Molecular characterization and evaluation of mycorrhizal capacity of Suillus isolates from Central Spain for the selection of fungal inoculants

Suillus fungal specimens of pine forests from a Mediterranean area of central Spain (Madrid region) were studied based on molecular and physiological analysis of sporocarps to obtain fungal native inocula to produce mycorrhizal Pinus halepensis Miller in nursery. Variation within the internal transcribed spacer (ITS) region of the ribosomal RNA genes of Suillus was examined by restriction fragment length polymorphism (RFLP) and direct sequencing of polymerase chain reaction products. Ribosomal DNA (rDNA) spacers were amplified from pure cultures obtained from fruit bodies of a range of Suillus species: Suillus bellinii (Inzenga) Watling, Suillus bovinus (Pers.) Kuntze, Suillus collinitus (Fr.) Kuntze, Suillus granulatus (L.) Snell, Suillus mediterraneensis (Jacquet. & Blum) Redeuil, Suillus luteus L. (Gray), and Suillus variegatus (Sw.) Kuntze. Interspecific variation in the length and number of restriction sites of the amplified ITS region was observed. This variation was confirmed by sequencing, which allowed us to identify some isolates. This is the first time that the ITS sequence of S. mediterraneensis is completely described. No intraspecific rDNA variation was observed within isolates of S. collinitus, S. mediterraneensis, and S. luteus. The phylogenetic analysis established the close relationship among these Mediterranean fungal species. As a further step to characterize the different isolates and to understand the relation between genetic and functional diversity, some physiological variables were evaluated. Intraspecific variation in axenic fungal growth and in mycorrhizal capacities was detected, especially within S. collinitus isolates. The fungal isolates stimulated the growth of P. halepensis in different rates. These studies indicated that ITS analysis, in conjunction with mycorrhizal tests, provides suitable combined tools for the analysis of Suillus spp. in a small geographic area for selecting isolates with final afforestation purposes.     

Antifungal activities of actinomycete strains associated with high-altitude sagebrush rhizosphere

The antifungal-producing potential of actinomycete populations from the rhizosphere of low-altitude sagebrush, Artemisia tridentata, has been examined. In a continued investigation of new sources of antifungal-producing microorganisms, this study examined the antifungal-producing potential of actinomycetes from the rhizosphere of high-altitude A. tridentata. With high-altitude sagebrush, rhizosphere soil actinomycete numbers were one to four orders of magnitude higher than those found in nonrhizosphere bulk soils and different from those found with the low-altitude plants. A total of 122 actinomycete isolates was screened against nine fungal species and six bacterial species for the production of antimicrobial compounds. Four rhizosphere isolates, Streptomyces amakusaensis, S. coeruleorubidus, S. hawaiiensis and S. scabies, showed broad-spectrum antifungal activity against three or more fungal species in plate assays. In liquid antagonism assays, mycelium production by Aspergillus niger was reduced by up to 50% by two of the actinomycete isolates. These results demonstrate the potential of rhizosphere microbiology in the search for new antimicrobials.     

Fungi associated with storage rots of cocoyams (Colocasia spp.) in Nsukka,Nigeria

Cocoyam (Colocasia spp.) corms and cormels showing spoilage symptoms were collected from many stores in Nsukka locality and examined for rot and associated fungal pathogens. Aspergillus niger, Botryodiplodia theobromae, Corticium rolfsii, Geotrichum candidum, Fusarium oxysporum, and F. solani were recovered from rotten cocoyams. The representative isolates of these species caused cocoyam rot in pathogenicity tests. The rot due to A. niger, B. theobromae and C. rolfsii was extensive resulting in complete maceration of cocoyam tissue. Potassium sorbate (0.1 mg/ml) protected cocoyams from fungal rot with the exception of C. rolfsii.     

Formation of ascochitine by plant pathogens of the genus Ascochyta

Strains of fungi isolated from pulse crops: pea (Pisum sativum) and faba beans (Vicia faba) plants with symptoms of Ascochyta blight, footrot and stems lesions have been examined under laboratory conditions for their ability to produce ascochitine and metabolites toxic toArtemia salina. BothAscochyta pisi Lib and Ascochyta fabae LK Jones isolates formed ascochitine in yields of 20–480mg/kg. The highest yield of ascochitine was produced on rice and the lowest on maize grain. Ascochyta pinodes andPhoma medicaginis varpinodella (LK Jones) Boerema (formerlyAscochyta pinodella LK Jones) did not produce ascochitine. Crystalline ascochitine was found to be of moderate toxicity toArtemia salina larvae (LC₅₀ = 85μg/cm³BSM*). Extracts ofPhoma medicaginis var,pinodella cultures were found to be highly toxic toArtemia salina.     

Ectomycorrhizal fungal community structure across a bog-forest ecotone in southeastern Alaska

We examined the ectomycorrhizal (ECM) fungal community across a bog-forest ecotone in southeastern Alaska. The bog and edge were both characterized by poorly drained Histosols and a continuous layer of Sphagnum species, ericaceous shrubs, Carex species, and shore pine [Pinus contorta Dougl. ex Loud. var. contorta]. The forest had better-drained Inceptisols and Spodosols, a tree community comprised of western hemlock [Tsuga heterophylla (Raf.) Sarg.], yellow cedar (Thuja plicata Donn ex D. Don.), Sitka spruce [Picea sitchensis (Bong.) Carr.] and shore pine, and an understorey of ericaceous shrubs and herbs. ECM root tip density (tips cm^–3 soil) was significantly greater in the forest than the edge or bog and ECM colonization was significantly different in all three plant communities. The below ground ECM fungal taxa were analyzed using molecular techniques (PCR-RFLP and DNA sequencing). Three ECM fungal taxa, Suillus tomentosus (Kauffman) Singer, Cenococcum geophilum Fr.:Fr, and a Russula species, differed in relative frequency, yet were among the four most frequent in all three plant communities. Although differences in ECM fungal richness were observed across plant communities, unequal sampling of ECM roots due to root density and colonization differences confounded richness comparisons. Using resampling procedures for creating taxon-accumulation curves as a function of sampled ECM roots revealed similarities in cumulative ECM fungal taxa richness across the ecotone.     

Accumulation of mansonones E and F in seedlings of Ulmus americana in response to inoculation with Ophiostoma ulmi

Summary The accumulation of mansonones E and F was investigated in Ulmus americana L. seedlings 5 weeks after inoculation with three aggressive and three non-aggressive isolates of Ophiostoma ulmi (Buism.) Nannf. The three non-aggressive isolates stimulated significantly more mansonone E and F accumulation than the three aggressive isolates of O. ulmi. Mansonone induction also varied within both the aggressive and the non-aggressive groups. Aggressive and non-aggressive isolates were recovered in equal frequencies from the inoculation wounds, whereas the aggressive isolates were recovered more frequently than the non-aggressive isolates 15 cm and 25 cm up the seedlings' stem. Vascular browning in the outer xylem of the seedlings correlated with mansonone E and F accumulation. Mansonone accumulation in U. americana seedlings is therefore associated with vascular browning and a reduction in fungal spread.     

Isolation and analysis of endophytic microorganisms in wheat (Triticum aestivum L.) leaves

The present investigation was undertaken in order to select the surface-sterilization technique most efficient for eliminating epiphytes, to document the spectrum of endophytes of healthy leaves from three wheat cultivars in Buenos Aires Province (Argentina) and to determine their infection frequencies at three growth stages. Surface-sterilization with undiluted commercial solution of sodium hypochlorite was reaffirmed as adequate for removing epiphytes on wheat leaves. From the 450 wheat leaf segments incubated, three bacterial isolates and 130 fungal isolates were obtained. From all the isolates, 19 fungal species were identified. Bacterial isolates were characterized as Bacillus sp. There were significant differences between microorganisms, stages of growth, and stages × microorganisms interaction. Differences between cultivars, stages × cultivars, microorganisms × cultivars and for the triple interaction were not significant. Frequency of microorganisms isolated increased with crop age, but it was statistically similar for the three wheat cultivars tested (Klein Centauro, Klein Dragón and Buck Ombú). Rhodotorula rubra, Alternaria alternata, Cladosporium herbarum and Epicoccum nigrum were isolated in the highest frequency. The other microorganisms were present at intermediate or low values. The species isolated may be assigned to three groups: (a) well-known and economically important pathogens of wheat, (b) commonly abundant phylloplane fungi considered to be primary saprobic and minor pathogens and (c) species occasionally present in wheat.     

The ability of 16 ectomycorrhizal fungi to increase growth and phosphorus uptake of Eucalyptus globulus Labill. and E. diversicolor F. Muell.

The effectiveness of 16 fungal isolates in forming ectomycorrhizas and increasing the growth and phosphorus uptake of Eucalyptus globulus Labill. and E. diversicolor F. Muell. seedlings was examined in the glasshouse. Seedlings were grown in yellow sand at 2 phosphorus levels (4 and 12 mg P kg^-1 sand). At the time of harvest (100 days), the non-inoculated seedlings and seedlings inoculated with Paxillus muelleri (Berk.) Sacc. and Cortinarius globuliformis Bougher had a low level of contamination from an unknown mycorrhizal fungi. Seedlings inoculated with Thaxterogaster sp. nov. and Hysterangium inflatum Rodway had developed mycorrhizas of the superficial type whereas Hydnangium carneum Wallr. in Dietr., Hymenogaster viscidus Massee & Rodway, Hymenogaster zeylanicus Petch, Setchelliogaster sp. nov., Laccaria laccata (Scop. ex. Fr.) Berk., Scleroderma verrucosum (Vaillant) Pers., Amanita xanthocephala (Berk.) Reid & Hilton, Descolea maculata Bougher and Malajczuk and Pisolithus tinctorius (Pers.) Coker & Couch formed typical pyramidal ectomycorrhizas. The dry weight of non-inoculated and inoculated E. globulus seedlings at 12 mg P kg^-1 sand did not differ, whereas several isolates caused growth depression of E. diversicolor. By contrast, at 4 mg P kg^-1 sand growth increases ranged from 0–13 times above that of non-inoculated seedlings. P. tinctorius produced the largest growth increase on both eucalypt species. In general, isolates which developed more extensive mycorrhizas on roots produced the largest growth responses to inoculation. Isolates which increased plant growth also increased phosphorus uptake by the plant. Seedlings inoculated with L. laccata and S. verrucosum retained more phosphorus in their roots than plants inoculated with the other fungal isolates.     

Taxonomic and functional characterisation of fungi from the Sebacina vermifera complex from common and rare orchids in the genus Caladenia

The terrestrial orchid genus Caladenia contains many species which are threatened with extinction. They have highly specific associations with Sebacina vermifera and closely related fungi, and conservation of these terrestrial orchids, in part, relies on symbiotic propagation to produce plants for reintroduction and ex situ conservation collections. However, little is known of the diversity of mycorrhizal fungi associating with natural populations. Here, restriction fragment polymorphism analysis, internal transcribed spacer and nuclear large subunit sequencing and symbiotic seed germination were used to investigate the taxonomic and functional diversity of fungal isolates from single populations of six endangered Caladenia species and one common species across the same biogeographic range. Fifty-nine fungal isolates were collected for investigation including ten isolates from the six endangered species Caladenia audasii, Caladenia amoena, Caladenia sp. aff. fragrantissima (Central Victoria), Caladenia sp. aff. patersonii, Caladenia rosella and Caladenia orientalis and 49 isolates from six populations of the common species Caladenia tentaculata. While the common species associated with three distinct S. vermifera-like taxa, the six endangered species were restricted to one of these fungal taxa. No direct relationship between the taxonomic identity of the fungi and their ability to stimulate seed germination was observed; however, the majority of the fungi isolated from the Caladenia species were capable of germinating seed in vitro, indicating their mycorrhizal status and potential for symbiotic propagation in conservation programmes.     

MYCORRHIZAE AND MYCORRHIZAL FUNGI OF CALYPSO BULBOSA

The seasonal development and fungal endophytes of the mycorrhizal roots of Calypso bulbosa (L.) Oakes were studied using fresh collections from Alberta and herbarium specimens from six herbaria. Typically, a single pair of mycorrhizal roots are produced at the base of a single corm each growing season. No evidence was found to support the putative existence of a coralloid rhizome in this species. The pattern of fungal infection, peloton formation, and breakdown is similar to other nonsaprophytic, terrestrial orchids. The endophytic fungi of a single mycorrhizal root can belong to a number of different fungal taxa. Fungi isolated and described include Rhizoctonia anaticula Currah, Thanatephorus pennatus Currah, Leptodontidium orchidicola Sigler and Currah, Phialocephala fortinii Wang and Wilcox, and two unnamed isolates of Rhizoctonia.     

Parasitic Bacteria and Fungi on Common Mistletoe (Viscum album L.) and Their Potential Application in Biocontrol

This study was carried out to identify pathogenic bacteria and fungi on mistletoe (Viscum album L.) and investigate their potential use in biological control of this parasitic plant. For this purpose, a total of 48 fungal isolate and 193 bacterial strains were isolated from contaminated V. album during the summers 2005–2006. The isolated bacterial strains and fungal isolates were identified by using the Sherlock Microbial Identification System (MIS; Microbial ID, Newark) and microscopic methods, respectively. The bacterial strains that induced hypersensitive reaction (HR) on tobacco (Nicotiana tabacum L.) and fungal isolates were tested for pathogenicity on young shoots of mistletoe by using injection methods. The pathogenic bacterial strains and fungal isolates were also tested for their activity against mistletoe using spray methods. Five bacterial strains (two Burkholderia cepacia, one each of Bacillus megaterium, Bacillus pumilus and Pandoraea pulminicola) were HR and pathogenicity positive when injected but none of them when sprayed on mistletoe. When fungi were injected, 32 isolates were pathogenic but only thirteen when sprayed on mistletoe. Alternaria alternata VA?‐202, VA?‐205, VA?‐217 and Acremonium kiliense VA‐11 fungal isolates were the most effective ones and caused strong disease symptoms on mistletoe. The present study is the first report on the efficiency of potential biocontrol agents against mistletoe in Turkey.     

DNA fingerprinting of Peronospora parasitica,a biotrophic fungal pathogen of crucifers

The fungus Peronospora parasitica (Pers. ex Fr.) Fr. is an obligate biotroph infecting a wide range of host species in the family Cruciferae. Isolates from different hosts are morphologically similar, and pathotypes are usually distinguished on the basis of host range. Random Amplified Polymorphic DNA (RAPD) fingerprints were generated from a range of P. parasitica isolates from different Brassica species. Reaction conditions, in particular DNA template, primer and Mg²⁺ concentrations, were optimized to ensure that amplifications were reproducible. Possible artefacts arising through host plant DNA were assessed by including such DNA in control reactions. Confirmation that diagnostic RAPD bands were generated from fungal DNA was also obtained by Southern hybridization of a RAPD band to genomic fungal DNA. By screening 20 decamer primers, 2 were found to detect sufficient genetic variation to allow complete differentiation between pathotypes. These results illustrate the potential value of RAPDs for detecting polymorphisms between isolates of a non-culturable plant pathogenic fungus.     

The effect of soil pH on the ability of ectomycorrhizal fungi to increase the growth of Eucalyptus globulus Labill.

We examined the effect of two levels of soil pH (5 and 6) on the ability (effectiveness) of ectomycorrhizal fungi to increase the growth of Eucalyptus globulus Labill. at a deficient supply of P. Plants were inoculated with one of six fungal isolates [Laccaria laccata (Scop. ex Fr.) Berk. and Br. (isolates A and B), Pisolithus tinctorius (Pers.) Coker and Couch (isolates A and B), Descolea maculata Bough. and Mal. and Setchelliogaster sp. nov.] and were grown in a P-deficient sand, in pots, in a temperature-controlled glasshouse. Seedlings were harvested 89 days after planting and were assessed for dry matter production, tissue P concentrations, ectomycorrhizal colonization of roots and hyphal development in soil.Uninoculated plants had less than 5% of their fine root length colonized by ectomycorrhizal fungi. In contrast, inoculated plants had 30% or greater of their fine root length ectomycorrhizal. Inoculation increased the uptake of P and growth of plants for all isolates and at both levels of soil pH, although growth responses to inoculation were greater at pH 6, particularly for the two L. laccata isolates. Isolates which colonized roots most extensively increased plant growth to the greatest extent. D. maculata was the most effective fungal isolate at pH 5, and both D. maculata and L. laccata A were most effective at pH 6. The effects of soil pH on plant growth were also related to some extent to the effects of soil pH on colonized root length. Growth responses to inoculation were related less well to hyphal development in soil. The L. laccata isolates formed more hyphae in soil (on a per pot, per m of fine root, and per m of colonized fine root basis) than other fungal isolates, but were not always more effective in increasing plant grown.     

Intraspecific variability of isozymes in Penicillium nodositatum Valla,a fungus inducing ‘myconodules’ on the root-system of Alnus sp.

A comparison of mycelial extracts of 17 isolates of Penicillium nodositatum collected from the root system of grey alder (Alnus incana (L.) Moench.) and Italian alder (A. cordata Desf.) grown at different sites was made using isoenzyme analysis of esterases, acid phosphatase, malate dehydrogenase and phosphoglucose isomerase. Jaccard similarity coefficient analysis demonstrated that interspecific variability existed both among and within sites. In most cases, the enzyme patterns of isolates were distinct. Comparison of these isolates and three other Penicillium species closely related to P. nodositatum showed no similarity for the enzymes tested.     

Phenotypic variability of environmental isolates of the entomopathogenic fungus <Emphasis Type="Italic">Beauveria bassiana</Emphasis>

A total of 35 isolates of Beauveria bassiana (Bals.) Vuill. isolates obtained from various insects of Novosibirsk oblast were investigated. The fungal morphotypes were found to include cultures of high, medium, and low virulence. Low correlation (r < 0.48) was observed between virulence and the morphophysiological characteristics of the isolates (lipase and protease activity, biomass, radial growth rate, conidia productivity, and relief). Isolates exhibiting high virulence to insects of a certain order proved to be virulent to the insects of other orders. A high correlation (r > 0. 74) was revealed between the virulence of the isolates to the potato beetle Leptinotarsa decemlineata Say and the locusts Calliptamus barbarus Costa and Locusta migratoria L. Isolates obtained from insects of the same species in the same site may differ significantly in virulence.     

Comparison of phosphatase localization in the intraradical hyphae of arbuscular mycorrhizal fungi,Glomus spp. and Gigaspora spp.

The localization of acid and alkaline phosphatases in the intraradical hyphae of the arbuscular mycorrhizal fungi, Glomus mosseae (Nicol. and Gerd.) Gerd. and Trappe (Gm), Gl. etunicatum Becker and Gerd. (Ge) and Gigaspora rosea Nicol. and Schenck (Gir) were compared. Marigold (Tagetes patula L.) and leek (Allium porrum L.) were inoculated with each of the three fungi. The mycorrhizal roots were harvested at 3, 4, 5 and 6 weeks after sowing (WAS), treated with a digestion solution containing cellulase and pectinase, and then stained for phosphatase activities at pH 5.0 and pH 8.5. The development of fungal structures in the host root was also examined. Gm formed fine-branched (mature) arbuscules only at the early phase of infection (3 to 4 WAS). Mature arbuscules of Ge and Gir were observed from the early phase (4 WAS) up to the end of experiment. At pH 5.0, the localization of the phosphatase activities of the three fungi were similar irrespective to host plant species. The activity appeared in mature arbuscules and intercellular hyphae, whereas the collapsed arbuscules were inactive. Ten millimolar NaF, an acid phosphatase inhibitor, inhibited the phosphatase activities of Gm and Ge but did not affect that of Gir. At pH 8.5, a difference among the fungal species was found in the localization of phosphatase activity while that between host species was not. The mature arbuscules were also the active sites in all three species. Only Gir showed the activity in the intercellular hyphae while the two Glomus spp. did not. Five millimolar EDTA inhibited the activity of Gir at pH 8.5 while the activities of Ge and Gm were not affected by either 5 mM EDTA or 10 mM KCN (both are alkaline phosphatase inhibitors).     

The occurrence of keratinophilic fungi in texas soil

Summary A total of 137 soils, 27 coming from caves and 110 from outdoor lands of Texas, were examined for the presence of keratinophilic fungi by the use of the ToKaVa hairbaiting technique. Twenty three and 69 fungal isolates, respectively, were recovered from these areas. Microsporon gypseum was the most common isolate, followed byTrichophyton mentagrophytes, andT. terrestre. M. gypseum was recovered from caves in a very high frequency (67 %), in comparison to its presence in the outdoor soils (10 %).Fifteen strains ofChrysosporium, belonging to four species, were isolated. Fourteen of these isolates were recovered from shady areas under trees. None of these had been isolated from Texas soil before.     

Endophytic fungi associated with the Antarctic grass <Emphasis Type="Italic">Deschampsia antarctica</Emphasis> Desv. (<Emphasis Type="Italic">Poaceae</Emphasis>)

Deschampsia antarctica Desv. (Poaceae) represents one of the two vascular plants that have colonized the Antarctic continent, which is usually exposed to extreme environmental conditions. In this work, we have characterized the endophytic fungi associated with the leaves of D. antarctica. Endophytic fungi were recovered from 91 individual plants from different points of Admiralty Bay at King George Island, Antarctica. A total of 26 fungal isolates were obtained from 273 leaf fragments. All isolates were identified by analysis of the sequences of the internal transcribed spacer region (ITS) of the rDNA. Alternaria and Phaeosphaeria were the most frequent genera associated with the plant. Other fungal isolates were identified as Entrophospora sp. and several undescribed Ascomycete species. An interesting result was obtained for the isolates UFMGCB 215 and UFMGCB 262, which were related to fungi associated with bryophytes present in boreal ecosystems. Some isolates showed low identity in the ITS sequences to sequences of fungal species deposited in GenBank, suggesting that these fungi could be new species. This work is the first report on fungal endophytes associated with leaves of the Antarctic grass D. antarctica.     

Differential responses of three fungal species to environmental factors and their role in the mycorrhization of<Emphasis Type="Italic"> Pinus radiata</Emphasis> D. Don

Three ectomycorrhizal (ECM) isolates of Rhizopogon luteolus, R. roseolus and Scleroderma citrinum were found to differ markedly in their in vitro tolerance to adverse conditions limiting fungal growth, i.e. water availability, pH and heavy metal pollution. S. citrinum was the most sensitive, R. luteolus intermediate and R. roseolus the most tolerant species. Pinus radiata D. Don seedlings were inoculated in the laboratory and in a containerised seedling nursery with spore suspensions of the three ECM species. Colonisation percentage was considerably lower under nursery conditions, probably due to competition by native fungi. The effects of nursery ECM inoculation on seedling growth depended on the fungal species. Only R. roseolus-colonised plants showed a significantly higher shoot growth than non-mycorrhizal plants. All three fungi induced significantly higher root dry weights relative to control plants. Despite the low mycorrhizal colonisation, mycorrhization with all three species improved the physiological status of nursery-grown seedlings, e.g. enhanced root enzyme activity, shoot nutrient and pigment content, net photosynthesis rate and water use efficiency. Of the three fungal species, R. roseolus was the most effective; this species was also the most adaptable and showed the greatest range of tolerance to adverse environmental conditions in pure culture. It is, therefore, proposed as a promising fungal species for ECM inoculation of P. radiata in the nursery.     

寒温带针叶林优势树种倒木分解真菌群落多样性及功能差异

为了揭示寒温带针叶林不同树种倒木分解中真菌群落的分布格局,探讨影响倒木真菌群落分布的养分驱动因子。采用Illumina MiSeq高通量测序技术和R语言等分析方法对微生物多样性数据进行信息挖掘,解析白桦(Betula platyphylla Suk.)、兴安落叶松(Larix gmelinii(Rupr.)Kuzen)、樟子松(Pinus sylvestris var. mongolica Litv.)倒木分解初期真菌群落的多样性及功能差异。研究发现,寒温带针叶林中白桦、樟子松倒木优势菌群为Basidiomycota(担子菌门)、Trichaptum(附毛菌属),兴安落叶松倒木优势菌群为Ascomycota(子囊菌门)、Acidea菌属。多样性分析表明,不同树种倒木真菌群落的Alpha多样性由高到低依次为兴安落叶松、白桦、樟子松,树种的差异极显著的改变了操作分类单元(OTU)、属水平上倒木真菌群落的Beta多样性。菌群生态分析表明,腐生型是3种倒木上优势真菌的主要生态类型,木质腐生为白桦、樟子松倒木上真菌的主要生活方式,土壤腐生为兴安落叶松真菌类群的主要生活方式。养分关联分析表明,pH、全碳(TC)、全氮(TN)、碳氮比(C/N)、半纤维素、木质素等养分指标在3种倒木间存在显著性差异,其中含水率(MC)、TC、TN、纤维素、半纤维素是影响倒木优势真菌群落分布的主要养分因素。不同树种对倒木真菌群落的富集具有差异性,这种差异带来的微生物多样性及功能变化对寒温带森林生态系统的物质循环具有重要的科学意义。