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J. APIC. SCI. Vol. 64 No. 1 2020J. APIC. SCI. Vol. 64 No. 1 2020
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FLOWERING, FORAGE VALUE, AND INSECT POLLINATION IN BORAGE
(BORAGO OFFICINALIS L.) CULTIVATED IN SE POLAND
Ernest Stawiarz
Anna Wróblewska
Marzena Masierowska*
Dagmara Sadowska
Abstract
The three-year study on borage was conducted in Lublin, SE Poland. The aims were to
investigate the owering pattern and abundance, and the attractiveness (in terms of
nectar and pollen production) for ower-visiting insects, mainly bees. Insect visitation
and the effect of pollinators on fruit set and seed set were assessed as well. Flowering
of borage started in the latter half of June and lasted eight weeks. The mean number of
owers · m-2 of the crop was 4570 per season. A borage ower produced on average 4.0
mg of nectar with a mean sugar concentration of 31.5%. The mean total sugar amount
secreted in nectar was 1.2 mg. The pollen amount · ower-1 was 1.1 mg. A borage plant
can supply insects with 1.1 g of nectar sugars and 1.1 g of pollen. The estimated nectar
sugar yield and pollen yield per 1 m2 of the crop were similar, i.e. 5.2 g. Bees accounted
for 73.0% of all insect visits to the borage owers. The presence of insect pollinators
increased the fruit set by 43.3% and seed set by 26.8%.
Keywords: bee pasture, owering pattern, nectar production, pollen production and mor-
phology
Department of Botany and Plant Physiology, University of Life Sciences in Lublin,
Poland
INTRODUCTION
Borage (
Borago ofcinalis
L.), Boraginaceae,
is an annual species native to the Mediterra-
nean region. It has been naturalized in Central,
Eastern, and Western Europe and North America
(Gupta & Singh, 2010; Pieszak, Mikołajczak, &
Manikowska, 2012). In Poland, borage is a rare
plant, cultivated mainly in home gardens but
sometimes treated as a weed (Szafer, Kulczyński,
& Pawłowski, 1988; Trzaskowska, 2013). It is not
grown in large areas of the country (Suchorska
& Osińska, 1997).
Borage has a rosette of basal leaves and a main
stem, 60-100 cm in height, which branches into
several axillary stems. Its actinomorphic owers
have ve sepals and the same number of petals
and stamens (Fig. 1a), and are gathered in
scorpioid cymose inorescences. The bases of
the petals and stamens are fused with white
throat scales, creating a reservoir for nectar.
The pistil has a four-loculed ovary (Fig. 1bc). At
the bud stage, the petals are pink, but later their
colour changes to intense blue. The stamens,
borne on short and attened laments, have
brown elongated anthers bent towards the
style, forming a characteristic cone (Fig. 1a).
Borage has been cultivated for centuries for
wide culinary and medicinal use (Pieszak,
Mikołajczak, & Manikowska, 2012). Its young
leaves and owers are used in salads, soups,
vegetable and meat dishes and drinks (Biscotti
& Pieroni, 2015). As a valuable medicinal plant
and herb (Gupta & Singh, 2010; Asadi-Samani et
al., 2014), it is mainly grown for borage seed oil,
the richest plant source of γ-linolenic acid (GLA).
Borage herb (
Boraginis
herba
) collected during
owering contains mucous compounds, tannins,
saponins, avonoids, phenolic acids, organic
acids, scopoletin, soluble silica and mineral salts
(Zemmouri et al., 2014). Due to the content of
biologically active components, borage is used
in the production of the dietary supplements
(Pieszak, Mikołajczak, & Manikowska, 2012).
*corresponding author: mlm25@up.lublin.pl
Received: 05 August 2019; accepted: 23 December 2019
DOI: 10.2478/JAS-2020-0005DOI: 10.2478/JAS-2020-0005
Original Article
J. APIC. SCI. VOL. 64 NO. 1 2020J. APIC. SCI. VOL. 64 NO. 1 2020
Stawiarz et AL.Stawiarz et AL.
2
Flowering, forage value and pollination in borage
In beekeeping literature, borage is described as a
nectariferous plant recommended for cultivation
near apiaries (Osborne, 1999). Its owers attract
a diversity of ower-visiting insects, including
Hymenoptera, Lepidoptera, and Diptera, but
they are foraged mostly by honey bees and
bumblebees (Hedtke, 1996; Davis, Mitchell, &
Junor, 1997; Osborne, 1999; Carreck & Williams,
2002; Carvell et al., 2006; Simmons, Sagili, &
Martens, 2013). Results of pollen analyses of
honeys (Ricciardelli D’Albore & Battaglini, 1971;
Sejo et al., 1994; Salonen et al., 2009; Aronne
et al., 2012; Kilic, Kutlu, & Ozdemir, 2016) and
pollen loads (Aronne et al., 2012; Salman &
Azzazy, 2013; Dimou et al., 2014) have shown
that honey bees are interested in collecting
both nectar and pollen from borage owers. In
the UK, borage crops are listed among principal
honey ows (Williams, Carreck, & Little, 1993).
It is in described as a source of varietal honeys
in Italy, Spain, the Netherlands, Finland, Norway,
and Sweden (Persano Oddo et al., 2004). Borage
honey is pale, runny and slow to granulate,
whereas pollen loads are beige (Hodges, 1984)
or creamy-white (Osborne, 1999). According to
Demianowicz (1961), unioral borage honey is
creamy-white. The attractiveness of borage
owers to bumblebees was conrmed by pollen
analysis of faeces and pollen loads of
Bombus
terrestris
(Teper, 2006; Carvell et al., 2006).
Despite the popularity of borage as a bee plant
in western and southern Europe, the data on
its forage value in the eastern part of the EU
are incomplete. For example, in Poland, some
studies of the melliferous value of borage were
conducted in the 1960s (Demianowicz et al.,
1960; Demianowicz, 1961; Maksymiuk, 1961),
and since then, no detailed studies on borage
as a forage source for insects have been carried
out. However, a steady increase in borage
honey production has been noted in Poland
(Semkiw et al., 2008). Thus, the main objectives
of the present study were to investigate (i) the
borage owering pattern and abundance in the
Fig. 1. Morphology and microstructure of a
Borago ofcinalis
ower. a. Front view of a ower. b. Four-
loculed ovary with a nectary ring below (arrow). c. Four-lobed nectary ring (SEM). d. Nectary epidermis with
a nectarostoma (SEM). Abbreviations: s - sepal, o - ovary, n - nectary lobe.
J. APIC. SCI. Vol. 64 No. 1 2020J. APIC. SCI. Vol. 64 No. 1 2020
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environmental conditions prevailing in SE Poland
and (ii) to evaluate its attractiveness (in terms
of nectar and pollen production) for ower-vis-
iting insects, mainly bees. Since borage is grown
as a seed crop, the insect visitation (iii) and the
effect of pollinators (iv) on fruit set and seed
set were assessed as well. Furthermore, mor-
phological features of borage pollen grains (v)
that are useful in palynological studies of bee
products were studied.
MATERIAL AND METHODS
Study site
The study was conducted in Lublin (51°16’N,
22°30’E), SE Poland between 2007 and 2009.
The study area is characterized by an average
annual air temperature of 8.3°C and average
annual precipitation of 550.6 mm.
Experimental plots sized 6 m x 3 m were es-
tablished on grey brown podsolic soil. The plots
were fertilised before sowing with Azofoska
(Inco S.A., Poland) fertiliser, with the 13:6:17 NPK
ratio plus S, Ca, and microelements. The seeds
were sown directly into the soil in the middle
of April. The spacing between rows was 60 cm.
After emergence, the seedlings were thinned to
obtain a ca. 40 cm distance between plants in
a row. The average density of the plants was
5 · m-2 plot.
Flowering pattern and abundance
During the period 2007-2009, the owering
onset and termination were recorded. In 2007,
the seasonal owering pattern was examined
as well. To this end, six plants were randomly
chosen and marked prior to the opening of
the rst owers. On the consecutive days of
blooming, the number of open owers on each
plant was counted until blooming terminated.
The daily owering patterns were observed on
the 16th and 17th July 2007 at the peak owering
of the species, and the number of newly opened
owers on 8 stems was recorded every two
hours from 8:00 to 20:00 (GMT + 2 hrs). Addi-
tionally, the total number of owers developed
per plant and per 1 m2 area was determined. The
ower life span was observed from the loose
bud stage until the petals were shed. These ob-
servations were performed on six owers each
ye a r.
Floral nectaries, nectar and pollen production
The distribution of nectaries in fresh owers
was investigated under an Olympus SZX12 ste-
reoscopic microscope (Tokyo, Japan). Next, the
nectaries were prepared for SEM. The ower
bases were xed in 2.5% glutaraldehyde in
phosphate buffer (pH 7.4; 0.1 M) at 4°C for
twelve hours. Then, the material was washed
in phosphate buffer and dehydrated in a graded
acetone series. Afterwards, plant material was
critical-point dried using liquid CO2, sputter-coat-
ed with gold and examined with TESCAN/VEGA
LMU SEM (TESCAN, Brno, Czech Republic) at an
accelerating voltage of 30 kV.
To quantify the 24-hr rate of nectar secretion,
the ower buds were isolated in the eld and
the accumulated nectar was collected (Corbet,
2003) using Jabłoński’ pipettes and weighed (in
mg). In total, fty-three nectar samples were
collected during this study. A single sample
contained nectar collected from ten owers.
The nectar sugar concentration (% wt/wt) was
measured with the RL-4 refractometer (PZO,
Warsaw Poland). Then, the nectar amount
and nectar sugar concentration were used to
calculate the total sugar amount (mg) secreted
in nectar · ower-1 (Jabłoński, 2002).
The pollen amount available to insects was
determined with the modied ether method
(Warakomska, 1972). Every year, twelve samples
were collected, each consisting of fty mature
stamens. The anthers were removed from
randomly chosen ower buds and placed on
previously tarred watch glasses. The samples
were then placed in an air dryer (SUP-65G Wamed,
Poland) at 30°C. After anthers dehiscence pollen
grains were washed from the them with pure
ether and subsequently with 70% ethanol. The
empty anthers were removed from the watch
glasses. Next, the pollen samples were dried
and weighed on a balance (WA 34 PRL T A14
MERA-KFM, Poland), which allowed the calcula-
tion of the mass of air-dried pollen. The results
were expressed in mg · ower-1.
Stawiarz et AL.Stawiarz et AL.
4
Flowering, forage value and pollination in borage
Moreover, both the total sugar amount secreted in
nectar and the pollen mass · plant-1 and m-2 of the
crop available to insects were estimated. To this
end, plant density · m-2 of a plot and data on the
average number of owers on a plant already
formed during a given growing season were
used. The pollen grains were mounted in glyc-
erol-gelatine on microscopic slides (n = 10). Each
slide was prepared from a mixture sample of
pollen collected from 120 owers. Pollen grains
dimensions were determined by the measuring
of the length of the polar and equatorial axes
using a NIKON ECLIPSE E 600 LM at a magnica-
tion of 40 x 15. At least fty pollen grains were
measured on each slide (Andrejev, 1926).
Insect visits and pollination
In 2007, the intensity of diurnal insect visits to
the borage owers was monitored. The number
of visits was counted for ve minutes, three
times every two hours, from 8:00 to 20:00 (GMT
+ 2 hrs). Counting was performed in four marked
areas; each sized 1 m2, established inside the
experimental plot. The procedure was repeated
three times during the full bloom of the species
in sunny and not windy weather. The observa-
tions revealed ve insect categories: honey bees,
bumblebees, non-
Apis
and non-
Bombus
bees,
ies (Diptera) and others (butteries, beetles
and thrips). The fruit set and seed set between
owers bagged to exclude insects (n = 399) and
those freely pollinated (n = 315) were compared
to determine the role of insects as pollinators of
borage crops. The pollination treatments were
conducted on eight randomly chosen plants. On
each plant, six stems with a similar number of
ower buds in the same developmental phase
were marked. Then, three stems were bagged in
tulle isolators (mesh size 1 mm) until owering
cessation, whereas the others stayed unbagged
for free pollination. After fruit ripening, the
percentage of fruit set in relation to the owers
open on the stems was determined. The seed set
was calculated as a percent of the number of
seeds harvested from a ower in comparison
to the maximum potential number per ower
(four seeds per ower). The eld pollination
experiment was performed in 2007.
Statistical analyses
All analyses were performed using STATISTICA
v.13 (StatSoft, Poland, Kraków). The total
number of owers · plant-1 and the total number
of owers · m-2 were tested using Kruskal-Wallis
non-parametric ANOVA and H-test. Differences
in the nectar amount, nectar sugar concentra-
tion, total sugar amount in the nectar and the
pollen amount between the years of the study
were compared using one-way ANOVAs. When
signicant differences were found, the ANOVAs
were followed by the HSD Tukey test at p = 0.05.
The Chi-square contingency test was applied for
the fruit set and the seed set.
RE SULTS
Flowering biology and abundance
In the climatic conditions of SE Poland, borage
blooming started sixty days after sowing in
the latter half of June and often lasted until
the latter half of August. The detailed dates
of the seasonal blooming periods are shown in
Table 1. The owering period on average lasted
eight weeks. The time of blooming differed
among the years of the study and depended on
the weather conditions. Generally, the thermal
conditions in all growing seasons were similar
and hot weather prevailed - the daily mean tem-
peratures of June, July and August exceeded
the multiyear mean values by approx. 1.3ºC.
However, the extremely dry weather during the
nal ten days of June 2007 (total precipitation
3.2 mm) accelerated the blooming process in the
plants by ten to eleven days, compared to 2008
and 2009.
During the rst week of owering, the owers
on the borage plants developed at a slow rate,
but the process intensied in the second week.
Peak owering was recorded in the third and
fourth week of blooming. In the fth week, the
number of open owers steadily decreased and
the termination of blooming started in the sixth
week (Fig. 2).
The observations of the daily owering pattern
(Fig. 3) showed that the greatest number of
owers opened before 8:00 and between 14:00
and 20:00. The lowest portion of newly opened
J. APIC. SCI. Vol. 64 No. 1 2020J. APIC. SCI. Vol. 64 No. 1 2020
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owers was noted during noon hours. During the
peak owering of the species, the daily number of
all open owers per plant exceeded thirty (Fig. 2).
The detailed data on the blooming abundance
of borage are shown in Tab. 1. The effect of
the growing season on the number of owers
formed per plant and per area unit was not sig-
nicant (H 2, 26 = 1.14, p = 0.57 and H 2, 26 = 0.67,
p = 0.71). The life span of a borage ower, on
average 22 hours, was similar in each year of
the study (H 2, 18 = 1.62, p = 0.45) (Tab. 1).
Nectaries and nectar production
Nectar in a borage ower is produced by an
irregular four-lobed nectary ring located at
the base of the ovary (Fig. 1bc). The nectary
is surrounded by thickened bases of laments.
Five apertures formed in the non-thickened part
of the lament base lead to the nectar, and the
throat scales in the corolla are located opposite
these holes. Nectar is released through necta-
rostomata in the nectary epidermis (Fig. 1d).
The nectar secretion begins at the loose bud
stage and lasts throughout the entire life of the
ower.
Fig. 2. Seasonal owering pattern of
Borago ofcinalis
plants in 2007. The bars represent mean values (n = 6).
Fig. 3. Daily pattern of opening
Borago ofcinalis
owers per stems (n = 8) recorded on the 16th and 17th June
2007. The bars represent mean values.
Stawiarz et AL.Stawiarz et AL.
6
Flowering, forage value and pollination in borage
The characteristics of nectar produced by
borage owers in consecutive growing seasons
are shown in Tab. 2. All the parameters, i.e.
nectar amount, nectar sugar concentration and
nectar sugar amount varied among the years
of the study (although not statistically; F 2, 50 =
0.21, p = 0.81; F 2, 45 = 2.68, p = 0.80, and F 2, 50 =
2.92, p = 0.06, respectively).
Nectar amount · ower-1 was on average 4.0
± 2.2 mg (n = 53). The nectar sugar concen-
tration was moderate but ranged widely from
10 to 66%. The mean sugar amount secreted
in nectar · ower-1 was 1.2 ± 0.5 mg (n = 53).
The estimated production of nectar sugars per
plant and per 1 m2 of the crop showed no year
effect (F 2, 23 = 1.22, p = 0.31 and F 2, 50 = 2.34,
p = 0.11, respectively). Throughout the growing
Table 1.
Flowering phenology and abundance of
Borago ofcinalis
L. in the years of study.
Mean values (± SD) are given, SD - standard deviation. The results for life span of the ower,
number of owers · plant-1 and number of owers · m-2 of plot do not signicantly differ between
years of study (p > 0.05).
Year Flowering time
(days)
Life span
of a ower
(hours)
Number of owers
plant-1 m-2 of plot
2007 20.06-07.08
(49)
21.3 ± 1.15
n = 6
1024 ± 628
n = 6
4866 ± 2981
n = 6
2008 17. 0 6 -14.08
(59)
20.6 ± 1.53
n = 6
999 ± 365
n = 10
4744 ± 1731
n = 10
2009 22.06-20.08
(60)
21.7 ± 2.08
n = 6
863 ± 332
n = 10
4100 ± 1578
n = 10
mean (56) 21. 2 ± 1. 0 0
n = 18
953 ± 414
n = 26
4570 ± 1968
n = 26
Table 2.
Nectar production parameters in
Borago ofcinalis
L. in the growing seasons 2007-2009. Mean
values (± SD) are given, SD - standard deviation. The results for all nectar parameters do not
signicantly differ among the years of the study (p > 0.05).
Year
Amount · ower-1 of: Sugar concentration
of nectar
(% wt/wt)
Amount of sugars secreted
in nectar:
nectar
(mg)
sugars
secreted in
nectar (mg)
plant-1 (g) m-2 of crop (g)
2007 4.3 ± 2.4
n = 20
0.9 ± 0.2
n = 20
26.7 ± 10.9
n = 20
1.0 ± 0.6
n = 6
4.5 ± 1.2
n = 20
2008 4.0 ± 2.2
n = 14
1.3 ± 0.6
n = 14
36.3 ± 18.8
n = 14
1.3 ± 0.5
n = 10
6.3 ± 3.0
n = 14
2009 3.8 ± 2.2
n = 19
1.3 ± 0.6
n = 19
33.8 ± 4.9
n = 19
1.1 ± 0.4
n = 10
5.1 ± 2.5
n = 19
mean 4.0 ± 2.2
n = 53
1.2 ± 0.5
n = 53
31.5 ± 13.1
n = 53
1.1 ± 0.5
n = 26
5.2 ± 2.3
n = 53
J. APIC. SCI. Vol. 64 No. 1 2020J. APIC. SCI. Vol. 64 No. 1 2020
7
season, on average 1.1 ± 0.5 g (n = 26) of sugars
could be collected by insects from one borage
plant. The estimated mean nectar sugar yield ·
m-2 of this crop was 5.21 ± 2.34 g (n = 53), i.e.,
52.1 kg · ha-1.
Pollen release and production
Borage owers are protandrous. Mature anthers
open towards the inside of a conical staminal
tube consisting of tightly packed anther heads
where pollen grains are released and accumu-
Fig. 5. Insect visits expressed as the percentage of total visits to
Borago ofcinalis
owers recorded in
2007 and diurnal visitors to owers.
Fig. 4. Micrographs of
Borago ofcinalis
pollen grains. a. Polar view, LM. b. Equatorial view, LM. c. Polar view,
SEM. d. Equatorial view, SEM.
Stawiarz et AL.Stawiarz et AL.
8
Flowering, forage value and pollination in borage
lated. When the anthers are empty, the style
extends and protrudes beyond the anthers,
while the stigma is getting receptive (Fig. 1a).
The amounts of pollen · ower-1 differed sig-
nicantly among the years of the study (F 2, 30
= 14.77, p = 0.00). The highest average value
of 1.3 ± 0.5 (n = 12) mg per ower was found
in 2007, whereas the values for the following
years of study were 15-23% lower (Tab. 3).
The estimated pollen amount · plant-1 showed
no effect of the year (F 2, 23 = 1.65, p = 0.22),
whereas the pollen amount · 1m-2 of the crop
differed signicantly among the years of the
study (F 2, 33 = 4.61, p = 0.02). During the growing
season, one borage plant provided 1.1 ± 0.5 g (n
= 52) of pollen, i.e. 5.21 ± 2.01 g (n= 36) · m-2 of
the crop.
Borage pollen grains are stephanocolporate (Fig.
4) with the average length of the polar axis (P)
of 33.5 mm (range 30.3-38.7 mm) and that of the
equatorial axis (E) of 34.0 mm (range 31.3-39.2
mm). The shape index (P/E) is 0.99.
Table 3.
Pollen production in
Borago ofcinalis
during growing seasons 2007-2009.
Mean values (± SD) are given, SD - standard deviation.
Year
Pollen amount:
ower-1 (mg) plant-1 (g) m-2 of crop (g)
2007 1.3a ± 0.5
n = 12
1.4 a ± 0.8
n = 6
6.4a ± 2.6
n = 12
2008 1.1b ± 0.2
n = 12
1.1a ± 0.4
n = 10
5.1a ± 1.2
n = 12
2009 1.0b ± 0.4
n = 12
0.9a ± 0.3
n = 20
4.2b ± 1.5
n = 12
mean 1.1 ± 0.4
n = 36
1.1 ± 0.5
n = 26
5.2 ± 2.0
n = 36
Means in columns with the same letters do not differ signicantly; the HSD Tukey test, p = 0.05
Fig. 6. Bees foraging on
Borago ofcinalis
owers. a. Honey bee gathering nectar. b. Bumblebee collecting
nectar and pollen with a visible corbicular pollen load (arrow).
J. APIC. SCI. Vol. 64 No. 1 2020J. APIC. SCI. Vol. 64 No. 1 2020
9
Insect visitation and pollination
Hymenopterans were the principal visitors to the
borage owers (Fig. 5). Their visits accounted
for 73% of all insect visits observed. Honey
bees dominated among them, but bumblebees
as well as non-
Apis
and non-
Bombus
bees
were similarly abundant (Fig. 5). The owers
were visited by a number of dipterans as well.
Bees collected both nectar and pollen from
the owers (Fig. 6). Microscopic analysis of
grey-beige corbicular pollen loads of honey
bees and bumblebees conrmed the presence
of numerous borage pollen grains (unpublished
data).
Insects foraged on the owers from early
morning to evening (Fig. 7). The most intense
visitation was observed between 10:00 and
14:00 when the majority of new owers were
open, providing nectar and pollen.
The presence of insects signicantly increased
both the fruit set and the seed set in borage
(χ2 test, df = 1, p < 0.00 in both cases). In freely
pollinated owers, the percent fruit set was
45.1% (n = 315) whereas it was 1.8% (n = 399)
when pollinators were excluded. The seed set
reached 27.9% (n=1596) in the freely pollinated
plants and only 1.1% (n = 1260) in inorescenc-
es bagged to prevent insect access.
DISCUSSION
In the conditions of SE Poland, borage is a long-
owering summer crop blooming from June to
late August, which coincides with the period of
the foraging activity of many bees. Borage can
bloom from April to October depending on the
sowing date and geographical location (Osborne,
1999; Decourtye, Mader, & Desneux, 2010;
Simmons, Sagili, & Martens, 2013). In Lublin,
the owering of the plants lasts eight weeks,
which is twice longer than it was reported for
the same region by Kołtowski (2006). In East
Europe, borage blooms even up to 11.5 weeks
(Głuchov, 1974). The long owering of borage
crops is an advantageous trait, useful for the
long seasonal cycle of bumble bee and honey
bee colonies (Osborne, 1999).
Borage is a mass-owering crop with a mean
of 4570 owers · m-2 developed during the
growing season. This abundance is similar to
that reported by Demianowicz et al. (1960) but
almost twofold lower than the data provided by
Maksymiuk (1961) - 7428 owers · m-2 of borage
crop. Our study shows that borage in SE Poland
was most attractive to the ower-visiting insects
in the second and third week of owering when
it reached the peak oral display.
Borage owers persist for twenty-two hours
on average and produce nectar during their
entire life. Nectar is secreted by a four-lobed
Fig. 7. Number of insect visits (mean and SD) to
Borago ofcinalis
crops throughout the day in the 2007
season (n = 252 records).
Stawiarz et AL.Stawiarz et AL.
10
Flowering, forage value and pollination in borage
nectary ring located at the base of the ovary
and released via nectarostomata. Similar locali-
zation and morphology of oral nectaries and
the mode of nectar release were found in the
other species from the Boraginaceae family, e.g.,
Symphytum ofcinale
(Stpiczyńska, 2003) and
Echium russicum
(Chwil & Weryszko-Chmielews-
ka, 2007)
.
Borage offers an ample nectar reward to insect
visitors. The nectar sugar amount · ower-1
(1.2 mg) was similar to that reported previously
(1.1 mg · ower-1) in Poland (Demianowicz et
al., 1960; Maksymiuk, 1961) and within ranges
(0.2-4.9 mg · ower-1) found in the US crops (Thom
et al., 2016 and references herein). Our results
show that one borage ower can provide more
nectar sugars than a single ower of winter
rape (0.95-1.07 mg) (Kołtowski, 2002) or white
mustard (0.25 mg) (Masierowska, 2003), which
are important honey crops grown in the environ-
mental conditions of SE Poland. The estimated
sugar yield of 52.1 kg · ha-1 also indicates that
borage is a good value crop in terms of nectar
production. However, this value is much lower
than the estimated sugar yield in winter rape -
90-120 kg · ha-1 or white mustard - 71.2 kg · ha-1,
mainly due to the less abundant owering of
borage plants.
Regardless of the year of the study, borage
nectar was moderately concentrated although
the values ranged from 10-66%. Previous
studies on borage nectar showed a signicant
variability of this trait from 19-77% (Demianow-
icz et al., 1960; Głuchov, 1974; Osborne, 1999).
Such nectar offers an energetic reward for such
various nectar-consumers as ies and short- and
long-tongued bees (Willmer, 2011). Indeed, both
hymenopterans and dipterans were important
visitors to borage owers in our eld study.
Borage owers provide pollen food for insects
as well. To our knowledge, the pollen output of
borage has not been investigated yet, and only
a few studies have given evidence that honey
bees and bumblebees actively collect borage
pollen (Osborne, 1999; Teper, 2006; Aronne
et al., 2012). As demonstrated by Ricciardelli
D’Albore (1998), the pollen harvest from borage
is small, which has been conrmed in our study
(1.1 mg · ower-1). The estimated pollen yield
per crop area unit (5.2 g · m-2, i.e., 52 kg · ha-1)
is comparable with the lowest pollen yield of
white mustard crops (53 kg · ha-1) (Masiero-
wska, 2012), a valuable pollen source for bees
in Poland. However, borage crops can improve
pollen ow and thus honey bee nutrition in late
summer, when a natural decline in the avail-
ability of pollen occurs. For example, the use
of borage as a supplemental source of pollen in
late summer cropping systems was proposed in
the UK (Carreck & Williams, 2002) and the USA
(Simmons, Sagili, & Martens, 2013).
The honey bees observed in the borage owers
primarily exploited the nectar and less readily
the pollen, which is in accordance with results
of the previous studies (Davis, Mitchell, &
Junor, 1997; Teper, 2006; Salonen et. al., 2009;
Simmons, Sagili, & Martens, 2013; Dimou et al.,
2014; Kilic, Kutlu, & Ozdemir, 2016). Bumblebees
and honey bees in minority formed grey-beige
corbicular pollen loads, in which the presence
of the borage pollen was conrmed.
Bombus
terrestris
and
B.
lucorum
, in particular, are
known to collect borage pollen (Osborne, 1999;
Teper, 2006; Carvell et al., 2006).
Wild and domesticated bees most frequently
visited borage owers in Lublin, with dominance
of honey bees. Our observations are in
agreement with studies conducted in southern
and western Europe (Hedtke, 1996; Carreck &
Williams, 2002; Carvell et al., 2006; Barbir et al.,
2015) and conrm the apiarian value of borage
crops in various geographical regions. Moreover,
a considerable number of dipterans were noted,
unlike in the study conducted by Barbir et al.
(2015), who demonstrated low attractiveness
of borage to hoveries (Diptera, Syrphidae).
Carreck and Williams (2002) reported low
diversity of dipterans in borage combined with
a moderate abundance of their visits (15%). In
general, the daily pattern of insect visitation to
borage owers can be linked to the daily pattern
of opening of new owers on the plant and thus
the availability of food resources.
Borage benets from the presence of insects
signicantly increasing both fruit set and seed
set. The plant species is considered self-com-
J. APIC. SCI. Vol. 64 No. 1 2020J. APIC. SCI. Vol. 64 No. 1 2020
11
patible but its owers are protandrous to avoid
self-pollination (Montaner, Floris, & Alvarez,
2000). Thus, a biotic pollen vector is necessary
to achieve full reproductive success. The need
for insects, in particular honey bees, for borage
pollination has been documented so far by Davis,
Mitchell and Junor (1997) and Goreno et al.
(2017), who both attributed the effectiveness
of pollination by honey bees to their highest
visitation frequencies. The pollination effective-
ness of different borage pollinators in Polish
conditions needs further more detailed studies.
In conclusion, our study has demonstrated that
borage in the environmental conditions of SE
Poland is a valuable nectar and pollen sources
during the summer period. Borage owers
produce abundant amounts of sugar in their
nectar and provide a great nectar resource
for pollinators from various taxonomic groups,
including honey bees. Moreover, borage can be
a supplemental pollen source and improve bee
nutrition in late summer. The forage value of
the borage crop is the highest in the second and
third weeks of owering when plants reach the
peak oral display.
Borage is strongly dependent on pollinators and
their presence decisively impacts seed yield. As
honey bees are predominant visitors to borage
owers, their presence should be promoted, in
particular, in seed crops. Finally, we recommend
a wider use of borage in the agricultural
landscape of Poland.
ACKNOWLEDGMENTS
This research was supported nancially by
the Ministry of Science and Higher Education
of Poland as part of statutory activities of the
Department of Botany and Plant Physiology
(project OKB/DS/1), University of Life Sciences
in Lublin.
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