New perspectives on forest soil carbon and nitrogen cycling processes: Roles of arbuscular mycorrhizal versus ectomycorrhizal tree species

Nearly all tree species develop symbiotic relationships with either arbuscular mycorrhizal (AM) or ectomycorrhizal (EM) fungi to acquire nutrients from soils, and hence influence soil carbon (C) and nitrogen (N) cycles in terrestrial ecosystems. It is crucial to understand the differences in soil C and N cycles between AM and EM forests and the underlying mechanisms. In this review, we first compared the differences in the soil C and N cycles between AM and EM forests, and synthesized the underlying mechanisms from perspectives of the inputs, stabilization, and outputs of soil C and N in forest ecosystems. We also compared the responses of soil C and N cycles between AM and EM forests to global changes. In this field, one major research priority is comparing the structure and function (including the soil C and N cycles) between AM and EM forest ecosystems to provide theoretical basis and solid data for improving forest productivity and ecosystem services. The second research focus is deepening the understanding of the effects of interactions between aboveground litter and belowground mycorrhiza and free-living microbes on soil C and N cycles to reveal the potential underlying mechanisms in forests with different mycorrhizal symbioses. Third, the research methodology and new techniques need refining and applying to explicitly focus on scaling up the fine-scale measurements to better expound and predict the C and N cycles in forest ecosystems. Finally, more studies on the stability of soil organic matter among different mycorrhizal forests are needed to precisely assess responses of the structure and function of forest ecosystems to global changes.     

亚热带丛枝菌根与外生菌根森林对土壤氮循环的影响

菌根真菌能促进植物获取氮素从而调节土壤氮循环过程,但不同类型菌根影响土壤氮循环的特征尚待更多研究.本试验选择中国亚热带典型次生林植被,设置丛枝菌根(AM)和外生菌根(ECM)树种优势样地,对比分析两种菌根类型森林土壤氮状态的差异,以探究菌根类型影响土壤氮循环的可能作用机制.结果 表明,AM与ECM森林的土壤总氮和铵态氮...     

丛枝菌根真菌在土壤氮素循环中的作用

作为植物需求量最大的营养元素,氮素是陆地生态系统初级生产力的主要限制因子。丛枝菌根真菌能与地球上80%以上的陆生植物形成菌根共生体,帮助宿主植物吸收土壤中的P、N等矿质养分。目前,丛枝菌根真菌与氮素循环相关研究侧重于真菌对氮素的吸收形态以及共生体中氮的传输代谢机制,却忽略了丛枝菌根真菌在固氮过程、矿化与吸收过程、硝化过程、反硝化过程以及氮素淋洗过程等土壤氮素循环过程中所起到的潜在作用,并且越来越多的证据也表明丛枝菌根真菌是影响土壤氮素循环过程的重要因子。总结了丛枝菌根真菌可利用的氮素形态及真菌的氮代谢转运相关基因的研究现状;重点分析了丛枝菌根真菌在调控土壤氮素循环过程中的潜在作用以及在生态系统中的重要生态学意义,同时提出了丛枝菌根真菌在土壤氮素循环过程中一些需要深入研究的问题。     

Contrasting responses to ectomycorrhizal inoculation in seedlings of six tropical African tree species

Five caesalpinioid legumes, Afzelia africana, Afzelia bella, Anthonotha macrophylla, Cryptosepalum tetraphylum and Paramacrolobium coeruleum, and one Euphorbiaceae species, Uapaca somon, with a considerable range in seed sizes, exhibited different responses to inoculation by four species of ectomycorrhizal (ECM) fungi, Scleroderma dictyosporum, S. verrucosum, Pisolithus sp. and one thelephoroid sp. in greenhouse conditions. Thelephoroid sp. efficiently colonized seedlings of all of the five caesalpinioid legumes except U. somon, but provided no more growth benefit than the other fungi. Thelephoroid sp. and S. dictyosporum colonized seedlings of U. somon poorly, but stimulated plant growth more than the other fungi. The relative mycorrhizal dependency (RMD) values of the caesalpinioid legumes were never higher than 50%, whilst U. somon had RMD values ranging from 84.6 to 88.6%, irrespective of the fungal species. The RMD values were negatively related to seed mass for all plant species. Potassium concentrations in leaves were more closely related than phosphorus to the stimulation of seedling biomass production by the ECM fungi. Our data support the hypothesis that African caesalpinioid legumes and euphorbe tree species with smaller seeds show higher RMD values than those with the larger seeds.     

Contrasting rhizosphere soil nutrient economy of plants associated with arbuscular mycorrhizal and ectomycorrhizal fungi in karst forests

Plant and Soil - Plants growing in the soils of karst forests associate with arbuscular mycorrhizae (AM) or ectomycorrhizae (ECM) to acquire nutrients. We researched how these different mycorrhizal...     

常绿阔叶林外生、内生菌根树种细根化学计量学性状对N添加的响应

为揭示不同菌根类型树种细根化学计量学性状对N添加的塑性响应,在福建省建瓯市万木林自然保护区常绿阔叶林内选择外生菌根树种罗浮栲(Castanopsis faberi)和内生菌根树种木荷(Schima superba)为研究对象,采用根袋法开展N添加试验,细根在根袋内生长半年后测定化学计量学指标(C、N、P、C/N、N/P、C/P)。结果表明:根序对细根化学计量学性状有显著影响,随着根序的增加,罗浮栲与木荷细根C浓度、C/N、C/P明显增加,N浓度与P浓度明显下降。N添加对细根C、N浓度均有极显著的促进作用,但对细根P浓度影响不显著,从而导致细根C/N维持稳定,但N/P、C/P升高,细根受P限制增加。细根化学计量学性状对N添加的塑性响应在不同序级间以及在外生菌根树种罗浮栲和内生菌根树种木荷之间均无显著差异。结论表明,研究所选内生、外生菌根树种细根化学计量学性状对N添加具有基本相似的响应。     

Correction to: Contrasting rhizosphere soil nutrient economy of plants associated with arbuscular mycorrhizal and ectomycorrhizal fungi in karst forests

Plant and Soil - A Correction to this paper has been published: https://doi.org/10.1007/s11104-021-05032-6     

An arbuscular mycorrhizal fungus significantly modifies the soil bacterial community and nitrogen cycling during litter decomposition

Arbuscular mycorrhizal fungi (AMF) perform an important ecosystem service by improving plant nutrient capture from soil, yet little is known about how AMF influence soil microbial communities during nutrient uptake. We tested whether an AMF modifies the soil microbial community and nitrogen cycling during litter decomposition. A two‐chamber microcosm system was employed to create a root‐free soil environment to control AMF access to ¹³C‐ and ¹⁵N‐labelled root litter. Using a 16S rRNA gene microarray, we documented that approximately 10% of the bacterial community responded to the AMF, Glomus hoi. Taxa from the Firmicutes responded positively to AMF, while taxa from the Actinobacteria and Comamonadaceae responded negatively to AMF. Phylogenetic analyses indicate that AMF may influence bacterial community assembly processes. Using nanometre‐scale secondary ion mass spectrometry (NanoSIMS) we visualized the location of AMF‐transported ¹³C and ¹⁵N in plant roots. Bulk isotope ratio mass spectrometry revealed that the AMF exported 4.9% of the litter ¹⁵N to the host plant (Plantago lanceolata L.), and litter‐derived ¹⁵N was preferentially exported relative to litter‐derived ¹³C. Our results suggest that the AMF primarily took up N in the inorganic form, and N export is one mechanism by which AMF could modify the soil microbial community and decomposition processes.     

常绿阔叶林外生和丛枝菌根树种细根形态和构型性状对氮添加的可塑性响应

以中亚热带常绿阔叶林外生菌根树种罗浮栲和丛枝菌根树种木荷为研究对象,采用根袋法进行野外原位氮添加试验,研究了细根形态性状(比根长、比表面积、组织密度、平均根直径)和构型性状(分枝数、分枝比、根长增长速率、根尖密度、分枝密度),分析不同菌根树种细根形态和构型性状对氮沉降的响应.结果表明:随序级增加,外生和丛枝菌根树种细根...     

Differential effects of tropical arbuscular mycorrhizal fungal inocula on root colonization and tree seedling growth: implications for tropical forest diversity

The potential for mycorrhizae to influence the diversity and structuring of plant communities depends on whether their affinities and effects differ across a suite of potential host species. In order to assess this potential for a tropical forest community in Panama, we conducted three reciprocal inoculation experiments using seedlings from six native tree species. Seeds were germinated in sterile soil and then exposed to arbuscular mycorrhizal fungi in current association with naturally infected roots from adults of either the same or different species growing in intact forest. The tree species represent a range of life histories, including early successional pioneers, a persistent understory species, and emergent species, typical of mature forest. Collectively, these experiments show: (i) the seedlings of small-seeded pioneer species were more dependent on mycorrhizal inocula for initial survival and growth; (ii) although mycorrhizal fungi from all inocula were able to colonize the roots of all host species, the inoculum potential (the infectivity of an inoculum of a given concentration) and root colonization varied depending on the identity of the host seedling and the source of the inoculum; and (iii) different mycorrhizal fungal inocula also produced differences in growth depending on the host species. These differences indicate that host–mycorrhizal fungal interactions in tropical forests are characterized by greater complexity than has previously been demonstrated, and suggest that tropical mycorrhizal fungal communities have the potential to differentially influence seedling recruitment among host species and thereby affect community composition.     

Growth strategies of tropical tree species: disentangling light and size effects

An understanding of the drivers of tree growth at the species level is required to predict likely changes of carbon stocks and biodiversity when environmental conditions change. Especially in species-rich tropical forests, it is largely unknown how species differ in their response of growth to resource availability and individual size. We use a hierarchical bayesian approach to quantify the impact of light availability and tree diameter on growth of 274 woody species in a 50-ha long-term forest census plot in Barro Colorado Island, Panama. Light reaching each individual tree was estimated from yearly vertical censuses of canopy density. The hierarchical bayesian approach allowed accounting for different sources of error, such as negative growth observations, and including rare species correctly weighted by their abundance. All species grew faster at higher light. Exponents of a power function relating growth to light were mostly between 0 and 1. This indicates that nearly all species exhibit a decelerating increase of growth with light. In contrast, estimated growth rates at standardized conditions (5 cm dbh, 5% light) varied over a 9-fold range and reflect strong growth-strategy differentiation between the species. As a consequence, growth rankings of the species at low (2%) and high light (20%) were highly correlated. Rare species tended to grow faster and showed a greater sensitivity to light than abundant species. Overall, tree size was less important for growth than light and about half the species were predicted to grow faster in diameter when bigger or smaller, respectively. Together light availability and tree diameter only explained on average 12% of the variation in growth rates. Thus, other factors such as soil characteristics, herbivory, or pathogens may contribute considerably to shaping tree growth in the tropics.     

Depth-dependent effects of ericoid mycorrhizal shrubs on soil carbon and nitrogen pools are accentuated under arbuscular mycorrhizal trees

Plant mycorrhizal associations influence the accumulation and persistence of soil organic matter and could therefore shape ecosystem biogeochemical responses to global changes that are altering forest composition. For instance, arbuscular mycorrhizal (AM) tree dominance is increasing in temperate forests, and ericoid mycorrhizal (ErM) shrubs can respond positively to canopy disturbances. Yet how shifts in the co-occurrence of trees and shrubs with different mycorrhizal associations will affect soil organic matter pools remains largely unknown. We examine the effects of ErM shrubs on soil carbon and nitrogen stocks and indicators of microbial activity at different depths across gradients of AM versus ectomycorrhizal (EcM) tree dominance in three temperate forest sites. We find that ErM shrubs strongly modulate tree mycorrhizal dominance effects. In surface soils, ErM shrubs increase particulate organic matter accumulation and weaken the positive relationship between soil organic matter stocks and indicators of microbial activity. These effects are strongest under AM trees that lack fungal symbionts that can degrade organic matter. In subsurface soil organic matter pools, by contrast, tree mycorrhizal dominance effects are stronger than those of ErM shrubs. Ectomycorrhizal tree dominance has a negative influence on particulate and mineral-associated soil organic matter pools, and these effects are stronger for nitrogen than for carbon stocks. Our findings suggest that increasing co-occurrence of ErM shrubs and AM trees will enhance particulate organic matter accumulation in surface soils by suppressing microbial activity while having little influence on mineral-associated organic matter in subsurface soils. Our study highlights the importance of considering interactions between co-occurring plant mycorrhizal types, as well as their depth-dependent effects, for projecting changes in soil carbon and nitrogen stocks in response to compositional shifts in temperate forests driven by disturbances and global change.     

Contrasting mechanisms of secondary metabolite accumulation during leaf development in two tropical tree species with different leaf expansion strategies

Young leaves of most species experience remarkably higher herbivore attack rates than mature leaves. Considerable theoretical effort has focused on predicting optimal defense and tradeoffs in defense allocation during leaf expansion. Among others, allocation to secondary chemistry may be dependent on growth constraints. We studied flavanoid production during leaf development in two species of Inga (Fabaceae: Mimosoideae) with different expansion strategies: Inga goldmanii, a species with slowly expanding young leaves, and Inga umbellifera, a species with fast-expanding young leaves. In these two species, the most abundant and toxic class of defensive compounds is flavanoids (which include tannins). We measured their concentration by leaf dry weight, their total content per leaf, their HPLC chemical profile and their toxicity to a generalist herbivore at different expansion levels. Although in both species the flavanoid concentration decreased with increasing leaf expansion, that decrease was twice as pronounced for I. umbellifera as it was for I. goldmanii. I. umbellifera leaves produced flavanoids only during the first half of their development while I. goldmanii leaves continued production throughout. The changes in flavanoid HPLC profiles and toxicity were also more dramatic for I. umbellifera, which had different flavanoids in young than in mature leaves. Relative to I. umbellifera, I. goldmanii showed smaller changes in both flavanoid composition and toxicity in the transition from young to mature leaves. These results indicate that, even though young leaves suffer higher rates of attack and are predicted to have better chemical defenses than mature leaves, growth constraints may modulate defense allocation and thus, evolution of defense strategies.Electronic Supplementary Material Supplementary material is available for this article at and is accessible for authorized users.     

Environmental and genetic effects on the formation of ectomycorrhizal and arbuscular mycorrhizal associations in cottonwoods

Although both environment and genetics have been shown to affect the mycorrhizal colonization of host plants, the impacts of these factors on hosts that can be dually colonized by both ectomycorrhizal (EM) and arbuscular mycorrhizal (AM) fungi are less understood. We examined the influence of environment and host crosstype on the EM and AM colonization of cottonwoods (Populus angustifolia and natural hybrids) by comparing levels of colonization of trees growing in common gardens that differed in elevation and soil type. We also conducted a supplemental watering experiment to determine the influence of soil moisture on AM and EM colonization. Three patterns emerged. First, garden location had a significant impact on mycorrhizal colonization, such that EM colonization was 30% higher and AM colonization was 85% lower in the higher elevation garden than the lower elevation garden. Second, crosstype affected total (EM + AM) colonization, but did not affect EM or AM colonization. Similarly, a significant garden × crosstype interaction was found for total colonization, but not for EM or AM colonization. Third, experimental watering resulted in 33% higher EM colonization and 45% lower AM colonization, demonstrating that soil moisture was a major driver of the mycorrhizal differences observed between the gardens. We conclude that environment, particularly soil moisture, has a larger influence on colonization by AM versus EM fungi than host genetics, and suggest that environmental stress may be a major determinant of mycorrhizal colonization in dually colonized host plants.     

Contrasting species responses to continued nitrogen and phosphorus addition in tropical montane forest tree seedlings

Global changes in nutrient deposition rates are likely to have profound effects on plant communities, particularly in the nutrient‐limited systems of the tropics. We studied the effects of increased nutrient availability on the seedlings of six tree species in montane forests of southern Ecuador in situ. After five years of continued N, P, or N+P addition, naturally grown seedlings of each of the two most common species at each elevation (1000, 2000, and 3000 m asl) were harvested for analyses of leaf morphology, nutrient content, herbivory, and tissue biomass allocation. Most species showed increased foliar N and P concentrations after addition of each respective element. Leaf tissue N:P ratios of >20 in the control plants of all species suggest that P is more growth‐limiting in these forests than N. Leaf morphological responses to nutrient addition were species and nutrient specific, with some species (Hedyosmum purparescens, Graffenrieda emarginata) exhibiting increased specific leaf area (SLA), and others (Graffenrieda harlingii) increased leaf area ratios (LAR). Pouteria torta (1000 m) had lower SLA and LAR after P addition. Increased herbivory was only evident in G. emarginata (after N and N+P addition). Only the species from 3000 m asl modified biomass allocation after nutrient addition. In general, N and N+P addition more strongly affected the species studied at the upper elevations, whereas P addition had a similar range of effects on the species at all elevations. We conclude that the responses of the studied tropical montane forest tree seedlings to chronic N and P addition are highly species‐specific and that successful adaptation to increased nutrient availability will depend on species‐specific morphological and physiological plasticity.     

Leaf 15N abundance of subarctic plants provides field evidence that ericoid,ectomycorrhizal and non-and arbuscular mycorrhizal species access different sources of soil nitrogen

The natural abundance of the nitrogen isotope 15, ¹⁵N, was analysed in leaves of 23 subarctic vascular plant species and two lichens from a tree-line heath at 450 m altitude and a fellfield at 1150 m altitude close to Abisko in N. Sweden, as well as in soil, rain and snow. The aim was to reveal if plant species with different types of mycorrhizal fungi also differ in their use of the various soil N sources. The dwarf shrubs and the shrubs, which in combination formed more than 65% of the total above-ground biomass at both sites, were colonized by ericoid or ectomycorrhizal fungi. Their leaf ¹⁵N was between–8.8 and–5.5 at the heath and between–6.1 and –3.3 at the fellfield. The leaf ¹⁵N of non- or arbuscular mycorrhizal species was markedly different, ranging from –4.1 to –0.4 at the heath, and from –3.4 to+2.2 at the fellfield. We conclude that ericoid and ectomycorrhizal dwarf shrubs and shrubs utilize a distinct N source, most likely a fraction of the organic N in fresh litter, and not complexed N in recalcitrant organic matter. The latter is the largest component of soil total N, which had a ¹⁵N of –0.7 at the heath and +0.5 at the fellfield. Our field-based data thus support earlier controlled-environment studies and studies on the N uptake of excised roots, which have demonstrated protease activity and amino acid uptake by ericoid and ectomycorrhizal tundra species. The leaves of ectomycorrhizal plants had slightly higher ¹⁵N (fellfield) and N concentration than leaves of the ericoids, and Betula nana, Dryas octopetala and Salix spp. also showed NO _inf3 ^sup- reductase activity. These species may depend more on soil inorganic N than the ericoids. The ¹⁵N of non- or arbuscular mycorrhizal species indicates that the ¹⁵N of inorganic N available to these plants was higher than that of average fresh litter, probably due to high microbial immobilization of inorganic N. The ¹⁵N of NH _inf4 ^sup+ -N was +12.3 in winter snow and +1.9 in summer rain. Precipitation N might be a major contributer in species with poorly developed root systems, e.g. Lycopodium selago. Our results show that coexisting plant species under severe nutrient limitation may tap several different N sources: NH _inf4 ^sup+ , NO _inf3 ^sup- and organic N from the soil, atmospheric N₂, and N in precipitation. Ericoid and ectomycorrhizal fungi are of major importance for plant N uptake in tundra ecosystems, and mycorrhizal fungi probably exert a major control on plant ¹⁵N in organic soils.     

Rhizosphere soil bacterial communities and nitrogen cycling affected by deciduous and evergreen tree species

Deciduous and evergreen trees differ in their responses to drought and nitrogen (N) demand. Whether or not these functional types affect the role of the bacterial community in the N cycle during drought remains uncertain. Two deciduous tree species (Alnus cremastogyne, an N₂‐fixing species, and Liquidambar formosana) and two evergreen trees (Cunninghamia lanceolata and Pinus massoniana) were used to assess factors in controlling rhizosphere soil bacterial community and N cycling functions. Photosynthetic rates and biomass production of plants, 16S rRNA sequencing and N‐cycling‐related genes of rhizosphere soil were measured. The relative abundance of the phyla Actinobacteria and Firmicutes was higher, and that of Proteobacteria, Acidobacteria, and Gemmatimondaetes was lower in rhizosphere soil of deciduous trees than that of evergreen. Beta‐diversity of bacterial community also significantly differed between the two types of trees. Deciduous trees showed significantly higher net photosynthetic rates and biomass production than evergreen species both at well water condition and short‐term drought. Root biomass was the most important factor in driving soil bacterial community and N‐cycling functions than total biomass and aboveground biomass. Furthermore, 44 bacteria genera with a decreasing response and 46 taxa showed an increased response along the root biomass gradient. Regarding N‐cycle‐related functional genes, copy numbers of ammonia‐oxidizing bacteria (AOB) and autotrophic ammonia‐oxidizing archaea (AOA), N₂ fixation gene (nifH), and denitrification genes (nirK, nirS) were significantly higher in the soil of deciduous trees than in that of the evergreen. Structural equation models explained 50.2%, 47.6%, 48.6%, 49.4%, and 37.3% of the variability in copy numbers of nifH, AOB, AOA, nirK, and nirS, respectively, and revealed that root biomass had significant positive effects on copy numbers of all N‐cycle functional genes. In conclusion, root biomass played key roles in affecting bacterial community structure and soil N cycling. Our findings have important implications for our understanding of plants control over bacterial community and N‐cycling function in artificial forest ecosystems.     

Partitioning of soil phosphorus among arbuscular and ectomycorrhizal trees in tropical and subtropical forests

Partitioning of soil phosphorus (P) pools has been proposed as a key mechanism maintaining plant diversity, but experimental support is lacking. Here, we provided different chemical forms of P to 15 tree species with contrasting root symbiotic relationships to investigate plant P acquisition in both tropical and subtropical forests. Both ectomycorrhizal (ECM) and arbuscular mycorrhizal (AM) trees responded positively to addition of inorganic P, but strikingly, ECM trees acquired more P from a complex organic form (phytic acid). Most ECM tree species and all AM tree species also showed some capacity to take up simple organic P (monophosphate). Mycorrhizal colonisation was negatively correlated with soil extractable P concentration, suggesting that mycorrhizal fungi may regulate organic P acquisition among tree species. Our results support the hypothesis that ECM and AM plants partition soil P sources, which may play an ecologically important role in promoting species coexistence in tropical and subtropical forests.