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University of Torino, Department of Plant Biology, Viale Mattioli 25, I-10125 Torino, Italy
Paolo Gonthier
Giovanni Nicolotti
University of Torino, Department of Exploitation and Protection of Agricultural and Forestry Resources (Di.Va.P.R.A.), Plant Pathology, Via L. da Vinci 44, I-10095 Grugliasco, Italy
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ABSTRACT |
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The effects on mycoflora of Norway spruce stumps of biological and chemical treatments in the fight against Heterobasidion annosum coll. were investigated two yr after applications of these treatments. The biological treatments were Hypholoma fasciculare, Phanerochaete velutina, Vuilleminia comedens, Trichoderma harzianum and both the conidial suspension and culture filtrate of Verticillium bulbillosum; propiconazole was used as chemical treatment. Samplings were performed on 130 stumps, including controls with (C1) and without (C2) an autologous wood disk. Forty-nine fungal taxa were isolated, and most were Deuteromycetes. Trichoderma harzianum significantly reduced the number of taxa versus controls (three versus 25), while the other treatments showed more limited qualitative and quantitative effects. Cluster and correspondence analysis differentiated three groups of treatments: one including the three Basidiomycetes, V. bulbillosum and C1; one comprising propiconazole and C2; and one composed of the treatment with T. harzianum only. Because the same stumps already had been sampled one yr after treatments in a similar study, comparisons between data were possible and were very useful in the investigation of the temporal evolution of the effects of each treatment. Multivariate analysis showed that the strong effects of T. harzianum on stump mycocenoses increased over time. Transient effects were shown in most treatments (i.e., the three Basidiomycetes), whereas V. bulbillosum had the least impact on naturally occurring mycoflora.
Key words: Heterobasidion annosum, Hypholoma fasciculare, Phanerochaete velutina, propiconazole, stump mycocenoses, Trichoderma harzianum, Verticillium bulbillosum, Vuilleminia comedens
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The life cycle of this fungus is well known; it spreads via root grafts from infected trees or stumps to uninfected trees, causing root rot and/or butt rot, depending on the host species. Basidiospore deposition on fresh wood surfaces (i.e., freshly cut stumps) is known to be the primary cause for the increase in H. annosum infection centers and of new infections in previously uninfected forests.
Stumps are thus the primary sites of new H. annosum infection centers, and they also are potential reservoirs for fungal survival and spread. However, infections are markedly influenced by interactions with potential antagonists and by stresses due to physical phenomena, such as temperature and desiccation of stump surfaces. It should be noted that, while colonizing new stumps, the fungus is characterized by small biomass and hence by weak competitive saprotrophic ability. Therefore, stumps have been regarded as the most appropriate targets for treatments against the pathogen (Rishbeth 1959a, b).
The effectiveness of biological (Holdenrieder and Greig 1998) and chemical treatments (Pratt et al 1998) against H. annosum has been documented, whereas the effect of these treatments on other organisms has received little attention. Although the effect is assumed to be negligible because treatments are targeted exclusively to stump surfaces (Pratt et al 1999), recent studies proved that treatments have significant effects on both nontarget fungi and ground vegetation (Varese et al 1999, Westlund and Nohrstedt 2000).
Catastrophic events and forest and agricultural management practices disturb organisms. Few examples concerning fungi and their response to forestry-management practices (Miller and Lodge 1997, Garbelotto et al 2002) have been documented. Disturbance in the fungal community structure is assumed to be important because of the key role of fungi within ecosystems. Changes in the rates of decomposition and nutrient pool conversion, mainly connected with fungi, can affect the stability, productivity and, ultimately, the functioning of ecosystems (Friese et al 1997).
The results of an investigation on the effects of biological and chemical treatments in the fight against H. annosum on stump mycocenoses have been published (Varese et al 1999). Most of the treatments markedly affected the assemblage of fungi colonizing Norway spruce (Picea abies (L.) Karsten) stumps and some significantly reduced the fungal diversity, according to these data collected a yr after treatment. However, little is known about the persistence and the evolution of these effects over time.
This study describes the effects after two yr of six biological treatments and one chemical treatment against H. annosum on the microfungal communities of Norway spruce stumps in a forest in the Alps of northwestern Italy. Because this study involved the same stumps sampled by Varese et al (1999), an additional goal was to evaluate the evolution of the effects of such treatments over time by comparing the effects of each treatment one yr after the applications (Varese et al 1999) with the effects two yr after the applications.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The fungi used in biological treatments were Hypholoma fasciculare (Huds. : Fr.) Kummer, Phanerochaete velutina (Fr.) Karst., Vuilleminia comedens (Nees : Fr.) Maire, Trichoderma harzianum Rifai, and Verticillium bulbillosum W. Gams and Malla. The chemical treatment was propiconazole (TILT®: 25% concentrated emulsion).
Because the stumps sampled in this study were the same analyzed by Varese et al (1999), we refer to Varese et al (1999) for details regarding treatments and treatment applications. A summary of methods is given in Table I.
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The microfungal populations were evaluated by the methodology described by Varese et al (1999). The autologous wood disks were removed. Twenty-seven wood slivers (5–6 x 2–3 mm) were obtained by sampling systematically the whole surface of each stump. Two-thirds and one-third of them were plated onto malt-extract agar (MEA) and benomyl-amended agar medium, respectively, in 9 cm Petri dishes. Further details in Varese et al (1999).
Fungi were identified on the basis of their macroscopic and microscopic features. After the identification at the genus level (Domsch et al 1980, Von Arx 1981, Hanlin 1990, Kiffer and Morelet 1997), fungi were transferred onto the media suggested by the monographies of the different genera and identified at the species level.
The colonization frequency (F) was computed for each fungus as the number of infected stumps expressed as percentage of the total number of stumps examined for each treatment. The colonization density (D) was computed as the number of slivers infected expressed as the mean value of the percentage of the total number of slivers plated out for each stump because we have observed no significant differences in the fungal density values on either medium (MEA or benomyl amended medium). The control-treatment differences in fungal colonization density were examined for significance by means of nonparametric Kruskal-Wallis test for several independent groups with the Systat statistical package, release 5.2 (SCS 1992). It also was applied to test the significance in the number of species per treatment with respect to the control. Multivariate analysis of the numerical data was used to assess the effect of each treatment at the community level (Syntax-pc 1993). A block clustering to optimize the arrangement of rows and columns in a block matrix was done. It allowed a nonhierarchical clustering of fungal taxa and a more obvious relationship between treatments and groups of species. Different species were grouped by means of a constrained-block clustering with treatments constrained and fungal taxa randomly grouped. Because block clustering requires an a priori selection of the number of groups, this was determined for fungal taxa by cluster analysis using UPGMA (Unweighted Pair Group Method with Arithmetic Averaging) in the formation of the clusters and chord distance as a measure of dissimilarity. The block clustering was executed on the D values transformed in interval scale, using the pooled sum of squares as a measure of the sharpness of the block structure. The analysis runs interactively re-allocating fungal taxa in the groups, because the matrix attains the maximum-block sharpness (other details in Podani and Feoli 1991). The block matrix obtained from the clustering was analyzed with correspondence analysis, producing a more synthetic representation with the ordering in few axes of treatments and groups of fungal taxa. The results of these analyses were checked by comparing them with the dendrogram produced by cluster analysis on the mean-density values of the fungal taxa in each treatment, using distance as dissimilarity index and UPGMA in the formation of the clusters.
To study the evolution of the effects of the treatments over time, data of the first (e.g., one yr after the treatment, Varese et al 1999) and second sampling (e.g., two yr after the treatment, present study) were compared by the same multivariate approach as above. Because there was a difference in the number of stumps between the two samplings, statistical analysis was performed again on data of the first sampling, taking into account only stumps that were common to both samplings. Multivariate analysis conducted on these data confirmed that the sample of 130 stumps was representative of the 175 stumps sampled by Varese et al (1999) (data not shown).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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20% in one or more treatments. The number of fungal taxa isolated in the different treatments is generally lower with respect to the control C1 (25). However, only TH significantly reduced the number of species (three versus 25).
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60%): Epicoccum purpurascens, Penicillium simplicissimum, Alternaria alternata, Phoma putaminum and Mucor hiemalis f. hiemalis. Among these, E. purpurascens, A. alternata and P. putaminum still displayed high F values in all the treatments, except in TH. Penicillium simplicissimum showed F values similar to the control in PV, whereas it was infrequent or absent in the other treatments. Mucor hiemalis f. hiemalis displayed F values comparable or even higher with respect to C1 in the treatments with the three Basidiomycetes, FVB and VB; on the other hand, it was infrequent and absent in TI and TH, respectively.
Of the taxa with F 
60% in C1, Trichoderma viride showed F values comparable to C1 in HF, VC and TI, whereas it was significantly reduced in the other treatments. Penicillium miczynskii was significantly enhanced by treatments with the Basidiomycetes and VB but significantly reduced by other treatments. Phoma herbarum was detected only in TI, where it showed F value significantly higher than in C1. Rhizoctonia sp. and Cylindrocarpon magnusianum were significantly enhanced by FVB. Cladosporium cladosporioides was enhanced by all treatments except by TH.
Some species were absent in C1 and clearly linked to particular treatments: Fusarium tricinctum to VC; Gliocladium roseum to PV; Graphium anamorph of Ophiostoma piceae to VB; Phoma exigua to PV, FVB and TI. With regard to the biocontrol agents we used, Trichoderma harzianum was found exclusively on inoculated stumps (F = 100%), whereas V. bulbillosum was isolated from inoculated stumps (F = 44.4%) and from stumps treated with FVB (F = 41.6%) and TI (F = 12.5%).
Comparison of the fungal populations on untreated stumps with (C1) and without (C2) the wood disk showed that C2 were colonized by a lower number of taxa (22 versus 25). Epicoccum purpurascens and P. putaminum were dominant on C2 (F = 100%) followed by A. alternata, T. viride, C. cladosporioides and Aureobasidium pullulans var. pullulans. The first four species showed high F values also in C1, while the last two were infrequent. Mucor hiemalis f. hiemalis and P. simplicissimum, which were frequent in C1, were almost or completely absent in C2.
Block clustering placed the 49 taxa in 14 groups differing widely in number. The occasional species (18 species whose F and D values were too low to differentiate the treatments) were placed in Group 3, which virtually corresponds to the list at the bottom of Table II. Correspondence analysis (Fig. 1) gave a simultaneous ordering of the species groups and the treatments. The treatments that selected the most similar mycocenoses were also grouped. TH is separated from the other treatments along the first axis of the biplot and is strictly correlated with T. harzianum only. Two groups are recognizable along the second axis. The first one is wide and includes the treatments with the three Basidiomycetes (HF-PV-VC), VB, FVB and C1, which are correlated with species of groups 3–13. The second one includes C2 and TI, correlated with groups 1 and 2. The treatment groupings are confirmed by the cluster analysis on the mean D values (Fig. 2).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, as exemplified by the fact that 75.5% of taxa were re-isolated and most of them were Deuteromycetes. Most of the species already have been reported as colonizers of stumps or wounds on forest trees (Käärik and Rennerfelt 1957, Meredith 1959, 1960, Rayner 1977a, Mugnai and Capretti 1987, Nicolotti and Varese 1996). They mostly belong to nondecay fungi, although a few of them (i.e., Aureobasidium pullulans, Graphium anamorph of Ophiostoma piceae, Phoma herbarum) are well known soft-rot fungi (Domsch et al 1980, Matta 1996).
The mycocenoses associated with the control stumps protected with an autologous disk (C1) in the two yr of sampling are similar to each other, and the same is true for the unprotected control stumps (C2), as exemplified by the dendrogram in Fig. 4. This would indicate that the mycoflora composition of P. abies stumps is relatively stable over time. On the other hand, multivariate analyses clearly differentiated C1 from C2 in both samplings. The covered stumps supported more and differently composed species, probably because, as also reported by Varese et al (1999), the disk resulted in greater humidity and acted as a shield against radiation. It is clear now that the effects of each treatment on stump mycoflora were due to both the biological or chemical agent and the presence of the disk, which also significantly influenced the effectiveness of the different treatments against H. annosum (Nicolotti et al 1999).
From an ecological point of view, biological and chemical treatments might be considered disturbance factors on stump surfaces because they influence, sometimes greatly, the patterns of fungal colonization (Varese et al 1999). Data presented in this study, however, provide evidence that the effects of most treatments decrease over time, thus enabling the restoration of natural mycocenoses.
TH represents the main exception. This was the most divergent treatment from the control one yr after the applications (Varese et al 1999) and is still the most divergent two yr after treatments. High saprotrophic capacity of T. harzianum and its adaptation to low temperature might have encouraged its complete colonization of the stumps and drastically reduced fungal diversity, as reported by Varese et al (1999). Data suggest that the negative effects of TH on biodiversity have been increasing over time, as exemplified by the reduction in the number of species isolated from stumps one yr and two yr after treatments (eight and three, respectively) and by the multivariate analysis performed on the entire set of data. Trichoderma strains, inoculated as biocontrol agents, have been shown to strongly affect the species composition of both stump and soil mycoflora (Kallio and Hallaksela 1979, Yakimenko and Grodnitskaya 2000).
The impact of chemical compounds on fungal succession within stumps has received limited attention. However, fragmentary reports proved that they selectively might reduce or enhance the frequency of specific fungi (Rishbeth 1959b, Meredith 1960, Punter 1963, Hadfield 1968, Driver and Ginns 1969, Dowding 1970, Rayner 1977a, b, Lipponen 1991, Pratt and Quill 1996). In our study, the mycocenosis associated with TI is still more similar to C2 than to C1 and to either of the other treatments (Figs. 1, 2), as also found by Varese et al (1999). However, results show that qualitative and quantitative differences between TI and C1 decrease over time (Figs. 3, 4), providing evidence that mycocenosis associated with this treatment reacts to the disturbance represented by the treatment itself. This finding reinforces what already is known about propiconazole's compatibility with natural microbial ecosystems (Varese et al 1999), and this is especially important for this treatment because it has been suggested as a good candidate for the control of H. annosum in forests (Nicolotti et al 1999).
Treatments with the three lignivorous Basidiomycetes (HF, PV and VC) very similarly influenced the patterns of fungal colonization of spruce stumps. They were much more similar to each other than to all the other treatments one yr after the applications (Varese et al 1999), and they have converged in a similar way to the control in the second sampling. Such common patterns could be explained at least partially by an analogous behavior in the substrate exploitation that might have promoted the establishment of similar microfungal assemblages. Differences in F values among the three treatments are evident only for a few species, such as Gliocladium roseum, Penicillium brevicompactum and Mycelia sterilia dematiacea. In spite of the similarity in the effects of such treatments on stump mycoflora, their effectiveness in the forest against the pathogen is quite different and only PV adequately protects stumps (Nicolotti et al 1999).
The treatments with VB and FVB were the least divergent from the controls both after one and two yr. Their effects on the fungal community, indeed, were similar to the application of a wood disk only, as in C1. Verticillium bulbillosum, which is not usually associated with stumps, was surprisingly very persistent on inoculated stumps. Moreover, this study provided evidence that the fungus might spread from treated stumps to untreated ones, as exemplified by the fact that two yr after treatments it also has been isolated from stumps treated with propiconazole. It should be noticed that persistence and the ability to colonize new sites are among the most important features for a biocontrol agent. Because VB and FVB both have little impact on stump mycocenoses and are effective against the pathogen (Nicolotti et al 1999), they can be regarded as suitable treatments for use in the forest.
The methodology of sampling we used is unreliable in the detection of H. annosum stump infections. While a single CFU of the pathogen was isolated from stump surfaces (Varese et al 1999), several stumps sampled in this study were extensively infected by H. annosum just below their surfaces (Nicolotti et al 1999, Gonthier et al 2001). This fungus, like other Basidiomycetes, tends to spread vertically in narrow columns that can enlarge and coalesce to occupy a large proportion of the stump in the deep layers (Holdenrieder 1984, Redfern and Stenlid 1998) and thus is less likely to be isolated by our technique. The same patterns of colonization might explain the absence on stump surfaces of the three Basidiomycetes we used as biocontrol agents. Nevertheless, our methods allow careful investigation of fungal communities inhabiting stump surfaces, so that the effects of disturbance factors, such as stump treatments, can be detected. Fungal communities analyzed in this work were quite sensitive to treatmeants, and hence any variation in their qualitative and quantitative composition, over time as well, might represent a suitable indicator of the disturbance effects of treatments. The development of markers for risk assessment of field treatments is one of the most important goals in forest-disease management (Hintz et al 2001).
A necessary step in the development of sustainable forestry management will require identifying practices that permit controlled manipulations of the fungal community. For that purpose, research is needed to better understand the response of saprophytic, parasitic and mycorrhizal fungi to disturbances associated with different management practices (Miller and Lodge 1997). This was the focus of our study. Our results confirm that fungal colonization of P. abies stumps is influenced, sometimes greatly, by the treatments against H. annosum. Generally, however, the effects of treatments fall over time, with the exception of treatment with T. harzianum. Widespread inoculation of T. harzianum on stumps might represent a potential hazard because it can lead to an unwanted and persistent shift in the biodiversity of the stump ecosystem. Hence, the final choice of a biological or chemical treatment against H. annosum should not leave out of consideration the effect of these treatments on the other organisms inhabiting stumps. This is particularily important for saprotrophyc fungi because of the role they play in promoting and accelerating stump degradation needed for forest maintenance and/or in opposing fungal pathogens through direct antagonism and trophic competition (Rayner and Boddy 1988, Dix and Webster 1995). The need to prolong the treatments for many years and in wide areas makes the evaluation of such impact particularly important because possible negative effects could magnify over time.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Accepted for publication November 12, 2002.
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LITERATURE CITED |
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