THE PHENOLOGY OF FLOWERING AND POLLEN RELEASE IN FOUR SPECIES OF LINDEN (Tilia L.)

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1 Vol. 54 No Journal of Apicultural Science 99 THE PHENOLOGY OF FLOWERING AND POLLEN RELEASE IN FOUR SPECIES OF LINDEN (Tilia L.) E l ż b i e t a W e r y s z k o - C h m i e l e w s k a, D a g m a r a A n n a S a d o w s k a Department of Botany, University of Life Sciences in Lublin, ul. Akademicka 15, Lublin, Poland elzbieta.weryszko@up.lublin.pl Received 17 October 2010; Accepted 03 December 2010 S u m m a r y Linden trees belong to important forage plants that provide nectar and pollen for insects. The aims of the present study were to determine correlations between the flowering stages of four linden species that are frequently found in urban plantings in the city of Lublin, and the dynamics of occurrence and abundance of airborne pollen grains. The species under study included the following: Tilia cordata Mill., T. platyphyllos Scop., T. x europaea L., T. tomentosa Moench. The flowering phenophases were studied in the 2010 growing season. The pollen season patterns were studied in the seasons. Aerobiological monitoring was carried out using the volumetric method to investigate the linden pollen content of the air. Tilia platyphyllos, T. x europaea, T. cordata, and T. tomentosa bloomed successively during the 2010 growing season. The flowering duration of the first three species was 16 days, while for T. tomentosa it was 12 days. The total flowering duration for the four abovementioned species was 38 days, which largely corresponded to the duration of the pollen season period. Our study showed that the four abovementioned species provided forage for insects over a period of about 6 weeks. The maximum airborne linden pollen concentration occurred during the full bloom period of Tilia x europaea and T. cordata (26 June). Annual pollen counts of airborne linden pollen significantly varied between years. In the year in which the highest airborne pollen content was recorded (2006), four times more pollen grains were observed compared to the year in which a small amount of airborne pollen was recorded (2005). During the period in question, we found no clear phenological response of the linden species to air temperature increase. Further research may allow definite correlations to be demonstrated. Keywords: Tilia, flowering phenology, pollen seasons, pollen abundance, pollen monitoring, Lublin. INTRODUCTION Two linden species: Tilia cordata Mill. and T. platyphyllos Scop., are found in the natural conditions of Poland. The former one is common across most of the country, while the latter one can be encountered in the southern part of Poland where the northern boundary of its range is designated (Zając and Zając, 2001; Witkowska- Żuk, 2008). Linden trees rarely form dense tree stands. They are usually admixtures in dry-ground forests (oak-hornbeam-linden) or in linden-sycamore maple forests. The only old-growth linden forest in Poland is in the Poprad Landscape Park. In addition to linden, there is an admixture of beech and several other tree species. The Obrożyska Linden Forest nature reserve was established in this park (Rąkowski, 2004). Several dozen linden species and varieties can be found in urban plantings (Seneta and Dolatowski, 2007). Linden trees are valued park trees which are frequently planted along avenues and roads. Their valuable features include the regular shape of their crown, the early development of leaf buds, and abundant flowering. The high apicultural value of linden is emphasised in many papers (Demianowicz and Hłyń, 1960; Maksymiuk, 1960; Jabłoński, 1991; Jabłoński and Kołtowski, 1999;

2 100 Kołtowski, 2006). The tradition of collecting linden honey in forests has been continued by forest beekeepers for centuries, and this honey variety has always had a high price tag (Samojlik and Jędrzejewska, 2004; Samojlik, 2005). Linden honeys are gathered in the eastern and southern parts of Europe (Maurizio and Grafl, 1969; Persano Oddo et al., 2004). Bees also collect pollen abundantly produced by linden flowers. The existing research shows that one Tilia cordata flower produces pollen grains, while one inflorescence grains (Maurizio and Grafl, 1969). In the pollen load samples under investigation, Warakomska (1999) found as much as 77% of bee pollen loads contained linden pollen. Linden flowers are entomophilous, but a part of the pollen of this taxon floats in the air. The aim of the present study was to compare the flowering phenology of four linden varieties with the duration of the pollen season and pollen abundance determined using aerobiological analysis. MATERIALS AND METHODS Phenological observations of the flowering stages of four linden species: Tilia cordata, T. platyphyllos, T. x europaea, T. tomentosa, were conducted in Lublin in the city centre district in 2010 following the recommendations of Łukasiewicz (1984). Trees belonging to the abovementioned species are often found in urban green areas of Lublin. The dates of the following phenological phases were determined for each of the species: 1 - appearance of first flowers (several full-blown flowers) 2 - onset of full bloom (about 25% of open flowers) 3 - appearance of first overblown flowers (first flowers with a wilting perianth) 4 - end of full bloom (about 75% of flowers overblown) 5 - last blooming flowers 6 - end of flowering (all flowers overblown). The observations were conducted on sunny days at C. Aerobiological monitoring was carried out in Lublin in the period , using a VPPS Lanzoni 2000 volumetric trap. The sampler was installed at a height of 18 m on the roof of a building in the city centre. The linden pollen seasons were determined following the recommendations of the International Association for Aerobiology (Jäger, 2003). RESULTS 1. Flowering phenology Flowers of the linden species under observation bloom abundantly and they are frequently visited by bees (Phot. 1-4). The study conducted in 2010 shows that the flowering times of three species (Tilia platyphyllos, T. cordata and T. x europaea) partially overlap with each other, but the flowering of T. tomentosa occurs after the end of the flowering period of the other three taxa (Fig. 1, Tab. 1). Among the species in question, T. platyphyllos started flowering earliest (7 June), then T. x europaea (13 June) and T. cordata (16 June), while T. tomentosa flowered latest (2 July). The duration of flowering of the first three taxa was the same (16 days), whereas the flowering of T. tomentosa was shorter (12 days) (Fig. 1, Tab. 1). Differences in flower life span were observed between individual linden species. The flowers of T. cordata bloomed for the longest time (5 days), then T. x europaea (4 days), T. tomentosa and T. platyphyllos (3.5 days). This study demonstrates that there are a different number of days for the full bloom periods of individual species. On the average, this stage lasted 3.5 days, and for the respective taxa this number was as follows: T. cordata 4.5 days, T. x europaea 3.5 days, whereas T. platyphyllos and T. tomentosa 3 days (Tab. 2). One may expect that in 2010 abundant pollen shed of linden will occur during the period of simultaneous flowering of the three species that are frequently found

3 Vol. 54 No Journal of Apicultural Science 101 T a b l e 1 Flowering dates of four Tilia species in 2010, with the identification of phenological phases Phenological Species of Tilia phase T. platyphyllos T. x europaea T. cordata T. tomentosa Duration of flowering (days) appearance of first flowers (several full-blown flowers) 2 - beginning of full bloom (about 25% of open flowers) 3 - appearance of first overblown flowers (first flowers with a wilting perianth) 4 - end of full bloom (about 75% of flowers overblown) 5 - last blooming flowers 6 - end of flowering (all flowers overblown) T a b l e 2 Comparison of phenological phases of flowers of four linden species in the conditions of Lublin in 2010 Phenological phases of Tilia flowers Day Hours T. platyphyllos T. x europaea T. cordata T. tomentosa ^ ^ O O O O O in the conditions of Lublin; T. cordata, T. platyphyllos and T. x europaea. That period is from June. 2. Characteristics of the pollen seasons Linden pollen grains are trizonocolporate and average-sized. Depending on the view, O O O O O O O O O O O O O O O + Flower life span (days) The designation of phenological phases of flower development according to Krotoska (1958): ^ - bud - beginning of flowering (flower bud opening) O - full bloom - end of flowering (perianth wilting) + - seed setting they are differently shaped (Phot. 5, 6). Over the period of 6 years of study ( ), the linden pollen season started between 7 June and 23 June. The largest difference between the start of the pollen season was 15 days. The earliest +

4 102 Fig. 1. A flowering calendar of four linden species (Tilia spp.) in the conditions of Lublin, in 2010 Fig. 2. The linden pollen season pattern in 2010 T a b l e 3 Characteristics of linden pollen seasons on the basis of aerobiological monitoring in Lublin, in the period Year Investigated trait Average Start of season End of season Duration (days) Max. concentration (number of grains/m 3 ) Date of occurrence of max. concentration linden pollen shed was noted in 2010, whereas in 2006 the first airborne linden pollen was recorded as late as 23 June (Tab. 3). During the study years, the end of the linden pollen season was within the period from 17 July to 26 July. However, single pollen grains occurred in the air until the middle of September. The duration of the linden pollen season ranged between 29 and 44 days, averaging 37 days.

5 Vol. 54 No Journal of Apicultural Science 103 Maximum linden pollen concentrations (14-97 grains per 1m 3 ) were recorded in the atmosphere between 26 June and 4 July (Figs 2 and 3). This means that in the abovementioned period, the largest amount of pollen was also available to insects. The highest linden pollen concentration (97 grains/m 3 ) was recorded on 1 July 2006 (Fig. 3). The chart showing the average linden pollen content of the air in Lublin for the period (Fig. 4) demonstrates that the largest amount of linden pollen was in the air in the second and third decades of June and in the first days of July. The highest pollen concentrations also occurred in this period. Annual pollen counts per 1m 3 ranged from 157 to 624 grains, and on the average, were 359. Abundant linden pollen production occurred in the years 2006 and 2007, while the years 2005 and were characterized by pollen counts lower than or close to the average value (Fig. 5). 3. Comparison of the phenology of flowering and pollen release in linden In 2010, the highest number of linden pollen grains was recorded on 22 June and Fig. 3. The linden pollen season patterns in the period

6 104 Fig. 4. The average linden pollen content of the air in Lublin based on the study conducted in the period Fig. 5. Annual linden pollen counts ( ) and the 6-year average for the city of Lublin 26 June (Fig. 2). The flowering period of three linden species (Tilia platyphyllos, T. x europaea, T. cordata) occurred on June 22. The full bloom of two species, including T. cordata which is most frequently found in park and street plantings in Lublin, occurred on June 26 (see Figs 1 and 2, Tab. 1). During the flowering period of T. tomentosa (2-14 July) (Fig. 1), there were two minor peaks (Fig. 2), corresponding to the full bloom dates of this species (Tab. 1), in the curve representing the pollen season. The flowering of T. tomentosa lasted until 14 July, but linden pollen grains occurred in the atmosphere for several days longer. DISCUSSION The present study shows that in 2010 the duration of flowering of each of the three linden species (Tilia platyphyllos, T. x europaea, T. cordata) was 16 days, whereas T. tomentosa flowered for 12 days. The total duration of flowering of the abovementioned four species, with different blooming dates, was 38 days. The length of this period is in agreement with literature data which show that linden species flowering at different times can provide forage for insects over a period of 6 weeks (Lipiński, 1958; Szklanowska et al., 1999). On the other hand, Szymczak (2006) reports that a collection of cultivated linden trees can provide forage for bees for as long as 6-7 weeks. The average duration of the linden pollens season, determined

7 Vol. 54 No Journal of Apicultural Science 105 Photographs Captions: Phot. 1. T. platyphyllos inflorescences at the full bloom stage Phot. 2. T. cordata buds and full-blown flowers Phot Bees visiting T. tomentosa flowers Phot Linden pollen grains in different views (x700): 5 - polar view 6 - equatorial view

8 106 based on the present study, also confirms that flowers of different linden species can provide pollen forage over a period of 6 weeks. In 2010 linden flowered in the following sequence: T. platyphyllos, T. x europaea, T. cordata and T. tomentosa. Szklanowska et al. (1999) state that in other years, there was the same blooming sequence of the species mentioned above. Lipiński (1958) found that in central Poland, linden trees flowered from 10 June to 20 July. In 2010, the linden trees that we investigated in Lublin, flowered from 7 June to 14 July. The flowering period of the four linden species largely overlapped with the start and end dates of the pollen seasons in the same year. Moreover, we found that pollen grains floated in the air for several days after the end of the flowering period. This could have resulted from redeposition, that is, pollen grains which had earlier deposited on solid ground were again blown up into the air by air currents. These grains could have also originated from flowers of other linden species that flower later, e.g. T. japonica or T. insularis (Lipiński, 2010). In 2010, the flowering of T. platyphyllos lasted from 7 June to 23 June, while T. cordata started flowering 9 days later (16 June) and finished on 2 July. The average start date (for the period of 6 years) of the linden pollen season (14 June) probably corresponds to the blooming dates of T. platyphyllos. This species is the earliest linden tree to start flowering. If we take into account two dates, 7 June and 14 June, as the beginning of flowering of T. platyphyllos in the period , then these dates are similar to the data given by Lipiński (2010) for the period , Czubacki (1996) for the period , and Jabłoński et al. (2000) for the years Only the results reported by Demianowicz and Hłyń (1960) for the period (20 June and 26 June) and relating to the area of Poznań, indicate a much earlier onset of flowering in Lublin in the year 2010 (6-13 days). However, these differences are within the deviations of the blooming dates in particular years which, according to Lipiński (2010), are days for T. platyphyllos. Over the period of 6 years, the extreme dates, determined by us and defining the pollen season of the genus Tilia, occurred between 7 June and 26 July. These dates largely coincide with the time of flowering (8 June - 31 July) of 12 linden species mentioned in a paper by Lipiński (2010), which includes data for the period As a result of the present study, we found that maximum linden pollen concentrations in the air of Lublin in 2010 corresponded exactly with the full bloom period of the linden species under investigation. Annual pollen counts per 1m 3 in particular study years varied significantly. The extreme values occurred in the years 2005 and In 2006, four times more pollen (624 grains) was found in the air of Lublin than in 2005 (157 grains). Szklanowska et al. (1999), and Jabłoński et al. (2000) showed that in the case of Tilia cordata abundant and poor flowering occurred alternately in consecutive years. But under the present study, covering a period of 6 years, no biannual cycle of abundant pollen shed was observed for linden. Tilia cordata is one of the species which determine the phenological seasons of the year. The flowering of this taxon defines the beginning of summer (Krotoska, 1958). Research on the phenological response of plants to air temperature increase is currently underway in Europe (Jatczak, 2007; Jatczak and Walawender, 2009). These studies demonstrate that there is a clear tendency towards an earlier occurrence of spring phenophases and an extended growing season. These changes apply to a lesser degree to plants flowering during the summer season, and linden belongs to such plants. We hope that the continuation of our phenological and aerobiological research will allow the abovementioned correlations to be determined more accurately in the case of linden species.

9 Vol. 54 No Journal of Apicultural Science 107 References Czubacki W. (1996) - Niektóre szczegóły biologii kwitnienia i nektarowania lip (Tilia platyphyllos Scop. i Tilia cordata Mill.). / Some details of the biology of flowering and nectar production of linden trees (Tilia platyphyllos Scop. and Tilia cordata Mill.). Pszczeln. Zesz. Nauk., 40(1): Demianowicz Z., Hłyń M. (1960) - Porównawcze badania nad nektarowaniem 17 gatunków lip. / A comparative study on nectar production of 17 linden species. Pszczel. Zesz. Nauk., 4(3-4): Jabłoński B. (1991) - Pożytki pszczele z lip. / Bee forage from linden trees. [In]: Lipy. Nasze drzewa leśne. Monografie popularnonaukowe, 15. / Linden trees. Our forest trees. Popular scientific monographs, 15. Białobok S. (ed.). Agencja Arkadia, Poznań: Jabłoński B., Kołtowski Z. (1999) - Nektarowanie różnych gatunków i mieszańców lipy (Tilia L.). Pszczeln. Zesz. Nauk., 43: Jabłoński B., Kołtowski Z., Szklanowska K., Teper D. (2000) - Z badań biologii kwitnienia, nektarowania i pylenia lip. / Research on the biology of flowering, nectar production and pollen release in linden trees. Pszczelarstwo, 51(7): 4-5. Jatczak K. (2007) - Fenologiczna odpowiedź na tendencje zmian klimatu w Polsce na tle zmian zachodzących w Europie. / The phenological response to climate change trends in Poland relative to the changes occurring in Europe. Wiadomości Meteorologii Hydrobiologii Gospodarki Wodnej, 51(1): Jatczak K., Walawender J. (2009) - Average rate of phenological changes in Poland according to climatic changes - evaluation and mapping. Advances in Science and Research, 1: 1-4. Jäger S. (2003) - The European Pollen Information System (epi). Data bank (EAN), Web sites and forecasting. Postępy Dermatologii i Alergologii, 20(4): Kołtowski Z. (2006) - Wielki atlas roślin miododajnych. / The Great Atlas of Melliferous Plants. Przedsiębiorstwo Wydawnicze Rzeczpospolita, Warszawa. Krotoska T. (1958) - Pory roku w życiu roślin. Obserwacje fenologiczne w zespołach roślinnych. / Seasons in the life of plants. Phenological observations in plant associations. PWN, Poznań. Lipiński M. (1958) - Pożytki pszczele: zapylanie i miododajność roślin. / Bee forage. Pollination and honey productivity of plants. PWRiL, Warszawa. Lipiński M. (2010) - Pożytki pszczele. Zapylanie i miododajność roślin. / Bee forage. Pollination and honey productivity of plants. PWRiL, Warszawa. Łukasiewicz A. (1984) - Potrzeba ujednolicenia metodyki fenologicznej w polskich ogrodach botanicznych i arboretach. / The need to standardise the phenological method in Polish botanical gardens and arboreta. Wiadomości Botaniczne, 28(2): Maksymiuk I. (1960) - Nektarowanie lipy drobnolistnej (Tilia cordata Mill.) w rezerwacie Obrożyska koło Muszyny. / Nectar production of small-leaved linden (Tilia cordata Mill.) in the Obrożyska nature reserve near Muszyna. Pszczeln. Zesz. Nauk., 4(2): Maurizio A., Grafl I. (1969) - Das Trachtpflanzenbuch. Nektar und Pollen die wichtigsten Nährungsquellen der Honigbiene. Band 4. Ehrenwirth Verlag, München. Persano Oddo L., Piana L., Bogdanov S., Bentabol A., Gotsiou P., Kerkvliet J., Martin P., Morlot M., Ortiz Walbuena A., Ruoff K., von der Ohe K. (2004) - Botanical species giving unifloral honey in Europe. Apidologie, 35: Rąkowski G. (2004) - Parki Krajobrazowe w Polsce. / Landscape parks in Poland. Instytut Ochrony Środowiska, Warszawa. Samojlik T. (2005) - Drzewo wielce użyteczne - historia lipy drobnolistnej (Tilia cordata) w Puszczy Białowieskiej. / A highly useful tree - the history of small-leaved linden (Tilia cordata) in the Białowieża Primeval Forest. Rocznik Dendrologiczny, 53:

10 108 Samojlik T., Jędrzejewska B. (2004) - Użytkowanie Puszczy Białowieskiej w czasach Jagiellonów i jego ślady we współczesnym środowisku leśnym. / The use of the Białowieża Primeval Forest in the time of the Jagiellons and its traces in the contemporary forest environment. Sylwan 11: Seneta W., Dolatowski J. (2007) - Dendrologia. / Dendrology. Wydawnictwo Naukowe PWN, Warszawa. Szklanowska K., Teper D., Jabłoński B., Kołtowski Z. (1999) - Wybrane zjawiska biologii kwitnienia różnych gatunków i mieszańców lipy (Tilia L.) oraz oblotu ich przez pszczoły. / Some occurenses of blooming biology of selected species and hybrids of lime-tree (Tilia L.) and their foraging by bees. Pszczeln. Zesz. Nauk., 43: Szymczak P. (2006) - Rośliny dla pszczół: Lipa. / Plants for bees: Linden. Pszczelarz Polski, 119(9): Warakomska Z. (1999) - Rośliny ogrodowe i ruderalne Puław w obrazie pyłkowym obnóży pszczelich. / Garden and ruderal plants of Puławy in the pollen spectrum of bee pollen loads. Bibliotheca Fragmenta Botanica, 6: Witkowska-Żuk L. (2008) - Atlas roślinności lasów. / The Atlas of Forest Vegetation. Multico Oficyna Wydawnicza, Warszawa. Zając A., Zając M. (2001) - Atlas rozmieszczenia roślin naczyniowych w Polsce. / The Atlas of Distribution of Vascular Plants in Poland. Pracownia Chorologii Komputerowej Instytutu Botaniki Uniwersytetu Jagiellońskiego, Kraków. FENOLOGIA KWITNIENIA I PYLENIA CZTERECH GATUNKÓW LIPY (Tilia L.) W e r y s z k o - C h m i e l e w s k a E., S a d o w s k a D. A. S t r s z e c z e n i e Lipy należą do ważnych roślin pożytkowych dostarczających owadom nektaru i pyłku. Celem badań było ustalenie zależności między fazami kwitnienia czterech gatunków lipy, często spotykanych w nasadzeniach miejskich Lublina a dynamiką i obfitością występowania ziaren pyłku w powietrzu atmosferycznym. Badane gatunki to: Tilia cordata Mill., T. platyphyllos Scop., T. x europaea L., T. tomentosa Moench. Fenofazy związane z kwitnieniem badano w sezonie wegetacyjnym 2010 roku, a przebieg sezonów pyłkowych w latach Do badań zawartości pyłku lipy w powietrzu zastosowano monitoring aerobiologiczny przeprowadzony metodą wolumetryczną. Wykazano, że w sezonie wegetacyjnym 2010 zakwitają kolejno Tilia platyphyllos, T. x europaea, T. cordata i T. tomentosa. Długość kwitnienia trzech pierwszych gatunków wyniosła 16 dni, a ostatniego z wymienionych 12 dni. Długość kwitnienia czterech wymienionych gatunków trwała łącznie 38 dni, co pokrywało się w dużym stopniu z długością sezonu pyłkowego. Z badań wynika, że wymienione gatunki dostarczają pożytku owadom przez okres około 6 tygodni. Maksymalne stężenie pyłku lipy w powietrzu przypadało na okres pełni kwitnienia T. x europaea i T. cordata (26.06). Zarejestrowane w powietrzu sumy roczne ziaren pyłku lipy znacznie się różniły w latach badań. W roku największej zawartości pyłku w powietrzu (2006) zanotowano 4 razy więcej ziaren niż w roku niewielkiej ich ilości w atmosferze (2005). W badanym okresie nie stwierdzono wyraźnej fenologicznej reakcji gatunków lipy na wzrost temperatury powietrza. Być może dalsze badania pozwolą na wykazanie określonych zależności. Słowa kluczowe: Tilia, fenologia kwitnienia, sezony pyłkowe, obfitość pylenia, monitoring pyłkowy, Lublin.