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POLISH JOURNAL OF ECOLOGY 60 2 225–240 2012 (Pol. J. Ecol.)
Regular research paper
Agnieszka SŁABY* and Maja LISOWSKA
Zdzisław Czeppe Department of Polar Research and Documentation, Institute of Botany, Jagiellonian University, 27 Kopernika st, 31-501 Cracow, Poland *e-mails: [email protected] (corresponding author), [email protected]
EPIPHYTIC LICHEN RECOLONIZATION IN THE CENTRE OF CRACOW (SOUTHERN POLAND) AS A RESULT OF AIR QUALITY IMPROVEMENT
ABSTRACT: Epiphytic lichen distribution Cecchetti 2001). They take up water, to- and diversity were investigated in seven locali- gether with different dissolved contaminants, ties in the centre of Cracow (South Poland). Field over the entire surface of the organism, di- studies were carried out in the years 2007–2009. rectly from the atmosphere (Nimis and A total of 39 species were recorded at 434 sites; Purvis 2002). Direct relationship between 6 species are new to Cracow. Compared to pre- lichen survival and air pollution was first no- vious surveys, the overall situation has generally improved, with higher lichen species richness and ticed by Nylander in Paris in the year 1866. cover rate. The area of former ‘lichen desert’ in the Numerous further studies have been focused city centre has disappeared and it has been colo- on the influence of sulphur dioxide (SO2) (e.g. Nash 1973) and nitrogen oxides (NO ) (e.g. nized by SO2 sensitive macrolichen species. Dom- x inance of nitrogen- and dust-tolerant species has Nash 1976, van Dobben et al. 2001) on li-
been observed. The health of lichen thalli has im- chens. Methods of SO2 level assessment using proved and many young specimens were recorded epiphytic lichens (e.g. Hawksworth and in the study area. These changes follow air quality Rose 1970) have been widely used in urban improvement, mainly the SO2 decline, during the and industrial areas in Europe since 1970s. Li- last twenty years. Transport-related NO and dust x chens have also been used as biomonitors of have become the main pollutants in the centre of many other contaminants, e.g. heavy metals, Cracow. The recolonization process seems to be not completed yet and further improvement in li- fluorides, radionuclides, phosphorus, diox- chen distribution and diversity is expected. Thus ins, furans (e.g. Gilbert 1971, Olech et al. long-term biomonitoring is required. 1981, Conti and Cecchetti 2001, Garty et al. 2003, Augusto et al. 2007, Augusto KEY WORDS: lichens, recolonization, air et al. 2009). Lichens respond rapidly to de-
pollution, SO2, NOx creasing concentrations of air pollution, thus even annual changes of the air pollutants can 1. INTRODUCTION be detected using lichens (Loppi et al. 2004).
For many years SO2 has been considered Lichens are effective bioindicators of air as the main and most harmful substance caus- quality because of their morphological and ing decline of lichens in cities and industrial physiological characteristics (Conti and regions throughout the world (Purvis et al. 226 Agnieszka Słaby and Maja Lisowska
2003). The places where no epiphytic lichens and lichen bioindication were investigated can exist are called ‘lichen deserts’ (Purvis by Lojka (1868), Jabłoński (1872), Ber- et al. 2003). The correlation between high dau (1876), Rehman (1879) and Bober- concentrations of SO2 in the atmosphere and ski (1886) (after Kiszka and Kościelniak lichen decline is well documented (Seaward 1996). Later studies, from the middle of the th 1993). Over the last decades emission of SO2 20 century, were mostly focused on epi- in most developed countries has started to phytic lichens. Zurzycki (1950) presented decrease in response to more severe emis- the first lichenoindication map of Cracow. In sion control regulations and socio-economic the 1970s research on lichens in the city and changes (Bates et al. 2001). As a result re- its surroundings, was undertaken by Kiszka colonization of ‘lichen deserts’ is visible. (1977), who documented the negative influ- Recovery of lichen biota and improvement ence of air contaminants on lichen distribu- in lichen diversity has been documented in tion. In the 1990s an updated lichenoindica- European cities and conurbations such as e.g. tion map of Cracow was presented by Kiszka London (Rose and Hawksworth 1981), and Kościelniak (1996). Both Zurzycki Munich (Kandler and Poelt 1984), Paris (1950), and Kiszka and Kościelniak (1996) (Seaward and Letrouit-Galinou 1991), observed large area of ‘lichen desert’ in the city Rome (Munzi et al. 2007) and Torino (Iso- centre (Fig. 1). During the latest studies (Kisz- crono et al. 2007) as well as in smaller towns ka and Kościelniak 1996) some young indi- (Loppi et al. 2002, Loppi and Corsini viduals of epiphytic lichens were found in the 2003, Loppi et al. 2003, Hultengren et inner parts of ‘lichen desert’, which suggested al. 2004, Loppi et al. 2004). In many urban the beginning of a recolonization process. areas SO2 concentrations are today equal or Despite numerous studies on lichen re- only slightly higher than in surrounding covery, there is still few information concern- rural areas, while NOx and other contami- ing conurbations of Central Europe, and this nants concentrations are still on a high level work tries to fill this gap. The aim of the study (Hultengren et al. 2004). This suggests that was to investigate the latest changes in epi- lichen growth in urban areas is no longer de- phytic lichen vegetation and probable lichen termined by SO2, but other factors play a ma- recolonization in the centre of Cracow, and jor role (Seaward 1997, Purvis et al. 2003). also to assess the state of air pollution in this The history of lichen biota of Cracow is area using lichens as biomonitors. The cur- well documented. The first studies on lichens rent study provides a complement to the data in Cracow were carried out in the middle of the about lichen dynamics in urban areas from 19th century. Problems related to physiography this part of Europe.
Vistula
Vistula
Cracow 0 5km
Fig. 1. General overview of Cracow with boundaries of the study area marked with dotted line; grey colour – extent of the ‘lichen desert’ in 1996 (after Kiszka and Kościelniak 1996). Lichen recolonization in the Cracow centre 227
2.STUDY AREA city (German 2007). There are about 25.1% windless days during the year, mostly in au- Cracow (50°03´41˝N, 19°56´18˝E), the tumn (Mikulska-Szostek 1988). Gener- capital of the Małopolska Voivodship, is the ally, the urban area of Cracow is warmer than largest city in the South of Poland with a its surroundings, which is called an urban population of 755 000 in the area of 327 km2 heat island (UHI) (Lewińska 2000). (Statistical Office in Cracow 2010). The city is situated in the valley of the Vistula River, 2.2. Air pollution between the Jura Highland in the north and the Carpathians in the south (Fig. 1). The Rapid industry development in Cracow main industrial facilities of Cracow are locat- after the Second World War caused a very ed in its eastern and southern parts, however severe atmosphere contamination, especially nowadays there is a tendency to move com- with particulates, SO2 and NOx. The ma- panies to the suburbs. Currently there are jor emission source has been the T. Sendzi- two major sources of substantial air pollution mir Steelworks (former V. Lenin Steelworks; in the city: ArcelorMittal Poland S.A. unit ArcelorMittal Poland S.A. today). In 1965 in Cracow (former T. Sendzimir Steelworks) approximately 124.5 103 tons of dust and 3 and Heat and Power Station “KRAKOW” SA 358.9 10 tons of SO2 were emitted to the at- (Report… 2009). According to the prevailing mosphere in Cracow, of which 53 and 13%, winds in Cracow, pollutants coming from the respectively, was emitted by V. Lenin Steel- adjacent Upper Silesian Industrial Region (in works (Hess 1969, Bokwa 2007). the west) and from a coal-fired electric power Data from the late 1980s and early 1990s station in Skawina (in the south-west from shows very high level of SO2 and particu- Cracow) have also considerable influence. lar matter PM10 in the air. Since then a sig- nificant improvement in air quality in the 2.1 Weather whole Małopolska Voivodship has been seen, following decrease of industrial emission According to long-lasting monitoring (Fig. 2). During the last 15 years significant (Matuszko 2007) average annual rainfall changes in economy led to modernization in Cracow is 679 mm, most of which is con- of technological process and development of centrated in summer period (July). Mean an- companies running according to new, pro- nual temperature is 8.7oC. The hottest month ecological technologies, which resulted in re- is July (18.9oC) and the coldest is January duction in the pollutants emissions. The av- o (–2.1 C). The prevailing winds are W and erage annual SO2 emission is now about two SW. The city location in the Vistula River Val- times lower than in the 1980s, and the level ley provides frequent fogs and temperature of PM10 emission has decreased almost fifteen inversion limiting natural ventilation in the times (Fig. 3). Nowadays concentrations of
160 dust 140 SO2 NOx 120
kg)
6 100
80
60
40
Emission (10 20 0 1985 1987 1989 1991 1993 1995 Years
Fig. 2. Changes of dust (PM10), SO2, NOx emission levels in the former Cracow Voivodship in the years 1985–1996. 228 Agnieszka Słaby and Maja Lisowska
Table 1. List of epiphytic lichen species noted in selected parts of Cracow in the 1970s (Kiszka 1977), 1990s (Kiszka and Kościelniak 1996) and in the years 2007–2009 and their tolerance (T) to nu- trients (after Smith et al. 2009). Epiphytic species recorded in 2009 only are in bold. a – acidophytic, d – dust tolerant, n – nitrophytic. Species T The Old Town Urban and industrial region 1977 1996 2009 19771 19962 20093 Amandinea punctata (Hoffm.) Coppins n +++ + + + & Scheid. Bacidina phacodes (Körb.) Vĕzda + + + + + + Buellia griseovirens (Turner & Borrer ex ––– – + – Sm.) Almb. Candelaria concolor (Dicks.) Stein n ––+ – – +
Candelariella aurella (Hoffm.) Zahlbr. d ––+ – – +
Candelariella xanthostigma (Pers.) Lettau ––++ – +
Chrysothrix chlorina (Ach.) J.R. Laundon ––– + ––
Cladonia coniocraea (Flörke) Spreng. a ––– +++
Cladonia fimbriata (L.) Fr. ––– +++ Diploschistes scruposus (Schreb.) dn ––+ ––+ Norman Hypocenomyce scalaris (Ach. ex Lilj.) a ––– – ++ Choisy Hypogymnia physodes (L.) Nyl. a ––+ ––+
Hypogymnia tubulosa (Schaer.) Hav. a ––– – – +
Lecanora albellula (Nyl.) Th. Fr. – – + – – + Lecanora albescens (Hoffm.) Flörke f. ––– – + – lignicola Lecanora conizaeoides Nyl. in Cromb. a +++ + + +
Lecanora dispersa (Pers.) Sommerf. dn ––+ – – +
Lecanora expallens Ach. ––– ++–
Lecanora hagenii (Ach.) Ach. n – ++ + + +
Lecanora muralis Schreb. dn ––+–––
Lecanora saligna (Schrad.) Zahlbr.4 – ++ + + +
Lecanora varia (Hoffm.) Ach. + –– + ––
Lecidella elaeochroma (Ach.) M. Choisy – – + – – –
Lepraria incana (L.) Ach. s.l. a +++ + + + Melanelixia fuliginosa subsp. fuliginosa a ––– – – + (Fr. ex Duby) O. Blanco Melanohalea exasperatula (Nyl.) O. n ––– – – + Blanco Micarea botryoides (Nyl.) Coppins – – – – – + continued Lichen recolonization in the Cracow centre 229
Micarea prasina Fr. – – – – – +
Opegrapha varia Pers. – – – – – +
Parmelia sulcata Taylor – – – – – +
Phaeophyscia nigricans (Flörke) Moberg dn ––+ – ++
Phaeophyscia orbicularis (Neck.) Moberg dn ––++++
Physcia adscendens (Fr.) H. Olivier n ––++++
Physcia caesia (Hoffm.) Fürnrohr dn ––++ – +
Physcia dubia (Hoffm.) Lettau dn ––++ – +
Physcia stellaris (L.) Nyl. – – + – – +
Physcia tenella (Scop.) DC. n ––+ – ++
Physconia grisea (Lam.) Poelt dn ––++++ Placynthiella uliginosa (Schrad.) Coppins ––– ++– & P. James Pseudosagedia aenea (Wallr.) Hafellner n ––– – – + & Kalb. Pseudevernia furfuracea (L.) Zopf a ––+ – – + Scoliciosporum chlorococcum (Graeve ex n ++++++ Stenh.) Vĕzda Strangospora pinicola (A. Massal.) ––– – – + Körb. Trapeliopsis flexuosa (Fr.) Coppins & P. a ––– +++ James Xanthoria parietina (L.) Th. Fr. n ––+ – – + 1, 2 Trees standing near the streets, in the Botanical Garden, in cemeteries, parks, gardens (Kiszka 1977, Kiszka and Kościelniak 1996). 3 Trees in the Jordan Park, the Krakowski Park, the Bednarski Park, the Rakowicki Cemetery, the Botanical Garden and in the Wawel Hill near the Vistula River. 4 Lecanora saligna counted together with the former Lecanora sarcopis (Wahlb.) Rohl
160 dust 140 SO2
120
kg)
6 100
80
60
40
Emission (10 20
0 1985 1990 1995 2000 2005 Years
Fig. 3. Average annual emission of airborne particular matter PM10 and SO2 in Małopolska Voivodship in the years 1985–2005 in particular years. 230 Agnieszka Słaby and Maja Lisowska
140 NOx PM10 120
-3 SO2
gm ) 100
m 80
60 PM 40 10 NOx 20 SO2
Concentration ( 0 2005 2006 2007 2008 2009 Years
Fig. 4. Average annual concentration of dust (PM10), SO2 and NOx in the atmosphere of Cracow in re- –3 cent years (2005–2009). Standard levels (μg m ): PM10-40; SO2-20; NOx -30. these two main pollutants in Cracow do not, Many individuals collected during the or slightly exceed standard levels but the high studies by Kiszka (1977), and Kiszka and level of NOx is still present (Fig. 4). Kościelniak (1996) were to some degree Air quality data have been provided for damaged or deformed. Thalli were undevel- Cracow and Małopolska from the air moni- oped or unable to produce spores. Shrink- toring network in the Małopolska region and ing, necrotic fragments were observed not reports by the Voivodship Inspectorate for only on foliose thalli of the genus Physcia, but Environmental Protection in Cracow. even on crustose thalli of Lecanora conizae- oides. However, in 1996 some occurrences of 2.3. Epiphytic lichen vegetation in the young, healthy specimens were noted, mainly Cracow centre – state till 1990s in the outskirts of the city, but also in the Bo- tanical Garden and the Rakowicki Cemetery In the 1970s the Old Town area was a part (Kiszka and Kościelniak 1996). The rich- of ‘lichen desert’, which spread throughout est biota was found on old willow trees, ash the city centre, except for parks and cemeter- trees and poplars (Kiszka 1977). ies (Kiszka 1977). In the Old Town and sur- rounding areas less than 1% out of more than 3. MATERIAL AND METHODS 900 investigated tree trunks supported single, minute and damaged crustose lichen thalli. 3.1. Field studies Lichens developed only in cracks of the trees bark. No major changes were observed twen- Field studies were carried out in the years ty years later by Kiszka and Kościelniak 2007–2009 in the centre of Cracow, in 7 locali- (1996). Epiphytic lichens found in the city ties: the Old Town, and six urban green areas. centre both in 1977 and in 1996, were only Within each locality deciduous trees (with only crustose species: Amandinea punctata, Bacid- three exceptions) with the highest number of ina phacodes, Lecanora conizaeoides, Lepraria lichen species were chosen as study sites. Trees incana s.l. and Scoliciosporum chlorococcum totally devoid of lichens were extremely rare in (Kiszka 1977, Kiszka and Kościelniak the study area and were not taken into account 1996) (Table 1). The most abundant species when performing analyses. A study site was was Lecanora conizaeoides, however green alga defined as a single tree or rarely a group of two Pleurococcus viridis dominated. Outside the to three trees of the same species. Within the city centre, mainly in parks, gardens and cem- Old Town (the Market Square and the adjacent eteries, 20 epiphytic lichen species were found Planty Park) (Fig. 5), which was a part of a for- (Table 1) both in 1970s and in 1990s (Kiszka mer ‘lichen desert’ (Fig. 1), 288 study sites were 1977, Kiszka and Kościelniak 1996). selected. The remaining 146 sites were located Lichen recolonization in the Cracow centre 231 in the 6 localities around the Old Town: Jor- The nomenclature was given accord- dan Park (28 sites), Krakowski Park (17 sites), ing to Fałtynowicz (2003) and updated Rakowicki Cemetery (23 sites), Botanical Gar- according to the Index Fungorum (http:// den (11 sites), Bednarski Park (57 sites) and www.indexfungorum.org). Aggregate names the area near the Vistula River, located next have been applied for Lepraria incana and to the Wawel Hill (10 sites) (Fig. 5). Although Lecanora saligna. The species names used in this last area belongs to the Old Town, it was the studies by Kiszka (1977) and Kiszka treated separately because of the direct vicinity and Kościelniak (1996) were updated ac- of the Vistula River and increased air humid- cording to the Index Fungorum (http://www. ity, which can strongly affect lichen growth. indexfungorum.org). Tree trunks were investigated from their bases to about 180 cm from the ground. Lichen 4. RESULTS species present and their cover (estimated as a percentage of the investigated surface) were 4.1. General characteristics of lichen recorded, together with general information biota in the Cracow centre about each site (localization, tree species, trunk girth). Samples for further taxonomic identi- A total of 39 epiphytic species were re- fication were collected when necessary. Addi- corded at 434 sites, with almost 70% of the bi- tional information about any abnormalities of ota (26 species) being noted in the Old Town morphology of thalli (colour, shape; small but (Table 1). Six species (Diploschistes scruposus, healthy thalli without soralia or apothecia were Hypogymnia tubulosa, Lecanora albellula, Mi- considered as young) was also gathered. carea botryoides, Opegrapha varia, Strangos- pora pinicola) are new to Cracow, and two of 3.2. Analysis methods them (Diploschistes scruposus and Lecanora albellula) were found not only in parks, but The results were compared with cor- also in the Old Town (Table 1). Twenty spe- responding data from the previous studies cies were recorded for the first time in the (Kiszka 1977, Kiszka and Kościelniak study area (Table 1). Six species (Buellia gris- 1996). Significance of differences in species eovirens, Chrysothrix chlorina, Lecanora albe- richness between localities were tested us- scens var. lignicola, L. expallens, L. varia, Pla- ing one-way analysis of variance (ANOVA), cynthiella uliginosa) which had been recorded which was also employed to test the effects previously form the study area (Kiszka 1977, of tree species diversity and tree diameter on Kiszka and Kościelniak 1996), were not species richness at a site. Analogical analyses found during the present survey (Table 1). in the case of cover rate were performed us- Four species are legally protected in Po- ing the Kruskal-Wallis one-way analyses of land (Hypogymnia tubulosa, Melanelixia fu- variance. Two sample proportion Z test was liginosa, Melanohalea exasperatula, Pseude- employed to analyse the difference in num- vernia furfuracea) (Regulation by Polish bers of acidophilic and nitrophilic species. Minister of Environment 2004) and three The statistical analyses were performed using (Hypogymnia tubulosa, Opegrapha varia, STATISTICA software (version 9.0) (StatSoft, Strangospora pinicola) are rare and have been Inc. 2009). included in the Red List of Plants and Fungi Discrimination between acidophilic and in Poland (Cieśliński et al. 2006). nitrophilic species followed Smith et al. Five species (Candelariella aurella, Dip- (2009), also other publications (van Herk loschistes scruposus, Lecanora dispersa, L. mu- 1999, Seaward and Coppins 2004, Da- ralis, Physcia caesia) usually reported in Po- vies et al. 2007) were taken into account. land from rocks and concrete (Fałtynowicz
Species tolerance to SO2 was assessed using 2003), were currently observed on tree trunks the eleven-grade (0–10) biological scale by – Candelariella aurella, Diploschistes scrupo- Kiszka (1992) which is the modification of sus, Lecanora dispersa and Physcia caesia in the Hawksworth and Rose’s qualitative the whole study area, while Lecanora muralis scale (1970) adopted to Polish lichen biota in the Old Town at a single site only. Cande- composition. lariella aurella, Diploschistes scruposus and the 232 Agnieszka Słaby and Maja Lisowska
4
3
2 1 5
7
6
Fig. 5. The location of the study areas in city centre of Cracow (South Poland). 1 – Market Square with the Planty Park (the Old Town); 2 – the Jordan Park; 3 – the Krakowski Park; 4 – Rakowicki Cemetery; 5 – Botanical Garden; 6 – the Bednarski Park; 7 – the Wawel Hill
Physcia dubia Phaeophyscia orbicularis Physcia adscendens Lepraria incana Lecanora dispersa Physcia tenella Hypogymnia physodes Lecanora conizaeoides Parmelia sulcata Candelariella xanthostigma Xanthoria parietina Amandinea punctata Cladonia fimbriata Physconia grisea Scolicosporum chlorococcum Bacidina phacodes Lecanora hagenii Melanohalea exasperatula Lecanora saligna Pseudevernia furfuracea Cladonia coniocraea Physcia caesia Phaeophyscia nigricans Trapeliopsis flexuosa Lecanora albellula Hypogymnia tubulosa Melanelixia fuliginosa Candelaria concolor Candelariella aurella Strangospora pinicola Diploschistes scruposus Physcia stellaris Micarea botryoides Hypocenomyce scalaris Opegrapha varia Lepraria lobificans Protoparmeliopsis muralis Lecidella elaeochroma Micarea prasina Pseudosagedia aenea
01 02 03 04 05 06 07 08 09 0
%of s ites Fig. 6. Frequency (% of sites) of lichen species at all sites in the centre of Cracow (2009). Lichen recolonization in the Cracow centre 233
10 The difference in numbers of acidophil- 9 ic and nitrophilic species recorded in the 8 whole study area is statistically significant (P <0.001). 7 Number of lichen species at a site spanned 6 from 1 to 9. The majority of sites (25%) sup- 5 ported 3 different lichen species (Fig. 7).
4 Sites with 4 or 5 species were also frequent, occupying 17 and 12%, respectively. It is a 3 huge change in comparison with the former
Number of species 2 years when the majority of trees were de-
1 void of lichens (Kiszka 1977, Kiszka and Kościelniak 1996). The locality with the 0 highest average number of species at a site Green areas Old Town General was the Jordan Park and with the lowest the Median Old Town (Figs. 7 and 8). 25%-75% Non-outlier range Coverage of most of the tree trunks was Outliers up to 10%, however in some cases the trunks Fig. 7. The average number of lichen species at a were almost entirely (up to 90%) covered by site in all green areas together, in the Old Town lichens (Fig. 9). The locality with the highest and in the whole study area in general (2009). average cover was Rakowicki Cemetery and with the lowest – the Wawel Hill (Fig. 10). The most numerous trees in the study area two Lecanora species are new to the epiphytic were maples (Acer spp.), mainly Acer pseudo- lichen biota of the study area, while Physcia platanus, representing more than one-third caesia was previously present on single trees (overall 154) of all studied trees and dominat- close to the roads (Kiszka 1977) (Table 1). ing mostly in the Old Town. Maples supported The two commonest species in the in- the highest number of lichen species (overall 32 vestigated area were nitrophilic and dust spp.). Other frequent tree species were: Fraxinus tolerant Physcia dubia and Phaeophyscia or- excelsior (overall 70), Tilia cordata (overall 34) bicularis which occurred in more than 60% and Betula pendula (overall 31). They also sup- of all sites (Fig. 6). Two other nitrophytes, ported a high number of lichen species, overall Physcia adscendens and Lecanora dispersa, 28 spp., 25 spp. and 25 spp., respectively. Analy- together with acidophilic Lepraria incana sis of variance showed that tree species and tree s.l., were recorded in more than 20% of all diameter diversity didn’t contribute to the diver- sites. Nitrophilic Physcia tenella and acido- sity of the number of species, as well as to the philic Hypogymnia physodes and Lecanora diversity of the cover rate. conizaeoides were recorded in more than The lichen thalli in the study area were 10% of all sites (Fig. 6). generally healthy and well-developed. Many
As far as the tolerance to SO2 is concerned, young individuals were also recorded. The Hypogymnia physodes, Phaeophyscia orbicu- most frequent damage observed on thalli laris and Physcia tenella represent the 4th grade were feeding traces of invertebrates. Thalli of Hawksworth and Rose’s qualitative scale of Lecanora conizaeoides without apothecia (Hawksworth and Rose 1970, Kiszka were often recorded. and Kościelniak 1996), Physcia adscendens belongs to the 3rd grade, while Lepraria incana 4.2. The Old Town s.l. and Lecanora conizaeoides belong to the 2nd grade. The most SO2-sensitive lichens found In the area of the Old Town a total of 26 during the present study – Candelaria concol- epiphytic lichen species were recorded in or (1% of all sites), Melanohalea exasperatula 288 sites (Table 1), which is a huge change in (3%), Opegrapha varia and Physcia stellaris comparison with the previous studies. Both th (both less than 1%) represent the 5 grade of of the most SO2 sensitive lichens found dur- Hawksworth and Rose’s scale (Fig. 6). ing the present studies, Candelaria concolor 234 Agnieszka Słaby and Maja Lisowska and Physcia stellaris, were noted, at single 4.3. Green areas sites, in this area. The most abundant lichens were nitro- In the six green urban areas a total of 37 gen- and dust-tolerant Physcia dubia and Pha- epiphytic lichen species were recorded at 146 eophyscia orbicularis, being noted at approxi- sites. The most abundant species was, as in mately three-quarters of all sites (83, and 76% the Old Town, nitrogen- and dust- tolerant of sites, respectively). Other frequent species, Physcia dubia, being noted at almost 80% of Physcia adscendens, Lecanora dispersa and all sites. Only in the Rakowicki Cemetery aci- Physcia tenella, also connected with nitrogen- dophilic Lepraria incana s.l. dominated (91% and dust-enriched environment, were noted of 23 sites). The most SO2 sensitive lichens at 37, 24 and 22% of sites, respectively. Three found during the present studies, Candelar- most abundant acidophilic species, Lepraria ia concolor, Physcia stellaris and Opegrapha incana s.l., was found at 10% of sites, and two varia, were noted at single sites, only in the other acidophytes, Hypogymnia physodes and Bednarski Park. Most of the study sites (17%) Lecanora conizaeoides, at 7 and 6% of sites, re- supported 3 lichen species; sites with 4 and 5 spectively. Most of the study sites supported different species were also frequent (15 and 3 lichen species (29%), however at two sites 8 16%, respectively) (Fig. 7). At six sites situ- species at a site were recorded (Fig. 7). Trees ated in the Jordan Park, 9 different species at in the Old Town supported significantly less a site were noted. The locality with the high- lichen species than those in other localities est average number of lichen species at a site counted together (P <0.001) (Fig. 7). The big- was the Jordan Park and with the lowest – the gest percentage of the sites (62%) had a cover Bednarski Park (Fig. 8). The biggest percent- rate up to 10%, and approximately one-quarter age of the sites (46%) had a cover rate up to of sites (26%) was covered with lichens up to 10%, and more than one-fifth of sites (22%) 20%. One site with a cover rate up to 80% was was covered with lichens up to 20% (Fig. 9). found (Fig. 9). Differences in coverage between Two sites, one in the Bednarski Park and the Old Town and other localities proved sta- second in the Rakowicki Cemetery, with a tistically significant (P <0.001). The Old Town, cover rate up to 90% were found. The locality as well as the Wawel Hill (Fig. 10), are the two with the highest average cover was the Rako- localities with the lowest average cover. wicki Cemetery and with the lowest - Wawel The lichen thalli were well-developed. Many Hill (Fig. 10). The lichen thalli were mostly young individuals were noted. Discoloured healthy, and often young. thalli, especially of Xanthoria parietina, were of- ten recorded, mainly on the Market Square.
10 9
8
7
6
of species 5
4
3
Number 2
1 0 Jordan Park Krakowski Park Botanical Garden Rakowicki Cemetery Wawel Hill Bednarski Park Median 25%-75% Min-Max
Fig. 8. The average number of lichen species at a site in each locality, included to green areas, separately (2009). Lichen recolonization in the Cracow centre 235
81-90 81-90
71-80 71-80
61-70 61-70
51-60 51-60
41-50 41-50 31-40
Cover (%) Cover (%) 31-40
21-30 21-30
11-20 11-20
up to 10 up to 10
Green areas Old Town General Jordan Park Krakowski Park Botanical Garden Rakowicki Cemetery Wawel Hill Bednarski Park
Median Median 25%-75% 25%-75% Non-outlier range Non-outlier range Outliers Outliers Extreme values Fig. 9. The average lichen cover at a site in all Fig. 10. The average lichen cover at a site in each green areas together, in the Old Town and in the locality, included to green areas, separately (2007). whole study area in general (2009).
5. DISCUSSION vegetation is not always associated with the complete disappearance of ‘lichen desert’, as During the last 10 years major changes in was the case e.g. in Pistoia, Central Italy. The epiphytic lichen vegetation have taken place presence of the ‘lichen desert’ in this town in the centre of Cracow, following the air was explained by the constantly high levels of quality improvement. As predicted, huge im- NOx (Loppi and Corsini 2003). provement in lichen vegetation is clearly seen. More than a half of all taxa identified (20 The ‘lichen desert’ is no longer present as a species) are new to the study area. They are compact area, as it was in the 1990s (Fig. 1), mostly nitrophilic and associated with dust and only single trees devoid of lichens are contaminated substrata (Table1). Several of found. Places where formerly only extremely these species, Candelariella aurella, Diploschi- pollution tolerant lichens had been recorded, stes scruposus, Lecanora dispersa and L. mu- have now been colonized by more sensitive ralis, rarely grow on trees in Poland, occupy- macrolichen species. Macrolichens were also ing mostly calcareous rocks and man-made recorded in the area of the former ‘lichen substrata. Three of them (Candelariella au- desert’. In other cities where comparison with rella, Lecanora dispersa, L. muralis) had been historical data was possible, the reduction of present within the study area in the past, but the ‘lichen desert’ was observed as well, e.g. limited only to rocks and concrete (Kiszka in London (Rose and Hawksworth 1981), 1977, Kiszka and Kościelniak 1996). The Rome (Munzi et al. 2007) and Torino (Iso- appearance of epilithic lichens on trees in ur- crono et al. 2007). The authors agree that ban areas has been also observed elsewhere in declining SO2 concentration is the main fac- Europe, e.g. in London (Davies et al. 2007, tor responsible for this trend. The general im- Larsen et al. 2007), as well as in Poland provement of lichen vegetation in the study (Lisowska 2011). In the Netherlands appear- area is in line with the results from both ur- ance of epilithic species on trees was associ- ban (e.g. Loppi et al. 2003, Hultengren et ated with increase in bark pH, which had been al. 2004, Isocrono et al. 2007) and indus- noted in this area (van Herk 2002, Wolseley trial areas (e.g. Showman 1997, Ranta et al. 2006). Lecanora hagenii, noted during 2001, Bačkor et al. 2003) across Europe and present research on tree trunks, was previously North America. Similar results were also ob- recorded by Kiszka (1977) on decaying wood. tained in Skawina, Poland (Lisowska 2011). Several species currently present in the However, the general improvement of lichen centre of Cracow, e.g. Candelaria concolor, 236 Agnieszka Słaby and Maja Lisowska
Hypogymnia physodes, Melanohalea exasper- no et al. 2007). Although Lepraria incana atula, and Pseudevernia furfuracea, had been s.l. prefers lower substratum pH, it seems observed previously within the city boundar- to be tolerant to NOx (Davies et al. 2007), ies, but mainly in the western part, only on which might explain its high frequency in the the outskirts of the city. Pseudevernia furfu- study area. Conversely, Hypogymnia physodes racea up till now has been recorded in three seems to be very sensitive to NOx (Bates et sites (Kiszka 1977) and later in one site only al. 2001). Several authors (e.g. van Herk (Kiszka and Kościelniak 1996). 2001; Hultengren et al. 2004, Sparrius Some species recorded previously in a 2007) have shown a significant decline of H. very few sites, were not found again in the physodes in several European countries. In present survey. It can be explained by their SE England, for example, despite it was by far phorophytes being cut down or by differences the most common macrolichen recorded on in sampling sites. They may have also been oak trees, it had shown a spectacular decrease overlooked during the field studies or did not with falling SO2 (Bates et al. 2001). The con- manage to survive. tinuing decline of this species was also con- The commonest lichens in the study area firmed by Purvis et al. (2003) and Davies et were foliose species of medium tolerance to al. (2007) in London. According to Purvis
SO2 (Hawksworth and Rose 1970). One et al. (2003) NOx coupled with particles, and fruticose macrolichen, Pseudevernia furfura- not falling SO2 level, were the major factors cea, was also found. The most SO2 sensitive responsible for damaging Hypogymnia phy- lichens recorded (Candelaria concolor, Mela- sodes near London. nohalea exasperatula and Physcia stellaris) are Strongly acidophilic Lecanora conizae- classified to the 5th grade of Hawksworth and oides was not a very frequent species in the
Rose’s (1970) scale. This suggests that SO2 level study area, being noted in less than 15% of is no longer a limiting factor for epiphytic li- sites, which corresponds with the consider- chens in the centre of Cracow, that corresponds ably low SO2 level (Fig. 3). This lichen often with other studies (e.g. Purvis et al. 2003). grows in SO2- polluted areas where more sen- The majority of the species in the study sitive species are not able to exist, and it used area, including the most frequent ones, are to dominate in urban and industrial areas for nitrophilic (Table 1), which is in agreement a long time, as long as the SO2 level in the at- with numerous studies (e.g. van Herk 1999, mosphere remained high (Bates et al. 2001, Seaward and Coppins 2004, Wolseley et Larsen et al. 2007, Davies et al. 2007). al. 2006, Davies et al. 2007). The dominance The decline of SO2 concentrations in recent of nitrophilic species is also reported from years has caused loss of L. conizaeoides, e.g. other European cities and towns. For exam- in Skawina, Poland (Lisowska 2011), and ple, in London the most common species are also in SE England (Bates et al. 2001), where Physcia adscendens (Purvis et al. 2003), pre- it was explained by the fact that this species sented on 70% of the examined trees, togeth- require elevated SO2 inputs (or some closely er with Xanthoria parietina and Phaeophyscia related chemical factor) for healthy growth. orbicularis (Davies et al. 2007). Similarly, There may be also other explanations for this. in Torino P. orbicularis and P. adscendens, According to recent investigations (Hauck et present in over 80% of the sampling stations, al. 2008) the extremely high SO2 tolerance in are the most common species (Isocrono et lichens is strongly correlated with hydropho- al. 2007). However, in Rome (Munzi et al. bicity of the thallus surface. Thus the success
2007) epiphytic lichens recorded are known of L. conizaeoides in SO2 polluted areas can be to prefer acid and subacid bark, what can be attributed to the superhydrophobicity of its associated with the proximity of the sea, as is surface and also to its high dispersal ability the case in Portugal (Pinho et al. 2008). (Hauck et al. 2008). Other factors e.g. com- On the other hand, two species consid- petitive interactions with other epiphytes and ered as acidophytes (van Herk 2002), Lep- attacks by the parasitic fungus Athelia arach- raria incana s.l. and Hypogymnia physodes, noidea were also taken into consideration were frequently observed in the study area, (Bates et al. 2001, Hultengren et al. 2004). as was the case e.g. in Torino, Italy (Isocro- This might be the case in Cracow, since many Lichen recolonization in the Cracow centre 237
fungus-infected specimens were observed between NO2 concentrations and the diversity during the present study. The competition of epiphytic lichens in the proximity of a rural with dust and nitrogen tolerant Lecanora dis- highway in Central Italy was found, probably persa and other ecologically similar species because of low NO2 values measured (Frati might be also a limiting factor. Most likely et al. 2006). This suggests that in the coming
Lecanora conizaeoides will not increase sig- years the kind of the effect of NOx on lichens nificantly in the coming years. in Cracow will strongly depend on its level
Many grayish specimens of normally in the air. Synergistic effects of SO2 and NOx, yellow nitrophilic Xanthoria parietina were which are observed when concentrations are found during the current studies, mainly in below, or at the threshold for, individual in- the Market Square. The same tendency was jury response (Balaguer et al. 1997), also observed in London by Davies et al. (2007) cannot be neglected. It is often very difficult and explained by the fact that orange colour to separate the effects of different pollutants of the thallus is inversely related to NOx. This (Loppi et al. 2002), especially when their lev- suggests the considerably high level of NOx in els are low. the Cracow centre. Nitrophilic lichens, such as Phaeophyscia Currently, the main source of atmospheric orbicularis, Physcia spp. and Xanthoria pari-
NOx pollution in Cracow is most likely vehic- etina were found most often in the study area ular traffic. In the whole Małopolska Voivod- on poplars (Populus spp.), while acidophilic ship the number of road vehicles is steadily Hypogymnia physodes, Lecanora conizaeoides increasing. In the years 2000–2009 the num- and Lepraria incana s.l. preferred Quercus ber of registered passenger vehicles increased robur and Betula pendula, which have acid by almost 66%, from ca 829 000 to ca 1 375 barks. Many authors agree that bark pH, in-
000 (Statistical Office in Cracow 2010), and creasing in response to declining SO2 levels, further increase is very probable. Since the had caused shifts in the epiphytic lichen biota level of SO2 is relatively low, transport-related observed in polluted areas (van Dobben and NOx is considered to have a major impact on Ter Braak 1999, van Herk 2001, Marmor lichen distribution and diversity in the study and Randlane 2007, Sparrius 2007). Da- area. Numerous studies support this scenario. vies et al. (2007) suggested that generally In Montecatini Terme, Central Italy (Loppi while nitrophytes are connected with trans- et al. 2004), as well as in Genova province, port-related pollutants, acidophytes are asso- NW Italy (Giordani 2007), despite the gen- ciated with bark pH. In the centre of Cracow, eral improvement of lichen vegetation, lichen while generally bark pH must have increased presence is negatively affected by NOx derived in response to the falling SO2, no substrate from vehicular traffic. In the case of Seville, over-eutrophication is visible, since the eco- Spain (Fuentes and Rowe 1998) ‘lichen logical preferences of lichen species and bark desert’ still exist due to high traffic vehicles pH of the phorophytes seem to be well linked. emissions. In Pistoia, Central Italy (Loppi and On the other hand, according to the most re- Corsini 2003), lichen recolonization is deter- cent research (Spier et al. 2010) the more mined by declining SO2 concentrations, while important factor influencing lichen vegeta- major injuries to lichen communities are tion may be the tree species, while bark pH caused by the constantly high levels of NOx. alone is of less importance. Also other factors The combination of suspended particles and e.g. tree age, roughness, water holding, capac- nitrogen from traffic emissions also seems to ity, other bark chemical properties besides influence lichen growth (Pur vis et al. 2003, pH etc. may play a role (Spier et al. 2010).
Isocrono et al. 2007). However, whereas SO2 However, during the current studies neither is highly toxic, nitrogen is a nutrient and only tree species, nor trunk diameter had a statis- becomes toxic in excess to those species that tically significant effect on the lichen species are sensitive (Wolseley et al. 2006). Posi- richness. tive correlation between nitrophytes and road Both species richness and cover differ sig- proximity was established e.g. in Grenoble, nificantly between localities, the lowest val- France (Gombert et al. 2003, Gombert et ues being recorded in the Old Town and the al. 2004). On the other hand, no associations Wawel Hill. This corresponds with the extent 238 Agnieszka Słaby and Maja Lisowska of the former ‘lichen desert’. However, within Zarzycki, W. Wojewoda, Z. Szeląg) –Institute the former ‘lichen desert’ some of the most of Botany, Pol. Acad. Sci. Kraków, 99 pp. Conti M.E., Cecchetti G. 2001 – Biologi- SO2 sensitive and rare macrolichens were re- corded. 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Received after revision September 2011