Studi Trent. Sci. Nat., Acta Biol., 81 (2004), Suppl. 1: ISSN Museo Tridentino di Scienze Naturali, Trento 2005

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1 Studi Trent. Sci. Nat., Acta Biol., 81 (2004), Suppl. 1: ISSN Museo Tridentino di Scienze Naturali, Trento 2005 Monitoring epiphytic lichen biodiversity in a subalpine Norway spruce woodland at Lavazè Pass and in a thermophilous pubescent oak woodland at Pomarolo, Trentino, North Italy Elena Gottardini *, Fabiana Cristofolini & Antonella Cristofori IASMA Research Center, Natural Resources Department, Via E. Mach 1, I San Michele all Adige (TN), Italy * Corresponding author elena.gottardini@iasma.it Summary - Monitoring epiphytic lichen biodiversity in a subalpine Norway spruce woodland at Lavazè Pass and in a thermophilous pubescent oak woodland at Pomarolo, Trentino, North Italy - Epiphytic lichens were analyzed at two forestry sites, part of an integrated monitoring programme (ICP - IM International Cooperative Program on Forest and Integrated monitoring ): a subalpine Norway spruce woodland at Lavazè Pass and a thermophilous Pubescent oak woodland at Pomarolo, in Trentino - North Italy, with the aim of obtaining information about environmental conditions. Many studies demonstrated that lichens are excellent indicators of environmental change; by virtue of their sensitivity to phytotoxic gases, the diversity of epiphytic lichens is used to estimate the effects of atmospheric pollution. Observations were conduced on the trunk of 10 trees of Picea excelsa and Pinus cembra at Lavazè Pass and Quercus sp. and Larix decidua at Pomarolo. Two methods were adopted to evaluate lichen biodiversity (BL): the BL method and line cover. Lichen biodiversity data were moreover compared with those obtained in a previous investigation in 1992 in the same areas. The whole data lead to formulate a naturality judgement for the environmental quality at Lavazè Pass, while at Pomarolo more factors contribute to a situation of semi-alteration, inducing to suggest the presence of some environmental stress, probably air pollution. RIASSUNTO - Monitoraggio della biodiversità di licheni epifiti in una pecceta subalpina a Passo Lavazè e in un querceto termofilo a Pomarolo, Trentino, Nord Italia - è stata condotta l osservazione dei licheni epifiti in due diverse aree forestali inserite in un programma integrato di monitoraggio (ICP - IM International Cooperative Program on Forest and Integrated monitoring ): la pecceta sub-alpina di Passo Lavazè e il querceto termofilo di Pomarolo, in Trentino - Italia settentrionale. Obiettivo principale è stato ottenere informazioni relative alla situazione ambientale. Molti studi dimostrano come i licheni siano eccellenti indicatori di cambiamenti ambientali: grazie alla loro sensibilità ai gas fitotossici, la diversità dei licheni è utilizzata per stimare l effetto degli inquinanti atmosferici. I dati sono stati raccolti dall osservazione dei licheni rinvenuti su 10 alberi di Picea excelsa e Pinus cembra al Passo Lavazè e Quercus sp. e Larix decidua a Pomarolo. Per valutare la biodiversità lichenica sono stati adottati sia il metodo BL sia la copertura lineare. I dati di biodiversità (BL) sono stati inoltre comparati con i valori rilevati in un indagine svolta nel 1992 nelle stesse aree. I dati portano a formulare un giudizio di naturalità relativamente a Passo Lavazè, mentre a Pomarolo più fattori contribuiscono a determinare una situazione di semi-alterazione, inducendo a supporre la presenza di alcuni fattori di stress ambientale, tra cui l inquinamento dell aria. Key words: epiphytic lichens, biodiversity, forest, ecosystem, naturality, North Italy Parole chiave: licheni epifiti, biodiversità, foresta, ecosistema, naturalità, Nord Italia 1. Introduction It is often difficult and expensive to measure environmental parameters of an ecosystem, while it is easier and more convenient to measure the signal from a specific indicator and to use it for estimating environmental conditions. Many studies demonstrated that lichens are excellent indicators of environmental change (Will-Wolf et al. 2002a). By virtue of their sensitivity to phytotoxic gases, the diversity of epiphytic lichens is used to estimate the effects of atmospheric pollution (Nimis et al. 1989; Piervittori 1999; Giordani et al. 2002; Loppi et al. 2002). Lichens are very sensitive also to microclimatic conditions, determined by differences in forest structure: in fact this affects light and moisture regimes, and these, in turn, influence the distribution and composition of lichen assemblages.

2 246 Gottardini et al. lichen biodiversity forest Lichens communities can be used to get informations about forest management practices and, more generally, about environmental functionality (Will-Wolf et al. 2002b). It has been shown, for example, that fruticose and pendulous lichens like Bryoria, Usnea, Alectoria, etc. are indicators of forest management as well as air quality; these lichens are more abundant in older forests and/or where air quality is better. Ecological indices, which express endurance spectrum for an ecological factor, can be associated to each species; on the basis of lichen vegetation composition is therefore possible to interpret ecological characteristics of a site. The aim of the present study is to describe the epiphytic lichen biodiversity (BL) to estimate the ecosystem response to stress factors in two forest areas: a subalpine Norway spruce woodland at Lavazè Pass and a thermophilous pubescent oak woodland at Pomarolo, Trentino, North Italy. Since 1992 these two areas are part of the Integrated Monitoring Program (ICP-IM) of the UN-ECE. 2. Matherials AND methods 2.1. Choice of host trees All observations and measures were carried out on lichens colonizing tree trunks. For the selection of the tree species, forest composition was evaluated at each site and then dominant species were chosen: Picea excelsa (Lam.) and Pinus cembra L. at Lavazè Pass, and Quercus sp. L. and Larix decidua Miller at Pomarolo. Lichen observations were done on ten trees for each tree species selected, for a total of 40 observations. Trees were selected privileging those inside the delimited areas for integrated monitoring (ICP-IM) and discarding trees with evident trunk damage, severe knottiness, girth < 50 cm and trunk inclination > 10. If enough trees were not present inside the delimited area, trees were searched the outside, starting from those closer to the monitoring site. Field work was carried out in 2001 at Lavazè Pass and in 2003 at Pomarolo Sampling of epiphytic lichen The following methods were applied for each tree species Lichen Biodiversity (BL) A 50x30 cm sampling grid divided in ten units was used. The grid was positioned along the trunks, with the base at 100 cm above ground, on the side where lichen cover was highest. For each tree additional informations were recorded: cardinal exposure of the grid center, trunk girth at grid base, bark condition, etc. For each tree, all lichen species present within the sampling grid were identified, following Wirth (1980) and Nimis (1987); species nomenclature follows Nimis (2003). A frequency value was assigned, according to the number of units were each species occurred; the sum of frequencies of all species present within the grid was the BL value of the tree. The BL of the station was calculated for each tree species as the arithmetic mean of the ten trees examined. This bioindication method, formerly named Index of Atmospheric Purity (IAP), was applied in the same areas in 1992 (Sittoni & Gottardini 1994), and comparison of the two data sets enabled to draw conclusions on environmental change. In the absence of a calibrated scale for interpreting BL values in these two forest areas, the scale calibrated in Mediterranean areas for Tilia-Quercus (deciduous) by Loppi et al. (2002) (Tab. 1) was adopted for the Pomarolo data; in sub-alpine area Lavazè Pass, the BL values were compared with those surveyed in forest ecosystems of Trentino and Veneto natural parks (Nascimbene & Caniglia 2000). Tab. 1 - Interpretative scale of BL values on lime and deciduous oaks from the Tyrrhenian side of Italy. Tab. 1 - Scala interpretativa dei valori di BL rilevati su tiglio e querce decidue nell area tirrenica italiana. BL Interpretation 0 lichen desert 1-25 alteration Semi-alteration Semi-naturality >75 Naturality BL data for the two monitoring sites were also compared with those (named IAP) previously recorded in a preceding monitoring survey carried out in 1992, and statistically analyzed by t-test to find out eventual significant differences. The ecology of each station was evaluated indirectly through the use of ecological indices, peculiar for each species, relating to the following parameters (Nimis 2003). Substratum ph: 1. very acid substratum (e.g., non eutrophyzed conifer bark); 2. subacid substratum (e.g., Quercus petraea (Mattuschka) Liebl. Bark) 3. subneutral substratum; 4. slightly basic substratum; 5. basic substratum (e.g., bark with considerable calcareous dusts deposition).

3 Studi Trent. Sci. Nat., Acta Biol., 81 (2004), Suppl. 1: Eutrophication: 1. no eutrophication; 2. very weak eutrophication; 3. weak eutrophication; 4. relatively high eutrophication; 5. very high eutrophication. Poleophoby: 0, 1, 2, 3 - growing degrees of tolerance to pollutants. The ecological characterization of the two sites was carried out calculating weighted mean indices, following the suggestions reported by ANPA (2001), but the values are express as classes without reduction to decimals Linear covering Around each tree trunk, 100 cm above ground, was positioned a metric rule; starting from the north, the presence along the upper side of the cord of different lichen species was recorded, registering the start and the end of each thallus in millimeters. Summing coverings of single species on each plant and relating them to trunk girth, it was possible to calculate percentage coverings for each lichen taxa. Converting lichen taxa presence on the trunk in degrees it was possible to individuate preferential cardinal exposures in relation to different tree species. 3. Results and discussion 247 A list of all lichen taxa found applying the BL method, along with frequency values, is reported for each tree (Tab. 2-5). Species with higher frequency at Lavazè Pass are those classified as rather to extremely common in the subalpine phytoclimatical belt of Trentino-South Tyrol (Nimis 2003). As for as species surveyed in Pomarolo are concerned, they are representative of the sub-mediterranean phytoclimatic belt and present a rather high tolerance to atmospheric pollutants (Nimis 2003). Lichen biodiversity values surveyed at Pomarolo (Tab. 6), reported to the scale of table 1, show a situation of semi-alteration, while the BL value of Lavazè Pass are similar to those surveyed in Trentino and Veneto natural parks by Nascimbene & Caniglia (2000). These authors measured values of lichen biodiversity (IAP) of 77 on Picea excelsa and 71 on Pinus cembra. On the same tree species, at Lavazè Pass the BL values were 74 and 79 respectively. By this comparison, it seems reasonable to refer Lavazè Pass to a situation of naturality. This conclusion is further confirmed by the information derived from visual estimation of lichen vitality, especially for fruticose lichens (Tab. 6): at Pomarolo a limited number of thalli was found on few trees; in the subalpine Norway spruce woodland, fruticose lichens were present on each sampled tree, constituting more than 25% of the total. Tab. 2 - Lichen frequencies surveyed with the BL method on Picea excelsa at Lavazè Pass. Tab. 2 - Valori di frequenza lichenica rilevati con il metodo BL su Picea excelsa al Passo Lavazè. Lavazè Pass Picea excelsa Survey exposition in degrees (N= 0) Tree circumference (cm) Number of lichen species BL Usnea sp Parmeliopsis ambigua (Wulfen) Nyl Platismatia glauca (L.) W.L. Culb. & C.F. Culb Hypogymnia physodes (L.) Nyl Bryoria sp Calicium viride Pers Lepraria sp Pseudoevernia furfuracea (L.) Zopf Tuckermannopsis chlorophylla (Willd.) hale Hale Evernia divaricata (L.) Ach Candelariella xanthostigma (Ach.) Lettau Parmelia sulcata Taylor Pertusaria amara (Ach.) Nyl. 1 3 Vulpicida pinastri (Scop.) J.E. Mattsson & J. Lai 1 2 Opegrapha sp. 3 Lecanora sp. 1 1 Lecidella sp.elaeochroma (Ach.) M.Choisy 2

4 248 Gottardini et al. lichen biodiversity forest Tab. 3 - Lichen frequencies surveyed with the BL method on Pinus cembra at Lavazè Pass. Tab. 3 - Valori di frequenza lichenica rilevati con il metodo BL su Pinus cembra al Passo Lavazè. Lavazè Pass Pinus cembra Survey exposition in degrees (N=0) Tree circumference (cm) Number of lichen species BL Hypogymnia physodes (L.) Nyl Usnea sp Bryoria sp Platismatia glauca (L.) W.L. Culb. & C.F. Culb Parmeliopsis ambigua (Wulfen) Nyl Lepraria sp Tuckermannopsis chlorophylla (Willd.) hale Hale Pseudoevernia furfuracea (L.) Zopf Parmeliopsis hyperopta (Ach.) Arnold Evernia divaricata (L.) Ach Amandinea punctata (Hoffm.) Coppins & Scheid Tuckneraria laureri (Kremp.) Randlane & Thell Calicium viride Pers Parmelia sulcata Taylor non identified crustose Pertusaria amara (Ach.) Nyl Vulpicida pinastri (Scop.) J.E. Mattsson & M.J. Lai Lecanora sp Cladonia coniocraea (Flörke) Spreng. 6 1 Mycoblastus sp. 1 1 Tab. 4 - Lichen frequencies surveyed with the BL method on Larix decidua at Pomarolo. Tab. 4 - Valori di frequenza lichenica rilevati con il metodo BL su Larix decidua a Pomarolo. Pomarolo Larix decidua Survey exposition in degrees (N= 0) Tree circumference (cm) Number of lichen species BL Melanelia fuliginosa (Duby) Essl. subsp. glabratula Parmelia sulcata Taylor Lepraria sp non identified crustose Pertusaria sp Lecanora sp Physcia tenella (Scop.) DC Hypogymnia physodes (L.) Nyl Candelariella xanthostigma (Ach.) Lettau Flavoparmelia caperata (L.) Hale Evernia prunastri (L.) Ach. 6 Caloplaca sp. 1 5 Usnea sp. 3 1 Hyperphyscia adglutinata (Flörke) H. Mayrhofer & Poelt 3 Parmeliopsis hyperopta (Ach.) Arnold 2 1 Lecidella elaeochroma (Ach.) M.Choisy 2 Pseudoevernia furfuracea (L.) Zopf 2 Punctelia borreri (Sm.) Krog 1 Parmelina tiliacea (Hoffm.) Hale 1 Ramalina sp. 1

5 Studi Trent. Sci. Nat., Acta Biol., 81 (2004), Suppl. 1: Tab. 5 - Lichen frequencies surveyed with the BL method on Quercus sp. at Pomarolo. Tab. 5 - Valori di frequenza lichenica rilevati con il metodo BL su Quercus sp. a Pomarolo. Pomarolo Quercus sp. Survey exposition in degrees (N= 0) Tree circumference (cm) Number of lichen species BL Melanelia fuliginosa (Duby) Essl. subsp. glabratula Lepraria sp Parmelia sulcata Taylor Candelariella xanthostigma (Ach.) Lettau Physcia adscendens (Fr.) H. Olivier Flavoparmelia caperata (L.) Hale 10 1 Punctelia subrudecta (Nyl.) Krog 9 Parmelina tiliacea (Hoffm.) Hale 8 1 non identified crustose 3 Hyperphyscia adglutinata (Flörke) H.Mayrhofer & Poelt 2 Evernia prunastri (L.) Ach. 1 Tab. 6 - Summary data for biodiversity (BL, No. of taxa), growth on Picea excelsa (PE), Pinus cembra (PC), Larix decidua (LD) and Quercus sp. (QU). Tab. 6 - Dati riassuntivi di biodiversità lichenica (BL, N. di taxa) su Picea excelsa (PE), Pinus cembra (PC), Larix decidua (LD) e Quercus sp. (QU). Site Lavazè Pass Pomarolo Host tree PE PC LD QU Average BL (+SD) Number of lichen taxa (mean) Number of lichen taxa (min) Number of lichen taxa (max) % crustose species % foliose species % fruticose species No. of tree with fruticose sp./no. of surveyed trees 10/10 10/10 4/10 1/10 A substantial difference between the two surveyed areas emerged from the ecological indices (Tab. 7): eutrophication and poleophoby values are lower at Lavazè than Pomarolo; the ph index of tree substratum naturally acid at Lavazè Pass because the survey was done on conifers shows higher values at Pomarolo even on the conifer L. decidua, indicating a higher bark ph. This agrees with the suggestions of Ambrosi et al. (2002) and Marchetti et al. (2002) according to whom higher precipitations ph at Pomarolo than at Lavazè Pass would be caused by the high quantity of coarse particulate matter, originating from calcareous soils, present at low altitudes. By the use of the linear cover method (Tab. 8), a confirmation of a lower lichen biodiversity at Pomarolo than Lavazè Pass is evident. In this second monitoring site, mean linear cover on spruce trunks Tab. 7 - Ecological indices of lichens surveyed on Picea excelsa (PE), Pinus cembra (PC), Larix decidua (LD) and Quercus sp. (QU); the prevalent class is in heavy type. Tab. 7 - Indici ecologici dei licheni osservati su Picea excelsa (PE), Pinus cembra (PC), Larix decidua (LD) e Quercus sp. (QU); la classe prevalente è in grassetto. Site lavazè Pass Pomarolo Host tree PE PC LD QU Ph index Eutrophication index Poleophoby index is about 60%, while on Pinus cembra is 33%; values decrease drastically at Pomarolo situation: here linear cover reaches a maximum of 10% on oak. Furthermore, the pendulous lichen Usnea sp. covers more than 2% of the observed circumferences in Lavazè Pass

6 250 Gottardini et al. lichen biodiversity forest Tab. 8 - Values (%) of the line cover method. Tab. 8 - Valori (%) di copertura lichenica rilevati con il metodo lineare. Lavazè Pass Lavazè Pass Lichen taxa on Picea excelsa Mean % Cover Lichen taxa on Pinus cembra Mean % Cover Calicium viridae Pers Calicium viridae Pers Hypogymnia physodes 4.9 Platismatia glauca 4.1 Platismatia glauca 4.3 Hypogymnia physodes 3.8 Usnea sp. 2.3 Parmeliopsis ambigua 3.2 Parmeliopsis ambigua 1.2 Usnea sp. 2.6 Others 3.7 Others 5.3 Total % cover 59.1 Total % cover 33.2 Pomarolo Pomarolo Lichen taxa on Larix decidua Mean % Cover Lichen taxa on Quercus sp. Mean % Cover Melanelia fuliginosa (Duby) Essl. subsp. glabratula glabratula Melanelia fuliginosa (Duby) Essl. subsp Parmelia sulcata Taylor 2.7 Lepraria sp. 2.9 Lepraria sp. 1.8 Flavoparmelia caperata (L.) Hale hale 1.5 Others 0.2 Others 2.0 Total % cover 8.1 Total % cover Picea excelsa Pinus cembra Larix decidua Quercus sp Lavazè Pass Min-Max 25%-75% Median value BT N-NE NE-E E-SE SE-S S-SW SW-W W-NW NW-N Fig. 1 - Percent presence of lichen thalli (y axis) on the different tree species, in relation to cardinal exposure. Fig. 1 - Valori percentuali di presenza dei talli lichenici (asse y) sulle differenti specie arboree, in relazione all esposizione Pomarolo Picea abies 1992 Pinus cembra 1992 Larix decidua 1992 Quercus sp Picea abies 2001 Pinus cembra 2001 Larix decidua 2003 Quercus sp Fig. 2 - Comparison between BL values surveyed at Lavazè Pass and Pomarolo in 1992 and Fig. 2 - Confronto tra valori di BL rilevati a Passo Lavazè e a Pomarolo nel 1992 e nel and it is one of the five more frequently found taxa by using this method. In figure 1, percentages of lichen thalli present on different tree species are shown in relation to cardinal exposure. Between west and east there were more lichens; on Larix decidua, between east and south-west, lichens were totally absent. Only on Quercus sp. lichens seem to colonize indifferently each side of the trunk. Comparing the present lichen biodiversity data with those recorded in 1992, important informations emerged (Fig. 2): significant differences in BL values on Picea excelsa as well as on Pinus cembra were not found in the Norway spruce woodland at Lavazè. On the contrary, lichen biodiversity showed to be significantly different on Quercus sp. (P<0.01) as well as on Larix decidua (P<0.01) at Pomarolo, indicating a worsening of environmental conditions. 4. conclusions Informations obtained from epiphytic lichens allow to formulate, on the whole, a positive judgement for the environmental situation at Lavazè Pass: high biodiversity, presence of species sensitive to atmospheric pollutants, fruticose species abundant; it is noteworthy

7 Studi Trent. Sci. Nat., Acta Biol., 81 (2004), Suppl. 1: that this situation remained unchanged during the last decade. The situation observed in the thermophilous pubescent oak woodland at Pomarolo is different: dominant presence of species less sensitive or more tolerant to atmospheric pollutants, lower biodiversity values, scarcity of fruticose species, higher eutrophication of tree bark. This lead to formulate, on the whole, a judgement of environmental semi-alteration. This indicates that in this site environmental stress, probably air pollution, is present. Furthermore, in this site a significant reduction in lichen biodiversity was found during the last decade. ACKNOwLEDGEMENTS This work was supported by a funding from Autonomous Province of Trento (EFOMI project: Ecological Valuation in Alpine Forest Ecosystems by Integrated Monitoring). references Ambrosi P., Bertagnolli A., Confalonieri M., La Porta N., Marchetti F., Maresi G., Minerbi S., Salvadori C. & Valentinotti R., Eight years of integrated monitoring in Alpine forest ecosystems of Trentino and South Tyrol, Italy. J. Limnol., 61, Suppl. 1: ANPA, I.B.L. Indice di Biodiversità Lichenica. Manuali e linee guida, 2/2001. Giordani P., Brunialti G. & Alleteo D., Effects of atmospheric pollution on lichen biodiversity (LB) in a Mediterranean region (Liguria, northwest Italy). Environ. Pollut., 118: Loppi S., Giordani P., Brunialti G., Isocrono D. & Piervittori R., Identifying deviations from naturality of lichen diversity for bioindication purposes. In: Nimis P.L., Scheidegger C. & Wolseley P.A. (eds), Monitoring 251 with Lichens Monitoring Lichens. Kluwer Accademic Publishers, Dordrecht: Marchetti F., Tait D., Ambrosi P. & Minerbi S., Atmospheric deposition at four forestry sites in the Alpine Region of Trentino - South Tyrol, Italy. J. Limnol., 61, Suppl. 1: Nascimbene J. & Caniglia G., Licheni, indicatori della qualità ambientale degli ecosistemi forestali nei Parchi Naturali di Paneveggio - Pale di San Martino (Trento) e delle Dolomiti d Ampezzo (Belluno). Studi Trent. Sci. Nat., Acta Biol., 74: Nimis P.L., I macrolicheni d Italia, chiavi analitiche per la determinazione. Atti Museo Friul. St. Nat., 8: Nimis P.L., Checklist of the Lichens of Italy 3.0. University of Trieste, Dept. of Biology, IN3.0/2 (http: //dbiodbs.univ.trieste.it/). Nimis P.L., Ciccarelli A., Lazzarin G., Bargagli R., Benedet A., Castello M., Gasparo D., Lausi D., Olivieri S. & Tretiach M., I licheni come bioindicatori di inquinamento atmosferico nell area di Schio-Thiene-Breganze (VI). Bollettino Mus. Civ. St. Nat. Verona, 16: Piervittori R., Licheni come bioindicatori della qualità dell aria: stato dell arte in Italia. In: Piccini C. & Salvati S. (a cura di), Atti del Workshop Biomonitoraggio della qualità dell aria sul territorio nazionale. Roma, novembre ANPA, Serie Atti 2/1999: Sittoni L. & Gottardini E., Biomonitoraggio della qualità dell aria mediante licheni. Applicazione in pecceta subalpina e querceto termofilo. Bollettino ISMA, 2: Will-Wolf S., Scheidegger C. & McCune B., 2002a - Methods for monitoring biodiversity and ecosystem function. In: Nimis P.L., Scheidegger C. & Wolseley P.A. (eds), Monitoring with Lichens Monitoring Lichens. Kluwer Accademic Publishers, Dordrecht: Will-Wolf S., Essen P.A. & Neitlich P., 2002b - Monitoring biodiversity and ecosystem function: forests. In: Nimis P.L., Scheidegger C. & Wolseley P.A. (eds), Monitoring with Lichens Monitoring Lichen. Kluwer Accademic Publishers, Dordrecht: Wirth V., Flechtenflora. Ulmer, Stuttgart: 552.

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