(2014). Concordance Between Vascular

Research Article - doi: 10.3832/ifor1199-008 ©iForest – Biogeosciences and Forestry

of great help in quantifying biological diver- Concordance between vascular plant and sity for less well-known groups and less easily detectable taxa (Pharo et al. 1999, macrofungal community composition in Schmit et al. 2005, Öster 2008, Qian & Ricklefs 2008). Moreover, the possibility of broadleaf deciduous forests in central Italy high congruence between different taxa, which is extremely interesting from an ecological viewpoint, can reduce the time and (1-2) (2) (2) (2) Marco Landi , Elena Salerni , Elia Ambrosio , Maria D’Aguanno , costs necessary for planning conservation ac- Alessia Nucci (2), Carlo Saveri (1), Claudia Perini (2), Claudia Angiolini (2) tions, although no single biotic group shows a perfect match with any other. The “taxon surrogacy” hypothesis (Ryti 1992) is based We examined the concordance between vascular plants and macrofungi on the assumption of concordance among (grouped into trophic groups) in Mediterranean forest habitats (central Italy). species richness or patterns of community Our goal was to test how consistently plant and fungi groups classify plots in a composition across different taxonomic broadleaf deciduous forest dominated by Quercus cerris. Our hypothesis was groups (Virolainen et al. 2000, Su et al. that groups of plants can be used as surrogates for the classification of macro- 2004). Nevertheless, the selection of surro- fungal communities. The test of concordance comprised two steps: (1) the gate taxonomic groups is not straightfor- plant species data sets were subjected to cluster analysis, to obtain three clas- ward, and different methods have been ap- sifications based on presence of all plants, presence and frequency of only plied by various authors. In fact, over the woody species; (2) Multiple Response Permutation Procedures (MRPP) was used last 20 years, conservation biologists have to test the performance of each plant classification applied to the fungi data discussed the use of surrogate species in sets. Sample scores on the first PCA axis were used to investigate the relation- conservation planning at great length, deba- ships between compositional patterns. In the concordance analysis, the classifi- ting both the advantages and disadvantages cation based on woody plants only provided better results than the classifica- of this approach (Murphy et al. 2011). There tion obtained using both herbaceous and woody plants. Cross-tests gave the are several different types of surrogacy (Ma- best results when the “woody plants” classification was applied to ectomycor- gurran 2004), such as: (i) cross-taxon, where rhizal fungi (EMF) and, to a certain extent, to humicolous saprotrophs (Sh). high species richness in one taxon is used to The ordination analysis suggested that the frequency of woody plants follows a infer high species richness in others (Mortiz similar spatial distribution to EMF and Sh fungal groups and is therefore ex- et al. 2001); (ii) within-taxon, where generic pected to covariate along the same environmental gradients. Many EMF exhibit or familial richness is treated as a surrogate preferences for few (one or two) hosts. Significant associations were found of species richness (Balmford et al. 1996); among numerous EMF and woody plant species. Woody plants such as Sorbus and (iii) environmental, where parameters domestica and Prunus spinosa appear to be associated with many EMF. The such as temperature or topographical diver- combination of a high frequency of Fraxinus oxycarpa and Quercus petraea sity are assumed to reflect species richness seems to promote distinct assemblages of EMF and Sh fungi. Characteristic as- (Magurran 2004). Another approach is based semblages of fungi were found in association with certain tree and shrub com- on “community concordance” and describes binations. the degree to which patterns in community structure in a set of sites are similar in two Keywords: Deciduous Oaks, Ectomycorrhizal Fungi, Host Specificity, Sapro- different taxonomic groups (Paszkowski & trophic Fungi, Surrogates, Trophic Groups Tonn 2000). This method has been applied rarely, and mainly in aquatic ecosystems (Paszkowski & Tonn 2000, Paavola et al. Introduction on natural ecosystems has brought with it an 2003, Heino & Mykrä 2006, Landi et al. Finding strategies to identify the state of urgent need for the development of simple, 2012). biodiversity and to develop appropriate con- quick and cost-effective methodologies for According to various authors, vascular flo- servation and monitoring programs is one of quantifying and monitoring changes in bio- ra has a great potential to determine the di- the most important issues in the field of ecological diversity (Berglund & Jonsson 2001, versity of other groups because it constitutes logy (Gaston 2000, Berglund & Jonsson Heino & Mykrä 2006, Santi et al. 2010). the bulk of total biomass and provides physi- 2001, Similä et al. 2006). The growing im- Surrogate species, whose primary purpose cal structure for other ecosystem components pact of human activities that contribute to is to ascertain and test which groups of orga- (fauna and ecological processes) through the habitat fragmentation and decrease diversity nisms reflect the diversity of others, can be establishment of vegetation (Ryti 1992, Young 2000, Öster 2008). In addition, a (1) Ufficio Territoriale per la Biodiversità di Siena, Corpo Forestale dello Stato, v. Cassia long tradition and much experience has been Nord 7, I-53100 Siena (Italy); (2) Department of Life Sciences, University of Siena, v. P.A. gained in the sampling of vascular plants, Mattioli 4, I-53100 Siena (Italy) relatively easy to perform, and plant taxonomy is sufficiently well described and stan- @ Claudia Perini ([email protected]) dardized as well (Sætersdal et al. 2003, Chiarucci et al. 2005, Schmit et al. 2005). Received: Dec 10, 2013 - Accepted: May 15, 2014 Because fungi are heterotrophic organisms Citation: Landi M, Salerni E, Ambrosio E, D’Aguanno M, Nucci A, Saveri C, Perini C, Angiolini mainly dependent on vascular plants, the C, 2014. Concordance between vascular plant and macrofungal community composition in existence of a relationship between the com- broadleaf deciduous forests in central Italy. iForest (early view): e1-e8 [online 2014-08-22] position of plant and fungal communities has URL: http://www.sisef.it/iforest/contents/?id=ifor1199-008 been hypothesized (Chiarucci et al. 2005). Coherently, consistent correlations have Communicated by: Alberto Santini

© SISEF http://www.sisef.it/iforest/ e1 iForest (early view): e1-e8 Landi M et al. - iForest (early view): e1-e8 been found between macrofungi and patterns Palazzo (43° 20′ N, 11° 04′ E) and Cornoc- absence and frequency of the following tro- of vascular plants (Brussaard et al. 2001, chia (43° 23′ N, 11° 10′ E). The reserves co- phic groups: (i) EMF, ectomycorrhizal fungi; Packham et al. 2002). However, among the ver about 800 ha of meadows and pastures (ii) Sh, humicolous saprotrophs; (iii) Sl, lit- taxa investigated macrofungi are generally on hillsides, with a slope of about 15-25 de- ter saprotrophs; (iv) Sw, lignicolous sapro- overlooked and rarely considered in reserve grees and elevation from 330 to 530 m a.s.l. trophs; and (v) P, parasites. Coprophilous planning because of their small size, their The two areas are similar in terms of bedrock saprotrophs were absent. The above appro- ephemeral fruit bodies, their difficult identi- (limestone, sandstone and siltstone), near- ach was adopted because many macrofungi fication, and the paucity of expertise con- neutral soils, and forest type, composition are related to woody plant species by their cerning their taxonomy and ecology (Hawks- and density. No logging or harvesting have trophic requirements and trophic groups may worth 1991, Chiarucci et al. 2005, McMul- been carried out in either reserve in the last be strongly shaped by forest composition lan-Fisher et al. 2009). Nevertheless, their 40 years. The climate is Mediterranean and and structure (e.g., mycorrhizal species and inclusion in conservation planning and ma- characterized by a dry summer and rain in many saprotrophic fungi - Roberts et al. nagement is important because of their vital spring and autumn; the hottest months are 2004, De Bellis et al. 2006, Santos-Silva et functional roles in ecosystems (Lodge et al. July-August and the coldest January-Februa- al. 2011). 2004, Öster 2008, McMullan-Fisher et al. ry. The mean annual precipitation is approxi- Sampling of plant species was carried out 2009) and their great richness estimated mately 800 mm and the mean annual tempe- in June and July 2010, when leaves were worldwide (Hawksworth 2001). However, rature is 13.5 °C at the nearest meteorologi- fully extended. Sampling of macrofungi was while at large spatial scales communities cal station (Pentolina), situated 450 m a.s.l. conducted from April 2009 to November with high tree-species richness have been (ARSIA data for the period 1992-2006). 2011, with a higher frequency (up to once a found to have correspondingly high macro- Such sites provide a good location to study month) from September to December, when fungal species richness (Schmit et al. 2005), the relationships between fungal and plant conditions were generally optimal for fungal low correlations have been found at local communities since mushroom gathering and fruiting. Nomenclature of plant species was scales (e.g., Virolainen et al. 2000, Sætersdal timber extraction are not permitted. In addi- given according to Conti et al. (2005). Fun- et al. 2003, Similä et al. 2006, Santi et al. tion, they represent fairly well the type of na- gal species nomenclature was based on the 2010). tive forest common in the Mediterranean ba- CABI Bioscience Database of Fungal Names In this investigation we examined the con- sin and notoriously rich in fungi (Onofri et (http://www.indexfungorum.org/Names/nam cordance between vascular plants (grouped al. 2005, Salerni & Perini 2007). es.asp). as woody plants and all plants) and macrofungi (grouped into trophic groups) at the lo- Sampling design and recording of Statistical analysis cal scale, within two nature reserves in Me- plants and fungi Data collected from the two study sites diterranean forest habitats. To our knowled- Thirty 100 m2 permanent plots (10×10m, were pooled, since all plots shared similar ge, this is a new approach to specifically test marked by metal stakes in each corner) were features as for forest structure, environmen- the concordance between vascular plant and randomly placed in the deciduous broadleaf tal characteristics and history over the last 40 macrofungi communities in broadleaf deci- forests (fifteen for each reserve). The plots years. Only the EMF (ectomycorrhizal fun- duous forests. Our primary goal was to test were previously identified and mapped gi), Sh (humicolous saprotrophs) and Sw (li- how consistently plant and fungi groups (scale 1:5000) by photo-interpretation, with gnicolous saprotrophs) datasets could be classify plots in broadleaf deciduous forest a buffer zone of about 20 m around each po- used in the analysis, as Sl (litter saprotrophs) ecosystems. We hypothesized that plot grou- lygon to reduce possible edge effects. Data and P (parasites) were only present in a few ping based on plant species can be used as a were collected in each plot for all vascular plots. Accordingly, the analysis was carried surrogate for the classification of macrofun- plants (presence-absence), woody plants and out using three plant data sets and six fungal gal communities. We also investigated the fungal species (presence-absence and fre- data sets (18 combinations), following two association between plant and fungi species quency). As for vascular plants, herbs, seed- main steps. In the first step, a hierarchical for data sets showing a significant concor- lings, shrubs and trees were sampled. Woody cluster analysis using the Bray-Curtis dis- dance, through the analysis of correlation co- species frequency was obtained by counting similarity index (1 − Sørensen’s index) and efficients, to ascertain whether plant commu- the number of individuals per species per flexible beta (β = -0.25) was applied on the nity composition could be used as an “ecolo- plot, including trees or shrubs with DBH > 2 three plant species data sets following the re- gical indicator” for specific groups of fungi. cm or height > 2 m. Macrofungi were identi- commendations of McCune & Grace (2002), This information will improve managers’ fied based on morphology with the help of and three classifications were obtained based ability to plan effectively for the presence of general analytic keys and monographs (Sa- on: (1) presence/absence of all plants; (2) these important macrofungal resources in de- lerni et al. 2010). To quantify their abun- presence/absence of woody species; and (3) ciduous forest ecosystems. dance, their frequency was recorded as the frequency of woody species. number of carpophores (fruiting bodies) > 1 In the second step, Multiple Response Per- Materials and methods mm per species in each plot (Arnolds 1981). mutation Procedures (MRPP) were used to Although above-ground fruiting bodies do test the performance of each classification Study site not necessarily represent the abundance of applied to the fungi data sets. Cluster groups The study was carried out in two nearby fungi, they provide reliable information con- were subjected to a set of cross-tests on the temperate deciduous broadleaf forests cha- cerning forest diversity without excessive ef- macrofungi data sets and a cross-test was racterized by Quercus cerris, widely domi- fort and cost (Tóth & Barta 2010). Each ma- only accepted when significant (p<0.05). nant in the canopy layer, followed by Fraxi- crofungal taxon was attributed to the most Moreover, MRPP for a posteriori classifica- nus ornus and Q. pubescens. The number of likely trophic group, according to Arnolds et tion (self-test) was applied to obtain the trees with diameter at breast height (DBH) > al. (1995) and to personal field observations. “best possible” values of such statistics, for 2 cm ranged from 7 to 33 trees per 100 m2. Three data sets were then obtained for the numerical comparison with the values of the The mean density of trees was 17 ± 7 (SD) plants (presence-absence of all vascular a priori classification (cross-test). MRPP is per 100 m2. plants, presence-absence and frequency of a data-dependent permutation test that com- These sites are located in Tuscany (central woody plants) and ten data sets were obtai- pares dissimilarities within and among Italy), within the State Nature Reserves of ned from the carpophores of fungi (presence- groups, but does not require any assump-

iForest (early view): e1-e8 e2 © SISEF http://www.sisef.it/iforest/ Concordance between plant and macrofungal community

Tab. 1 - Results of the cross-test based on Multiple Response Permutation Procedures (MRPP) carried out on classifications of plants applied to trophic groups of fungi. Clusters are reported in columns and fungal groups are displayed in rows. P-values are reported for significant cross-tests only. Self-tests performed with a posteriori classification to compare A and T values obtained by MRPP are also shown. (n.s.): not significant.

Woody plants All plants Data Type Fungi Presence-absence data Frequency data Presence-absence data A T p A T p A T p Self test - 0.151 -8.972 - 0.261 -14.236 - 0.092 -8.947 - Presence-absence EMF - Ectomycorrhizal 0.020 -2.420 0.016 0.018 -2.164 n.s. 0.014 -1.684 n.s. data Sw - Lignicolous saprotrophs -0.006 0.599 n.s. -0.008 0.850 n.s. -0.006 0.583 n.s. Sh - Humicolous saprotrophs -0.004 0.419 n.s. -0.014 -1.434 n.s. -0.003 0.273 n.s. Frequency data EMF - Ectomycorrhizal 0.019 -3.149 0.005 0.013 -2.274 0.021 0.014 -1.929 0.038 Sw - Lignicolous saprotrophs 0.008 -1.036 n.s. -0.014 1.496 n.s. 0.002 -0.210 n.s. Sh - Humicolous saprotrophs 0.005 -0.621 n.s. 0.017 -2.166 0.037 0.011 -1.446 n.s. tions of multivariate normality and homo- lauer 2003). Ordination analysis was perfor- podium sylvaticum, B. rupestre, Viola alba geneity of variance to test the hypothesis of med using the CANOCO v. 4.5 software pa- and Melica uniflora. no differences among groups of sampling ckage (ter Braak & Šmilauer 2002). The po- units assessed through a Monte Carlo per- tential use of the compositional patterns of Fungal community composition mutation procedure (Zimmerman et al. 1985, vascular plant data sets as surrogates for A total of 333 macrofungal species were Biondini et al. 1988). This consists of the A those of different macrofungal data sets was found in the study plots. The three most re- statistics, which estimates the within-group tested by Spearman’s rank correlation of the presentative trophic groups were: ectomy- homogeneity (higher values indicate a high sample scores along the first PCA axis (a to- corrhizal fungi (EMF) with 157 species and degree of homogeneity), and the T statistics, tal of nine PCAs were extracted). Significant a mean number per plot of 20.6 ± 7.7 (SD); which measures the among-group separabili- (positive or negative) correlation indicates a humicolous saprotrophs (Sh) with 81 species ty (large negative value of T indicates a high concurrent variation in the species composi- and a mean number per plot of 8.3 ± 3.4; and separability of groups). When A=0, the with- tion among taxonomic groups. Furthermore, lignicolous saprotrophs (Sw) with 78 spe- in-group community heterogeneity equals Spearman’s correlation coefficient was used cies, whose mean number per plot was 11.0 that expected by chance, while if A<0 the to assess the association between plant and ± 4.4. Mycena vitilis (Sw) was the most heterogeneity exceeds that expected by chan- fungi species usng the data sets for which common species (present in 93% of plots), ce. The MRPP analysis was performed using significant concordance was found. followed by Cortinarius rigens (EMF), En- the software package PCORD (McCune & toloma rhodopolium and Rhodocollybia bu- Mefford 2011). Results tyracea (Sh). Litter saprotrophs (Sl), with 10 Ordination analysis, formerly applied to in- species, and parasites (P), with 7 species, vestigate the congruence among taxonomic Plant community composition had the lowest mean number of carpophores groups, including fungal species (Sætersdal A total of 108 plant species were found, in- (1.8 and 0.9, respectively) and were not de- et al. 2003, Similä et al. 2006, Santi et al. cluding 18 species of trees and shrubs taller tected in many plots. 2010), was used to evaluate the congruence than 2 m (woody plants). The mean number of species composition between the plant of species per plot was 27 ± 8 (SD) and that Community concordance between and the macrofungal data sets considered. To of woody plants was 4.3 ± 1.7. Concerning plants and fungi investigate the main gradients in the species trees, Quercus cerris was dominant in all The three classifications identified by clus- data for the two taxonomic groups, Detren- plots, with a higher mean number of indivi- ters analysis (see “Materials and Methods”) ded Correspondence Analysis (DCA) was duals (11.2 /100 m2) than other tree species were cut to hierarchical levels (nodes) corre- applied for each group (Hill & Gauch 1980), (such as Fraxinus ornus, Quercus pubescens sponding to three distinct groups, each con- including down-weighting of rare species. and Ulmus minor). Tall shrubs (such as Cor- taining at least 2 plots (from 5 to 19 plots for Principal Component Analysis (PCA), was nus mas, Crataegus monogyna, Juniperus each group). Among the cut levels of classi- then used to analyse the congruence of the communis and Prunus spinosa) and vines fications the percentage of information left data sets because of: (i) the relatively short (Hedera helix and Tamus communis) were had quite similar values (from 10 to 20%). length of the compositional gradients; and also frequent. The most common herbaceous The cross-test concordance analysis carried (ii) their potential use with empty samples, plants were perennials with underground tis- out revealed five significant results out of contrary to unimodal methods (Leps & Smi- sues (rhizomes and bulbs), such as Brachy- eighteen combinations (Tab. 1), and all the

Tab. 2 - Spearman’s rank correlation coefficients (ρ) between the sample scores on the first PCA axis performed on plant (columns) and fungi (rows) data sets. The variance accounted for by the first axis of each PCA is shown in brackets. (**): p<0.01; (*): p<0.05.

Woody plants All plants Variance Data set Fungi Trophic Group Presence data Frequency data Presence data (%) (60.2) (78.9) (47.4) Presence-absence data EMF - Ectomycorrhizal (31.9) -0.14 0.47** -0.32 Sw - Lignicolous saprotrophs (36.2) -0.06 -0.02 -0.05 Sh - Humicolous saprotrophs (30.9) -0.07 0.38* -0.26 Frequency data EMF - Ectomycorrhizal (25.1) -0.14 0.23 -0.31 Sw - Lignicolous saprotrophs (30.8) 0.04 -0.08 0.09 Sh - Humicolous saprotrophs (51.4) 0.14 -0.45* 0.05

© SISEF http://www.sisef.it/iforest/ e3 iForest (early view): e1-e8 Landi M et al. - iForest (early view): e1-e8 three classifications gave the best results sed on frequency data also gave significant The correlations between the sample scores when applied to the fungal data set based on results when applied to the frequency of hu- on the first PCA axis for the different groups frequency (number of fruiting bodies per micolous fungi. On the other hand, the clas- were weak and mostly not statistically signi- species - see MRPP statistics and signifi- sifications based on fungal presence-absence ficant (Tab. 2). The two groups, plants and cance). All the three classifications showed data gave poor results (woody plant presen- fungi, did not follow comparable composi- significant concordance when applied to my- ce/absence data applied to mycorrhizal fun- tional gradients (presence-absence data) as corrhizal fungi. Considering each classifica- gi). Lignicolous fungi gave no significant re- revealed by rather different positions of the tions individually, that of woody plants ba- sults. plots in the PCA scatter-plots (not shown).

Tab. 3 - Spearman’s rank correlation coefficients (ρ) between woody plants and ectomycorrhizal fungi (EMF), based on frequency data. The symbol (+) indicates ρ > 0.50 and p-value <0.01. s a i a a n s s a n i i p y a s l e l a c s u r u r a e i g i r o r l s u i a e t x s t a f r a o t r o o m u s n i s e n a c r r t s l i r n a e t n n e y n e i e m i i a i

o o p e m p c x m

b o m p s

p o p

r m s s o y s c m s o r

m u

c s

o s p u u s d s s u Species a c a t s s s u

u r n n c c u c s u u u s u i s n

a c r r e i r u n r g n u c x r a m e u o i u r e i p l e e e y a b u b u r y r x p C c r r r a r Q r u U i t t a a P E Q o o A s P F r n a Q C S S r u O F J C Amanita pantherina - - - - - + ------+ - - Amanita phalloides ------+ - - - - Boletus fechtneri ------+ - - Cortinarius argutus ------+ ------Cortinarius betuletorum ------+ - - Cortinarius bolaris ------+ ------Cortinarius casimiri ------+ ------+ - - - Cortinarius decipiens ------+ ------Cortinarius dionysae ------+ ------Cortinarius rufo-olivaceus ------+ - - Cortinarius trivialis ------+ - - Craterellus cornucopioides ------+ - - - - Genea fragrans ------+ ------Hebeloma gigaspermum - - + ------Hebeloma sinapizans ------+ - - - - - Hygrophorus arbustivus ------+ ------Hygrophorus roseodiscoideus - - - - - + ------+ - - - - Inocybe cincinnata - - - + ------Inocybe flavella - - - + ------Inocybe glabripes ------+ - - - - Inocybe godeyi ------+ ------Inocybe oblectabilis ------+ ------Inocybe obscurobadia ------+ ------Inocybe praetervisa ------+ ------Lactarius acerrimus + ------Lactarius camphoratus - + ------Lactarius scrobiculatus - - - - + ------+ - - Leccinellum crocipodium ------+ - - Otidea alutacea ------+ - - Russula atropurpurea ------+ - - Russula aurea ------+ - - Russula chloroides - + ------Russula curtipes ------+ - Russula cyanoxantha ------+ - - - - Russula delica - + ------+ ------Russula grata - + ------Russula maculata - - - - - + ------Russula pectinatoides - - - - + ------+ - - Russula pseudointegra ------+ ------Russula rubra - + ------+ ------Russula rutila ------+ Thelephora anthocephala ------+ ------Tricholoma columbetta ------+ - Tricholoma orirubens ------+ ------Tricholoma ustaloides - - - - - + ------Tuber excavatum ------+ ------iForest (early view): e1-e8 e4 © SISEF http://www.sisef.it/iforest/ Concordance between plant and macrofungal community

Tab. 4 - Spearman’s rank correlation coefficients (ρ) between woody plants and humicolous saprotrophs (Sh), based on frequency data. The symbol (+) indicates ρ > 0.50 and p-value <0.01. s i s a a s s n a i n i p a l e l a c u r e u r a e i r o l s a i e c t x t a f a t r o m u s s i s e n c r t s l i a e e t n e n y i e m i a i

e p b p x m r b o m p s p p o

u r o y s

c o r m u

s c

p o s p d s Species s a c a t s s

u s r c c s u u u s

s n

a c e u i r u n r n r u c a u c i u r i e p e e y b u b r r y r x p c r r r Q r u e i t a a P E o o A s P u r n Q C S S u O F Q J Agaricus fuscofibrillosus ------+ - Clathrus ruber - - - - + - + ------Clavariadelphus pistillaris - - - + - - - - - + - - - Entoloma hirtipes - - + ------Entoloma rhodopolium ------+ - - Galerina graminea ------+ - Gymnopus dryophilus ------+ - - - - - Hygrocybe ceracea - + ------Hygrocybe conica ------+ - - - - Lepiota lilacea - + - - - + ------Lepiota subincarnata ------+ Macrolepiota procera ------+ - Macrotyphula juncea ------+ - Mycena epipterygia - - - + - - - - - + - - - Mycetinis alliaceus ------+ - - - - - Pluteus ephebeus ------+ - Psathyrella obtusata + ------Psathyrella tephrophylla + - - - - + ------Scutellinia armatospora - - - - - + ------

The correlations between woody plants (fre- that broadleaved deciduous forests domi- thus affecting the composition of the Sh fun- quency data) and EMF (presence/absence nated by Quercus cerris support a high fungal community. Moreover, it is possible that data) and Sh (presence/absence and frequen- gal richness. the species classified as Sh have expanded cy data) fungi were significant. According to observations from previous their trophism (Whitfield 2007). studies (Paavola et al. 2003, Landi et al. The ordination analysis applied in this Associations between plants and 2012), each plant data set gave a better value study revealed that the scores on the ordina- mycorrhizal fungi of MRPP statistics under a posteriori classi- tion axes for woody species were signifi- Results of the correlation analysis between fication (self-test) than under a priori classi- cantly correlated with those obtained for woody and fungi species (EMF and Sh) fication (cross-test). EMF and Sh species, clearly indicating a based on frequency data are reported in Tab. Considering the a priori classification, bet- spatial covariation of EMF and Sh fungal 3 and Tab. 4. Overall, a significant positive ter results were obtained in the MRPP analy- groups and woody species along the same association was detected between 46 EMF sis when the classification based only on environmental gradients. and 17 woody plants, including tree and woody species was used, in comparison with Concerning the association between com- shrub species (Tab. 3). Sorbus domestica the classification obtained including both munities of woody plants and fungi, it is and Prunus spinosa were correlated with a herbaceous and woody species. Such result well known that many EMF show a degree greater number of EMF (11 and 8 correla- may be interpreted as due to the fact that of host specificity (Molina et al. 1992, Tyler tions, respectively) than any other plants. herbaceous species are not functionally rele- 1992, Whitfield 2007). Moreover, multiva- The genus Russula includes the largest num- vant to EMF species, therefore their inclu- riate statistics have shown that macrofungal ber of EMF species correlated with woody sion in the analysis provides a lower varian- communities can be clearly defined and de- plants; all species of the genus Russula ce accounted for in the data sets analyzed. lineated from the abundance patterns of their found in this study were included in Tab. 3. The concordance between the woody species host tree species in temperate forests (Hum- Concerning Sh fungi, significant positive as- community with the EMF community found phrey et al. 2000, Ferris et al. 2000, Buée et sociation were found between 19 Sh fungi in this investigation agrees with previous al. 2011, O’Hanlon & Harrington 2012). In and 13 woody plants (Tab. 4). Tree species studies demonstrating that the EMF commu- this study, EMF were associated with woody as Fraxinus oxycarpa and Quercus petraea nity composition is mainly related to tree plants, including not only trees but also aged were associated exclusively to the same and shrub species (Kernaghan et al. 2003, shrubs (taller than 2m). assembly of EMF (Cortinarius casimiri and Cripps 2004, Lodge et al. 2004, De Bellis et In Italy, the intensive exploitation occurred Hygrophorus roseodiscoideus) and Sh fungi al. 2006, Kirk et al. 2008). A similar concor- in the past has deeply modified the forest (Clavariadelphus pistillaris and Mycena dance was also found between the woody composition and structure, affecting in par- epipterygia). species and the Sh fungi communities, but ticular the understorey layer that was re- only when both data sets were based on fre- moved to ensure optimal growing conditions Discussion quency. Analogously, this may be interpre- to trees. On the other hand, the results of this The high number of fungal species found ted as an effect of the chemical composition study suggest that the presence of old shrubs in this investigation confirmed the evidence of the litter that varies among different plant in the understorey have an overriding influ- previously reported by Salerni et al. (2001) communities (Berg & McClaugherty 2007), ence on EMF communities in broadleaf de-

© SISEF http://www.sisef.it/iforest/ e5 iForest (early view): e1-e8 Landi M et al. - iForest (early view): e1-e8 ciduous forests dominated by Quercus cer- retaining different structures in broadleaf de- 4: 22-31. - doi: 10.1016/j.funeco.2010.07.003 ris. Indeed, it may be hypothesized that the ciduous forests of the Mediterranean area. Chevalier G, Desmas C, Frochot H, Riousset L presence of a shrub understorey can be used To test the general applicability of the rela- (1978). L’espèce Tuber aestivum Vitt. II. Ecolo- as an “ecological indicator” for EMF, which tionships found in this study, and to predict gie [The species Tuber aestivum Vitt. II. Eco- seem to prefer mature forests (e.g., genus the fungal communities based on the woody logy]. Mushroom Science 10 (1): 977-993. [in Russula - Mason et al. 1982, Dighton et al. species communities in Mediterranean de- French] 1986, Deacon & Fleming 1992). ciduous forests, further investigations are Chiarucci A, D’Auria F, De Dominicis V, Laganà Our data indicates that many EMF exhibit needed including more replications over a A, Perini C, Salerni E (2005). Using vascular preferences for one or two hosts. However, broader range of sites. plants as a surrogate taxon to maximize fungal some woody plants, such as Sorbus dome- species richness in reserve design. Conservation stica and Prunus spinosa, appear to be asso- Acknowledgements Biology 19: 1644-1652. - doi: 10.1111/j.1523- ciated with many EMF. To our knowledge, This work was partly supported by a Mana- 1739.2005.00202.x these species are not thought to host sym- gement Project of the Italian Forest Service Conti F, Abbate G, Alessandrini A, Blasi C biotic fungi, though it has been hypothesized (Corpo Forestale dello Stato). We thank all (2005). An annotated checklist of the Italian vas- that they play an important role during the our colleagues who participated in the sam- cular flora. Palombi Editore, Rome, Italy, pp. fruiting process of some fungal species pling efforts, particularly Pamela Leonardi, 420. (Chevalier et al. 1978, Bencivenga et al. Flavio Frignani, Martino Danielli and Lo- Cripps CL (2004). Fungi in forest ecosystems: 1990). McDonald et al. (2010) identified ec- renzo Pecoraro, also for their precious help systematics, diversity and ecology. The New tomycorrhizal species of the genera Cortina- with plant and fungal determination, and York Botanical Garden, New York, USA, pp. rius, Inocybe and Tricholoma that form epi- Emma Thorley for language editing. 363. geous fruiting bodies with a species of Deacon JW, Fleming LV (1992). Interactions of Rosaceae. On the other hand, compared to References ectomycorrhizal fungi. In: “Mycorrhizal Func- other higher taxa of the northern hemisphere Arnolds E (1981). 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