Response of Tilia sp. L. to climate warming in urban conditions – Phenological and aerobiological studies

Urban Forestry & Urban Greening 43 (2019) 126369

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Original article

Response of Tilia sp. L. to climate warming in urban conditions – Phenological and aerobiological studies

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Elżbieta Weryszko-Chmielewskaa, Krystyna Piotrowska-Weryszkoa, , Agnieszka Dąbrowskab a b

Department of Botany and Plant Physiology, University of Life Sciences in Lublin, Akademicka 15, 20-950 Lublin, Poland Botanical Garden, Maria Curie-Skłodowska University, Sławinkowska 3, 20-810 Lublin, Poland

A R T I C LE I N FO

A B S T R A C T

Handling Editor: Wendy Chen

Lindens belong to valued trees that are frequently planted in urban green areas. Nevertheless, during their flowering they can pose a risk to sensitive people in cities due to their allergenic pollen. This paper presents the results of a 3-year phenological study (2016–2018) and an 18-year aerobiological study (2001–2018) conducted in Lublin (Poland). The flowering phenology data for the following five species: T. americana, T. cordata, T. × euchlora, T. platyphyllos, and T. tomentosa, were compared with the data regarding Tilia pollen seasons. It was shown that the largest amounts of airborne Tilia pollen grains occur during the full flowering period of T. cordata and that the flowering sequence of the linden species studied is constant during the growing season: T. platyphyllos, T. americana, T. cordata, T. × euchlora, and T. tomentosa. We found pollen seasons to start earlier by 14 days and to be extended by 15 days. Throughout the study period, the annual Tilia pollen sum did not change significantly. However, in 2018 in which there was a significant increase in temperature above the average for the previous 17 years, flowering and pollen release distinctly accelerated, and the annual pollen sum increased more than three times compared to the average for the previous 17 years. In central-eastern Poland, the risk of pollen allergy due to the presence of Tilia pollen occurs in May, June, and July. We recorded the highest linden pollen concentrations in June. Due to the acceleration of flowering and pollen release in linden trees as a result of global warming, the incidence of pollen allergy in central Europe can be expected to become more intense already in the second half of May. Therefore, linden plantings in new urban green areas should be planned to be established at some distance from residential estates.

Keywords: Acceleration Allergy risk Global warming Linden Pollen seasons Time of blooming Urban greenery

1. Introduction The genus Tilia (Tiliaceae) comprises more than 60 species (Seneta and Dolatowski, 2008) found in the temperate zone of the Northern Hemisphere (Szweykowska and Szweykowski, 2003). It is difficult to determine the number of Tilia species due to their polymorphism as well as a large number of transitional forms and hybrids (Boratyńska and Dolatowski, 1991). Linden trees are widely distributed in many countries across Europe where they grow in the wild as well as are commonly used for urban vegetation in public parks and along streets (Pigott, 1991; Seneta and Dolatowski, 2008; Weryszko-Chmielewska and Sadowska, 2010; Kupryjanowicz et al., 2004; Massetti et al., 2015). Lindens are usually lowland species, rarely encroaching mountains (Boratyńska and Dolatowski, 1991). Currently in Europe, there are five species of the genus Tilia: T. cordata Mill., T. platyphyllos Scop., T. tomentosa Moench, T. rubra DC.,

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and T. dasystyla Steven (Browicz, 1968; Kupryjanowicz et al., 2004). T. cordata, which is found almost across the entire area of the continental part of Europe, except for northern Scandinavia, has the largest range. The range of T. platyphyllos covers central and southern Europe, whereas T. tomentosa and T. rubra only occur in the Balkans (Boratyńska and Dolatowski, 1991). T. dasystyla, on the other hand, is considered to be endemic to the Crimea (Browicz, 1968). In Poland only T. cordata and T. platyphyllos belong to native linden species (Zając and Zając, 2001; Seneta and Dolatowski, 2008). T. cordata usually grows in mixed forests and is encountered more frequently than T. platyphyllos, which grows on limestone rocks and in Poland reaches the northern limit of its range (Szweykowska and Szweykowski, 2003). T. cordata belongs to indicator species used in plant phenology in Poland (Niedźwiedź and Jatczak, 2008) and in other European countries, among others in Austria (Koch et al., 2008), Croatia (Vučetić et al., 2008), the Czech Republic (Nekovář et al., 2008), Hungary (Szalai et al., 2008), Latvia (Grišule and Briede, 2008), and Romania

Corresponding author. E-mail address: [email protected] (K. Piotrowska-Weryszko).

https://doi.org/10.1016/j.ufug.2019.126369 Received 11 March 2019; Received in revised form 5 June 2019; Accepted 11 June 2019 Available online 12 June 2019 1618-8667/ © 2019 Elsevier GmbH. All rights reserved.

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2. Material and methods

(Teodosiu and Mateescu, 2008). In the above-mentioned countries, different phenological phases of T. cordata are monitored, inter alia, leaf unfolding that marks early spring and first flowers open that indicate full summer (Sokołowska, 1980). The phenological phases of T. platyphyllos, on the other hand, are recorded in Bulgaria (Kazandjiev, 2008), Germany (Zimmerman et al., 2008), and Slovenia (Črepinšek et al., 2008). Apart from the above-mentioned linden species, a number of other species and varieties of this genus are grown in Poland as well as planted in parks and as landscape tree plantings, whereas some of them also along roads. These include, among others, T. americana, T. amurensis, T. dasystyla, T. x euchlora, T. insularis, T. japonica, T. michauxii, and T. tomentosa (Seneta and Dolatowski, 2008; Dąbrowska et al., 2016). Due to its high resistance to drought, dust, and industrial smoke, T. tomentosa is perfectly suitable for street plantings and tree stands around industrial centers (Szweykowska and Szweykowski, 2003). In Tilia, five-petaled flowers in clusters most often numbering 3–7 are borne in cymose inflorescences. They produce yellowish-white petals and bright green sepals, on which trichomatous nectary glands are located (Szweykowska and Szweykowski, 2003; Konarska, 2013). In the androecium with numerous stamens, whorls of 5 stamens are distinguished (Maurizio and Grafl, 1969). It has been calculated that one T. cordata flower produces 43,500 pollen grains (Szczepanek, 2003). Linden flowers are entomogamous, but large amounts of pollen of this taxon are also carried by the wind. In terms of the ecology of pollination, there is a balance between two pollination mechanisms in Tilia: entomophily and anemophily. The anemophily syndrome in this taxon includes the relatively open flowers and slightly sticky pollen (Proctor et al., 1996; Willmer, 2011). Anemophily plays a subsidiary but important role in pollination of Tilia, especially in poor weather, when insects are scarce (Anderson, 1976; Willmer, 2011). Many investigations in recent years concern the effect of climate change on plant phenology (Kramer, 1995; Chmielewski and Rötzer, 2001; Menzel et al., 2006; Wielgolaski, 2003; Primack et al., 2004; Juknys et al., 2012; Czernecki and Jabłońska, 2016). Plant responses to climate change are also reflected in the results of aerobiological studies (Frei and Gassner, 2008; Weryszko-Chmielewska and Sadowska, 2010; Puc et al., 2015; Zhang et al., 2015; Dąbrowska et al., 2016; Galán et al., 2016; Ruiz-Valenzuela and Aguilera, 2018). Temperature is the main climatic factor that affects plant phenology (Wielgolaski, 2001; Schleip et al., 2009). Furthermore, it has been shown that intra-urban thermal differences cause phenological consequences in trees growing in urbanized areas (Mimet et al., 2009; Ohashi et al., 2012; Massetti et al., 2015). It has also been found that precipitation is a much less influencing factor with regard to phenological phases than temperature (Kramer, 1995; Wielgolaski, 2003). Tilia pollen grains cause allergy that manifests itself in the incidence of rhinoconjunctivitis and cough (Mur et al., 2001). Some researchers consider the allergenicity of Tilia to be low (Mur et al., 2001), or even moderate (Igić et al., 2005; Kuchcik et al., 2016; Mrđan et al., 2017). Due to the fact that in the temperate climate of Europe Tilia sp. is frequently planted in parks and alley greenery, the allergenic index for this species can be high (Carinanos and Casares-Porcell, 2011; Mrđan et al., 2017). Given the risk from linden pollen to sensitive urban residents, the aim of this study was to compare Tilia pollen seasons in Lublin over a period of 18 years, with special attention to the start and end of pollen seasons, their length as well as pollen abundance. Due to existing climate change, trend lines were determined for the investigated parameters. The morphological characteristics of flowers and flowering phenology of the five species of the genus Tilia, most frequently used in urban plantings in Lublin, were compared. Their flowering times were compared with the peak pollen periods in curves representing the pollen seasons. The pollen season pattern in the years with the highest pollen production was analyzed in detail.

2.1. Linden trees in Lublin’s green areas Among the twelve parks established in Lublin, five of them are characterized by a predominance of high vegetation, with trees and shrubs accounting for 65–85% in these parks. The Saxon Park (Park Saski) and the University Park (Park Akademicki), located closest to the Śródmieście district, are characterized by a high density of woody vegetation plantings, with their percentage standing at 75% and 85%, respectively. In all Lublin’s parks, linden trees belong to the dominant species (Pudelska and Przegalinska-Matyko, 2006; Adamiec and Trzaskowska, 2012a). Moreover, the inventory of trees and shrubs in the Śródmieście district included many interesting specimens of the genus Tilia growing in the streets and squares. More than 12% of trees managed by the Municipality of Lublin belong to T. cordata (Adamiec and Trzaskowska, 2012b). After Prunus cerasifera, Tilia cordata (218 individuals) is the second ranking species among the most frequently used trees, whereas the less often encountered T. platyphyllos comprises 38 individuals (Dąbski et al., 2006). 2.2. Morphology of flowers and flowering phenology Phenological observations of flowering of the following five species: T. americana L., T. cordata Mill., T. × euchlora K. Koch, T. platyphyllos Scop., and T. tomentosa Moench, were carried out over the period 2016–2018 in the Botanical Garden of the Maria Curie-Skłodowska University in Lublin, central-eastern Poland (51°14′37.2′'N, 22°32′25.3′'E; 197 m above sea level). The studied linden specimens grew surrounded by various tree and shrub species in sunny places on loess-derived luvisol. The observations of specific flowering stages were carried out continuously on the same individuals. For this purpose, two branches (one from the southern side and one from the northern side) were selected on each experimental tree right before the onset of anthesis. Next, the flower opening rate was determined every day between 10.00 and 12.00. The phenological observations of flowering were conducted according to the BBCH (Biologische Bundesanstalt, Bundessortenamt und Chemische Industrie) scale of phenological identification, taking into account the following growth stages: beginning of flowering (BBCH 61), full flowering (BBCH 65), end of flowering (BBCH 67) (Hess et al., 1997). The morphological analysis of linden flowers was made at the full flowering stage. 2.3. Aerobiological study Average daily concentrations of Tilia pollen were monitored in Lublin over the period 2001–2018. The study was carried out by the volumetric method using a Hirst-type trap (Lanzoni VPPS 2000), which was installed on the flat roof of a building of the University of Life Sciences (51°14′37.38″N, 22°32′24.73″E; 197 m above sea level) at a height of 18 m. The aerobiological sampling station was located in the city center of Lublin and was adjacent to the streets along which longstanding T. cordata specimens grow. The pollen trap used to monitor airborne pollen contents operated on a continuous basis. After a week-long exposure of an adhesivecoated tape, microscopic slides corresponding to 24 -h intervals were prepared. The sampling and analysis were conducted following the minimum recommendations proposed by the European Aerobiology Society Working Group on Quality Control (Galán et al., 2016). Besides our monitoring station is subject to quality inspections within the European network (Sikoparija et al., 2017). The results of the palynological analysis were expressed as average daily airborne pollen counts in 1 m3 of air (P/m3). The basic statistics, like arithmetic mean, minimum, maximum, and standard deviation, coefficient of variation, and coefficient of skewness were considered. The linden pollen seasons in individual years are 2

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3.2. Flowering phenology Over the 3-year period, the studied linden species exhibited high variation in flowering abundance. T. platyphyllos showed the most uniform abundance of flowering from year to year. The other taxa, among them T. cordata, clearly bloomed alternately. In the years 2016 and 2018, they flowered abundantly, whereas in 2017 poorly or did not bloom at all (T. × euchlora and T. tomentosa). There were large differences in flowering time between years (Fig. 2). Every year, T. platyphyllos was the first to bloom. In 2016 and 2017, its flowering period started on June 9 and June 10, respectively, whereas in 2018 on May 25. The end of the flowering period of this linden species coincided with the beginning of flowering or full flowering of T. americana and T. cordata. Tilia cordata, which is found in large numbers in Lublin’s green areas, started flowering on average on June 21 in 2016 and 2017, whereas in 2018 on June 4. During the flowering period of this linden, two other taxa successively began flowering: T. × euchlora and T. tomentosa. The lindens bloomed at 3-9day intervals from one another. The average flowering duration of the studied taxa was 10–15 days. The total flowering period lasted 4.5–5 weeks; i.e. in 2016 from June 9 to July 10, whereas in 2018 from May 25 to June 28. The blooming sequence of the specific taxa did not change during the study period. Tilia cordata was characterized by the longest flowering period, whereas T. americana had the shortest one. Full flowering usually occurred on the 2nd – 3rd day of flowering and lasted from 3 to 11 days, depending on the taxon (Fig. 2) and weather conditions.

Fig. 1. Graphical representation of the dynamics in the achievement of the annual pollen sum. Pollen season stages: (1) 1–5%, (2) 5–25%, (3) 25–50%, (4) 50%, (5) 50–75%, (6) 75–95%, and (7).95–99%.

shown using graphs illustrating the dynamics in the achievement of the annual pollen sum. They show the duration of the successive stages of the season, corresponding to the achievement of the successive percentages of the annual pollen sum (Latałowa et al., 2002; Fig. 1). The Shapiro-Wilk test was used to determine the normality of distribution of the seasonal characteristics. Using correlation analysis, it was checked whether the temporal variability of the specific seasonal characteristics was statistically significant. Linear regression equations were developed for the normal distribution characteristics. Relationships between seasonal parameters and air temperature in individual months of the year were determined using Spearman’s correlation analysis.

3. Results 3.1. Morphological characteristics of flowers The flowers of the studied lindens were actinomorphic, 5-petaled, bisexual, with a diameter of 1–1.5 cm. T. americana was characterized by the largest flowers, 1.5 cm in diameter. In most of the lindens, the petals were white-yellow, and only T. × euchlora had yellow flowers. During anthesis, the sepals in the two native species, i.e. T. platyphyllos and T. cordata, were open, while in the other taxa they adhered to the corolla. The sepals in T. tomentosa were characterized by silver pubescence. The epipetalous stamens were borne in five whorls. The number of stamens in the flowers of the specific taxa varied, ranging 30–58 (Table 1). T. cordata had the lowest number of stamens per flower – on average 30.4 ± 2.6, T. × euchlora - 43.5 ± 2.0, while in the other species the number of stamens exceeded 50. The stamens in the flowers of T. platyphyllos were longer than the petals, in the flowers of T. americana and T. tomentosa – shorter than the petals, whereas in the flowers of T. cordata and T. × euchlora – equal to the petal length. Moreover, in the flowers of T. americana and T. tomentosa there were five epipetalous leafy staminodes. In the flowers of T. americana, the style was longer than in the other species and protruded outside the flower. The linden flowers were borne in cymes that were hanging on a slender peduncle fused with a large ligulate bract. The erect inflorescence occurred only in T. cordata. The number of flowers per inflorescence ranged 5.9 ± 0.3 (T. platyphyllos) – 15.2 ± 1.5 flowers (T. cordata) (Table 1). The flowers of the investigated lindens gave off a pleasant scent of different intensity. The flowers T. tomentosa were distinguished by a strong odorous smell.

3.3. Start and duration of the pollen season The start dates of Tilia pollen seasons throughout the study period ranged from May 25 (2018) to June 24 (2004), with the average date on June 12 (Table 2). The coefficient of variation for this parameter was exceptionally low, standing at 4.22%. Based on Pearson’s correlation analysis, a statistically significant variation was found for season start and duration (respectively −0.6193; p = 0.006, 0.6775; p = 0.002). As far the other parameters are concerned, the correlation coefficients were statistically insignificant. The calculated correlation coefficient indicates a statistically significant acceleration in the start date of the linden pollen season, but the fit of the regression model was 38% (Fig. 3). It was calculated that the acceleration in the linden pollen season onset was almost 14 days. The linden pollen season length was within the range of 21–51 days, with an average of 36 days (Table 2). This season characteristic exhibited higher variability (V = 19.76%) than season start. The analysis of the data concerning the length of the pollen season reveals an extension in the season, as shown by the upward trend line (Fig. 4). The fit of the linear regression model is 46%. The regression equation coefficients for season start and length were statistically significant. Over the study period, the season length increased by 15 days. Pollen season end dates, on the other hand, did not change significantly (Fig. 5). Data from the entire period were analyzed except for the outlier year 2018. The analysis revealed acceleration of the onset of the Tilia pollen season (slightly over 9 days) and extended duration of the season (by almost 13 days).

Table 1 Number of flowers per inflorescence and number of stamens per flower in the Tilia taxa studied in 2018. Takson

T. T. T. T. T.

platyphyllos americana cordata × euchlora tomentosa

Number of flowers per inflorescence

Number of stamens per flower

3.4. Annual pollen concentration

mean

± SD

V (%)

mean

± SD

V (%)

5.9 7.2 15.2 6.2 6.7

0.3 0.6 1.5 0.6 0.9

5.3 8.8 9.7 10.2 14.1

53.0 58.5 30.4 43.5 55.0

2.3 5.7 2.6 2.0 2.1

4.3 9.8 8.7 4.5 3.8

There were statistical differences in the annual sums of daily concentrations of Tilia pollen grains throughout the study period. The seasonal total ranged 79–968 grains, with an average of 332 grains. A very high variability (V = 67.30%) was noted for this parameter of the pollen season (Table 2). A very high seasonal total in 2018, which exceeded more than three times the average value obtained during the previous 17-year study period, deserves special attention.

SD - standard deviation, V - coefficient of variation. 3

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Fig. 2. Flowering periods of various species of Tilia against the background of the pollen season in 2016–2018.

3.5. Maximum pollen concentration

Lublin between June 9 and July 9 (Table 2). The maximum concentrations of pollen grains were from 9 to 243 P/m3, with an average of 54.2 P/m3. A very high coefficient of variation (V = 98.31%)

The dates of maximum linden pollen concentration were noted in 4

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Table 2 Statistics of the parameters of the Tilia pollen season in Lublin in 2001–2018. Statistics

Mean Min Max SD V%

Pollen season Start 12.06 25.05 (2018) 24.06 (2004) 6.9 4.2

Peak End 17.07 02.07 (2002) 31.07 (2015) 7.0 3.5

3

Duration (days) 36.2 21 (2002) 51 (2018) 7.1 19.8

P/m 54.2 9(2014) 243 (2018) 53.3 98.3

Annual Date 26.06 09.06 (2018) 09.07 (2004) 8.2 4.7

pollen sum 332.0 79 (2002) 968 (2018) 223.4 67.3

Min – the earliest date or the lowest number, Max – the latest date or the highest number, SD - standard deviation, V - coefficient of variation.

this phase is the main part of the pollen season, that is, the period of the constant presence of airborne pollen concentrations, with an average season length of 36 days. The other stages of airborne pollen grains throughout the season differed in length in most cases (Fig. 8). Exceptionally, a great similarity of the stages from 5% to 95% pollen grains was observed in 2004 and 2015 as well as in 2001 and 2018. The linden pollen seasons were not symmetrical. Due to the fact that the period that included the stages after reaching the cumulative percentage of 50% pollen grains was longer, the pollen seasons can be considered to be right-skewed. The calculated coefficient of skewness was in the range of 0.8 – 4.9.

confirms the large differences in these values between years. The linear trend determined for all study years shows a slight increasing trend in maximum pollen concentrations (Fig. 6). 3.6. Dynamics of pollen seasons The values of linden pollen concentrations varied considerably between years and parts of the season (Table 3). The highest mean percentage of total pollen grains was found in June (63.8%). In July the average linden pollen content was much lower (34.6%), while in May and August it was only 0.3% and 1.3%, respectively. In particular years, the airborne linden pollen content in June ranged between 10.2% and 97.4%, whereas in July from 1.3% to 85.1%. In August the amounts of linden pollen grains did not exceed 5% and ranged from 0.4% to 4.6%. In June and July, the amounts of pollen grains showed higher standard deviation values. The curves representing the pollen season pattern were almost exclusively multimodal due to many peaks, which is associated with the flowering and pollen release of the respective Tilia species at different times. This characteristic is clearly seen in the years with the highest Tilia pollen concentration (Fig. 7). In Lublin linden pollen seasons markedly differed with regard to the date when 50% of the annual airborne pollen sum was reached (Fig. 8). The years 2012 and 2013 were an exception. During the first 9 years of the study (2001–2009), the stage when 50% of pollen grains had been released occurred in the first 10 days of July or in the third 10 days of June. In the next 9 years (2010–2018), on the other hand, in most cases the cumulative percentage of 50% pollen grains was reached in the third 10 days of June or earlier (2010–2014, 2016–2018). During 13 years out of the 18-year study period, the stages of cumulative pollen grain percentages from 25% to 75% had a similar duration (8–10 days). This fact is evidence that the phase of releasing large amounts of linden pollen was short and rapid. At the same time,

3.7. Flowering phenology in relation to the pollen season pattern The curves depicting Tilia pollen seasons based on the average daily concentrations over the period 2016–2018 differed significantly from one another (Fig. 2). During the 2017 pollen season, one of the lowest total annual pollen sums was recorded. A comparison of these curves with the graphs representing the flowering phenology of the five linden species shows that the individual peaks correspond to the full flowering period in the successive flowering seasons of T. platyphylla, T. americana, T. cordata, T. x euchlora, and T. tomentosa. The highest peak occurred during full flowering of T. cordata, which indicates the highest percentage of this taxon’s pollen in the annual Tilia pollen concentration. 3.8. Effect of temperature on pollen seasons The statistical analysis demonstrated that there is a statistically significant correlation between some pollen season parameters and temperature (Table 4). Spearman’s correlation analysis shows that the onset of the pollen season started earlier when the mean temperatures

Fig. 3. Comparison of the start dates of the linden pollen season in Lublin in 2001–2018 and the trend line. 5

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Fig. 4. Length of the Tilia pollen seasons in Lublin in 2001–2018 and the trend line.

species covered a period of 12 to 17 days. T. cordata had the longest flowering period, while T. americana the shortest one. In 2018 the blooming date of the linden species in question was recorded two weeks earlier than during the three-year period investigated by Dąbrowska et al. (2016) or in 2016 and 2017. In all years of the study, the linden species under observation bloomed in the same sequence: T. platyphyllos, T. americana, T. cordata, T. × euchlora, and T. tomentosa. The same sequence had also been recorded previously by other researchers for most of the above-mentioned species (Faliński and Pawlaczyk, 1991; Jabłoński and Kołtowski, 1999). Because T. cordata has a wide range in Europe (Boratyńska and Dolatowski, 1991) and in many countries it is an important indicator for phenological seasons (Nekovář et al., 2008), the blooming of this species sometimes serves as a “phenoindicator” in planning agronomic operations (Faliński and Pawlaczyk, 1991). In the years 2016 and 2018, the beginning of airborne dispersal of Tilia pollen occurred concurrently with the recorded onset of flowering of the first species, T. platyphyllos. Nonetheless, the pollen season lasted longer than the flowering of the five species observed, which could have been due to pollen redeposition or later flowering of other linden

in April and May were high. On the other hand, the end of the pollen season is significantly dependent on the mean temperature in March and May. A higher temperature in May contributes to earlier occurrence of maximum Tilia pollen concentrations (peak day). 4. Discussion Long-term phenological observations and aerobiological monitoring aimed at determining the content of pollen grains in aeroplankton allow plant responses to climate change to be studied. The aerobiological sampling station is located in Lublin in the central part of the city. In close vicinity to this station, there are two parks in which different linden species are used for urban vegetation as well as many T. cordata specimens can be found growing along some streets in the city. Therefore, quite substantial amounts of Tilia pollen grains are recorded on the tape of our sampler. Our study revealed that the average flowering duration of each of the five linden species in Lublin during the period 2016–2018 was from 10 to 15 days, whereas observations conducted by Dąbrowska et al. (2016) over the period 2012–2015 show that the flowering of the same

Fig. 5. End dates of the linden pollen seasons in Lublin in 2001–2018. 6

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Fig. 6. Variation in maximum daily linden pollen concentrations in Lublin in 2001–2018.

recorded a later onset of the pollen season, which was accompanied by poor flowering and low Tilia pollen production. Our study demonstrated that the full flowering stages of the five Tilia species used in urban plantings in Poland correspond to the individual peaks of the multimodal curves representing linden pollen seasons during the period 2016–2018. The highest peaks occur during full flowering of T. cordata, which is probably attributable to the fact that individuals of this species are the most numerous in Lublin’s green areas. We found a similar correlation in the case of four linden species in 2010 (Weryszko-Chmielewska and Sadowska, 2010) and four maple species during the period 2011–2012 (Weryszko-Chmielewska et al., 2016) in phenological and aerobiological studies that were carried out concurrently. Recording of airborne pollen of anemophilous and entomophilous plants done as part of aerobiological investigations support and confirm results of phenological investigations. Furthermore, aerobiological analysis enables us to determine years of abundant and poor pollen production of trees. Global warming that has occurred over the last decades causes a response of many plans as regards their flowering and pollen release. Our study demonstrates that over the last 18 years (2001–2018) in Lublin, there was an acceleration in the onset

Table 3 Percentage of Tilia pollen in particular months of the season. Values for the period 2001–2018. Statistics

Mean Min Max SD V%

Months May

June

July

August

0.3 0.0 2.7 (2018) 0.7 201.5

63.8 10.2 (2004) 97.4 (2002) 25.6 40.1

34.6 1.3 (2002) 85.1 (2004) 25.3 73.1

1.3 0.0 4.6 (2004) 1.3 98.7

Min – the lowest percentage of pollen, Max –the highest percentage of pollen, SD - standard deviation, V - coefficient of variation.

species introduced in Poland. Later blooming dates of linden species of foreign origin are reported by Faliński and Pawlaczyk (1991). On the other hand, the average Tilia pollen season for the period 2012–2015 was delayed by a week compared to the flowering times in these years and ended a week earlier (Dąbrowska et al., 2016). In 2017 we also

Fig. 7. Tilia pollen seasons in the 4 years (2006, 2007, 2015, and 2018) characterized by the highest annual total throughout the entire study period (18 years). 7

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Fig. 8. Dynamics of the Talia pollen seasons in 2001–2018.

8

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that the relatively high temperatures in April and May 2018 can be considered to be an important factor that contributes to accelerated flowering and increased pollen production by species of the genus Tilia. The observed response of trees of the genus Tilia as regards pollen shed is not only a response to climate change, but probably also to air temperatures in an urban environment affected by urban morphology, such as spatial organization, building density, and impervious surfaces. Massetti et al. (2015) found that the start and end of T. x euchlora flowering under urban conditions occurred 1.4 day earlier on impervious surfaces than in other parts of the city. In urban green spaces, the broadleaved trees, among them Tilia, play a major positive role. They reduce noise and the degree of pollution in the lower layers of air, absorb CO2 and release oxygen as well as create mild thermal conditions. The cooling effect, which is very important in summer months, causes a reduction in both ground and air temperatures (Shashua-Bar and Hoffman, 2000; Kuchcik, 2003; Błażejczyk et al., 2014). Linden trees have special properties associated with a high degree of shading provided by their canopies. In a study on solar radiation penetrating tree canopies, in the case of T. cordata it was shown that the mean ratio of direct total radiation below a foliated tree was only 8.8%, whereas the respective value for Betula pendula was 16.2% (Konarska et al., 2014). Apart from improving the urban climate, including thermal conditions, urban tall greenery may cause the incidence of allergies in sensitive people. As a result of the large variation in the amount of linden pollen contained in the aerosol, allergies occur with different intensity. Our study showed that the highest risk of allergy to linden pollen in central-eastern Poland occurs in June as well as at the beginning of July in some years. Given the tendency towards accelerated flowering and pollen release, one can expect earlier occurrence and greater intensity of allergies to linden pollen. Because the degree of allergenicity of linden pollen has not yet been determined unambiguously (whether it is low or moderate), linden plantings in biologically vital urban areas should be planned to be established at some distance from residential estates, playgrounds, and kindergartens. As shown in our research and the phenological observations conducted by Juknys et al. (2011), (2012), Tilia exhibits a clear response to global warming. Therefore, our plans include continuation of the phenological research of various species representing this genus. The record results related to Tilia pollen release in 2018 will be an important impulse for further aerobiological investigations, which will probably provide more data on the response of these trees to climate change.

Table 4 The list of significant Spearman’s correlations between the parameters of the Tilia pollen season in Lublin (2001–2018). Season parameter vs meteorological factor

Spearman coefficient

Mean Mean Mean Mean Mean

−0.471* −0.485* −0.655** −0.488* −0.625**

temperature temperature temperature temperature temperature

in in in in in

March & End April & Start May & Start May & End May & Peak date

Level of significance *0.05, **0.01.

of linden pollen seasons by 14 days. The analysis of the dynamics of Tilia pollen seasons also reveals that the stage of 50% pollen release was reached earlier in the second 9-year period of our study than in the first one. The acceleration in pollen seasons is also confirmed by the determined trend line, which shows earlier dates of occurrence of maximum linden pollen concentrations in recent years. A phenological study of other authors conducted in Lithuania demonstrates that T. cordata bud break accelerated by 11.3 days over a period of 55 years (Juknys et al., 2011, 2012). Many studies show earlier dates of first bloom of various herbaceous and woody plant species. Fitter and Fitter (2002) demonstrated an acceleration rate of at least 15 days for 60 species of British plants in 1991–2000 compared to the previous period. Menzel et al. (2006) also recorded in Europe a trend towards earlier flowering for several tree species, whereas Primack et al. (2004) report earlier flowering of many plant species during the period 1980–2002 in Boston. Clear trends towards an earlier start of the Betula pollen season have been found in many European countries (Rasmussen, 2002; Emberlin et al., 2002; van Vliet et al., 2002; Clot, 2003; Frei and Gassner, 2008; Puc, 2014). Smith et al. (2014) and Shang et al (2015) also demonstrated an accelerated onset of pollen seasons of several tree species. Malkiewicz (2014) reported an acceleration of the beginning of the Corylus pollen season. Our research found a distinct trend towards extending linden pollen seasons (by 15 days) over the 18-year study period. Juknys et al. (2011), (2012) found the linden pollen season to be extended by 21–23 days due to climate change. The authors of these studies observed earlier leaf blade development and later leaf fall in Tilia cordata. In the case of several tree species in central Europe, the growing season was shown to be extended on average by 23.8 days over a period of 35 years (1976–2010) (Kolářová et al., 2014). Prolongation of pollen seasons for several types of trees in Spain was reported by Ruiz-Valenzuela and Aguilera (2018). Fitter and Fitter (2002) report that entomophilous plants show a more distinct response to increased temperature than anemophilous plants. Many authors have found increased pollen production in plants as a result of global warming. Myszkowska et al. (2014) recorded in Cracow (Poland) a significant upward trend in the annual total of Corylus pollen, whereas Zhang et al. (2015) in the United States revealed a significant increase in the annual totals of daily pollen counts in different anemophilous species. Our study shows that over the 18-year study period there was an insignificant increasing trend in the annual totals of daily Tilia pollen counts. However, worth noting is the exceptional increase in the number of Tilia pollen grains recorded in 2018, which was more than three times higher than the average for the previous 17 years. The above increase is probably the effect of the persistence of much higher temperatures in April and May 2018, respectively 14.2 °C and 18.4 °C, than in the previous 17 years. The April average for the previous 17 years in Lublin was 9.7 °C, whereas in May it was 15.1 °C. According to the literature data (Faliński and Pawlaczyk, 1991), linden flower primadoria are formed in spring in the year of flowering. The authors of the above-mentioned paper stress that the rate of development of linden flowers and date of first bloom are largely dependent on the temperature in spring months. Therefore, it seems

5. Conclusions

• Based on the results of an 18-year study on Tilia pollen concentra• •

• • • 9

tions in the air of Lublin, we found a significant acceleration in the onset of pollen seasons and their substantial extension over the recent years. The risk of allergies caused by the presence of linden pollen in the air of Lublin occurs in May, June, and July. The main part of the studied Tilia pollen seasons, which covered the period of occurrence of 25–75% of airborne pollen grains, had a similar length in most years of the study and lasted very short (8–10 days); this can be evidence of rapid release of a large amount of pollen in a short time, which is characteristic of this genus. The pollen season length was 20–50 days. The sequence of flowering of the individual linden species during the growing season is constant: T. platyphyllos, T. americana, T. cordata, T. × euchlora, and T. tomentosa. The flowers of the five linden species in question have a varied number of stamens, which ranges 30–58 and averages 48. The highest number of stamens was found in T. americana, while the lowest one in T. cordata. We did not find a relationship between number of stamens and flower size in the species studied. The numerous peaks in the multimodal Tilia pollen curves for the

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•

•

period 2016–2018 correspond to full flowering of the five linden species studied, which are found in Lublin in natural stands and urban plantings. The largest amounts of pollen occur during full flowering of Tilia cordata. The response of plants to significant warming could be seen most clearly in the Tilia pollen season in 2018; with higher temperatures from April to July, this year showed accelerated pollen release, an increased pollen season length, and an annual total pollen concentration that was three times higher than the average for the previous 17 years. Further research is required to confirm this conclusion. Due to the allergenicity of linden pollen, new plantings of trees of this genus should be located at some distance from new residential estates.

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