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Mature non-native black-locust (Robinia pseudoacacia L.) forest does not regain the lichen diversity of the natural forest
Science of the Total Environment 421–422 (2012) 197–202
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Mature non-native black-locust (Robinia pseudoacacia L.) forest does not regain the lichen diversity of the natural forest Juri Nascimbene a,⁎, Pier Luigi Nimis a, Renato Benesperi b a b
Department of Life Sciences, University of Trieste, via Giorgieri 10-34100, Trieste, Italy Department of Evolutionary Biology, University of Florence, via La Pira 4, Florence, Italy
a r t i c l e
i n f o
Article history: Received 21 November 2011 Received in revised form 23 January 2012 Accepted 24 January 2012 Available online 16 February 2012 Keywords: Bark features Epiphytic lichens Forest management Habitat changes Species composition Species richness
a b s t r a c t The responses of lichens to habitat changes caused by invasive trees are poorly understood. Invasive forest trees may impact epiphytic lichens by altering both substrate and stand conditions. Previous research has demonstrated that black locust invasion, associated with intensive exploitation of native oak forests, led to dramatic shifts in lichen composition. However, it is not clear if, along with stand aging, black locust formations regain forest species. The main aim of this study was to test whether the succession of black locust stands promotes a lichen succession leading to assemblages in mature black locust stands which are similar to those of native forests. To test the influence of macro-environmental conditions, we performed the study in two bioclimatically different areas of Italy. The epiphytic lichen biota of native oak and chestnut stands was compared with that of black locust stands of different successional stages. In both regions we did not find a lichen succession in black locust stands of different age, and mature black-locust stands did not recover the diversity of epiphytic species, which are lost by the replacement of the native forests by black locust. The absence of this pattern may be caused by factors related to the management of black locust stands, and to bark features. The different bioclimatic conditions between the two study areas may explain differences in the lichen biota of native forests, while that of black locust stands tend to be similar between regions, suggesting that forest habitat changes associated with the spread of black locust could decrease lichen diversity among bioclimatically different regions. © 2012 Elsevier B.V. All rights reserved.
1. Introduction Epiphytic lichens are among the most sensitive components of the forest biota, being responsive to climate, forest structure, and substrate type (Marini et al., 2011; Fritz et al., 2008). In particular, they are threatened by human-related alterations of forests (Johansson, 2008), such as intensive management or the replacement of native forests with secondary formations (e.g. Aragón et al., 2010; Hedenås and Ericson, 2000; Humphrey et al., 2002; Moning and Müller, 2009; Nascimbene et al., 2007). These processes alter microclimatic conditions under the canopy as well as the availability of host tree species in the landscape, threatening forest- and substrate-specialist lichens (Rogers and Ryel, 2008). Despite the fact that a large body of literature has grown to evaluate the effects of forest management on epiphytic lichens (e.g. Aragón et al., 2010; Humphrey et al., 2002; Johansson, 2008; Nascimbene et al., 2007), their response to habitat changes caused by invasive trees is poorly understood.
⁎ Corresponding author. Tel./fax: + 39 043942894. E-mail address: [email protected] (J. Nascimbene). 0048-9697/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.scitotenv.2012.01.051
Invasive forest trees which replace native forest vegetation may impact the forest biota, acting as habitat ‘transformers’ (Richardson and Reimánek, 2011). In particular, they may impact epiphytic organisms by altering both substrate and stand conditions related to their management. An example of this process is provided by the spread of black locust (Robinia pseudoacacia L.) which in northern and central Italy is replacing native broadleaf forests over large areas from lowlands to the lower montane belt (Caprio et al., 2009; Motta et al., 2009). This process is favored by the fast and highly competitive growth of this tree, intensive exploitation of native forests, chestnut blight, and urbanization (Celesti-Grapow et al., 2009; Motta et al., 2009). In a previous study, Nascimbene and Marini (2010) demonstrated that black locust invasion, associated with intensive exploitation of oak native forests, led to dramatic shifts in lichen composition which mainly involved forest-specialist lichens. That study showed that the lichen biota of native oak remnants was mainly composed of forest-dwelling acidophytic and nitrogen intolerant species, while that of black locust forests was mainly composed of nitrogen tolerant species related to disturbed habitats. However, in that study only relatively young black locust stands were considered and it is not clear if, along with stand aging, mature
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black locust formations regain forest species which may migrate from native remnants. We therefore hypothesized that along with stand aging (i.e. increasing shading and humidity under the canopy, increasing tree age) a lichen succession should evolve. This process should lead to lichen assemblages composed by forest acidophytic species since bark pH of black locust, ranging between 4 and 5 (Passialis et al., 2008) and bark texture with deep cervices are similar to that of deciduous oaks (Barkman, 1958). On the other hand, we should also consider two additional factors: 1) in Italy, black locust forests are mainly managed with short-rotation cycles for fire-wood production (Pividori and Grieco, 2003). This silviculture management based on a very frequent disturbance regime may hinder black locust stands evolving adequate habitat continuity for forest lichen species; 2) other bark features than pH (e.g. high buffer and water capacity, nutrient enrichment) may drive species-host affinities between lichens and black locust trees. In this case, we hypothesized that these factors may hamper a lichen succession along with stand aging, hindering black locust forests from acquiring lichen assemblages comparable to those of native forests. In this study, we addressed these hypotheses and compared epiphytic lichen species richness and composition of different successional stages of black locust stands, and coppiced stands dominated by native broadleaved trees (mainly oaks). The main aim was to test whether the succession of black locust stands promoted a lichen succession leading to assemblages in mature black locust stands which are similar to those of native forests. To test the influence of macro-environmental conditions on the patterns of lichen diversity across stand types, we performed the study in two bioclimatically different areas of Italy. 2. Materials and methods 2.1. Study areas The study was carried out in two forested areas of Italy reflecting different bioclimatic conditions: 1) Montello, in NE Italy (Veneto, 46°48′ N, 12°08′ E), in the dry sub-Mediterranean region where the epiphytic lichen flora is generally poor and the suboceanic component is weak (Nimis and Martellos, 2008), and 2) the hills in the province of Pistoia, in Central Italy (Toscana, central Apennine, 43°59′ N, 10°53′ E), in the humid sub Mediterranean region which is under the influence of humid maritime winds, promoting more favorable conditions for epiphytic lichens, including several sub oceanic species (Nimis and Martellos, 2008). The Montello area is a large hill in the northern part of the Venetian plain (NE-Italy, Veneto, Treviso), extending over 5000 ha. The mean elevation is 200 m (maximum 369 m), 100 m higher than the surrounding plain. Mean annual temperature is 12.9 °C, January being the coldest month (mean temperature 3–4 °C) and July the warmest one (mean temperature 22.7 °C). Mean annual rainfall is 1100 mm, with maxima in spring and autumn. Forty percent of the Montello area is managed for extensive agriculture (arable fields, hay meadows, and vineyards), while the remnant is covered by forests. The forest landscape is a rather continuous black locust matrix with interspersed oak-dominated patches. Pure black locust stands are the main forest type, covering over 90% of the forested area. Remnant patches of oak forest (Quercus petraea (Mattuschka) Liebl. and Quercus robur L.) can be found in the central part of the hill, being coppiced for firewood production. The hilly area in the Province of Pistoia is delimited northward by the Tuscan-Emilian Apennines ridge and southward by the Pistoia plain. Elevation ranges between 100 and 900 m. Mean annual temperature is 14.4 °C and 9.4° in the lower (100–500 m) and higher (500– 900 m) areas respectively. Mean annual rainfall ranges between 1300 and 1900 mm with two maxima in spring and autumn. At lower elevations, the landscape is dominated by cultivated (olive-groves and
vineyards) and forested areas mainly dominated by black locust formations. At higher elevations, native forests prevail, while black locust formations are interspersed in a matrix of deciduous broadleaf formations including chestnut, oak (Quercus cerris L.) and hop hornbeam, coppiced for firewood production. In both sites, black locust forests are managed with 20–30 year rotation cycles, mainly for firewood production. Stands are usually clear-cut and spontaneously replaced by a new generation of trees. 2.2. Sampling design According to the stage of the management cycle, black locust stands were classified into three main forest successional stages (Table 1) corresponding to even-sized and even-aged formations: 1) young stands including trees with a circumference of 20–40 cm (age c.10 years), 2) intermediate (adult) stands including trees with a circumference of 40–60 cm (age c.20 years), and, 3) mature stands, including trees with a circumference >60 cm (age 30–40 years). For each type of black locust forest stand, as well as for forest stands composed of native species, seven 30 × 30 m plots were randomly selected in different parts of the two study areas in order to encompass the variability of each stand type in each area. In Montello, native stands were generally older (60–90 years) and have higher mean DBH than any mature black locust stand, while in Tuscany it was possible to find native stands whose age (30–50 years) and mean DBH are comparable to those of black locust mature stands. Slope, altitude, and canopy cover were comparable among stand types in each area (Table 1). In particular, canopy cover was always higher than 75%. Minimum distance between plots of the same stand type was greater than 500 m to reduce spatial dependence. The borders of the plots were at least 30 m far from the forest edge to avoid any edge-effects. In black locust stands, only black locust individuals were considered for the lichen sampling, while in native tree stands the dominant species were considered: oaks in Montello, and chestnut (5 plots) and oak (2 plots) in the Pistoia province. In each plot, six trees (circumference ≥40 cm) were selected for lichen inventory by random sampling, for a total of 336 trees (42 in each stand type in each of the two study areas). In mature black locust stands, the mean circumference of sampled trees was 90 ± 9 cm and 93 ± 14 cm in Montello and Pistoia respectively, while that of sampled trees in native stands was 153 ± 24 cm for Montello and 98 ± 25 cm for Pistoia. The lichen sampling followed the European guidelines for lichen monitoring (Asta et al., 2002). Lichens were sampled using four standard frames of 10× 50 cm as sampling grids, subdivided into five 10× 10 cm quadrats, which were attached to the tree trunk at the cardinal points with the low side at 100 cm from the ground. All lichen species inside the frames were listed, and their frequency was computed as the number of 10 × 10 cm quadrats in which the species occurred. Nomenclature of lichens followed Nimis and Martellos (2008). 2.3. Data analysis A two-way analysis of variance (ANOVA) was applied to test the effects of study area and stand type on species richness (cumulative number of species per plot calcutated as the sum of the species found on the six trees) and on the contribution of the guild of nitrogen tolerant species (expressed as percentage of the plot species richness) defined by the ecological indicator value for eutrophication ranging from 4 (rather high eutrophication) to 5 (very high eutrophication) in the on-line checklist of Italian lichens (Nimis and Martellos, 2008). These species are considered as indicative of substrate eutrophication and habitat disturbance. In these analyses, the plot was used as replicate to avoid pseudo-replication. After the ANOVA, a Tukey's honest significance test for multiple
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Table 1 Mean features (± SD) of the four types of stands in the two sites (Montello and Pistoia province). BL_Y = young black locust stands; BL_A = adult black locust stands; BL_M = mature black locust stands; Native = stands composed by native tree species. Montello
Mean circumference (cm) Mean number of trees/plot Canopy cover % Slope (%) Elevation (m)
Pistoia
BL_Y
BL_A
BL_M
Native
BL_Y
BL_A
BL_M
Native
36.2 ± 3.6a 102 ± 13a 79.3 ± 6.7a 5.7 ± 3.5a 240 ± 68 a
50 ± 8.6b 96 ± 28a 80.7 ± 7.3a 6 ± 4.5a 241 ± 59 a
68.8 ± 2.8c 92 ± 6a 86.4 ± 5.5a 7.1 ± 6.2a 231 ± 53 a
128.8 ± 16.9 d 36 ± 14b 85.4 ± 6.7a 8.6 ± 6.3a 216 ± 41a
36 ± 4a 120 ± 111a 80 ± 6.4a 9 ± 4.9a 465 ± 163a
47.7 ± 5.2b 98 ± 20a 85.7 ± 4.5a 14.2 ± 7.8a 488 ± 195a
68.1 ± 9.2c 70 ± 5b 86.4 ± 6.2a 11.4 ± 8.5a 462 ± 247a
77.8 ± 15c 65 ± 8b 83.5 ± 6.9a 5 ± 3.6a 636 ± 244a
Significant different values among stand types (P b 0.05; one-way ANOVA test for each region) are marked with different letters (a, b, c, d).
comparison was applied to detect differences between stand types (P b 00.05). Compositional differences among stand types were tested by multi response permutation procedures (MRPP) as implemented in PC-ORD (McCune and Mefford, 1999), using the Sørensen distance measure. MRPP was used to test differences between stand types as well as for the total, i.e. all the stand types pooled together. The test statistic “A” in MRPP describes the separation between stands. The pattern of species composition was also visually evaluated using non-metric multidimensional scaling (NMDS; McCune and Grace, 2002) as implemented in PC-ORD (McCune and Mefford, 1999), using the “slow and thorough” autopilot mode with the Sørensen distance measure. This procedure performed 40 runs with the real dataset compared with 50 randomized runs, each run with 400 iterations. This iterative ordination method is based on ranked distances between sample units in the data matrix, known as “species space” (McCune and Grace, 2002); it does not assume normally distributed data and is therefore suited for most ecological data. A final 2-dimensional solution was selected (stress 9%, instability 0.004).
successional stages, while in Pistoia it tended to decrease with significantly lower values in adult and mature stands than in young stands. 3.2. Species composition
3. Results
MRPP revealed significant differences in lichen species composition among black locust and native stands, while black locust stands of different successional stages did not differ (Table 4). The visual interpretation of the NMDS ordination (Fig. 1; total variation in species composition explained by the two axes was 88.5%; 56.3% axis 1 and 32.2% axis 2) corroborated these results, black locust stands of both regions and of different successional stage being interspersed and clearly separated from native stands. Species associated with black locust stands were mainly neutrophytic, heliophytic and nitrogen tolerant lichens, while species associated with native stands were mainly sub-acidophytic, shade tolerant, and nitrogen intolerant species. In the NMDS ordination, native stands of the two regions were separated, indicating for this forest differences in species composition which may depend on the region. Only a few species were centered in native stands of Montello, while a large species pool was associated with native stands of Pistoia.
3.1. Species richness
4. Discussion
Sixty-nine species were found (Appendix 1): 26 in Montello, and 62 in the Pistoia province, 27.5% of them being shared. The study area, as well as the stand type, had a significant effect on plot level species richness (Table 2). The overall number of species in each forest type was generally lower in Montello than in Pistoia (Table 3). All the black locust stands had the same species richness in the two study areas (Table 3). Species richness of native stands of Montello did not differ from that of all the black locust stands. On the contrary, native stands of Pistoia had a greater species richness of any black locust type of stand. In black locust stands of both study areas, nitrogen tolerant species contributed to a large part of the plot level species richness, irrespectively of the successional stage, while in native stands their contribution was negligible (Table 3). In Montello, the percentage of nitrogen tolerant species did not differ among black locust
In both regions we did not find a lichen succession in black locust stands of different age, and mature black-locust stands don't recover the diversity of epiphytic species, which are lost by the replacement of the native forests by black locust stands. The lichen biota of black locust stands differed from that of native forests, its distinctive trait being the occurrence of several nitrogen tolerant species. These lichens are usually associated with dry, well-lit conditions (Nimis and Martellos, 2008) and are very competitive in disturbed environments, being tolerant to phytotoxic pollutants and eutrophication (Loppi and Nascimbene, 2010; Van Herk et al., 2003). Their establishment in black locust stands may be favored by the same processes that drive the replacement of native trees by black locust, i.e. excessive thinning and consequent canopy openness (Motta et al., 2009). However, we would expect that, along with stand aging, canopy closure would disadvantage these lichens, triggering a
Table 2 Results of the two-way ANOVA test performed to compare plot level species richness and plot level % of nitrogen tolerant species in the two study areas (Montello and Pistoia) and in the four types of stands. Effect
Intercept Study area Stand type Study area ∗ stand type Error
Degr.of freedom
Plot level species richness SS
MS
F
P
SS
Plot level % nitrophytic species MS
F
P
1 1 3 3 48
6645 604.6 415.2 625.3 660.3
6644.6 604.57 138.4 208.42 13.75
483.03 43.94 10.06 15.15
b0.001 b0.002 b0.003 b0.004
103408.9 1251.8 18932.9 2060.7 5665.1
103408.9 1251.8 6311 686.9 118
876.18 10.6 53.47 5.82
b0.001 0.002 b0.001 0.002
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Table 3 Results of the Tukey's honest significance test for multiple comparisons (mean values±DS). Values marked with different letters (a, b, c) are significantly different at Pb 0.05. BL_Y = young black locust stands; BL_A = adult black locust stands; BL_M = mature black locust stands; Native = stands composed by native tree species. Site
Stand type
Total species richness
Plot level species richness
Plot level % nitrophytic species
Montello Montello Montello Montello Pistoia Pistoia Pistoia Pistoia
BL_Y BL_A BL_M Native BL_Y BL_A BL_M Native
16 19 13 16 24 24 26 57
8.5 ± 1a 8.8 ± 1.8a 6.7 ± 1.7a 6.3 ± 2.3a 11.1 ± 3.9a 11.8 ± 3.2a 9.3 ± 2.5a 24.4 ± 8.1b
58.5 ± 5.9abc 55.5 ± 8.6abc 58.6 ± 10.8ab 8.7 ± 9d 54.4 ± 16a 44.5 ± 8.4bc 40 ± 14.3c 14 ± 4.4d
succession toward forest lichen assemblages composed of acidophytic, shade tolerant and nitrogen intolerant species. The absence of this pattern may be caused by the co-occurrence of two different factors, one related to the management of black locust stands, and one related to black locust bark features. Management of black locust stands is based on short rotation cycles (Pividori and Grieco, 2003) implying frequent disturbances in the forest habitat which are known to favor generalist species (Nascimbene et al., 2007), while forest species need more habitat continuity (Fritz et al., 2008). Moreover, when mature stands are exploited, the few forest lichens which may be present with scattered individuals (as in our study) are completely eliminated, hindering their full establishment and further dispersal in neighboring stands. However, the permanence of nitrogen tolerant species in adult and mature black locust stands, where light availability is likely to be a limiting factor, may be explained also by considering bark features. Black locust bark has very high buffering and water retention capacity (Passialis et al., 2008) and is nutrient rich (Barkman, 1958), providing optimal substrate conditions for nitrogen tolerant species which may override the negative effect of canopy closure. The nutrient content of black locust bark is likely to be enhanced by an interaction with the soil (Gustafsson and Eriksson, 1995) whose chemistry is influenced by the nitrogen fixation activity of the bacteria associated with the roots of this tree (Boring and Swank, 1984; Rice et al., 2004). A similar situation was observed for riparian Salix-Populus forests (Nascimbene et al., 2008) where nitrogen tolerant species were found in dense canopied stands in which high soil nutrient content was maintained by frequent lime deposition. The soil–bark interaction is probably related to a mechanism of transportation of nutrients from the tree roots to the bark (Gustafsson and Eriksson, 1995). This mechanism regulates element translocation to leaves that, in black locust stands, were found to reflect soil element concentrations (Moshki and Lamersdorf, 2011).
Table 4 MRPP results. Effect size A, and P-values for the non-metric multi-response permutation procedures (MRPP) applied to the four types of stands pooled together (Total), as well as for pairwise comparisons between stand types. BL_Y = young black locust stands; BL_A = adult black locust stands; BL_M = mature black locust stands; Native = stands composed by native tree species. Effect size Total BL_Y vs BL_A BL_Y vs BL_M BL_Y vs Native BL_A vs BL_M BL_A vs Native BL_M vs Native
A = 0.13 A = 0.01 A = 0.001 A = 0.19 A = 0.001 A = 0.15 A = 0.15
P b 0.001 n.s. n.s. P b 0.001 n.s. P b 0.001 P b 0.001
Fig. 1. Ordination diagram of stands in the species space based on NMDS results. The four stand types are indicated by different symbols. BL_Y = young black locust stands; BL_A = adult black locust stands; BL_M = mature black locust stands; Native = stands composed by native tree species. Total variation in species composition explained by the two axes was 88.5% (56.3% axis 1 and 32.2% axis 2).Abbreviations of species names are according to Appendix 1; “°” marks nitrogen tolerant species according to Nimis and Martellos (2008).
The different bioclimatic conditions between the two study areas are reflected by the lichen biota of native forests, which in Pistoia is enriched by several lichens including species which in Italy mainly have a Tyrrhenian distribution (Nimis and Martellos, 2008). On the contrary, the lichen biota associated with black locust stands tends to have similar richness and traits in the two survey areas, being largely composed by widespread species whose distribution reflects a pattern of human disturbance rather than bioclimatic conditions. This suggests that forest habitat changes associated with the spread of black locust could also decrease lichen heterogeneity among bioclimatically diverse regions, favoring the establishment of few disturbance-tolerant species. However, while in Montello the contribution of these species to the plot level lichen richness did not vary across successional stages of black locust stands, in Pistoia it tended to decrease. This pattern suggests an interaction between forest conditions and climate (Ellis et al., 2009) and may reflect a higher competition pressure related to the larger regional species pool in Pistoia. On these bases, the loss of forest species associated with black locust spread may be mitigated under favorable climatic conditions, while its negative effect may be exacerbated under unfavorable climate.
Acknowledgments F. Bortignon (Padova) and C.F. Faliero (Trieste) helped during the fieldwork in Montello. Bruno Foggi (Firenze) provided constructive discussions, comments and suggestions. Four reviewers and the Editor James P. Bennett provided relevant suggestions which greatly improved the effectiveness of the study.
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Appendix 1 Species list. Species are listed in alphabetical order. Species frequency is expressed as the percentage of plots for each stand type in each study area (Montello and Pistoia) in which the species occurred (n = 7). BL_Y = young black locust stands; BL_A = adult black locust stands; BL_M = mature black locust stands; Native = stands composed by native tree species. In the second column the abbreviation of species names used in Fig. 1 is reported. “°” marks nitrogen tolerant species according to Nimis and Martellos (2008). Nomenclature follows Nimis and Martellos (2008). Species
Abbr
Frequency % Montello
Agonimia allobata (Stizenb.) P.James Amandinea punctata (Hoffm.) Coppins & Scheid. Aplotomma turgida (A.Massal.) A.Massal. Arthonia radiata (Pers.) Ach. Arthonia spadicea Leight. Calicium abietinum Pers. Caloplaca ferruginea (Huds.) Th.Fr. Caloplaca obscurella (Körb.) Th.Fr. Caloplaca pyracea (Ach.) Th.Fr. Candelaria concolor (Dicks.) Stein° Candelariella efflorescens auct. eur.° Candelariella reflexa (Nyl.) Lettau° Candelariella xanthostigma (Ach.) Lettau Catillaria nigroclavata (Nyl.) Schuler Chaenotheca brunneola (Ach.) Müll.Arg. Cladonia coniocraea (Flörke) Spreng. Cladonia fimbriata (L.) Fr. Dimerella pineti (Ach.) Vezda Evernia prunastri (L.) Ach. Flavoparmelia caperata (L.) Hale Graphis scripta (L.) Ach. Hyperphyscia adglutinata (Flörke) H.Mayrhofer and Poelt° Hypogymnia physodes (L.) Nyl. Hypogymnia tubulosa (Schaer.) Hav. Lecania cyrtella (Ach.) Th.Fr. Lecanora carpinea (L.) Vain. Lecanora chlarotera Nyl.° Lecanora expallens Ach. Lecanora intumescens (Rebent.) Rabenh. Lecidella elaeochroma (Ach.) M.Choisy Lecidella flavosorediata (Vezda) Hertel and Leuckert Lepraria incana (L.) Ach. Lepraria lobificans Nyl. Melanelixia fuliginosa (Duby) O. Blanco, A. Crespo, Divakar, Essl., D. Hawksw. and Lumbsch Melanelixia subaurifera (Nyl.) O. Blanco, A. Crespo, Divakar, Essl., D. Hawksw. and Lumbsch Melanohalea laciniatula (H.Olivier) O.Blanco, A.Crespo, Divakar, Essl., D.Hawksw. and Lumbsch Normandina pulchella (Borrer) Nyl. Ochrolechia pallescens (L.) A.Massal. Opegrapha atra Pers. Parmelia saxatilis (L.) Ach. Parmelia submontana Hale Parmelia sulcata Taylor Parmelina pastillifera (Harm.) Hale Parmelina tiliacea (Hoffm.) Hale Parmotrema perlatum (Huds.) M.Choisy Pertusaria albescens (Huds.) M.Choisy and Werner Pertusaria amara (Ach.) Nyl. Pertusaria flavida (DC.) J.R.Laundon Pertusaria hymenea (Ach.) Schaer. Pertusaria leioplaca DC. Pertusaria pertusa (Weigel) Tuck. Phaeophyscia chloantha (Ach.) Moberg Phaeophyscia hirsuta (Mereschk.) Essl. Phaeophyscia orbicularis (Neck.) Moberg° Phlyctis argena (Spreng.) Flot. Physcia adscendens (Fr.) H.Olivier° Physcia stellaris (L.) Nyl. Physconia distorta (With.) J.R.Laundon Pleurosticta acetabulum (Neck.) Elix and Lumbsch Pseudevernia furfuracea (L.) Zopf v. furfuracea Punctelia borreri (Sm.) Krog Punctelia subrudecta (Nyl.) Krog Pyrenula nitida (Weigel) Ach. Ramalina fraxinea (L.) Ach. Rinodina exigua (Ach.) Gray Scoliciosporum umbrinum (Ach.) Arnold Tephromela atra v. torulosa (Flot.) Hafellner Usnea sp. Xanthoria parietina (L.) Th.Fr.°
agoal ampun apltur artrad artspa calabi calfer calobs calpyr cancon caneff canref canxan catnig chabru clacon clafim dimpin evepru flacap grascr hypadg hypphy hyptub leccyr leccar lecchl lecexp lecint lecela lecifla lepinc leplob melful melsub mellac norpul ochpal opatr parsax parsub parsul parpas partil parper peralb perama perfla perhym perlei perper phachl phahir phaorb phlarg phyads physte phydist pleace psefur punbor punsub pyrnit ramfra rinexi scoumb tepatr usnsp xanpar
Pistoia
BL_Y
BL_A
BL_M
Native
BL_Y
BL_A
BL_M
Native
0 0 0 0 0 0 0 0 0 100 14 100 0 86 0 0 0 29 0 0 0 100 0 0 71 0 57 0 0 29 0 0 14 0 0 0 14 0 0 0 0 0 0 0 0 0 0 0 0 0 0 100 14 0 0 100 0 0 0 0 29 0 0 0 0 0 0 0 0
14 0 0 0 0 0 0 14 0 100 71 100 43 71 0 0 0 71 0 0 0 100 0 0 14 0 14 0 0 14 0 0 0 0 0 0 57 0 0 0 0 0 0 0 0 0 0 0 0 0 0 71 0 14 0 86 0 0 0 0 14 0 0 0 0 0 0 0 14
0 0 0 0 0 0 0 0 0 100 14 100 0 29 0 0 0 57 0 0 0 100 0 0 43 0 14 0 0 14 0 0 0 0 0 0 29 0 0 0 0 0 0 0 0 0 0 0 0 0 0 86 0 0 0 86 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 100 0 0 0 0 14 0 29 14 0 0 43 0 100 0 29 0 0 0 0 0 0 0 0 0 0 29 14 100 0 0 0 71 0 0 0 0 0 0 0 43 0 0 0 0 0 0 14 14 0 0 0 0 0 0 0 14 0 0 0 0 0 0 0 0
0 0 0 29 0 0 0 0 0 86 0 100 43 43 0 14 0 0 0 29 0 100 0 0 43 29 29 0 0 57 0 14 0 14 0 0 43 0 0 0 0 29 0 14 0 0 0 0 0 0 14 0 0 71 0 100 0 14 0 0 0 29 100 0 0 0 0 0 71
0 0 0 0 0 0 0 0 0 71 0 100 86 43 0 0 0 0 0 57 0 86 0 0 57 14 71 0 0 43 0 14 0 43 0 0 100 1 0 0 0 0 29 0 0 14 0 0 0 0 0 0 14 14 71 14 100 0 0 0 0 0 29 100 1 0 0 0 0 0 14
0 14 0 14 0 0 0 0 0 43 0 71 29 57 0 29 0 29 0 0 14 57 0 0 0 14 14 0 0 14 0 29 0 0 0 0 0 0 0 0 0 0 0 29 0 0 0 0 0 0 0 29 14 71 14 86 0 14 0 0 0 14 0 14 14 0 0 0 0
0 71 43 43 0 14 14 0 29 14 0 57 57 0 14 100 29 29 43 86 0 14 43 14 0 71 71 14 57 57 0 71 0 86 29 14 100 14 29 71 14 86 29 86 71 86 14 71 29 43 86 0 0 14 86 71 14 14 14 14 0 14 14 86 29 14 14 14 14
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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Mature non-native black-locust (Robinia pseudoacacia L.) forest does not regain the lichen diversity of the natural forest Juri Nascimbene a,⁎, Pier Luigi Nimis a, Renato Benesperi b a b
Department of Life Sciences, University of Trieste, via Giorgieri 10-34100, Trieste, Italy Department of Evolutionary Biology, University of Florence, via La Pira 4, Florence, Italy
a r t i c l e
i n f o
Article history: Received 21 November 2011 Received in revised form 23 January 2012 Accepted 24 January 2012 Available online 16 February 2012 Keywords: Bark features Epiphytic lichens Forest management Habitat changes Species composition Species richness
a b s t r a c t The responses of lichens to habitat changes caused by invasive trees are poorly understood. Invasive forest trees may impact epiphytic lichens by altering both substrate and stand conditions. Previous research has demonstrated that black locust invasion, associated with intensive exploitation of native oak forests, led to dramatic shifts in lichen composition. However, it is not clear if, along with stand aging, black locust formations regain forest species. The main aim of this study was to test whether the succession of black locust stands promotes a lichen succession leading to assemblages in mature black locust stands which are similar to those of native forests. To test the influence of macro-environmental conditions, we performed the study in two bioclimatically different areas of Italy. The epiphytic lichen biota of native oak and chestnut stands was compared with that of black locust stands of different successional stages. In both regions we did not find a lichen succession in black locust stands of different age, and mature black-locust stands did not recover the diversity of epiphytic species, which are lost by the replacement of the native forests by black locust. The absence of this pattern may be caused by factors related to the management of black locust stands, and to bark features. The different bioclimatic conditions between the two study areas may explain differences in the lichen biota of native forests, while that of black locust stands tend to be similar between regions, suggesting that forest habitat changes associated with the spread of black locust could decrease lichen diversity among bioclimatically different regions. © 2012 Elsevier B.V. All rights reserved.
1. Introduction Epiphytic lichens are among the most sensitive components of the forest biota, being responsive to climate, forest structure, and substrate type (Marini et al., 2011; Fritz et al., 2008). In particular, they are threatened by human-related alterations of forests (Johansson, 2008), such as intensive management or the replacement of native forests with secondary formations (e.g. Aragón et al., 2010; Hedenås and Ericson, 2000; Humphrey et al., 2002; Moning and Müller, 2009; Nascimbene et al., 2007). These processes alter microclimatic conditions under the canopy as well as the availability of host tree species in the landscape, threatening forest- and substrate-specialist lichens (Rogers and Ryel, 2008). Despite the fact that a large body of literature has grown to evaluate the effects of forest management on epiphytic lichens (e.g. Aragón et al., 2010; Humphrey et al., 2002; Johansson, 2008; Nascimbene et al., 2007), their response to habitat changes caused by invasive trees is poorly understood.
⁎ Corresponding author. Tel./fax: + 39 043942894. E-mail address: [email protected] (J. Nascimbene). 0048-9697/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.scitotenv.2012.01.051
Invasive forest trees which replace native forest vegetation may impact the forest biota, acting as habitat ‘transformers’ (Richardson and Reimánek, 2011). In particular, they may impact epiphytic organisms by altering both substrate and stand conditions related to their management. An example of this process is provided by the spread of black locust (Robinia pseudoacacia L.) which in northern and central Italy is replacing native broadleaf forests over large areas from lowlands to the lower montane belt (Caprio et al., 2009; Motta et al., 2009). This process is favored by the fast and highly competitive growth of this tree, intensive exploitation of native forests, chestnut blight, and urbanization (Celesti-Grapow et al., 2009; Motta et al., 2009). In a previous study, Nascimbene and Marini (2010) demonstrated that black locust invasion, associated with intensive exploitation of oak native forests, led to dramatic shifts in lichen composition which mainly involved forest-specialist lichens. That study showed that the lichen biota of native oak remnants was mainly composed of forest-dwelling acidophytic and nitrogen intolerant species, while that of black locust forests was mainly composed of nitrogen tolerant species related to disturbed habitats. However, in that study only relatively young black locust stands were considered and it is not clear if, along with stand aging, mature
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black locust formations regain forest species which may migrate from native remnants. We therefore hypothesized that along with stand aging (i.e. increasing shading and humidity under the canopy, increasing tree age) a lichen succession should evolve. This process should lead to lichen assemblages composed by forest acidophytic species since bark pH of black locust, ranging between 4 and 5 (Passialis et al., 2008) and bark texture with deep cervices are similar to that of deciduous oaks (Barkman, 1958). On the other hand, we should also consider two additional factors: 1) in Italy, black locust forests are mainly managed with short-rotation cycles for fire-wood production (Pividori and Grieco, 2003). This silviculture management based on a very frequent disturbance regime may hinder black locust stands evolving adequate habitat continuity for forest lichen species; 2) other bark features than pH (e.g. high buffer and water capacity, nutrient enrichment) may drive species-host affinities between lichens and black locust trees. In this case, we hypothesized that these factors may hamper a lichen succession along with stand aging, hindering black locust forests from acquiring lichen assemblages comparable to those of native forests. In this study, we addressed these hypotheses and compared epiphytic lichen species richness and composition of different successional stages of black locust stands, and coppiced stands dominated by native broadleaved trees (mainly oaks). The main aim was to test whether the succession of black locust stands promoted a lichen succession leading to assemblages in mature black locust stands which are similar to those of native forests. To test the influence of macro-environmental conditions on the patterns of lichen diversity across stand types, we performed the study in two bioclimatically different areas of Italy. 2. Materials and methods 2.1. Study areas The study was carried out in two forested areas of Italy reflecting different bioclimatic conditions: 1) Montello, in NE Italy (Veneto, 46°48′ N, 12°08′ E), in the dry sub-Mediterranean region where the epiphytic lichen flora is generally poor and the suboceanic component is weak (Nimis and Martellos, 2008), and 2) the hills in the province of Pistoia, in Central Italy (Toscana, central Apennine, 43°59′ N, 10°53′ E), in the humid sub Mediterranean region which is under the influence of humid maritime winds, promoting more favorable conditions for epiphytic lichens, including several sub oceanic species (Nimis and Martellos, 2008). The Montello area is a large hill in the northern part of the Venetian plain (NE-Italy, Veneto, Treviso), extending over 5000 ha. The mean elevation is 200 m (maximum 369 m), 100 m higher than the surrounding plain. Mean annual temperature is 12.9 °C, January being the coldest month (mean temperature 3–4 °C) and July the warmest one (mean temperature 22.7 °C). Mean annual rainfall is 1100 mm, with maxima in spring and autumn. Forty percent of the Montello area is managed for extensive agriculture (arable fields, hay meadows, and vineyards), while the remnant is covered by forests. The forest landscape is a rather continuous black locust matrix with interspersed oak-dominated patches. Pure black locust stands are the main forest type, covering over 90% of the forested area. Remnant patches of oak forest (Quercus petraea (Mattuschka) Liebl. and Quercus robur L.) can be found in the central part of the hill, being coppiced for firewood production. The hilly area in the Province of Pistoia is delimited northward by the Tuscan-Emilian Apennines ridge and southward by the Pistoia plain. Elevation ranges between 100 and 900 m. Mean annual temperature is 14.4 °C and 9.4° in the lower (100–500 m) and higher (500– 900 m) areas respectively. Mean annual rainfall ranges between 1300 and 1900 mm with two maxima in spring and autumn. At lower elevations, the landscape is dominated by cultivated (olive-groves and
vineyards) and forested areas mainly dominated by black locust formations. At higher elevations, native forests prevail, while black locust formations are interspersed in a matrix of deciduous broadleaf formations including chestnut, oak (Quercus cerris L.) and hop hornbeam, coppiced for firewood production. In both sites, black locust forests are managed with 20–30 year rotation cycles, mainly for firewood production. Stands are usually clear-cut and spontaneously replaced by a new generation of trees. 2.2. Sampling design According to the stage of the management cycle, black locust stands were classified into three main forest successional stages (Table 1) corresponding to even-sized and even-aged formations: 1) young stands including trees with a circumference of 20–40 cm (age c.10 years), 2) intermediate (adult) stands including trees with a circumference of 40–60 cm (age c.20 years), and, 3) mature stands, including trees with a circumference >60 cm (age 30–40 years). For each type of black locust forest stand, as well as for forest stands composed of native species, seven 30 × 30 m plots were randomly selected in different parts of the two study areas in order to encompass the variability of each stand type in each area. In Montello, native stands were generally older (60–90 years) and have higher mean DBH than any mature black locust stand, while in Tuscany it was possible to find native stands whose age (30–50 years) and mean DBH are comparable to those of black locust mature stands. Slope, altitude, and canopy cover were comparable among stand types in each area (Table 1). In particular, canopy cover was always higher than 75%. Minimum distance between plots of the same stand type was greater than 500 m to reduce spatial dependence. The borders of the plots were at least 30 m far from the forest edge to avoid any edge-effects. In black locust stands, only black locust individuals were considered for the lichen sampling, while in native tree stands the dominant species were considered: oaks in Montello, and chestnut (5 plots) and oak (2 plots) in the Pistoia province. In each plot, six trees (circumference ≥40 cm) were selected for lichen inventory by random sampling, for a total of 336 trees (42 in each stand type in each of the two study areas). In mature black locust stands, the mean circumference of sampled trees was 90 ± 9 cm and 93 ± 14 cm in Montello and Pistoia respectively, while that of sampled trees in native stands was 153 ± 24 cm for Montello and 98 ± 25 cm for Pistoia. The lichen sampling followed the European guidelines for lichen monitoring (Asta et al., 2002). Lichens were sampled using four standard frames of 10× 50 cm as sampling grids, subdivided into five 10× 10 cm quadrats, which were attached to the tree trunk at the cardinal points with the low side at 100 cm from the ground. All lichen species inside the frames were listed, and their frequency was computed as the number of 10 × 10 cm quadrats in which the species occurred. Nomenclature of lichens followed Nimis and Martellos (2008). 2.3. Data analysis A two-way analysis of variance (ANOVA) was applied to test the effects of study area and stand type on species richness (cumulative number of species per plot calcutated as the sum of the species found on the six trees) and on the contribution of the guild of nitrogen tolerant species (expressed as percentage of the plot species richness) defined by the ecological indicator value for eutrophication ranging from 4 (rather high eutrophication) to 5 (very high eutrophication) in the on-line checklist of Italian lichens (Nimis and Martellos, 2008). These species are considered as indicative of substrate eutrophication and habitat disturbance. In these analyses, the plot was used as replicate to avoid pseudo-replication. After the ANOVA, a Tukey's honest significance test for multiple
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Table 1 Mean features (± SD) of the four types of stands in the two sites (Montello and Pistoia province). BL_Y = young black locust stands; BL_A = adult black locust stands; BL_M = mature black locust stands; Native = stands composed by native tree species. Montello
Mean circumference (cm) Mean number of trees/plot Canopy cover % Slope (%) Elevation (m)
Pistoia
BL_Y
BL_A
BL_M
Native
BL_Y
BL_A
BL_M
Native
36.2 ± 3.6a 102 ± 13a 79.3 ± 6.7a 5.7 ± 3.5a 240 ± 68 a
50 ± 8.6b 96 ± 28a 80.7 ± 7.3a 6 ± 4.5a 241 ± 59 a
68.8 ± 2.8c 92 ± 6a 86.4 ± 5.5a 7.1 ± 6.2a 231 ± 53 a
128.8 ± 16.9 d 36 ± 14b 85.4 ± 6.7a 8.6 ± 6.3a 216 ± 41a
36 ± 4a 120 ± 111a 80 ± 6.4a 9 ± 4.9a 465 ± 163a
47.7 ± 5.2b 98 ± 20a 85.7 ± 4.5a 14.2 ± 7.8a 488 ± 195a
68.1 ± 9.2c 70 ± 5b 86.4 ± 6.2a 11.4 ± 8.5a 462 ± 247a
77.8 ± 15c 65 ± 8b 83.5 ± 6.9a 5 ± 3.6a 636 ± 244a
Significant different values among stand types (P b 0.05; one-way ANOVA test for each region) are marked with different letters (a, b, c, d).
comparison was applied to detect differences between stand types (P b 00.05). Compositional differences among stand types were tested by multi response permutation procedures (MRPP) as implemented in PC-ORD (McCune and Mefford, 1999), using the Sørensen distance measure. MRPP was used to test differences between stand types as well as for the total, i.e. all the stand types pooled together. The test statistic “A” in MRPP describes the separation between stands. The pattern of species composition was also visually evaluated using non-metric multidimensional scaling (NMDS; McCune and Grace, 2002) as implemented in PC-ORD (McCune and Mefford, 1999), using the “slow and thorough” autopilot mode with the Sørensen distance measure. This procedure performed 40 runs with the real dataset compared with 50 randomized runs, each run with 400 iterations. This iterative ordination method is based on ranked distances between sample units in the data matrix, known as “species space” (McCune and Grace, 2002); it does not assume normally distributed data and is therefore suited for most ecological data. A final 2-dimensional solution was selected (stress 9%, instability 0.004).
successional stages, while in Pistoia it tended to decrease with significantly lower values in adult and mature stands than in young stands. 3.2. Species composition
3. Results
MRPP revealed significant differences in lichen species composition among black locust and native stands, while black locust stands of different successional stages did not differ (Table 4). The visual interpretation of the NMDS ordination (Fig. 1; total variation in species composition explained by the two axes was 88.5%; 56.3% axis 1 and 32.2% axis 2) corroborated these results, black locust stands of both regions and of different successional stage being interspersed and clearly separated from native stands. Species associated with black locust stands were mainly neutrophytic, heliophytic and nitrogen tolerant lichens, while species associated with native stands were mainly sub-acidophytic, shade tolerant, and nitrogen intolerant species. In the NMDS ordination, native stands of the two regions were separated, indicating for this forest differences in species composition which may depend on the region. Only a few species were centered in native stands of Montello, while a large species pool was associated with native stands of Pistoia.
3.1. Species richness
4. Discussion
Sixty-nine species were found (Appendix 1): 26 in Montello, and 62 in the Pistoia province, 27.5% of them being shared. The study area, as well as the stand type, had a significant effect on plot level species richness (Table 2). The overall number of species in each forest type was generally lower in Montello than in Pistoia (Table 3). All the black locust stands had the same species richness in the two study areas (Table 3). Species richness of native stands of Montello did not differ from that of all the black locust stands. On the contrary, native stands of Pistoia had a greater species richness of any black locust type of stand. In black locust stands of both study areas, nitrogen tolerant species contributed to a large part of the plot level species richness, irrespectively of the successional stage, while in native stands their contribution was negligible (Table 3). In Montello, the percentage of nitrogen tolerant species did not differ among black locust
In both regions we did not find a lichen succession in black locust stands of different age, and mature black-locust stands don't recover the diversity of epiphytic species, which are lost by the replacement of the native forests by black locust stands. The lichen biota of black locust stands differed from that of native forests, its distinctive trait being the occurrence of several nitrogen tolerant species. These lichens are usually associated with dry, well-lit conditions (Nimis and Martellos, 2008) and are very competitive in disturbed environments, being tolerant to phytotoxic pollutants and eutrophication (Loppi and Nascimbene, 2010; Van Herk et al., 2003). Their establishment in black locust stands may be favored by the same processes that drive the replacement of native trees by black locust, i.e. excessive thinning and consequent canopy openness (Motta et al., 2009). However, we would expect that, along with stand aging, canopy closure would disadvantage these lichens, triggering a
Table 2 Results of the two-way ANOVA test performed to compare plot level species richness and plot level % of nitrogen tolerant species in the two study areas (Montello and Pistoia) and in the four types of stands. Effect
Intercept Study area Stand type Study area ∗ stand type Error
Degr.of freedom
Plot level species richness SS
MS
F
P
SS
Plot level % nitrophytic species MS
F
P
1 1 3 3 48
6645 604.6 415.2 625.3 660.3
6644.6 604.57 138.4 208.42 13.75
483.03 43.94 10.06 15.15
b0.001 b0.002 b0.003 b0.004
103408.9 1251.8 18932.9 2060.7 5665.1
103408.9 1251.8 6311 686.9 118
876.18 10.6 53.47 5.82
b0.001 0.002 b0.001 0.002
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Table 3 Results of the Tukey's honest significance test for multiple comparisons (mean values±DS). Values marked with different letters (a, b, c) are significantly different at Pb 0.05. BL_Y = young black locust stands; BL_A = adult black locust stands; BL_M = mature black locust stands; Native = stands composed by native tree species. Site
Stand type
Total species richness
Plot level species richness
Plot level % nitrophytic species
Montello Montello Montello Montello Pistoia Pistoia Pistoia Pistoia
BL_Y BL_A BL_M Native BL_Y BL_A BL_M Native
16 19 13 16 24 24 26 57
8.5 ± 1a 8.8 ± 1.8a 6.7 ± 1.7a 6.3 ± 2.3a 11.1 ± 3.9a 11.8 ± 3.2a 9.3 ± 2.5a 24.4 ± 8.1b
58.5 ± 5.9abc 55.5 ± 8.6abc 58.6 ± 10.8ab 8.7 ± 9d 54.4 ± 16a 44.5 ± 8.4bc 40 ± 14.3c 14 ± 4.4d
succession toward forest lichen assemblages composed of acidophytic, shade tolerant and nitrogen intolerant species. The absence of this pattern may be caused by the co-occurrence of two different factors, one related to the management of black locust stands, and one related to black locust bark features. Management of black locust stands is based on short rotation cycles (Pividori and Grieco, 2003) implying frequent disturbances in the forest habitat which are known to favor generalist species (Nascimbene et al., 2007), while forest species need more habitat continuity (Fritz et al., 2008). Moreover, when mature stands are exploited, the few forest lichens which may be present with scattered individuals (as in our study) are completely eliminated, hindering their full establishment and further dispersal in neighboring stands. However, the permanence of nitrogen tolerant species in adult and mature black locust stands, where light availability is likely to be a limiting factor, may be explained also by considering bark features. Black locust bark has very high buffering and water retention capacity (Passialis et al., 2008) and is nutrient rich (Barkman, 1958), providing optimal substrate conditions for nitrogen tolerant species which may override the negative effect of canopy closure. The nutrient content of black locust bark is likely to be enhanced by an interaction with the soil (Gustafsson and Eriksson, 1995) whose chemistry is influenced by the nitrogen fixation activity of the bacteria associated with the roots of this tree (Boring and Swank, 1984; Rice et al., 2004). A similar situation was observed for riparian Salix-Populus forests (Nascimbene et al., 2008) where nitrogen tolerant species were found in dense canopied stands in which high soil nutrient content was maintained by frequent lime deposition. The soil–bark interaction is probably related to a mechanism of transportation of nutrients from the tree roots to the bark (Gustafsson and Eriksson, 1995). This mechanism regulates element translocation to leaves that, in black locust stands, were found to reflect soil element concentrations (Moshki and Lamersdorf, 2011).
Table 4 MRPP results. Effect size A, and P-values for the non-metric multi-response permutation procedures (MRPP) applied to the four types of stands pooled together (Total), as well as for pairwise comparisons between stand types. BL_Y = young black locust stands; BL_A = adult black locust stands; BL_M = mature black locust stands; Native = stands composed by native tree species. Effect size Total BL_Y vs BL_A BL_Y vs BL_M BL_Y vs Native BL_A vs BL_M BL_A vs Native BL_M vs Native
A = 0.13 A = 0.01 A = 0.001 A = 0.19 A = 0.001 A = 0.15 A = 0.15
P b 0.001 n.s. n.s. P b 0.001 n.s. P b 0.001 P b 0.001
Fig. 1. Ordination diagram of stands in the species space based on NMDS results. The four stand types are indicated by different symbols. BL_Y = young black locust stands; BL_A = adult black locust stands; BL_M = mature black locust stands; Native = stands composed by native tree species. Total variation in species composition explained by the two axes was 88.5% (56.3% axis 1 and 32.2% axis 2).Abbreviations of species names are according to Appendix 1; “°” marks nitrogen tolerant species according to Nimis and Martellos (2008).
The different bioclimatic conditions between the two study areas are reflected by the lichen biota of native forests, which in Pistoia is enriched by several lichens including species which in Italy mainly have a Tyrrhenian distribution (Nimis and Martellos, 2008). On the contrary, the lichen biota associated with black locust stands tends to have similar richness and traits in the two survey areas, being largely composed by widespread species whose distribution reflects a pattern of human disturbance rather than bioclimatic conditions. This suggests that forest habitat changes associated with the spread of black locust could also decrease lichen heterogeneity among bioclimatically diverse regions, favoring the establishment of few disturbance-tolerant species. However, while in Montello the contribution of these species to the plot level lichen richness did not vary across successional stages of black locust stands, in Pistoia it tended to decrease. This pattern suggests an interaction between forest conditions and climate (Ellis et al., 2009) and may reflect a higher competition pressure related to the larger regional species pool in Pistoia. On these bases, the loss of forest species associated with black locust spread may be mitigated under favorable climatic conditions, while its negative effect may be exacerbated under unfavorable climate.
Acknowledgments F. Bortignon (Padova) and C.F. Faliero (Trieste) helped during the fieldwork in Montello. Bruno Foggi (Firenze) provided constructive discussions, comments and suggestions. Four reviewers and the Editor James P. Bennett provided relevant suggestions which greatly improved the effectiveness of the study.
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Appendix 1 Species list. Species are listed in alphabetical order. Species frequency is expressed as the percentage of plots for each stand type in each study area (Montello and Pistoia) in which the species occurred (n = 7). BL_Y = young black locust stands; BL_A = adult black locust stands; BL_M = mature black locust stands; Native = stands composed by native tree species. In the second column the abbreviation of species names used in Fig. 1 is reported. “°” marks nitrogen tolerant species according to Nimis and Martellos (2008). Nomenclature follows Nimis and Martellos (2008). Species
Abbr
Frequency % Montello
Agonimia allobata (Stizenb.) P.James Amandinea punctata (Hoffm.) Coppins & Scheid. Aplotomma turgida (A.Massal.) A.Massal. Arthonia radiata (Pers.) Ach. Arthonia spadicea Leight. Calicium abietinum Pers. Caloplaca ferruginea (Huds.) Th.Fr. Caloplaca obscurella (Körb.) Th.Fr. Caloplaca pyracea (Ach.) Th.Fr. Candelaria concolor (Dicks.) Stein° Candelariella efflorescens auct. eur.° Candelariella reflexa (Nyl.) Lettau° Candelariella xanthostigma (Ach.) Lettau Catillaria nigroclavata (Nyl.) Schuler Chaenotheca brunneola (Ach.) Müll.Arg. Cladonia coniocraea (Flörke) Spreng. Cladonia fimbriata (L.) Fr. Dimerella pineti (Ach.) Vezda Evernia prunastri (L.) Ach. Flavoparmelia caperata (L.) Hale Graphis scripta (L.) Ach. Hyperphyscia adglutinata (Flörke) H.Mayrhofer and Poelt° Hypogymnia physodes (L.) Nyl. Hypogymnia tubulosa (Schaer.) Hav. Lecania cyrtella (Ach.) Th.Fr. Lecanora carpinea (L.) Vain. Lecanora chlarotera Nyl.° Lecanora expallens Ach. Lecanora intumescens (Rebent.) Rabenh. Lecidella elaeochroma (Ach.) M.Choisy Lecidella flavosorediata (Vezda) Hertel and Leuckert Lepraria incana (L.) Ach. Lepraria lobificans Nyl. Melanelixia fuliginosa (Duby) O. Blanco, A. Crespo, Divakar, Essl., D. Hawksw. and Lumbsch Melanelixia subaurifera (Nyl.) O. Blanco, A. Crespo, Divakar, Essl., D. Hawksw. and Lumbsch Melanohalea laciniatula (H.Olivier) O.Blanco, A.Crespo, Divakar, Essl., D.Hawksw. and Lumbsch Normandina pulchella (Borrer) Nyl. Ochrolechia pallescens (L.) A.Massal. Opegrapha atra Pers. Parmelia saxatilis (L.) Ach. Parmelia submontana Hale Parmelia sulcata Taylor Parmelina pastillifera (Harm.) Hale Parmelina tiliacea (Hoffm.) Hale Parmotrema perlatum (Huds.) M.Choisy Pertusaria albescens (Huds.) M.Choisy and Werner Pertusaria amara (Ach.) Nyl. Pertusaria flavida (DC.) J.R.Laundon Pertusaria hymenea (Ach.) Schaer. Pertusaria leioplaca DC. Pertusaria pertusa (Weigel) Tuck. Phaeophyscia chloantha (Ach.) Moberg Phaeophyscia hirsuta (Mereschk.) Essl. Phaeophyscia orbicularis (Neck.) Moberg° Phlyctis argena (Spreng.) Flot. Physcia adscendens (Fr.) H.Olivier° Physcia stellaris (L.) Nyl. Physconia distorta (With.) J.R.Laundon Pleurosticta acetabulum (Neck.) Elix and Lumbsch Pseudevernia furfuracea (L.) Zopf v. furfuracea Punctelia borreri (Sm.) Krog Punctelia subrudecta (Nyl.) Krog Pyrenula nitida (Weigel) Ach. Ramalina fraxinea (L.) Ach. Rinodina exigua (Ach.) Gray Scoliciosporum umbrinum (Ach.) Arnold Tephromela atra v. torulosa (Flot.) Hafellner Usnea sp. Xanthoria parietina (L.) Th.Fr.°
agoal ampun apltur artrad artspa calabi calfer calobs calpyr cancon caneff canref canxan catnig chabru clacon clafim dimpin evepru flacap grascr hypadg hypphy hyptub leccyr leccar lecchl lecexp lecint lecela lecifla lepinc leplob melful melsub mellac norpul ochpal opatr parsax parsub parsul parpas partil parper peralb perama perfla perhym perlei perper phachl phahir phaorb phlarg phyads physte phydist pleace psefur punbor punsub pyrnit ramfra rinexi scoumb tepatr usnsp xanpar
Pistoia
BL_Y
BL_A
BL_M
Native
BL_Y
BL_A
BL_M
Native
0 0 0 0 0 0 0 0 0 100 14 100 0 86 0 0 0 29 0 0 0 100 0 0 71 0 57 0 0 29 0 0 14 0 0 0 14 0 0 0 0 0 0 0 0 0 0 0 0 0 0 100 14 0 0 100 0 0 0 0 29 0 0 0 0 0 0 0 0
14 0 0 0 0 0 0 14 0 100 71 100 43 71 0 0 0 71 0 0 0 100 0 0 14 0 14 0 0 14 0 0 0 0 0 0 57 0 0 0 0 0 0 0 0 0 0 0 0 0 0 71 0 14 0 86 0 0 0 0 14 0 0 0 0 0 0 0 14
0 0 0 0 0 0 0 0 0 100 14 100 0 29 0 0 0 57 0 0 0 100 0 0 43 0 14 0 0 14 0 0 0 0 0 0 29 0 0 0 0 0 0 0 0 0 0 0 0 0 0 86 0 0 0 86 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 100 0 0 0 0 14 0 29 14 0 0 43 0 100 0 29 0 0 0 0 0 0 0 0 0 0 29 14 100 0 0 0 71 0 0 0 0 0 0 0 43 0 0 0 0 0 0 14 14 0 0 0 0 0 0 0 14 0 0 0 0 0 0 0 0
0 0 0 29 0 0 0 0 0 86 0 100 43 43 0 14 0 0 0 29 0 100 0 0 43 29 29 0 0 57 0 14 0 14 0 0 43 0 0 0 0 29 0 14 0 0 0 0 0 0 14 0 0 71 0 100 0 14 0 0 0 29 100 0 0 0 0 0 71
0 0 0 0 0 0 0 0 0 71 0 100 86 43 0 0 0 0 0 57 0 86 0 0 57 14 71 0 0 43 0 14 0 43 0 0 100 1 0 0 0 0 29 0 0 14 0 0 0 0 0 0 14 14 71 14 100 0 0 0 0 0 29 100 1 0 0 0 0 0 14
0 14 0 14 0 0 0 0 0 43 0 71 29 57 0 29 0 29 0 0 14 57 0 0 0 14 14 0 0 14 0 29 0 0 0 0 0 0 0 0 0 0 0 29 0 0 0 0 0 0 0 29 14 71 14 86 0 14 0 0 0 14 0 14 14 0 0 0 0
0 71 43 43 0 14 14 0 29 14 0 57 57 0 14 100 29 29 43 86 0 14 43 14 0 71 71 14 57 57 0 71 0 86 29 14 100 14 29 71 14 86 29 86 71 86 14 71 29 43 86 0 0 14 86 71 14 14 14 14 0 14 14 86 29 14 14 14 14
202
J. Nascimbene et al. / Science of the Total Environment 421–422 (2012) 197–202
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