CHARACTERISTICS of BLOOMING and POLLEN in FLOWERS of TWO Syringa SPECIES (F

ACTA AGROBOTANICA Vol. 66 (4), 2013: 65–72 Original Research Paper DOI: 10.5586/aa.2013.052

CHARACTERISTICS OF BLOOMING AND POLLEN IN FLOWERS OF TWO Syringa SPECIES (f. Oleaceae)

Bożena Denisow, Monika Strzałkowska-Abramek

Department of Botany, Laboratory of Horticultural Plant Biology, University of Life Sciences in Lublin Akademicka 15, 20-950 Lublin, Poland e-mail: [email protected]

Received: 12.06.2013

Abstract Asia and within the range of their origin are consid- The observations were conducted in long-term sequen- ered as insect pollinated [2]. Lilacs, due to delicious ce studies in the years 2006, 2009, 2013, in the Lublin area, fragrant and abundant blooming, are one of the most Poland (51o 16’ N, 22o 30’ E). The flowering phenology, diurnal widely cultivated ornamental trees and shrubs in tem- pattern of blooming, pollen production and insect visitation to perate regions of the world [3]. Several hundred culti- the shrubs of Syringa oblata Lindl. var. dilatata (Nakai) Rehd. vars have been developed through extensive hybridiza- and S. meyeri ‘Palibin’ Schn. were examined. tion and artificial selection [4]. The plants (e.g. Syrin- Syringa oblata var. dilatata and S. meyeri ‘Palibin’ blo- ga vulgaris) have been used ethnobotanically to reduce omed from the mid May till mid June. The species are characte- fever and treat malaria, as a perfume and a tonic, and ristic of early morning diurnal pattern of blooming, with approx. in homeopathy [5]. of 60% of daily instalment of flowers opened before 9.00 (GMT The flowers are tiny, from the basic single, and + 2h). Both species studied had the corolla tube 2-fold deeper during the pollen shedding phase compared to bud stage (mean semi-double to double. The genus Syringa is divided = 14.9 mm ± 3.2 SD vs. 7.8 mm ± 2.8). No species effect was into two subgenera, and one of these Ligustrina L. has found for the size of anthers, for the mass of pollen produced flowers with corolla tube shorter than corolla lobs. The in anthers and for the pollen viability. A constant number of second subgenus Syringa L. has generally corolla tube 2 stamens in the flowers of Syringa species entailed the pollen longer then calyx [6]. The single flowers of Syringa yield was derivative mainly to the number of developed flowers. species are reported to be visited by hummingbirds, Therefore significant differences were noted for the pollen yield bees and butterflies [7]. In the former Soviet Union, between individual shrubs (mean 0.9 kg for S. meyeri ‘Palibin’, the S. vulgaris was mentioned as nectariferous [8]. In and 8.1 kg/ha for S. oblata var. dilatata ). Poland S. reticulata is regarded as melliferous plant The Syringa oblata var. dilatata and S. meyeri ‘Palibin’ [9,10] and is attractive for bees [7]. The pollen grains due to their attractive flowering period, and the abundance of of the Syringa type are noted in bee products [11,12]. blooming are suitable for different ornamental designs in urban In Poland different ornamental species are rec- areas. Unfortunately, despite the entomophilous flower traits, the insect visitors appeared sporadically. ognised as a source of nectar for insect visitors [13–15]. The species from the genus Syringa are very popular in different garden designs mainly in urban areas [6,16], Key words: Syringa oblata var. dilatata, S. meyeri ‘Palibin’, it means reasonable, when a native knowledge is not phenology, abundance of blooming, mass of pollen yet available, to fulfil the gape in the aspects of lilack’s blooming biology. INTRODUCTION The main objective of the study was to 1) exa- mine floral phenology and diurnal dynamics of flowe- The genus Syringa L., lilacs, includes about ring for two ornamental shrubs species Syringa oblata 30 species, of woody, multi-stemmed shrub plants in var. dilatata and S. meyeri ‘Palibin’ 2) estimate the the family Oleaceae [1]. The species are native to the quantity of pollen, and 3) to monitor the activity and mountain areas of south-eastern Europe and eastern spectrum of insect visitors.

MATERIALS AND METHODS ity of pollinators, between 8.00 and 20.00 h (GMT + 2.00 h). The daily pattern of insect visitation for the full Study sites and study species. The observations flowering period was recorded in 2006 and 2009 for the were conducted in long-term sequence studies in 2006, o o individual shrubs. 2009, 2013, in the Lublin area, Poland (51 16’ N, 22 Data analysis. Data are presented as means with 30’ E). The shrubs of Syringa oblata Lindl. var. dilatata SD. The standard analysis of variance was applied [21]. (Nakai) Rehd. and S. meyeri ‘Palibin’ Schn. were grown Post hoc comparison of means for the number of flow- at the arboretum section in the Botanical Garden Maria ers, the pollen production and viability was tested by Curie-Skłodowska University. The species are known as the Duncan t-test. The flower life-span and the corolla frost resistant, they are decorative both in blooming and length were compared using the independent samples t- autumn leaf colour change phases, and are recommend- test. The level of statistical significance for all analyses ed as ornamentals. The experimental individuals shrubs was at a = 0.05. All analyses were performed using Sta- were grown on a loess originated soil. Standard plant tistica 6.0 (StatSoft Poland, Krakow). protection treatments were applied, when necessary. Flowering observations. During the growing seasons detailed observations of flowering biology were RESULTS conducted. The onset and length of blooming period The detailed dates of seasonal phenology are was recorded. The observations of the diurnal model of shown in Table 1. During the study period, Syringa blooming were made in 2006 and 2009. Protocols de- oblata var. dilatata started to bloom insensibly ear- scribed by J a b ł o ń ski and Szklanowska [17] lier (2006), simultaneously (2009) or insensibly latter and Denisow [18] were applied. (2013) compared to S. meyeri ‘Palibin’. Generally, the The diurnal pattern of flowering was expressed flowering began in mid May and lasted till mid June. as the percentage of newly opened flowers in relation to The duration of flowering varied from 21–24 days (Sy- the total number of flowers opened during the day. The ringa oblata var. dilatata) and from 22–29 days (S. mey- development of flowers was noted in one-hour intervals, eri ‘Palibin’). The flowers opening noted was slightly between 8.00 and 20.00 h (GMT + 2h). To determine more intense for the S. meyeri ‘Palibin’ with approx. of flower life-span, the buds (n = 10 per each cultivar) were 60% of daily instalment of flowers have been peaking at randomly chosen on different individual shrubs. The 8.00 (Fig. 1). Most flowers of Syringa oblata var. dilata- buds were marked just before opening and their deve- ta were opened between 8.00–9.00 (GMT + 2h). In the lopment was observed. The flower life-span was defined following hours (10.00–18.00), ca. 1–10% of flowers as the period from bud-opening till the corolla withe- were opened in one hour intervals. ring. As the weather conditions were changeable during The species effect for the flower longevity was flowering periods the impact of air temperature on the found (t = 0.356, df = 37, p < 0.025). Irrespective of the flower longevity was assessed. weather conditions, a longer life-span was characteristic The average number of flowers produced per for a single flower of S. oblata var. dilatata (mean = 5.9 each individual shrub was established. The abundance ± 2.2 SD) than a single flower of S. meyeri ‘Palibin’ of blooming was determined on the basis of the number (mean = 4.5 ± 1.7 SD). The duration of floral longevity of flowers per inflorescence (n=30), the number of in- was also dependant on the air temperature (t = 0.156, df florescences per shoot (n=15), and the number of shoots = 37, p<0.041). per shrub. The considerable elongation of the corolla tube Pollen production was determined for the full was observed between the swollen bud phase and the blooming phase assayed using the standard method de- pollen presentation phase of the flower development. scribed in details by Denisow [19]. The fresh and dry Both species studied had the corolla tube 2-fold deeper mass of anthers with pollen was determined (ELCON during the pollen shedding phase compared to the swol- CL 65 dryer, at ca. 33oC), and then the pollen was rinsed len bud phase (mean = 14.9 mm ± 3.2 SD vs. 7.8 mm ± from anthers once with pure ether (1–2 ml) and then 2.8) (t = 0.456, df = 66, p < 0.032). 4–6 times with 70% ethanol (2–8 ml). Four replications The lilac flowers are arranged in compound pa- n = 100 anthers were collected every year. The mass of nicle. The single inflorescence of S. meyeri ‘Palibin’ produced pollen was calculated for 100 anthers, and per grouped more flowers (mean = 138.7) than S. oblata var. shrub. Pollen viability was tested in standard acetocar- dilatata (mean = 115.8) and the difference was statisti- mine slides. The secretion of nectar was checked, accord- cally significant (F1,68 = 29.22, p = 0.023). ing to J a b ł o ń ski [20] but not quantified in this study. New flowers were constantly developed on each Insect activity. Simultaneously to the blooming individual inflorescences and shrubs. The number of observations the pattern and intensity of insects visits flowers per shrub was species related (Table 1). Also were noted for three consecutive days at one-hour in- year-to-year variations were found for both species. tervals, at the time of the most intensive forage activ- The shrubs of S. oblata var. dilatata, developing 49,400

68 Bożena Denisow, Monika Strzałkowska-Abramek

Table 1 Flowering period, features of blooming and abundance of flowering in two Syringa species in the years 2006, 2009 and 2013, observed in SE Poland

Flower life-span Length of corolla (days) (mm) Number of flowers Number of flowers Flowering Species Year per inflorescence per shrub (thous.) period air temperature phase 10–15oC 20–25oC bud pollen shead min–max mean min–max mean

2006 13.05–2.06 5.1 4.2 7.9 15.3 61 – 167 110.6a 0.5 – 169.0 30.8

Syringa oblata 2009 9.05–1.06 7.2 5.4 8.3 16.1 54 – 214 142.6b 0.8 – 182.5 62.5

var. dilatata 2013 18.05–10.06 8.1 6.1 6.4 13.1 47 – 121 94.3a 0.7 – 153.8 54.9

mean 6.8 5.2 7.5 14.8 115.8A 49.4

2006 22.05–12.06 4.2 2.4 8.0 15.1 126 – 180 150.6b 1.1 – 10.8 4.2

Syringa meyeri 2009 12.05–9.06 6.4 4.1 9.1 15.8 134 – 199 163.6b 1.8 – 13.5 7.4

‚Palibin’ 2013 15.05–12.06 7.6 4.1 7.1 14.2 102 – 136 101.8a 1.0 – 12.5 6.4

mean 6.1 3.5 8.1 15.0 138.7B 6.0 Mean 6.5 4.4 7.8 14.9 127.3 27.7 Means in columns with the same letters are not significantly different at α = 0.05 (Duncan t-test)

Table 2 The fresh and dry mass of anthers, the mass of produced pollen, total pollen yield and pollen viability in two Syringa species in the years 2006, 2009 and 2013, observed in SE Poland

Mass of pollen per Dry mass of Viability Species Year 100 anthers 100 anthers (mg) inflorescence shrub (%) (mg) min–max mean (mg) (kg)

2006 29.2b 7.1–11.5 9.4b 20.8 5.8 89.4b

Syringa oblata 2009 32.1b 9.2–12.3 10.2b 29.1 12.8 82.3b

var. dilatata 2013 19.8a 4.8–7.7 5.1a 9.6 5.6 62.5a

mean 27.0A 8.2A 19.8 8.1 78.1A

2006 31.4b 7.8–11.2 9.0b 27.1 0.8 87.3b

Syringa meyeri 2009 26.9ab 8.2–12.8 8.7b 28.5 1.3 85.4b

‚Palibin’ 2013 23.4a 4.1–6.9 4.7a 9.6 0.6 52.4a

mean 27.2A 7.5A 21.7 0.9 75.0A Mean 27.1 7.9 20.8 4.5 76.6 Means in columns with the same letters are not significantly different at α = 0.05 (Duncan t-test)

DISCUSSION rise in the early morning or even at night. There are no adequate data about diurnal rhythm of Syringa spp. In the environmental conditions of south-eastern blooming found in the literature. Some authors insist Poland Syringa oblata var. dilatata and S. meyeri ‘Pali- on genetic determination or even phylogenetic con- bin’ bloomed from mid May till mid June. This is about straints of the trait [17,22]. However, the impact of en- one-three weeks later then an average blooming period vironmental factors on the diurnal pattern of blooming registered for western Poland [6]. The timing and dura- was found for different species [18,23,24]. In our study tion of a species’ flowering may be influenced by biotic no substantial difference for the pattern of diurnal se- and/or abiotic factors [22], and they indicate the discrep- quence of flower opening in Syringa spp. was revealed ancies in flowering between species, seasons and sites. between subsequent days or growing seasons, suggest- The diurnal pattern of blooming was similar for ing a very high degree of genetic influence. both species. Most flowers were opened in the morn- The flowers of Syringa species studied con- ing hours between (8.00–9.00 h), that indicates their forms to the general pattern of the family Oleaceae

[1]. The corolla forms a deep tube (10–17 mm). The mass of pollen offered by the anthers of Syringa oblata characteristic was described by Lipiń ski [7], who var. dilatata and S. meyeri ‘Palibin’ was similar but pointed out that the feature may limit the access of in- the value differed among years of study. J ę drzejuk sect visitors to floral reward. Flowers of the studied Sy- and Szlachetka [27] revealed the differentiation ringa species offered both nectar and pollen, although of pollen mother cells in anthers during bud breaking we quantified only pollen reward in this study. Differ- after winter dormancy in Syringa vulgaris. The air ent groups of insect visitors were observed on flowers, temperature drops during bud cracking in the studied including Apoidea bees, although their density was ex- Syringa species were noted in the year 2013, and re- tremely low (only 1–2 visitors per hour). We observed sulted in the decrease in both the mass of pollen pro- lepidopterans foraging on flowers of both Syringa spe- duced in anthers and the pollen viability. The noted cies early in the morning only. Szafer and Woj- dependence indicates that the microsporogenesis and tusiakowa [25] consider the lilacs among typical the pollen production in the studied Syringa species is lepidopterans pollinated species. The adult butterflies sensitive for external factors, i.e low temperatures. were able, using their long proboscis, to reach the nec- A constant number of 2 stamens in the flowers tar hidden at the base of deep corolla tube of lilacs ob- of Syringa species entail the pollen yield is derivative served. The short-tongue visitors occasionally foraged mainly to the number of developed flowers. There- for nectar, and only in mid-day hours. The flowering of fore significant differences were noted between pol- studied lilacs overlap with many other shrubs and trees len yield per shrub (0.9–8.1 kg/ha). The impact of the present in nearby surrounding. Some of them (e.g. Co- abundance of blooming for the total pollen yield was toneastr spp., Deutzia species) are regarded as very underlined by different authors [23,30]. good flow species [10], and in the selection between The average mass of pollen produced in the an- rewarding and nectar-less plants visiting insects could thers of studied lilacs was 7.5–8.2 mg per 100 anthers. avoid less attractive lilacs. The value is similar to obtained from anthers in Rosa The studied species produced numerous flow- multiflora (9.5 mg per 100 anthers), in Chaenomeles ers per inflorescence (94.3–163.6) and the number dif- sp. (3.6–11.5 mg) or in Aesculus hypocastanum (6.5– fered between species and among growing seasons. 10.6 mg per 100 anthers), but not in flowers [30–32]. Syringa species and cultivars are known of producing The dependence is clear comparing the androecium terminal panicles which differ in the number of flow- (2-stamens in Syringa vs. multi-stamens in Rosa or vs. ers [6]. The number of flowers developed per inflores- 5-9-stamens in Aesculus). cence is considered a genetic feature [22] and also is In conclusion, the Syringa oblata var. dilatata highly dependant on weather factors [17]. Studies of and S. meyeri ‘Palibin’ due to their attractive flowering trees grown in temperate climate showed that differen- period, and the abundance of blooming are suitable for tiation of flower organs continues through two growing different ornamental designs in urban areas. Unfortu- seasons [26]. In Syringa vulgaris the flower primordia nately, despite the entomophilous flower features, due differentiation and flower organ development starts in to very deep corolla tube, the insect visitors used the midsummer and lasts until autumn and is completed in floral reward offered sporadically. six to eight weeks during the spring following the year of initiation [27]. In our study both Syringa species de- Acknowledgements veloped the smallest number of flowers in 2013, when flowering followed the summer and autumn of 2012, Research was supported financially by the Mi- with the lack of precipitation (August/September c.a. nistry of Science and Higher Education of Poland as a 180–240 % lower than in long-term). This indicates part of statutory activities of the Department of Bota- the drought as limiting factor for the bud formation in ny, University of Life Sciences in Lublin. examined Syringa species and consequently for the abundance of blooming. Authors’ contributions In the flowers of studied Syringa species most The following declarations about authors’ con- anthers dehisced in mid-day hours. This is a trait com- tributions to the research have been made: designed mon in many plant species [19], and is derivative to the experiments: BD; performed the experiments: the mechanisms of anther dehiscence that is related to MSA; analyzed the experimental data: BD; wrote the daily cycles of declining the relative humidity and ris- paper: BD, MSA ing the air temperature that enhance evaporative water loss from the locular fluid and accelerate the structural changes in plant tissue that lead to dehiscence [28,29]. REFERENCES According to our knowledge, the study are the 1. H e y w o o d V H . Flowering plants of the world. London: first on the pollen production of Syringa species. The Croom Helm; 1985.

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© The Author(s) 2013 Published by Polish Botanical Society Characteristics of blooming and pollen in flowers of two Syringa species (f. Oleaceae) 71 produkowanego pyłku oraz żywotność pyłku nie różniły Krzewy Syringa oblata var. dilatata i S. meyeri się istotnie pomiędzy gatunkami. Stała liczba pręcików ‘Palibin’, ze względu na atrakcyjny termin kwitnienia (2) w kwiecie powoduje, że wydajność pyłkowa krze- oraz obfite kwitnienie nadają się do wykorzystania wów zależy głównie od liczby wytworzonych kwia- w założeniach miejskich. Niestety, kwiaty pomi- tów. Stąd notowano znaczne różnice w produktywności mo typowych cech entomofilnych są sporadycznie pyłku, średnio 0.9 kg/ha z krzewów S. meyeri ‘Palibin’, odwiedzane prze owady. oraz 8.1 kg/ha z krzewów S. oblata var. dilatata.

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