenance of forest canopy cover, for example through emissions are lowered if forests are planted on peat soils163 as the
successive harvesting campaigns as the opposite of clearcutting of transpiration of trees lowers the water table level in the peatland
whole forest stands, helps conserve carbon stocks and biodiversity and increases the thickness of the soil oxic zone where CH4 is
and retain the connectivity of ectomycorrhizal networks across the oxidized by methylotrophic microorganisms164.
forest life cycle. Because of the latter, seedling establishment is
promoted due to availability of root-symbiotic fungi16. Prescribed burning
To mitigate mega-fires, prescribed burning helps reduce wildfire
Nitrogen fertilization intensity and, thus, the amount of nutrients that are lost during fires
In nitrogen-limited boreal forests, nitrogen fertilization was of high intensity, helping conserve the desired functionality of forest
demonstrated to increase soil carbon stocks due to increased input ecosystems165.
of carbon in the form of root-associated mycelium54. The effect of
fertilization may, however, be undesirable from a biodiversity Restoration of converted lands
perspective. Restoration of forests converted to other land use could offset
the negative effects of global change. It was recently estimated that
Deadwood retention restoring 15% of converted lands in priority areas could avoid 60%
It is not fully clear how deadwood decomposition contributes to of expected extinctions while sequestering 299 Gt of carbon dioxide
carbon storage161, yet considering the size of the global deadwood (CO2) (ref. 166).
pool, this contribution may be significant. Deadwood retention
appears to increase both the carbon storage and diversity of the Biodiversity conservation
microbiome as well as the diversity of insect communities154. A recent meta-analysis indicated that biodiversity increased
ecosystem functioning in both ambient conditions and under
Increase in stress resistance simulated climate change. Positive effects were larger in stressful
Controlling stand density at intermediate levels may increase environments induced by global change drivers, indicating that
forest resistance to drought by alleviating competition among high-diversity communities were more resistant to environmental
individuals162. The stress resistance of forest stands may be change167.

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