Tilia L. - Journal of Apicultural Science

Vol. 54 No. 2 2010
Journal of Apicultural Science
99
THE PHENOLOGY OF FLOWERING AND POLLEN RELEASE
IN FOUR SPECIES OF LINDEN (Tilia L.)
Elżbieta Weryszko-Chmielewska, Dagmara Anna Sadowska
Department of Botany, University of Life Sciences in Lublin,
ul. Akademicka 15, 20-950 Lublin, Poland
e-mail: [email protected]
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 2005 - 2010 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; WitkowskaŻu k, 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;
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 43 000 pollen grains,
while one inflorescence 200 000 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 22-25°C.
Aerobiological monitoring was carried
out in Lublin in the period 2005-2010, 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
(Jäg er, 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
Vol. 54 No. 2 2010
Journal of Apicultural Science
101
Table 1
Flowering dates of four Tilia species in 2010, with the identification of phenological phases
Species of Tilia
Phenological
phase
T. platyphyllos
T. x europaea
T. cordata
T. tomentosa
1
07.06.2010
13.06.2010
16.06.2010
02.07.2010
2
09.06.2010
15.06.2010
22.06.2010
04.07.2010
3
15.06.2010
22.06.2010
26.06.2010
09.07.2010
4
18.06.2010
25.06.2010
28.06.2010
11.07.2010
5
22.06.2010
28.06.2010
01.07.2010
13.07.2010
6
23.06.2010
29.06.2010
02.07.2010
14.07.2010
Duration of
flowering (days)
16
16
16
12
1 - 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)
Table 2
Comparison of phenological phases of flowers of four linden species in the conditions
of Lublin in 2010
T. tomentosa
^
∩
10.00
O
O
12.00
O
O
O
18.00
O
O
O
O
3
10.00
O
O
O
O
4
10.00
O
O
O
O
O
O
∩
T. cordata
^
∩
T. x europaea
18.00
∩
T. platyphyllos
1
∩
Hours
∩
Phenological phases of Tilia flowers
Day
+
5
10.00
∩
6
10.00
+
∩
O
7
10.00
+
+
∩
2
+
Flower life span (days)
3.5
4.0
5.0
3.5
∩
∩
The designation of phenological phases of flower development according to Kr o t o s k a (1958):
^ - bud
- beginning of flowering (flower bud opening)
O - full bloom
- end of flowering (perianth wilting)
+ - seed setting
in the conditions of Lublin; T. cordata,
T. platyphyllos and T. x europaea. That
period is from 16 - 23 June.
2. Characteristics of the pollen seasons
Linden pollen grains are trizonocolporate
and average-sized. Depending on the view,
they are differently shaped (Phot. 5, 6).
Over the period of 6 years of study
(2005-2010), 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
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
Table 3
Characteristics of linden pollen seasons on the basis of aerobiological monitoring
in Lublin, in the period 2005-2010
Year
Investigated trait
Average
2005
2006
2007
2008
2009
2010
Start of season
19.06
23.06
08.06
14.06
14.06
07.06
14.06
End of season
17.07
26.07
21.07
17.07
22.07
19.07
20.07
Duration (days)
29
34
44
34
39
43
37
Max. concentration (number of grains/m )
14
97
82
46
50
31
53
Date of occurrence of max. concentration
04.07
01.07
19.06
29.06
02.07
26.06
28.06
3
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.
Vol. 54 No. 2 2010
Journal of Apicultural Science
Maximum linden pollen concentrations
(14-97 grains per 1m3) 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/m3) was recorded on 1 July 2006
(Fig. 3).
The chart showing the average linden
pollen content of the air in Lublin for the
period 2005-2010 (Fig. 4) demonstrates
that the largest amount of linden pollen was
in the air in the second and third decades
103
of June and in the first days of July. The
highest pollen concentrations also occurred
in this period.
Annual pollen counts per 1m3 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 2008-2010
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 2005-2009
104
Fig. 4. The average linden pollen content of the air in Lublin based on the study
conducted in the period 2005-2010
Fig. 5. Annual linden pollen counts (2005-2010) 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
Vol. 54 No. 2 2010
Journal of Apicultural Science
Photographs Captions:
Phot. 1. T. platyphyllos inflorescences at the full bloom stage
Phot. 2. T. cordata buds and full-blown flowers
Phot. 3-4. Bees visiting T. tomentosa flowers
Phot. 5-6. Linden pollen grains in different views (x700):
5 - polar view
6 - equatorial view
105
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 2005-2010,
then these dates are similar to the data
given by Lipiński (2010) for the period
1948-1980, Czubacki (1996) for the
period 1994-1995, and Jabłoński et al.
(2000) for the years 1995-1998. Only the
results reported by Demianowicz and
Hłyń (1960) for the period 1957-1958 (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 14-17 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 19481980.
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 1m3 in particular study
years varied significantly. The extreme
values occurred in the years 2005 and
2006. 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.
Vol. 54 No. 2 2010
Journal of Apicultural Science
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FENOLOGIA KWITNIENIA I PYLENIA
CZTERECH GATUNKÓW LIPY (Tilia L.)
Weryszko-Chmielewska E., Sadowska 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 2005-2010. 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.