Variation in Nectar Volume and Sugar Concentration of Allium ursinum L. ssp. ucrainicum in Three Habitats

Abstract

Floral nectar volume and concentration of ramson (Allium ursinum L. ssp. ucrainicum) were investigated in three different habitats, including two types of sessile oak-hornbeam association on brown forest soil with clay illuviation and a silver lime-flowering ash rock forest association on rendzina. Daily nectar production ranged from 0.1 to 3.8 μL per flower with sugar concentrations of 25 to 50%. Mean nectar volumes and concentrations showed significant differences between freely exposed flowers and covered flowers, which had been isolated from flower visitors 24 h prior to nectar studies. Both the amount and quality of nectar were affected by microclimatic conditions and soil properties and varied between populations at different habitats. In the silver lime-flowering ash rock-forest association mean nectar volumes and concentrations were lower than in a typical sessile oak-hornbeam association on three occasions, the difference being significant in two cases. During full bloom, the date of sampling did not have a profound effect on either nectar volume or concentration.

Full text

The Scientific World Journal
Volume 2012, Article ID 138579, 7pages
doi:10.1100/2012/138579
The cientificWorldJOURNA
L
Research Article
Variation in Nectar Volume and Sugar Concentration of
Allium ursinum
L. ssp.
ucrainicum
in Three Habitats
´
Agnes Farkas,1R´
eka Moln´
ar,1Tam ´
as Morschhauser,2and Istv´
an Hahn3
1Department of Pharmacognosy, Medical School, University of P´
ecs, R´
okus u. 2. 7624 P´
ecs, Hungary
2Department of Plant Systematics and Geobotany, Faculty of Natural Sciences, University of P´
ecs, Ifj´
us´
ag u. 6., 7624 P´
ecs, Hungary
3Department of Plant Taxonomy and Ecology, Lor´
and E¨
otv¨
os University, P´
azm´
any stny. 1., 1117 Budapest, Hungary
Correspondence should be addressed to ´
Agnes Farkas, agnes.farkas@aok.pte.hu
Received 28 October 2011; Accepted 22 December 2011
Academic Editor: Pekka Kaitaniemi
Copyright © 2012 ´
Agnes Farkas et al. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Floral nectar volume and concentration of ramson (Allium ursinum L. ssp. ucrainicum) were investigated in three different habitats,
including two types of sessile oak-hornbeam association on brown forest soil with clay illuviation and a silver lime-flowering ash
rock forest association on rendzina. Daily nectar production ranged from 0.1 to 3.8µL per flower with sugar concentrations of
25 to 50%. Mean nectar volumes and concentrations showed significant differences between freely exposed flowers and covered
flowers, which had been isolated from flower visitors 24h prior to nectar studies. Both the amount and quality of nectar were
affected by microclimatic conditions and soil properties and varied between populations at different habitats. In the silver lime-
flowering ash rock-forest association mean nectar volumes and concentrations were lower than in a typical sessile oak-hornbeam
association on three occasions, the difference being significant in two cases. During full bloom, the date of sampling did not have
a profound effect on either nectar volume or concentration.
1. Introduction
Allium ursinum L. (ramson or wild garlic) is a perennial
plant, widely distributed in Europe, occurring in various
deciduous woodlands, preferring damp shadow places,
meso- and eutrophic, neutral to moderately acid soils of the
hilly and the mountainous vegetation belt [1]. In Hungary,
the largest populations can be found in Bakony and Mecsek
hills, in the form of a continuous underwood layer in horn-
beam-oak and beech forests [2,3]. The flower stalk of ssp.
ursinum is densely papillated and rough as opposed to the
smooth pedicels of ssp. ucrainicum that lack papillae. The
European distribution of ssp. ursinum is confined to the
western and southern parts, being a subatlantic-submedi-
terranean flora element, while ssp. ucrainicum is distributed
in East Europe, with a western pontic-western sarmatic
character [3]. The populations selected for the purposes of
the present study belong to ssp. ucrainicum.
Besides being consumed fresh or cooked, ramson is a
popular medicinal plant, lowering blood pressure, being ef-
fective against arteriosclerosis, diarrhea, and indigestion [4].
The plant is valued by bee keepers, as well, since ramson
flowers can serve as pollen and nectar sources for honeybees,
completing the spring bee pasture [5]. Ramson blooming
starts in the second half of April and finishes in the first
half of May. The umbel-like inflorescence comprises 8–12
trimeric flowers, with a septal nectary between the base of
the ovary and the stamens of the inner circle, characteristic
for the Alliaceae family [6–9].
In the genus Allium, nectar secretion starts at the time
of anthesis and ceases parallel with the wilting of the tepals,
stamens, and style [10]. Allium species tend to secrete highly
concentrated nectar: Akopyan [11] measured 70–75% sugar
concentration in the nectar of A. cepa, while Hagler et al. [12]
reported 52–65% for the same species. Kumar and Kumar
Gupta [13] found similarly high concentrations in vegetable
alliums, measuring 52.8–82.6% and 42.0–72.8% nectar sugar
content in A. cepa and A. fistulosum,respectively.The24h
sugar value in the latter two species varied between 0.219 and
0.767 mg/flower.
According to Silva et al. [14] nectar sugar concentration
in A. cepa did not change significantly throughout the day,

2The Scientific World Journal
while mid- to late-morning and late evening peaks were ob-
served in nectar volume. Rate of nectar secretion was influ-
enced by both floral age and environmental factors, from
which relative humidity was the most important, being sig-
nificantly and inversely related to nectar production. Simi-
larly, environmental factors were found to affect the nectar
production of ramson, ranging from 0.16 to 0.42 mg
nectar/flower/day, with an average of 52.13% sugar content
[5]. In this study, sugar value was 0.14–0.25 mg in sunny
weather, but remained below 0.1 mg in changeable, cool
weather.
Although the rewards offered by A. ursinum flowers can
play an important role in the strengthening of bee colonies
before the bloom of black locust (Robinia pseudoacacia L.),
which is a major bee pasture in several countries, to date
little is known about the nectar secretion process and nectar
composition of ramson. Investigating the nectar traits of
wild garlic can provide valuable information for beekeepers
as well as for consumers of the honey derived from the
floral nectar of A. ursinum. Although some data are available
regarding the effect of environmental factors such as relative
humidity and air temperature on nectar production in the
Allium genus, the impact of different habitats on the nectar
producing capacity of wild populations has largely been
neglected. Therefore, the present study aims at demonstrat-
ing variation in nectar volume and sugar concentration in
various populations of A. ursinum and at determining the
possibleroleofhabitatdifferences in this variation.
2. Materials and Methods
2.1. Location and Time of Studies. Field studies were done
at three different locations in the Mecsek hills (South
Transdanubia, Hungary) in the springs of 2007, 2008, and
2010. The selected sampling sites included two of the most
dominant wood types and an edaphic one (for details see
Tabl e s 1and 2).
2.2. 24-Hour Nectar Production Studies. Nectar was extracted
with glass capillaries from 30 to 50 pollen-shedding flowers
each day, at the time of peak nectar secretion, which was
found to occur either at 9 hr or 17 hr in our pilot study. Each
sampled flower represented a separate individual. In certain
experimental designs the flowers have previously been
isolated with a tulle net in order to exclude visiting insects
(covered flowers). The volume of nectar produced in the
preceding 24 hours was determined directly upon sampling
the flowers with calibrated 5 µL micro pipettes (DURAN), by
reading the length of the nectar column within the capillary.
The refractive index—corresponding to the concentration
of nectar—was measured immediately with hand refrac-
tometers (ATAGO N-50E and OG 101/A). Since sucrose
refractometers are calibrated directly in g sucrose per 100 g
solution (% Brix) and the presence of hexose sugars scarcely
affects the relationship between solute concentration and
refractometer reading [15], the refractive index was directly
used for characterizing the concentration of nectar.
In addition, at site 3, repeated nectar sampling was
performed from previously covered, pollen-shedding flowers
on 5 consecutive days (15–19 April, 2007). All 5 study days
fell within the main bloom of ramson. Each day, 25 to 30
flowers were sampled. Each flower was sampled only once
during this period, that is, nectar was measured in different
flowers on different days.
2.3. Statistical Analysis. Means of data measured in cov-
ered/uncovered flowers, at different sites and on different
days were compared with either two-sample t-test or ANOVA
with Tukey’s multiple comparisons test. Homogeneity of
variances was tested with F-test or Bartlett’s test. If the
variances differed significantly, Welch test was applied. The
normality of data series was checked by using Kolmogorov-
Smirnov test. If the normality assumption was violated,
either Mann-Whitney test or Kruskal-Wallis test with Dunn’s
multiple comparisons post test was applied. For statistical
evaluation of the results, the software GraphPad InStat (re-
lease 3.0.5) was used.
3. Results
3.1. The Effect of Flower Isolation on Nectar Volume and
Concentration. Ramson flowers produced low to medium
volumes (extreme values: 0.1–3.8 µL/flower) of highly con-
centrated (extreme values: 25–55%) nectar at all three
sampling sites on all occasions, with sugar values varying
between 0.17 and 0.69 mg/flower in the three years of our
study. The 24h sugar values were within the range (0.219 to
0.767 mg/flower) calculated for the flowers of A. cepa and A.
fistulosum [13], but were higher than the values determined
in a previous study on A. ursinum (0.14–0.25 mg) [5].
The effect of 24-hour isolation of flowers preceding nec-
tar measurements was investigated at site 3 on two different
occasions (covered versus uncovered flowers in Tab l e 2 ). In
both cases, mean nectar volumes in covered flowers were
significantly higher than in uncovered flowers (Tab le 3).
Similarly, mean nectar concentration values of covered flow-
ers exceeded those of freely exposed flowers in both years,
but in 2010 the difference was not statistically significant
(Tabl e 4 ). The above results were taken into account in
further evaluation of data, that is, data from covered and
uncovered flowers were not pooled, and comparisons be-
tween various sites or dates were done either for covered
flowers or freely exposed flowers.
3.2. Effect of the Habitat on Nectar Volume and Concentration.
In order to analyze the effect of the habitat on nectar
volume and concentration,ramson flowers that had not
been previously isolated were sampled on three occasions.
On April 27 mean nectar volumes differed significantly in
2007, but in 2008 we did not find any statistically relevant
differences between the three study sites (Tab l e 5 ). On 9 May,
2008 there was a significant difference in the mean nectar
volumes of site 1 and site 2, and mean values at site 3 differed
from those at the other two sites. Mean nectar volumes at site
2 were lower than at site 1 on all three days of investigation,
the difference being significant in two cases.
Similarly to the amount of nectar, its mean concentration
also showed significant differences at the three different

The Scientific World Journal 3
Tab le 1: Characteristics of the sampled forest stands.
Stand ID
Location; latitude (◦);
longitude (◦);
elevation (m); aspect;
slope (◦)
Bedrock; soil type;
soil pH (H2O; KCl)
H: humus content
Plant association; status;
dominant species in canopy layer
(c); shrub layer (s); herb layer (h)
Site description
Status of Allium
ursinum ssp.
ucrainicum
Site 1
Orf˝
uvalley
West-Mecsek hills
N46
◦07.041;E
18◦10.825; 370 m;
NE; 26◦
Loess; brown forest
soil with clay
illuviation (luvisol);
pH: 4.97; 4.05; H:
5.54%
Sessile oak-hornbeam
association: Asperulo
taurinae-Carpinetum So ´
oet
Borhidi in So ´
o, 1962; zonal; c:
Carpinus betulus,Fagus sylvatica,
Quercus dalechampii;s:scarce;h:
Allium ursinum ssp. ucrainicum
The middle of a
typical occurrence of
sessile oak-hornbeam
forest.
Optimal, cool and
humid; dominant
Site 2
Tubes hill
Mid-Mecsek hills;
N46
◦06.652;E
18◦11.899; 535 m;
S-SW; 26◦
Limestone; rendzina
soil (leptosol); pH:
6.37; 5.91; H: 6.93%
Silver lime-flowering ash rock
forest association: Aconito
anthorae-Fraxinetum orni
(Borhidi-Kevey 1996); edaphic;
c: Tilia argentea,Quercus cerris,
Q. pubescens and Q. virgiliana,
Fraxinus ornus s: Cornus mas h:
Allium ursinum ssp. ucrainicum
Close to the border of
the calciphilous oak
association
(Tamo-Quercetum
virgilianae).
Not optimal, warm
and dry; dominant
Site 3
´
Arp´
ad peak
East-Mecsek hills
N46
◦08.511;E
18◦15.386; 410 m;
NE; 8◦
Loess; brown forest
soil with clay
illuviation
(luvisol);pH: 4.44;
3.51;H: 2.29%
Sessile oak-hornbeam
association: Asperulo
taurinae-Carpinetum So ´
oet
Borhidi in So ´
o 1962; zonal; c:
Quercus dalechampii, Carpinus
betulus;s:sparse,Crataegus
oxyacantha, h: Melica uniflora,
Allium ursinum ssp. ucrainicum
Next to the border of
Turkey oak wood.
This habitat is
receiving relatively
more irradiation from
the direction of the
Turkey oak wood.
Not optimal, less
humid, more acidic;
mosaic appearance
Tab le 2: Sampling dates and sites, with bloom stage. C: covered flowers; UC: uncovered flowers.
Year Date Bloom stage Site 1
Orf˝
uvalley
Site 2
Tubes hill
Site 3
´
Arp´
ad peak
2007
April 14 Full UC UC
April 15 Full C
April 16 Full C
April 17 Full C
April 18 Full C C
April 19 Full C
April 26 End C UC C
April 27 End UC UC
April 28 End C
2008
April 25 Full UC
April 27 Full UC UC C and UC
April 29 Full UC C
May 9 End UC UC UC
2010 May 4 End C and UC
habitats on both April 27, 2007 and May 9, 2008, but no
such differences were found on April 27, 2008. Mean nectar
concentrations were lower at site 2 on all three sampling dates
compared to those measured at site 1—the difference being
significant in two out of three cases (Table 6 ).
3.3. Effect of the Sampling Dates on Nectar Production. In
2007, previously isolated flowers were sampled on five con-
secutive days during full bloom at site 3. Neither nectar
volume (Figure 1) nor concentration (Figure 2) changed sig-
nificantly during this period.
4. Discussion
According to our previous studies, the nectar producing pe-
riod lasts for 4 days in individual ramson flowers, with peak
production on the 2nd day of anthesis [16]. This was in
contrast with the study of Zimmermann and Pyke [17],

4The Scientific World Journal
Tab le 3: The effect of flower isolation on nectar volume at site 3.
April 27, 2008 May 4, 2010
nmean (µL) std nmean (µL) std
Covered 50 1.656∗0.930 32 0.637∗0.525
Uncovered 50 1.318∗0.677 32 0.172∗0.117
Method Welch-test, P=0.0415 Mann-Whitney test, P<0.0001
Abbreviations: n: sample size; std: standard deviation; ∗indicates significant difference between covered and uncovered samples.
Tab le 4: The effect of flower isolation on nectar concentration at site 3.
April 27, 2008 May 4, 2010
nmean (%) std nmean (%) std
Covered 50 38.340∗4.556 32 33.250 6.754
Uncovered 49 35 .898∗4.793 23 31.130 2.668
Method t-test, P=0.0108 Welch test, P=0.1149
Abbreviations: n: sample size; std: standard deviation; ∗indicates significant difference between covered and uncovered samples.
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
1.8
2
14 15 16 17 18 19 20
Days in April
Changes of nectar volume between 15 and 19 April, 2007
Nectar volume (µl)
Figure 1: Nectar volume (mean and standard deviation) in covered
ramson flowers at site 3, on five consecutive days of full bloom in
April 2007.
who found that individual flowers of another mass-flowering
species, Polemonium foliosissimum, produce equivalent nec-
tar volumes every day of their lives within a single blooming
season. Although the intensity of nectar production in A.
ursinum flowers was expected to vary also at the popula-
tion level on different days of full bloom, no significant
differences were found either in volumes or concentrations
of nectar on five consecutive days during full bloom. This
might be explained by the different approach applied in
the two studies: our previous investigation [16] monitored
nectar secretion from the bud stage until flower senescence,
sampling the same flowers on each consecutive day; whereas
in the present study all flowers were at the stage of anthesis,
and they were sampled on a single occasion.
Standing crop, that is, the quantity of nectar found in
freely exposed flowers at a given time [15] tends to be lower
than nectar volumes measured in isolated flowers, as demon-
strated by several studies (e.g., [18]). The significantly higher
nectar volumes of covered versus uncovered ramson flowers
might be explained by the foraging activity of pollinators
from freely exposed flowers. Various bees, including Apis
20
25
30
35
40
45
50
14 15 16 17 18 19 20
Nectar refraction (%)
Days in April
Changes of nectar refraction between 15 and 19 April, 2007
Figure 2: Nectar concentration (mean and standard deviation) in
covered ramson flowers at site 3, on five consecutive days of full
bloom in April 2007.
mellifera L., A. cerana F., A. dorsata F., A. florea F. and
Trigona iridipennis Smith, and flies like Musca domestica L.,
Calliphora vicina Robineau-Desvoidy, Episyrphus balteatus
De Geer, Eristalinus aeneus Scopoli, and Eupeodes sp. have
been reported as frequent visitors of Allium species [19–23].
In our field studies, the most important visitors of wild garlic
flowers were honeybees and ants. The highly concentrated
nectar reported for various Allium species [10–13]canmake
it difficult for honeybees to collect the secretion product. In
our experience, ramson flowers might also produce nectar
with concentration values exceeding 50%; however, the
average values are in the range of 25 to 40%, which is suitable
for honeybees, allowing even the production of unifloral wild
garlic honey. Besides foragers, the slightly changed microcli-
mate due to the coverage of inflorescences, which results in
higher temperature and humidity, can contribute to differen-
ces in nectar production between covered and freely exposed
flowers.
Differences in microclimate can also lead to variation ob-
served between populations at different habitats. The rather
diluted nectar in covered flowers at site 1 can be explained by

The Scientific World Journal 5
Tab le 5: The effect of habitat on nectar volume.
27 April 2007, end of bloom 27 April 2008, full bloom 9 May 2008, end of bloom
nmean (µL) std nmean (µL) std nmean (µL) std
Site 1 33 1.339∗0.549 50 1.516 0.807 50 1.162∗0.549
Site 2 31 0.936∗0.526 50 1.422 0.772 50 0.732∗0.568
Site 3 49 1.318 0.677 50 0.104∗0.185
method t-test, P=0.0039 ANOVA, P=0.4298 Kruskal-Wallis test, P<0.0001
Abbreviations: n=sample size, std =standard deviation; ∗indicates significant differences between sites.
Tab le 6: The effect of habitat on nectar concentration.
April 27, 2007, end of bloom April 27, 2008, full bloom May 9, 2008, end of bloom
nmean (%) std nmean (%) std nmean (%) std
Site 1 33 36.182∗3.860 50 37.280 4.895 50 44.040∗4.247
Site 2 31 32.516∗3.548 50 35.640 4.129 50 40.080∗4.597
Site 3 49 35.898 0.685 14 32.429∗3.005
Method t-test, P=0.0002 ANOVA, P=0.1655 ANOVA, P<0.001
Abbreviations: n: sample size; std: standard deviation; ∗indicates significant differences between sites.
the more humid microclimate in the closed oak-hornbeam
association mixed with beech. The drier microclimate at the
border of the sessile oak-hornbeam and sessile oak-Turkey
oak woods in site 3 may stand in the background of large
amounts of concentrated nectar even in isolated flowers. In-
terpopulational differences in nectar production were found
in other plant species, as well: for example, in Impatiens
capensis the variation in nectar volume was not significant
among plants, but was nearly significant among populations
[24]. Microclimatic conditions were found to influence
nectar production in other melliferous plants like Ajuga
reptans,Lamium maculatum,Lamiastrum galeobdolon, and
Ocimum basilicum [25,26]. For the latter species, physico-
chemical soil properties were also found to be decisive: from
the three investigated soil types, the highest intensity in
nectar secretion was recorded on eutric cambisol, and daily
nectar peaks were measured at various times depending on
soil type: at 8 am on eutric cambisol, and at 10 am on fluvisol
and humoglay [26].
In our study, the humus content of the investigated soil
types can be considered as good on luvisol (site 1 and 3)
and excellent on leptosol (site 2, see Tab l e 1 ), in accordance
with the meso- and eutrophic soils preferred by ramson [1].
Ramson is known to prefer moderately acid soils, with the
pH (H2O) ranging from 5.5 to 7.9 [27]orevenfrom6.0to
7.5 [28], which corresponds to the values measured at site 2
(pH H2O 6.4). On the other hand, the pH values measured
at the other two study sites fell below the optimal level. The
relatively low pH values at site 3 may be responsible for the
scattered appearance of ramson at this habitat, as opposed
to the continuous coverage of ramson at the other two sites.
The production of new roots was found to be inhibited by the
even lower pH 3.6 in an experiment of Falkengren-Grerup
and Tyler [29]. Low pH combined with high aluminium
concentration has been reported to suppress root extension
and biomass production [30].
Plants with different life histories and reproductive strat-
egies (e.g., annuals versus perennials) may react differently
to the availability of resources. Burkle and Irwin [31]
demonstrated that nutrient addition increased aboveground
biomass and flower production as well as nectar production
in the monocarpic perennial Ipomopsis aggregata in the year
of treatment; whereas in the perennial Linum lewisii repro-
ductive output was not influenced by fertilization in the first
year, but delayed effects were seen in the next year. The nectar
secretion rate of Vaccinium macrocarpon was unaffected
by fertilizer application [32]. Species-specific responses of
nectar traits to variation in soil nitrogen availability were
observed also by Baude et al. [33], who found that litter
amendment to the soil led to an increase in total nectar
sugar content in Lamium amplexicaule, but not in two other
temperate grassland species, Mimulus guttatus and Medicago
sativa. Besides sugar content, amino acid levels of the nectar
can also be affected by soil conditions. Total amino acid
concentrations varied significantly at both the plant and
population level in Impatiens capensis [24]. In Agrostemma
githago, total amino acid concentrations increased signifi-
cantly with increasing fertilizer treatment [34].
A. ursinum applies Clan-of-Clone strategy which can be
characterized among other things with relatively small al-
location to vegetative reproduction, which prolongs local
persistence [35]. Despite being a clonal plant, sexual repro-
duction is prevalent over clonal reproduction in the majority
of natural populations [27,28,36]. Accordingly, A. ursinum
can be characterized with extraordinarily high values of
reproductive allocation, compared both to other woodland
perennials and related species of the Liliales [37]. In a habitat
that cannot provide enough nutrients during the time of
flowering, the plant is not able to invest sufficiently into
nectar production. This was demonstrated by our measure-
ments as well. From the three study sites, Tubes (site 2) was
the driest and warmest habitat, whose rendzina soil was char-
acterized by the highest humus content and pH values. The
high humus content can be advantageous if there is enough
precipitation in spring—typically in April, at full bloom of
ramson—since in this case nutrients are available in high

6The Scientific World Journal
amounts. Furthermore, rendzina soil is welldrained, which
is important for ramson. Later on—typically in May, at
the end of bloom—when there is less or no rain, the thin
rendzina soil becomes warmer and drier, therefore humus
decomposition is hindered and nutrients cannot be properly
absorbed by ramson. This may account for the fact that
nectar production was twice as high in April 2008 compared
to May 2008 at site 2, as opposed to the less pronounced
decrease in nectar production during the same period at site
1(Tabl e 5 ), characterized by a more humid microclimate and
medium humus content. At site 3 the humus layer is rather
shallow, and as ramson plants develop, the deeper pene-
trating roots reach a nutrient-poor soil layer, where lower
levels of potassium, phosphorous, and nitrate-nitrogen can
be measured [36]. The poorly drained soil with higher pro-
portion of clay and the lack of sufficient nutrients may
explain lower vigour of plants and consequently lower nectar
sugar production.
5. Conclusion
Our study demonstrated that floral nectar volume and con-
centration varies in different populations of A. ursinum,
which can be largely attributed to the varying conditions
provided by different habitats. Populations in the sessile oak-
hornbeam association, which is the typical habitat of ramson
and provides sufficient nutrient levels for nectar secretion,
produced higher volumes of nectar with higher nectar sugar
concentrations, compared with the population in the silver
lime-flowering ash rock forest, where A. ursinum cannot find
its optimal living conditions.
Acknowledgment
The project was funded by the Grant no. F 48815 from the
Hungarian Scientific Research Fund (OTKA).
References
[1] J.A Kov´
acs, “Data to the vegetation biology and coenological
relations of Allium ursinum L. stands in eastern Transylvania,”
Kani tzia, vol. 15, pp. 63–76, 2007.
[2] B. Kevey, Az Allium ursinum n¨
ov´
enyf¨
oldrajzi jellemz´
ese, k¨
ul¨
on¨
os
tekintettel a magyarorsz´
agi el˝
ofordul´
asi viszonyaira,Ph.D.the-
sis, Lajos Kossuth University of Debrecen, Debrecen, Hungary,
1977.
[3] B. Kevey, “Az Allium ursinum L. magyarorsz´
agi elterjed´
ese,”
Botanikai K¨
ozlem´
enyek, vol. 65, no. 3, pp. 165–175, 1979.
[4] L. Gy. Szab´
o and J. Per´
edi, “A medvehagyma (Allium
ursinum L.) botanikai ´
es fitok´
emiai jellemz´
ese, felhaszn´
al´
asi
lehet˝
os´
egei,” Olaj, szappan, kozmetika, vol. 48, no. 2, pp. 60–
63, 1999.
[5] J. P´
eter, “N´
eh´
any n¨
ov´
eny nekt´
artermel´
es´
er˝
ol,” M´
eh´
eszet, vol.
23, no. 7, p. 124, 1975.
[6] E. Daumann, “Das Bl¨
utennektarium der Monocotyledonen
unter besonderer Ber¨
ucksichtigung seiner systematischen und
phylogenetischen Bedeutung,” Feddes Reper, vol. 80, pp. 463–
590, 1970.
[7] K. Rahn, “Alliaceae,” in The Families and Genera of Vascular
Plants. III. Flowering Plants, Monocotyledons, Lilianae (except
Orchidaceae), K. Kubitzki, Ed., pp. 70–78, Springer, Berlin,
Germany, 1998.
[8]P.J.Rudall,R.M.Bateman,M.F.Fay,andA.Eastman,
“Floral anatomy and systematics of Alliaceae with particular
reference to Gilliesia, a presumed insect mimic with strongly
zygomorphic flowers,” American Journal of Botany, vol. 89, no.
12, pp. 1867–1883, 2002.
[9] H. ˚
Astr¨
omandC.A.Hæggstr
¨
om, “Generative reproduction
in Allium oleraceum (Alliaceae),” Annales Botanici Fennici, vol.
41, no. 1, pp. 1–14, 2004.
[10] J. L. Brewster, Onions and Other Vegetable Alliums, CAB Inter-
national, Wallingford, UK, 1994.
[11] G. A. Akopyan, “Pollination of onion seed plants,” Biologich-
eskii Zhurnal Armenii, vol. 30, no. 7, pp. 88–89, 1977.
[12] J.R.Hagler,A.C.Cohen,andG.M.Loper,“Productionand
composition of onion nectar and honeybee (Hymenoptera:
Apidae) foraging activity in Arizona,” Environmental Entomol-
ogy, vol. 19, no. 2, pp. 327–331, 1990.
[13] J. Kumar and J. Kumar Gupta, “Nectar sugar production
and honeybee foraging activity in 3 species of onion (Allium
species),” Apidologie, vol. 24, no. 4, pp. 391–396, 1993.
[14] E. M. Silva, B. B. Dean, and L. Hiller, “Patterns of floral
nectar production of onion (Allium cepa L.) and the effects
of environmental conditions,” Journal of the American Society
for Horticultural Science, vol. 129, no. 3, pp. 299–302, 2004.
[15] S. A. Corbet, “Nectar sugar content: Estimating standing crop
and secretion rate in the field,” Apidologie, vol. 34, no. 1, pp.
1–10, 2003.
[16] R. Moln´
ar and ´
A. Farkas, “ ´
Ujabb adatok a medvehagyma
nekt´
artermel´
es´
er˝
ol,” M´
eh´
eszet, vol. 56, no. 2, pp. 6–7, 2008.
[17] M. Zimmermann and G. H. Pyke, “Reproduction in Polemo-
nium: patterns and implications of floral nectar production
and standing crops,” American Journal of Botany, vol. 73, no.
10, pp. 1405–1415, 1986.
[18] D. Wolff, T. Witt, A. J¨
urgens, and G. Gottsberger, “Nectar
dynamics and reproductive success in Saponaria officinalis
(Caryophyllaceae) in southern Germany,” Flora, vol. 201, no.
5, pp. 353–364, 2006.
[19] J. Kumar, R. C. Mishra, and J. K. Gupta, “The effect of mode
of pollination on Allium species with observations on insects
as pollinators,” Journal of Apicultural Research, vol. 24, no. 1,
pp. 62–66, 1985.
[20] J. B. Free, Insect Pollination of Crops, Academic Press, London,
UK, 3rd edition, 1993.
[21] S. L. Clement, B. C. Hellier, L. R. Elberson, R. T. Staska, and
M. A. Evans, “Flies (Diptera: Muscidae: Calliphoridae) are
efficient pollinators of Allium ampeloprasum L. (Alliaceae) in
field cages,” Journal of Economic Entomology, vol. 100, no. 1,
pp. 131–135, 2007.
[22] S. Saeed, A. Sajjad, O. Kwon, and Y. J. Kwon, “Fidelity of
Hymenoptera and Diptera pollinators in onion (Allium cepa
L.) pollination,” Entomological Research, vol. 38, no. 4, pp.
276–280, 2008.
[23] D. P. Abrol, “Foraging behaviour of Apis florea F., an important
pollinator of Allium cepa L,” Journal of Apicultural Research,
vol. 49, no. 4, pp. 318–325, 2010.
[24] J. Lanza, G. C. Smith, S. Sack, and A. Cash, “Variation in nectar
volume and composition of Impatiens capensis at the individ-
ual, plant, and population levels,” Oecologia, vol. 102, no. 1,
pp. 113–119, 1995.
[25] M. Macukanovic-Jocic, S. Duleti´
c-Lauˇ
sevi´
c, and G. Joci´
c,
“Nectar production in three melliferous species of Lamiaceae
in natural and experimental conditions,” Acta Veterinaria, vol.
54, no. 5-6, pp. 475–487, 2004.

The Scientific World Journal 7
[26] S. V. Jari´
c, L. A. Durdevi´
c, M. P. Ma ˇ
cukanovi´
c-Joci´
c, and G. M.
Gaji´
c, “Morphometric characteristics and nectar potential of
Ocimum basilicum L. var. Genovese (Lamiaceae) in relation to
microclimatic and edaphic environmental factors,” Periodicum
Biologorum, vol. 112, no. 3, pp. 283–291, 2010.
[27] T. G. Tutin, “Allium ursinum L. Biological Flora of the British
Isles,” Journal of Ecology, vol. 45, pp. 1003–1010, 1957.
[28] J. P. Grime, J. G. Hodgson, and R. Hunt, “Comparative plant
ecology—a functional approach to common British species,”
Unwin Hyman,1988.
[29] U. Falkengren-Grerup and G. Tyler, “Soil chemical properties
excluding field-layer species from beech forest mor,” Plant and
Soil, vol. 148, no. 2, pp. 185–191, 1993.
[30] M. E. Andersson, “Aluminium toxicity as a factor limiting the
distribution of Allium ursinum (L.),” Annals of Botany, vol. 72,
no. 6, pp. 607–611, 1993.
[31] L. A. Burkle and R. E. Irwin, “The effects of nutrient addition
on floral characters and pollination in two subalpine plants,
Ipomopsis aggregata and Linum lewisii,” Plant Ecology, vol. 203,
no. 1, pp. 83–98, 2009.
[32] J. H. Cane and D. Schiffhauer, “Nectar production of cranber-
ries: Genotypic differences and insensitivity to soil fertility,”
Journal of the American Society for Horticultural Science, vol.
122, no. 5, pp. 665–667, 1997.
[33] M. Baude, J. Leloup, S. Suchail et al., “Litter inputs and plant
interactions affect nectar sugar content,” Journal of Ecology,
vol. 99, no. 3, pp. 828–837, 2011.
[34] M. C. Gardener and M. P. Gillman, “The effects of soil fertilizer
on amino acids in the floral nectar of corncockle, Agrostemma
githago (Caryophyllaceae),” Oikos, vol. 92, no. 1, pp. 101–106,
2001.
[35] B. Oborny, Z. Botta-Duk´
at, K. Rudolf, and T. Morschhauser,
“Population ecology of Allium ursinum, a space-monopolizing
clonal plant,” Acta Botanica Hungarica,vol.53,no.3-4,pp.
371–388, 2011.
[36] W. H. O. Ernst, “Population biology of Allium ursinum in
Northern Germany,” Journal of Ecology, vol. 67, pp. 347–362,
1979.
[37] A. Eggert, “Dry matter economy and reproduction of a
temperate forest spring geophyte, Allium ursinum,” Ecography,
vol. 15, no. 1, pp. 45–55, 1992.