Periodicity, fluctuations and successions of macrofungi in fir forests (Abies alba Miller) in Tuscany, Italy

E. Salerni

Fungi are among the most important organisms on earth, and they are essential components of terrestrial ecosystems. eir reproductive structures are strictly dependent and affected by environmental conditions, and community dynamics over time and space may be indirect indicators of the health status of forests. We combined macrofungal biodiversity indices in eight Mediterranean forests in Italy and surveyed 160 plots by standardized surveys, to evaluate the role of macrofungi as early predictors of change in the forest structure. e results show that indices of fungal diversity are influenced by geographic and floristic conditions, and interand intra-annual temperature and rainfall fluctuations affect the formation of fungal fruiting bodies. ese findings suggest that environmental changes could be reflected by macrofungi, and conservation initiatives should consider the pivotal role that fungi play in biodiversity monitoring.

The results of mycocoenological research conducted over a period of nearly 30 years in central southern Tuscany (Italy) are reported. The 599 fungal species found in 11 permanent plots include ubiquitous taxa and taxa linked preferentially or exclusively to certain types of forest ecosystems. Fungal 1 biodiversity was particularly high in evergreen oak forests of the Grosseto coast. Classification of samples brought out affinities and differences between the various fungal communities. Ordering by detrended correspondence analysis revealed that the relevés were disposed along a climate-altitude gradient. The health status of the forests, evaluated according to criteria proposed by Central European authors, was generally found to be good. The period of major fungal fruiting was autumn, though the duration of fruiting varied between different environments: in high altitude and coastal environ-ments, the fungal mycelium produced carpophores nearly all year round, whereas no carpophores...

Old-growth forests are key elements of ecosystem diversity and conservation strategies, providing niche differentiation and trophic pathways that produce structural and compositional heterogeneity. In these forests, deadwood is particularly important for saproxylic and mycorrhizal fungi, sustaining forest productivity and environmental services. In this study, the saproxylic fungal diversity in Mediterranean mountain forests, characterized by different management histories and forest types (holm oak and beech), was analyzed. The relationships between saproxylic fungal biodiversity and structural attributes were considered in three forest stands of the Apennines (Italy). In addition, descriptive environmental parameters and forest traits were related to prevailing fungal communities, in order to analyze the species composition and distribution patterns of saproxylic fungi resulting from the ordination processes. The study sites were selected on the basis of their late-serial stage of development. Species frequency was analyzed through multivariate techniques to test the relationships between fungi, structural attributes and environmental variables. A Detrended Correspondence Analysis (DCA) was used to investigate the response of the overall fungal community structure to environmental gradients. Living tree volume, altitude, vegetation type, and the frequency of species with ephemeral sporocarp lifespan played a crucial role in diversifying species distribution patterns. Deadwood volume and decay classes were related to taxonomic and trophic community diversity. However, differences between the considered climatic regions exerted a major role on the occurrence of fungi with ephemeral sporocarps more than deadwood abundance , utilized primarily as fructification substrate.

Forest Ecology and Management 169 (2002) 187–202 Periodicity, fluctuations and successions of macrofungi in fir forests (Abies alba Miller) in Tuscany, Italy A. Laganà*, C. Angiolini, S. Loppi, E. Salerni, C. Perini, C. Barluzzi, V. De Dominicis Dipartimento di Scienze Ambientali, Università degli Studi, Via P.A. Mattioli, 4, I-53100 Siena, Italy Received 3 July 2000; received in revised form 2 March 2001; accepted 31 May 2001 Abstract The present study, carried out in natural and planted Abies alba Miller woods, was undertaken as a contribution to knowledge of temporal changes occurring in fungal communities. Moreover, notes on fungal species and fungal communities in this type of wood are given. Correlations between meteorological variables and fungi (number of species and number of carpophores, as total or divided into trophic groups) were tested by Pearson’s product-moment coefficient. On a short time scale, weather parameters clearly play a major role, affecting periodicity and fluctuations; on a long time scale (10 years or more), correspondence analysis (CA) indicate that vegetation parameters and forest evolution affect successions. # 2002 Elsevier Science B.V. All rights reserved. Keywords: Fir forests; Macrofungi; Fungal temporal changes; Correspondence analysis 1. Introduction It is well known that fungal fruiting is a seasonal event that depends on meteorological factors, especially temperature and rainfall. High rainfall and mild temperatures in summer are normally considered to favour the formation of carpophores by the fungal mycelium (Arnolds, 1981). Many authors have tried to find direct relations between fungal fruiting and weather patterns; for example, it has been demonstrated that an important condition is a fairly wet period after a dry one (Becker, 1956; Heim, 1969), and that excess water in the soil inhibits carpophore production (Bujakiwicz, 1969). A complex network of relations * Corresponding author. Tel.: þ39-577-232871; fax: þ39-577-232860. E-mail address: lagana@unisi.it (A. Laganà). emerges, often complicated by interactions between different parameters. However, it should be borne in mind that the reaction of the mycelium to different weather conditions varies considerably from environment to environment. To explain the changes occurring in the fungal community over time, the following parameters (Arnolds, 1981) can be considered: periodicity, which is the presence of carpophores during a limited period of the year; fluctuation, which is the difference in species composition and density of carpophores in different years due to reversible variations in environmental factors—a major cause of fluctuations is variations in weather patterns; successions, which is differences in the number of carpophores and in species composition in different years due to irreversible environmental changes. 0378-1127/02/$ – see front matter # 2002 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 8 - 1 1 2 7 ( 0 1 ) 0 0 6 7 2 - 7 188 A. Laganà et al. / Forest Ecology and Management 169 (2002) 187–202 Clearly, these three processes can occur at the same time and it is difficult to establish which has the greatest weight at a given time. Information on periodicity can be obtained with only a year of observations, but fluctuations and successions require a much longer period of research; for successions Arnolds (1981) claims that more than 10 years of research is needed. The present study in woods of Abies alba Miller was undertaken as a contribution to knowledge of temporal changes occurring in fungal communities, especially in relation to meteorological factors. We investigated changes in the fungal community in a natural and a planted wood, to evaluate the effects of different forest origin on the various components of forest mycocoenoses. 2. Study area The research was conducted in two permanent stations of A. alba (Fig. 1) in the Natural Reserve of the Casentino Forests (Arezzo, central Italy). Station 1 (area 500 m2, altitude 1210 m, northern exposure, inclination 128, latitude 438480 3800 N, longitude 118510 0500 E) is a natural fir wood near Fangacci Pass; station 2 (area 900 m2, altitude 1115 m, southern exposure, inclination 38, latitude 438480 1800 N, longitude 118510 4500 E) is a fir wood planted on what was previously a natural pasture, at Stammerina. The substrate consists of ‘‘. . . turbiditic sandstones rich in quartz, feldspar, calcite, clastic dolomite and phyllosilicates, . . . alternating with gray-marly schist, . . . bordering the Scaglia Toscana which are variegated clayey schists and red, gray and greenish marls’’ (Merla and Selli, 1969). Climate is type A, very humid, with Im >100 according to Thornthwaite; mean annual temperatures oscillate between 9 and 118, annual rainfall is high (1250–2300 mm) (Rapetti and Vittorini, 1994). Vegetation can be classified in the alliance Fagion sylvaticae (Luquet 1926) Tx. et Diemont 1936 of the order Fagetalia sylvaticae Pawl. 1928. In view of the fact that the two studied plots are in a natural reserve, scarce or no human disturbance to soil or vegetation was present during the research periods. Nevertheless, there was in both periods no evidence of strong animal disturbance. 3. Materials and methods The data used in this study is from research conducted in two periods: from 1986 to 1989 (Perini Fig. 1. Map showing the position of the studied area (Ab ¼ A. alba Miller woods). A. Laganà et al. / Forest Ecology and Management 169 (2002) 187–202 et al., 1995) and in autumn 1998 (Laganà et al., 2001). Surveys, in which all species of macrofungi (on soil, on litter, on wood, either stumps or standing trees) were recorded and carpophores were counted, were made every month. Macrofungi are taken to be fungi visible to the naked eye and greater than 1 mm in size (Arnolds, 1981). We did not consider hypogean basidiomycetes, or corticioid and poroid species with resupinate and pileate fruiting bodies. The samples collected are deposited in the Herbarium Universitatis Senensis (SIENA). For details on methods, see Arnolds (1981). For nomenclature of fungal species we used Arnolds et al. (1995); for species not appearing in this list, the source is given in brackets in Table 2 next to the name. Authors names are abbreviated according to Brummitt and Powell (1992). Abundance of species is given as maximum density of carpophores per year (mDCy) (Arnolds, 1981). For some elaboration, species were assigned to a trophic group according to Arnolds et al. (1995) and to personal observations. During the elaboration of data, the approximate number of fruit bodies was calculated by an ‘‘ordinal transformation’’ (Arnolds, 1981) of the DCv scale: 1 2 3 4 ¼ ¼ ¼ ¼ 1.3 5.8 18 58 5 6 7 8 ¼ ¼ ¼ ¼ 180 580 1800 5800 Phytosociological relevés were conducted by the method of Braun-Blanquet (1964) in 1986 and 1998. Plant names are according to Pignatti (1982). Soil pH was measured in eight samples from each station, four taken at the surface and four at a depth of 10 cm, by the method described in Arnolds (1981); the samples were not mixed, and pH was measured on each of them. The reported values are stational means standard deviation calculated for each of the two study periods. Meteorological data for the study periods was obtained from the weather station at Badia Prataglia (altitude 843 m, Arezzo, Italy). Correlations between meteorological variables and fungi (number of species and number of carpophores, as total or divided into trophic groups) were tested by Pearson’s product-moment coefficient. Indirect analysis of gradient was done by processing species data 189 by correspondence analysis (CA) using the program CANOCO version 4.0 (Ter Braak and Šmilauer, 1998). The symbols 1a–e and 2a–e indicate stations 1 and 2, respectively, in the 5 years of observations. 4. Results and discussion Soil pH was found to have changed in the 10-yearinterval between the two study periods: in 1986 it was 4:7 0:1 and 5:8 0:2 at stations 1 and 2, respectively, whereas in 1998, it was 4:4 0:2 and 6:3 0:4, respectively. The change was only 3.7% at station 1, but þ8.8% at station 2. During Phytosociological surveys (Table 1), changes in the structure and composition of vegetation were observed, especially at station 2 (planted), where beech cover increased (especially in the shrub layer). At the same time, there was an increase in abundance of mesophilous and nemoral herbs, some of which are linked to eutrophic woods (Carex sylvatica Hudson, Melica uniflora Retz., Salvia glutinosa L., Senecio fuchsii Gmelin, Veronica montana L., Viola reichenbachiana Jordan), and a decrease in nitrophilous and ruderal species (Rubus hirtus W. et K., R. idaeus L., Urtica dioica L.). These results suggest that the rise in pH at station 2 could be caused by an increase in beech litter, which decomposes more readily than fir litter and has a less acidifying effect. Table 2 summarizes the mycocoenological data of the two study periods (Perini et al., 1995; Laganà et al., 2001). The total number of species found during the 5 years of research was 130, 32 of which were found in both periods and 21 of which were exclusive to 1998. The latter include some critical taxa (e.g. Russula urens), but most are readily visible and easily identified species (Collybia tuberosa, Cortinarius lividoochraceus, C. rufoolivaceus, Hygrocybe virginea, Psilocybe fascicularis, R. albonigra, R. fragilis, and so forth). Most are ubiquitous (Boletus ferrugineus, Cortinarius cinnamomeus, C. elegantior, C. lividoochraceus, R. albonigra, R. chloroides) or at least common in fir or conifer woods (R. urens, Mycena epipterygia var. lignicola) (Maas Geesteranus, 1992; Sarnari, 1998). There was a considerable increase in species cited as mycorrhizae of broadleafs, or specifically of beech; for example C. rufoolivaceus and Lactarius ichoratus (Marchand, 1971–1986), 190 A. Laganà et al. / Forest Ecology and Management 169 (2002) 187–202 Table 1 Synthesis of phytosociological surveys for both research periods cop. arborea % cop. arbustiva % cop. erbaacea % Abies alba Miller Acer platanoides L. Acer pseudoplatanus L. Adenostyles australis (Ten.) Nyman Aremonia agrimonioides (L.) D.C. Athyrium filix-foemina (L.) Roth. Atropa belladonna L. Campanula trachelium L. Cardamine bulbifera (L.) Crantz Cardamine chelidonia L. Cardamine heptaphylla (Vill.) O.E. Schulz Cardamine impatiens L. Cardamine kitaibelii Becherer Carex pendula Hudson Carex sylvatica Hudson Crataegus laevigata (Poiret) D.C. Cytisus scoparius (L.) Link Dactylis glomerata L. Daphne laureola L. Daphne mezereum L. Digitalis ferruginea L. Dryopteris filix-mas (L.) Schott Epilobium montanum L. Epipactis helleborine (L.) Crantz Euphorbia amygdaloides L. Fagus sylvatica L. Festuca heterophylla Lam. Fragaria vesca L. Galium levigatum L. Galium odoratum (L.) Scop. Galium rotundifolium L. Geranium nodosum L. Geranium robertianum L. Helleborus bocconei Ten. Hieracium gr. Murorum Luzula nivea (L.) Lam. et D.C. Malus sylvestris Miller Melica uniflora Retz. Milium effusum L. Mycelis muralis (L.) Dumort. Myosotis caespitosa C.F. Schultz Myosotis sylvatica Hoffm. ssp. subarvensis Grau Orchis maculata L. Oxalis acetosella L. Polysticum setiferum (Forsskal) Woynar Prenanthes purpurea L. Pteridium aquilinum (L.) Kuhn. Quercus cerris L. Rubus hirtus W. et K. Station 1 (1986) Station 1 (1998) Station 2 (1986) Station 2 (1998) 60 40 60 70 30 60 70 50 70 70 25 80 3 þ 3 þ 4 4 2 1 1 2 2 þ þ 1 þ 1 þ þ þ 2 1 þ þ þ 1 þ þ þ 1 þ 1 þ þ þ 1 1 þ þ þ þ þ þ þ þ þ þ þ þ þ þ 3 þ 3 1 1 2 1 þ 2 1 1 1 þ þ þ þ 1 1 1 1 2 þ 1 þ þ þ þ þ 1 þ þ þ 1 þ þ 1 þ þ þ þ 1 þ 1 þ 1 2 þ 2 þ 2 þ þ þ þ þ þ þ 2 1 þ þ 1 þ 1 þ þ þ þ 1 þ 1 2 1 þ 1 þ þ þ þ þ 3 1 þ 1 191 A. Laganà et al. / Forest Ecology and Management 169 (2002) 187–202 Table 1 (Continued ) Station 1 (1986) Rubus idaeus L. Salvia glutinosa L. Sambucus nigra L. Sanicula europaea L. Saxifraga rotundifolia L. Senecio fuchsii Gmelin. Silene dioica (L.) Clairv. Solidago virga-aurea L. Sorbus aucuparia L. Stachys sylvatica L. Stellaria nemorum L. Thalictrum aquilegifolium L. Urtica dioica L. Valeriana tripteris L. Veronica montana L. Viola reichenbachiana Jordan 2 þ 2 þ þ þ Station 1 (1998) 2 3 þ þ þ þ þ þ þ þ 1 þ 1 found in abundance at station 2. A number of species did not appear in the more recent survey; these included Cystoderma carcharias, Hymenoscyphus serotinus, Marasmius alliaceus, M. androsaceus, R. viscida and Xerula radicata, which were present at station 1 from 1986 to 1989, M. haematopus, characteristic of station 2, Clavulina coralloides and Lachnellula subtilissima, which seem to have disappeared gradually from both stations. A substantial decrease in the number of fungal species, especially symbionts, has recently been reported in ecosystems of central and northern Europe damaged by various types of pollution (Arnolds, 1987; Schlechte, 1987; Fellner, 1993; Boujon, 1997). A direct relation has been postulated between the percentage of mycorrhizal species (mycorrhizal ratio, M%) and the degree of forest disturbance: 40% < M < 60% latent disturbance; 20% < M < 40% acute disturbance; M < 20% lethal disturbance (Fellner, 1985, 1987; Schlechte, 1987; Fellner and Soukup, 1991). Fig. 2 shows the percentage of mycorrhizal species in the two stations in the 5 years of the study. At first sight, we see a low value of M% in all years, especially at station 1. This may simply be due to altitude or type of vegetation, as reported by Laganà et al. (1999); the plots, in fact, are in a nature reserve in a protected area (Casentino Forests), they have low human impact and are far from industrial centers. More important, however, is the pattern of the mycorrhizal ratio during the study period. No decrease in symbiont species is Station 2 (1986) Station 2 (1998) 1 þ þ 3 þ 3 þ 3 2 þ 3 1 þ þ þ þ þ þ þ 1 1 þ 1 observed, perhaps a small increase. Relevant factors could be stand history and the age of fir and beech (Dighton et al., 1986). As the phytosociological study showed, the cover of these two trees has changed to some extent, especially in the planted plot (station 2). The interactions between fir and beech have probably changed as well, and one of the many consequences may have been a change in the fungal community, especially the mycorrhizal component. It would be interesting to evaluate even the role of other parameters, such as tree number and size, either for beech or for silver fir, but no such informations were collected during past researches in the two studied plots. The first two axes emerging from CA (Fig. 3) explain 38.8 and 24.4% of the total variance. Axis 1, along which the relevé carried out at station 2 in 1998 is distanced from the others, may be regarded as a gradient of soil pH. In the quadrants positive with respect to this axis, we find species typical of neutral– basic soils, such as C. dyonisae, C. rufoolivaceus, Inocybe flocculosa, L. ichoratus, R. queletii and R. urens (Romagnesi, 1967; Marchand, 1971–1986; Stangl, 1991). Axis 2, along which the relevés carried out in both stations in 1998 are considerably distanced from the others, may be interpreted as a gradient of forest maturity. Species that seem to characterize relevé 1e (station 1, 1998) at the positive extreme of axis 2, are in fact mostly lignicolous saprotrophs (M. epipterygia, P. fascicularis, Gymnopilus sapineus, 192 Table 2 Synthesis of mycocoenological surveysa Species Sh Sw Sw Sw Sw M Sw M M Sh(M) Sh(M) Sl Sl(Sh) Sl Sl Sh Sh Sl Sl Sl(P) Sl(P) Sh Sh Sw Sw M M M M M M M M M M Sw Sh Sh Agaricus luteomaculatus (F.H. Möller) F.H. Möller Ascocoryne cylichnium (C. Tul.) Korf. Bertia moriformis (Tode:Fr.) De Not. Bisporella citrina (Batsch:Fr.) Korf and Carpenter Bisporella subpallida (Rehm) Dennis Boletus ferrugineus Schaeff. Calocera viscosa (Pers.:Fr.) Fr. Caloscypha fulgens (Pers.) Boud. Cantharellus cibarius Fr.:Fr. Clavulina coralloides (L.:Fr.) J. Schröt. ss. str. Clavulina rugosa (Fr.) J. Schröt. Clitocybe fragrans (With.:Fr.) P. Kumm. Clitocybe geotropa (Lam. and D.C.) Quél. Clitocybe gibba (Pers.:Fr.) P. Kumm. Clitocybe marginella Harmaja (Moser, 1983) Clitocybe rivulosa (Pers.:Fr.) P. Kumm. ss. str. Clitocybe sinopica (Fr.:Fr.) P. Kumm. Clitocybe trullaeformis (Fr.:Fr.) Quél. Collybia butyracea (Bull.:Fr.) P. Kumm. Collybia cookei (Bres.) J.D. Arnold Collybia tuberosa (Bull.:Fr.) P. Kumm. Conocybe pilosella (Pers.:Fr.) Kühner Conocybe tenera (Schaeff.:Fr.) Fayod Coprinus atramentarius (Bull.:Fr.) Fr. ss. str. Coprinus micaceus (Bull.:Fr.) Fr. ss. str. Cortinarius cinnamomeus (L.:Fr.) Fr. ss. str. Cortinarius dionysae R. Henry (Moser, 1983) Cortinarius elegantior Fr. (Moser, 1983) Cortinarius erythrinus (Fr.) Fr. Cortinarius infractus (Pers.:Fr.) Fr. Cortinarius lividoochraceus (Berk.) Berk. Cortinarius multiformis Fr. var. coniferarum M.M. Moser Cortinarius rufoolivaceus (Pers.:Fr.) Fr. (Brandrud et al., 1990–1994) Cortinarius uraceus Fr. ss. J.E. Lange Craterellus cornucopioides (L.:Fr.) Pers. Crepidotus cesatii (Rabenh.) Sacc. var. cesatii Cystoderma amianthinum (Scop.) Fayod ss. str. Cystoderma carcharias (Pers.) Fayod Station Station Station Station Station Station Station Station Station Station 1(1986) 1 (1987) 1 (1988) 1 (1989) 1 (1998) 2(1986) 2 (1987) 2 (1988) 2 (1989) 2 (1998) 2 4 6 5 4 2 4 5 3 4 3 2 5 3 4 4 6 2 3 2 2 2 3 3 1 3 4 1 2 2 3 1 2 2 1 2 2 3 2 1 2 1 1 1 1 2 1 2 1 2 2 2 6 3 3 4 4 1 1 3 5 5 4 5 5 2 3 3 3 2 3 2 5 2 2 4 2 1 2 1 2 A. Laganà et al. / Forest Ecology and Management 169 (2002) 187–202 TG Dacrymyces stillatus Nees:Fr. ss. str. Exidia thuretiana (Lév.) Fr. Galerina badipes (Fr.) Kuhner Galerina marginata (Batsch) Kühner ss. str. Galerina stylifera (G.F. Atk.) A.H. Sm. and Singer Gerronema strombodes (Berk. and Mont.) Singer (Moser, 1983) Gymnopilus sapineus (Fr.:Fr.) Maire Helvella crispa (Scop.:Fr.) Fr. Helvella elastica Bull.:Fr. Hemimycena gracilis (Quél.) Singer Hemimycena lactea (Pers.:Fr.) Singer Hydnum repandum L.:Fr. Hygrocybe virginea (Wulfen:Fr.) P.D. Orton and Watling Hygrophorus chrysodon (Batsch:Fr.) Fr. (Moser, 1983) Hygrophorus discoxanthus (Fr.) Rea Hygrophorus pudorinus (Fr.:Fr.) Fr. Hymenoscyphus scutula (Pers.:Fr.) W. Phillips Hymenoscyphus serotinus (Pers.:Fr.) W. Phillips Inocybe assimilata (Britzelm.) Sacc. Inocybe cervicolor (Pers.) Quél. Inocybe flocculosa (Berk.) Sacc. Inocybe fuscidula Velen. Inocybe geophylla (Fr.:Fr.) P. Kumm. Inocybe geophylla (Fr.:Fr.) P. Kumm. var. lilacina (Peck) Gillet Inocybe whitei (Berk. and Broome) Sacc. Laccaria amethystina (Huds.) Cooke Laccaria laccata s.l. Lachnellula subtilissima (Cooke) Dennis Lachnum bicolor (Bull.:Fr.) P. Karst. Lactarius ichoratus (Batsch) Fr. Lactarius piperatus (L.:Fr.) Pers. Lactarius salmonicolor R. Heim and Leclair (Moser, 1983) Lactarius subdulcis (Bull.:Fr.) Gray Lycoperdon atropurpureum Vittad. (Julich, 1989) Lycoperdon perlatum Pers.:Pers. Macrolepiota procera (Scop.:Fr.) Singer Marasmius alliaceus (Jacq.:Fr.) Fr. (Antonin and Noordel., 1993) Marasmius androsaceus (L.:Fr.) Fr. Marasmius bulliardii Quél. Marasmius cohaerens (Pers.:Fr.) Cooke and Quél. Marasmius rotula (Scop.:Fr.) Fr. Marasmius torquescens Quél. Marasmius wynnei Berk. and Broome 6 5 3 5 3 5 6 6 5 2 1 4 4 2 2 1 3 3 6 6 6 4 4 1 3 2 2 5 5 1 1 3 3 1 2 1 1 4 1 1 1 5 6 3 5 4 4 6 5 4 1 3 4 4 2 1 5 4 2 4 2 3 2 9 7 3 6 4 3 1 3 4 4 4 4 4 1 3 4 3 3 5 3 4 1 4 9 4 5 1 3 5 3 4 1 4 3 4 4 4 4 3 3 3 4 3 1 2 3 2 5 3 2 1 1 5 4 2 1 3 2 4 4 1 3 2 1 2 3 4 4 A. Laganà et al. / Forest Ecology and Management 169 (2002) 187–202 Sw Sw Sw Sw Sw(Sl) Sw Sw Sh Sh Sl Sl M Sh M M M Sl Sw M M M M M M M M M Sw Sw M M M M Sh Sh Sh Sl Sl Sl Sl Sw Sl(Sw) Sl 1 1 4 2 2 2 193 194 Table 2 (Continued ) TG Mollisia fusca (Pers.:Fr.) P. Karst. Mycena amicta (Fr.:Fr.) Quél. Mycena aurantiomarginata (Fr.:Fr.) Quél. Mycena citrinomarginata Gillet Mycena crocata (Schrad.:Fr.) P. Kumm. Mycena epipterygia (Scop.:Fr.) Gray Mycena epipterygia (Scop.:Fr.) Gray var. lignicola A.H. Smith Mycena epipterygia (Scop.:Fr.) Gray var. viscosa (Maire) Ricken Mycena erubescens Höhn. Mycena filopes (Bull.:Fr.) P. Kumm. ss. str. Mycena flavoalba (Fr.) Quél. Mycena haematopus (Pers.:Fr.) P. Kumm. Mycena leptocephala (Pers.:Fr.) Gillet Mycena metata (Fr.:Fr.) P. Kumm. Mycena polyadelpha (Lasch) Kühner Mycena pura (Pers.:Fr.) P. Kumm. Mycena sanguinolenta (Alb. and Schwein.:Fr.) P. Kumm. Mycena sepia J.E. Lange Mycena vitilis (Fr.) Quél. Mycena xantholeuca Kühner Mycena zephirus (Fr.:Fr.) P. Kumm. Panellus mitis (Pers.:Fr.) Singer Panellus violaceofulvus (Batch:Fr.) Singer (Courtecuisse and Duhem, 1994) Sw Pholiota lenta (Pers.:Fr.) Singer Sw Pluteus cervinus (Schaeff.) P. Kumm. Sl Pseudoclitocybe cyathiformis (Bull.:Fr.) Singer Sw Pseudohydnum gelatinosum (Scop.:Fr.) P. Karst. (Breitenbach and Kranzlin, 1986) Sw(Sl) Psilocybe aeruginosa (M.A. Curtis:Fr.) Noordel ss. str. Sw Psilocybe fascicularis (Huds.:Fr.) Noordel. Sl Rickenella fibula (Bull.:Fr.) Raithelh. M Russula albonigra (Krombh.) Fr. M Russula chloroides (Krombh.) Bres. M Russula cyanoxantha Schaeff.:Fr. M Russula delica Fr. ss. str. M Russula fragilis (Pers.:Fr.) Fr. ss. str. M Russula laurocerasi Melzer var. fragrans (Romagn.) Kuyper and Vuure Station Station Station Station Station Station Station Station Station Station 1(1986) 1 (1987) 1 (1988) 1 (1989) 1 (1998) 2(1986) 2 (1987) 2 (1988) 2 (1989) 2 (1998) 2 2 4 2 2 2 5 2 4 2 5 1 5 1 2 3 3 3 5 2 3 4 4 6 1 2 4 3 4 2 6 4 2 3 2 2 5 1 1 1 3 3 2 1 3 3 2 2 4 4 4 4 1 4 2 3 2 2 3 3 1 1 4 1 3 1 2 1 3 3 1 1 6 5 3 2 2 4 5 5 1 5 4 5 5 2 2 3 4 2 4 5 4 1 2 2 1 2 1 2 4 1 6 2 2 5 2 3 1 2 1 1 3 1 1 1 3 2 3 2 2 A. Laganà et al. / Forest Ecology and Management 169 (2002) 187–202 Sw Sl Sl Sl Sw Sl Sw Sl Sw Sl(Sw) Sl Sw Sl(Sw) Sl Sl Sl Sl Sl Sw Sw/Sl Sh Sw Sw Species a Russula melliolens Quél. Russula queletii Fr. ss. str. Russula urens Romell. Russula viscida Kudrna Sphaerobolus stellatus Tode:Pers. Tremella mesenterica Retz.:Fr. Tricholoma saponaceum (Fr.:Fr.) P. Kumm. Tricholomopsis rutilans (Schaeff.:Fr.) Singer Tubaria hiemalis Bon Xerula melanotricha Dörfelt (Breitenbach and Kranzlin, 1991) Xerula radicata (Relhan:Fr.) Dörfelt Xylaria hypoxylon (L.:Fr.) Grev. Xylaria longipes Nitschke 2 3 3 3 2 1 1 1 4 1 2 1 3 3 4 3 3 2 3 5 1 5 2 5 M: mycorrhizal; Sh: humicolous; Sl: litter saprotrophe; Sw: saprotrophe on wood; P: parasite. 2 6 5 2 1 2 3 4 3 3 2 1 A. Laganà et al. / Forest Ecology and Management 169 (2002) 187–202 M M M M Sw Sw M Sw Sw(Sl) Sw Sw(P) Sw Sw 195 196 A. Laganà et al. / Forest Ecology and Management 169 (2002) 187–202 Fig. 2. Percentage of mycorrhizal macromycetes observed in the two studied stations during each year of study. Galerina badipes and Pseudohydnum gelatinosum); their increase over the years is certainly related to the increased availability of substrate due to tree damage caused by heavy snow and the lower resistance of old wood to attack by fungal parasites. Note also the position of Tricholoma saponaceum, a late-stage species (Keizer, 1993). Relevé 2e (station 2, 1998) is near the positive extreme of both axes. It seems characterized by basophilous species and species linked to broadleafs or specifically beech (C. rufoolivaceus, L. ichoratus). This may be an indicator of the maturity of this artificial wood, which is evolving towards a more natural state, as shown by the increase in beech cover, especially in the shrub layer, the increase in nemoral and mesophilous herbs and the decrease in ruderal and nitrophilous species. The qualitative and quantitative changes observed in fungal communities of the two stations, therefore, seem at least partly due to succession phenomena. By continuing the research for a longer period, it will be possible to investigate this aspect in greater depth and reach more definitive conclusions. The graph of Fig. 4 was plotted to evaluate the periodicity with which the fungal species appear during the year and fluctuations from year to year. The number of species found in each station is shown against mean monthly temperature and monthly rainfall relevéd at the weather station at Badia Prataglia. The difference in number between the two stations may be due to different reactions to temperature and rainfall of the two areas, which differ in vegetation, slope, and forest origin. With regard to periodicity, we see that the greatest number of species is found in autumn (September– November) when there is usually abundant rain and mild temperatures. This is in accordance with Perini et al. (1989) and Barluzzi et al. (1992). A minor peak was generally also observed in spring and sometimes in summer. If we consider the general pattern of A. Laganà et al. / Forest Ecology and Management 169 (2002) 187–202 197 Fig. 3. Results of CA (1a–e: station 1 relatively in 1986–1989, and 1998; 2a–e: station 2 relatively in 1986–1989, and 1998). Only species useful for interpretation of axes are reported. species number during the whole study period, we see that 1989 and 1998 were the poorest years. This is particularly true for station 1. In 1988, 1989 and 1998, rainfall was less than in the previous years (1781 mm in 1986; 1696 mm in 1987; 1150 mm in 1988; 1471 mm in 1989; 1218 mm in 1998). However, the number of species found in autumn 1988 was very high (Fig. 4), considering the scarcity of rain in respect to the other years, especially in October (68 mm). The situation is, therefore, complex with many parameters to consider. The following observations can be made: 1987 was a very wet year (1696 mm), especially autumn (September–December 765 mm); the first months of 1988 were much wetter than those of 1989 and 1998 (January–March 324 mm in 1988 versus 190 mm in 1989 and 201 mm in 1998); the number of rainy days in 1989 and 1998 (109 and 115, respectively) was much lower, especially in autumn, than in the previous years (140 mm in 1986, 144 mm in 1987 and 145 mm in 1988); in October 1988, the mean monthly temperature was 13.5 8C whereas in 1989 and 1998 it was much lower (10.6 and 10.9 8C, respectively, the lowest recorded in the study period); the minimum temperatures in October were much lower in 1989 and 1998 (4.0 and 6.4 8C) than in 1988 (8.1 8C). It is not a simple task to interpret this data or to understand how the various meteorological parameters interact to influence fruiting of the fungal mycelium. It would be interesting to have soil moisture data, as it is probably not so much rainfall as the amount of water the soil retains, that influences mycelial productivity. This would explain why many species were observed in 1988 (in 1987, rainfall was abundant and substantially continuous; spring 1988 198 A. Laganà et al. / Forest Ecology and Management 169 (2002) 187–202 Fig. 4. Relation between species number, MMT and MR in the two studied stations. was wet, unlike those of the following years; autumn 1988 had the greatest number of rainy days although annual rainfall was lowest) and why station 2 seems to have been affected less than station 1 by drought in 1989 and 1998 (being less inclined, it presumably absorbs more water). Mean monthly temperature is certainly important but is difficult to interpret. Fig. 5 shows the number of carpophores found each month in each station against temperature and rainfall. The greatest number of carpophores was observed in autumn, with minor spring peaks. The numbers are largely made up of lignicolous saprotrophs that fruit abundantly (L. subtilissima and Xylaria hypoxylon). Fig. 5 is particularly complex to interpret. Abundance of carpophores is closely linked to the intrinsic characteristics of each species, as well as meteorological parameters, since some taxa (such as saprotrophs of wood and litter) fruit in large numbers whereas others only form isolated carpophores. In general, we see that a large number of species in Fig. 4 corresponds to a large number of carpophores in Fig. 5, except in 1989 when there were few taxa at station 1 but a large number of carpophores; in other words, few species but abundant carpophores. The interesting fact is that these were not only saprotrophs that by nature fruit abundantly, but also mycorrhizal fungi such as Cantharellus cibarius, Craterellus cornucopioides, Hygrophorus pudorinus, Laccaria amethystina, L. laccata, R. viscida and T. saponaceum. Many of these species fruit fairly abundantly, but in 1989 their productivity was particularly high (4–6 mDCy). These species seem to be particularly resistant to climatic stress, which seems to favor them with respect to other species. C. cibarius had previously been found only once, with abundance 2, and it was the first finding of C. cornucopioides and T. saponaceum at station 1. The number of carpophores of R. delica, Helvella crispa, M. androsaceus and M. flavoalba was very low or zero in 1989 and 1998, suggesting that they are very sensitive to climatic stress. Statistical analysis for direct correlations between meteorological parameters and fungal fruiting (Table 3) showed that in both stations, number of species and number of carpophores were negatively correlated A. Laganà et al. / Forest Ecology and Management 169 (2002) 187–202 Fig. 5. Relation between number of carpophores, MMT and MR in the two studied stations. 199 200 Table 3 Results of correlation analysisa of of of of of of of of of of of of of of of of of of of of of of of of species at station 1 species at station 2 carpophores at station 1 carpophores at station 2 M species at station 1 M species at station 2 M carpophores at station 1 M carpophores at station 2 Sh species at station 1 Sh species at station 2 Sh carpophores at station 1 Sh carpophores at station 2 Sl species at station 1 Sl species at station 2 Sl carpophores at station 1 Sl carpophores at station 2 Sw species at station 1 Sw species at station 2 Sw carpophores at station 1 Sw carpophores at station 2 asco species at station 1 asco species at station 2 asco carpophores at station 1 asco carpophores at station 2 MR High. MT Low. MT Abs. low. Abs. high. DT >108 RD 0.39** 0.52*** 0.61*** 0.48*** 0.33* 0.68*** 0.16 N.S. 0.38** 0.19 N.S. 0.65*** 0.04 N.S. 0.60*** 0.21 N.S. 0.29 N.S. 0.25 N.S. 0.03 N.S. 0.56*** 0.07 N.S. 0.69*** 0.29 N.S. 0.31* 0.13 N.S. 0.23 N.S. 0.13 N.S. 0.47*** 0.35* 0.50*** 0.05 N.S. 0.23 N.S. 0.23 N.S. 0.23 N.S. 0.17 N.S. 0.46** 0.24 N.S. 0.06 N.S. 0.01 N.S. 0.49*** 0.22 N.S. 0.48*** 0.06 N.S. 0.44** 0.43** 0.28* 0.26* 0.24* 0.37** 0.26* 0.20 N.S. 0.44** 0.56*** 0.03 N.S.b 0.53*** 0.37* 0.70*** 0.04 N.S. 0.54*** 0.23 N.S. 0.60*** 0.30* 0.66*** 0.27 N.S. 0.38** 0.13 N.S. 0.04 N.S. 0.59*** 0.01 N.S. 0.19 N.S. 0.09 N.S. 0.21 N.S. 0.01 N.S. 0.10 N.S. 0.03 N.S. 0.27 N.S. 0.39** 0.13 N.S. 0.40*** 0.24 N.S. 0.57*** 0.08 N.S. 0.43*** 0.10 N.S. 0.64*** 0.26* 0.65*** 0.10 N.S. 0.11 N.S. 0.21 N.S. 0.10 N.S. 0.43** 0.13 N.S. 0.07 N.S. 0.26* 0.09 N.S. 0.10 N.S. 0.01 N.S. 0.10 N.S. 0.38* 0.36* 0.12 N.S. 0.36** 0.36* 0.49*** 0.15 N.S. 0.47*** 0.30* 0.35* 0.42*** 0.62*** 0.18 N.S. 0.12 N.S. 0.20 N.S. 0.09 N.S. 0.54*** 0.01 N.S. 0.06 N.S. 0.30* 0.07 N.S. 0.09 N.S. 0.02 N.S. 0.09 N.S. 0.37* 0.54*** 0.19 N.S. 0.56*** 0.32* 0.67*** 0.04 N.S. 0.50*** 0.10 N.S. 0.64*** 0.18 N.S. 0.64*** 0.19 N.S. 0.46** 0.06 N.S. 0.14 N.S. 0.58*** 0.10 N.S. 0.34** 0.01 N.S. 0.21 N.S. 0.02 N.S. 0.14 N.S. 0.05 N.S. 0.01 N.S. 0.08 N.S. 0.19 N.S. 0.32** 0.09 N.S. 0.33* 0.17 N.S. 0.40*** 0.03 N.S. 0.30 N.S. 0.39*** 0.57*** 0.15 N.S. 0.22 N.S. 0.36** 0.02 N.S. 0.16 N.S. 0.33* 0.01 N.S. 0.20 N.S. 0.06 N.S. 0.15 N.S. 0.03 N.S. 0.14 N.S. 0.03 N.S. 0.01 N.S. 0.48*** 0.38*** 0.24 N.S. 0.07 N.S. 0.11 N.S. 0.57*** 0.12 N.S. 0.16 N.S. 0.16 N.S. 0.39*** 0.13 N.S. 0.15 N.S. 0.14 N.S. 0.11 N.S. 0.02 N.S. 0.15 N.S. 0.33* 0.14 N.S. 0.09 N.S. 0.03 N.S. 0.05 N.S. 0.09 N.S. a MMT: mean monthly temperature; MR: monthly rainfall; high MT: highest monthly temperature; low MT: low monthly temperature; abs. low.: absolute lowest temperature; abs. high: absolute highest temperature; DT >10 8C: number of days with temperature higher than 10 8C; RD: number of rainy days. b N.S.: not significant. * P < 0:05. ** P < 0:01. *** P < 0:001. A. Laganà et al. / Forest Ecology and Management 169 (2002) 187–202 Number Number Number Number Number Number Number Number Number Number Number Number Number Number Number Number Number Number Number Number Number Number Number Number MMT A. Laganà et al. / Forest Ecology and Management 169 (2002) 187–202 with mean monthly temperature (MMT) in the interval 10 C < MMT < 20 8C. A negative correlation with MMT was also obtained for number of mycorrhizal species (station 1: r ¼ 0:33, P < 0:05; station 2: r ¼ 0:68, P < 0:001), saprotrophs of humus at station 2 (r ¼ 0:65, P < 0:001), saprotrophs of wood at station 1 (r ¼ 0:56, P < 0:001), number of mycorrhizal carpophores at station 2 (r ¼ 0:38, P < 0:01), number of carpophores of humicolous saprotrophs at station 2 (r ¼ 0:60, P < 0:001) and number of carpophores of lignicolous saprotrophs at station 1 (r ¼ 0:69, P < 0:001). Monthly rainfall (MR) showed a negative correlation with number of species in both stations (station 1: r ¼ 0:47, P < 0:001; station 2: r ¼ 0:35, P < 0:05) but a positive correlation with carpophore number at station 1 (r ¼ 0:50, P < 0:001), as reported by other authors (Wilkins and Patrick, 1940; Wilkins and Harris, 1946; Thoen, 1976). Table 3 also indicates that extreme temperatures, both high and low, almost invariably inhibit fungal fruiting, as reflected by number of species and number of carpophores. As hypothesized above, the number of rainy days seems to be an important factor, and was found to be correlated positively with carpophore number. However, as stated by Arnolds (1988), it is very difficult to identify simple correlations between weather parameters and fungal fruiting. 5. Conclusions In this study useful indications were obtained regarding the mechanisms regulating temporal changes in the fungal community. On a short time scale, weather parameters clearly play a major role but statistical analysis failed to indicate simple direct relations between them and fungal fruiting. It has been strongly established in the literature that only weather data, such as rainfall and air temperature, do not explain the trend of fungal fruiting and hence temporal changes and fungal dynamics. Many other parameters are involved (Senn-Irlet and Bieri, 1999) which make even sophisticated models not work. On a long time scale (10 years or more), correspondence analysis indicated that vegetation parameters, 201 forest age and forest history affect successions. An important role is probably the one of soil microbiological conditions, surely different in stands with such a different history (station 2 was planted on what was previously a natural pasture while station 1 is a natural fir wood), but no data on this topic was reported by Perini et al. (1995) for the period 1986– 1989. Forest ageing and forest evolution towards climax have a considerable influence on the fungal component, especially mycorrhizal species, which are intrinsically linked to the vegetation. This was particularly evident in the planted forest (station 2), which was found to be evolving towards a more natural state. Acknowledgements The authors thank the Ministry of Agricultural Policy Office at Pratovecchio for meteorological data for Badia Prataglia. References Arnolds, E., 1981. Ecology and coenology of microfungi in grasslands and moist heathlands in Drenthe, The Netherlands. Part 1. Introduction and synecology. Bibl. Mycol. 83, 1–410. Arnolds, E., 1987. Decrease of ectomycorrhizal fungi in The Netherlands in relation to air pollution. In: R. Fellner (Ed.), Ekologie mykorrhiz a mykorrhiznı́ch hub. Imise a mykorrhiza. DT CSVTS, Pardubice, pp. 72–81. Arnolds, E., 1988. Dinamics of macrofungi in two moist heathlands in Drenthe, The Netherlands. Acta Bot. Neerl. 37, 291–305. Arnolds, E., Kuyper, Th.W., Noordeloos, E.M. (Eds.), 1995. Overzicht van de paddestoelen in Nederland. Nederlandse Mycologische Verening, Wijster, 872 pp. Barluzzi, C., Perini, C., De Dominicis, V., 1992. Coenological research on macrofungi in chestnut coppices of Tuscany. Phytocoenologia 20 (4), 449–465. Becker, G., 1956. Observations sur l’écologie des champignons supérieurs. Ann. Sci. Univ. Besançon (sér. 2, Bot.) 7, 15–128. Boujon, C., 1997. Diminution des champignons mycorrhiziques dans une forêt suisse: une étude rétrospective de 1925 à 1994. Mycologia Helvetica 9 (2), 117–132. Braun-Blanquet, J., 1964. Pflanzensoziologie. Grundzüge der Vegetationskunde. Wien, 864 pp. Brummitt, R.K., Powell, C.E. (Eds.), 1992. Authors of Plant Names. Royal Botanic Gardens, Kew, 732 pp. Bujakiwicz, A., 1969. Udzial grzybow wyzszych w lasach Xegowych i olesach puszczy bukowej pod Szczecinem. Badan. Fizjograf. nad Polska Zachodnia 23, 61–96. 202 A. 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An investigation into the influence of rainfall and temperature on the seasonal production of fungi in a beechwood and a pinewood. Ann. Appl. Biol. 33, 179–188.

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