DEPARTMENT OF BIOLOGICAL AND ENVIRONMENTAL SCIENCES Degree project for Master of Science (120 hec) with a major in conservation biology BIO797, 60 hec Second cycle Semester/year: Spring/Autumn 2020 Supervisor: Åslög Dahl, Department of Biological and Environmental Sciences Examiner: Johan Höjesjö, Department of Biological and Environmental Sciences BUZZY IN THE CITY Investigating exploitative competition between managed honeybees and wild bees in the city of Gothenburg Andrea Helene Albeck
ENVIRONMENTAL SCIENCES
Degree project for Master of Science (120 hec) with a major in
conservation biology
BIO797, 60 hec
BUZZY IN THE CITY
Andrea Helene Albeck
2
1.2 The western honeybee (Apis mellifera)
......................................................................5
1.2 Solitary bees
..............................................................................................................5
1.4 Study site
...................................................................................................................6
2.3.3 Plant-pollinator network analysis
............................................................................9
3.3 Plant-pollinator networks and resource-availability
.................................................. 11
3.4 Honeybee-pollen analysis
........................................................................................
12
4.1 Negative correlation between wild bee activity and
honeybee-colony density .......... 13
4.2 Seasonal effect on wild bee visitation rate
................................................................
13
4.3 Plant-pollinator networks and foraging preferences
.................................................. 14
4.4 Exploitative competition and suggested thresholds
.................................................. 15
5.0 CONCLUSIONS
............................................................................................................
16
APPENDIX 2
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22
APPENDIX 3
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22
APPENDIX 4
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APPENDIX 5
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24
APPENDIX 6
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24
making urban green areas increasingly interesting in terms of
conservation biology. In Sweden,
one third of the wild bee species are red-listed, and it is highly
important to optimize
conservational efforts. Parks and gardens often provide high
plant-biodiversity and long
flowering periods, making them suitable bee-habitats. However,
urban beekeeping has become
more and more popular and many European cities have reported high
increases of managed
honeybees. Researchers are now worried that the managed bees will
exert an exploitative
competition-pressure under high density beekeeping, as revealed in
a number of studies. In this
study, I therefore aimed to investigate if increasing numbers of
managed honeybee-colonies
influenced wild bee occurrence in the city of Gothenburg (the
second largest city in Sweden).
The study was conducted during the summer, investigating: wild bee
visitation rates in relation
to honeybee-colony density, seasonal effects on visitation rates
and plant-pollinator network
structures. Six different sites with honeybee-colony densities
ranging from 3 to 23 colonies
(within a 500-meter radius) were investigated at twelve occasions.
I found a negative correlation
between the visitation rate of wild bees and the density of
honeybee-colonies within a 500-
meter buffer zone. A seasonal effect was detected on wild bee
visitation rate, possibly connected
to shifts in pollen-hosts. Further, the interaction evenness
between bee-genera and visited plant-
species declined on sites with high numbers of honeybee-colonies
and low resource-
availability. Wild bee-activity seemed to decrease on sites with
high numbers of honeybees and
low resource-availability. The study-results agree with previous
studies conducted in different
countries and environments. Moreover, high resource abundance seems
to be an important
factor in preventing competition and increasing bee-biodiversity.
With this knowledge, one can
design guidelines to make future collaborations between beekeeping
and conservation biology
more feasible.
SAMMANFATTNING
Urbana grönområden har blivit allt mer intressanta i bevarandet av
vilda bin, eftersom binas
naturliga habitat minskar kraftigt i det moderniserade jordbruket.
Parker och trädgårdar kan
erbjuda hög biodiversitet och långa säsonger, vilket gör dem
lämpliga för vilda bin. Rapporter
om ett minskande antal pollinatörer har också gjort biodling mer
populärt, och från många
europeiska storstäder rapporteras att mängden honungsbin har ökat
kraftigt. Honungsbin lever
i stora samhällen med flera tusen individer per bikupa. Forskare
varnar därför nu att honungsbin
kan konkurrera ut de vilda bina, eftersom möjlig konkurrens har
rapporterats vid hög densitet i
olika studier och olika länder. Av Sveriges vilda bin är en
tredjedel rödlistade. Det är därför
viktigt att vi gör rätt naturvårdsinsatser på rätt ställen. I denna
studie har jag undersökt om
antalet vilda bin som besöker blommor i Göteborg, minskar när
mängden honungsbi-samhällen
(inom en 500-meters radie) ökar. Antalet besök av bin i blommor
registrerades genom att
observera utlagda rutor i 10 minuter. Totalt undersöktes sex olika
platser med 3–23 honungsbi-
samhällen vid tolv olika tillfällen. Det fanns en negativ
korrelation mellan mängden vilda bin
som besökte blommor och densiteten av honungsbin. Mängden vilda bin
varierade också över
säsongen. Interaktionen mellan bi-släkten och besökta blomarter
minskade med ökad densitet
av honungsbi-samhällen och minskad tillgång till blommor.
Resultaten från denna studie
stämmer överens med tidigare studier gjort i andra habitat och
länder, och stödjer hypotesen
om att hög densitet av honungsbin kan skapa konkurrens om
blomresurser. Slutligen verkar
tillgänglighet till blomresurser vara en mycket viktig faktor för
att gynna artrikedomen av bin
4
och motverka konkurrens. Med denna typ av information kan vi
utforma riktlinjer för det
framtida samarbetet mellan biodlare och naturvårdsbiologer.
Keywords: exploitative competition, wild bees, managed honeybees,
pollinator-conservation,
urban beekeeping
1.0 INTRODUCTION
More than 20 000 different bee-species exist worldwide and almost
all bee-species are
considered as good pollinators (IPBES, 2016). Amongst the
animal-pollinators, bees are often
regarded as the most important pollinators as they have a wide diet
breadth and are highly
specialized in pollen-foraging (IPBES, 2016). Many fruits,
vegetables, herbs and culturally
important plants are dependent on insects for reproduction, which
makes the ecosystem service
of pollination extremely important for the function of ecosystems,
maintenance of biodiversity
and agricultural production ((IPBES, 2016; Klein et al., 2006;
Steffan-Dewenter et al., 2005;
Gallai et al., 2009). During the last decades, ongoing declines of
wild bee-populations have
been reported in many countries, indicating that wild bees are
declining globally (IPBES, 2016;
Winfree, 2010). Insecticides, habitat destruction and
fragmentation, loss of flower richness and
diversity caused by agricultural intensification and changes in
land use, are thought to cause the
decline of many wild bee-species (IPBES, 2016; Winfree, 2010;
Linkowski et al., 2004).
At the same time, the number of managed
honeybees has increased globally with 45
percent the last 50 years. The global
increase in managed honeybees is mainly
connected to honey- and agricultural
production (Aizen & Harder, 2009;
agriculture (Potts et al., 2010) and is often
described as our only or most efficient
pollinating bee-species (Jordburksverket,
2020; Geslin et al., 2017; Carreck & Williams, 1998). Only
recently, focus has been directed
towards our native pollinators and their role in global pollination
(Goulson, 2003). Studies have
revealed that the presence of native bees can enhance crop yield,
even for self-pollinated crops
(Garibaldi et al., 2013; Greenleaf et al., 2006), which makes it
even more important to prevent
further decline of native wild bee-populations.
The consequences of increased amounts of monocultures and
pesticides has made agricultural
landscapes less desirable for wild bees and beekeeping activities
(Otto et al., 2016). Although
controversial, urban environments have therefore become more
important for sustaining wild
bee diversity as their natural environments disappear. Cities have
proven to host greater
diversity of wild bees than first thought, as urban parks and
gardens provide high plant diversity
over long time periods and smaller amounts of pesticides than in
rural areas (Sirohi et al., 2015;
Harrison & Winfree, 2015; Fortel et al., 2014). For the same
reasons, urban beekeeping can be
favorable. Many European cities have experienced significant
increases of managed honeybees
during the last years (Ropars et al., 2019; Stange et al., 2017) as
citizens have been encouraged
to install apiaries in urban environments as conservational efforts
(Ropars et al., 2019)
Figure 1 Assessment of the world stock of honeybee hives (FAO,
2019)
5
Maintenance and expansion of wild bee populations depend on
resource accessibility as wild
bees feed their larva with pollen. One of the most constraining
factors for wild bee populations
is therefore pollen access (Larsson & Franzèn, 2007). Studies
so far have not revealed any direct
aggressive competition between managed honeybees and wild bees.
However, studies have
shown that high densities of managed honeybees in natural
environments, can cause
competition for flower resources and negatively affect wild
bee-fauna, so called exploitative
competition (Ropars et al., 2019; Henry & Rodet, 2018;
Mallinger et al., 2017; Geslin et al.,
2017; Lindström et al., 2016; Torné-Noguera et al., 2015; Goulson
& Sparrow, 2009). Managed
honeybees are broadly polylectic(generalists) and efficient pollen
collectors. One honeybee-
colony can contain 60 000 bees; thus, they often outnumber the
local native bee-fauna (Geslin
et al., 2017). During a three months period a single managed
honeybee-colony can collect the
amount of pollen needed to feed 110 000 progenies of an average
sized solitary bee (Cane &
Tepedino, 2016). The sudden increase of managed honeybees in urban
environments have
therefore caused scientist to worry if high densities of managed
honeybees can outcompete local
wild bee populations (Ropars et al., 2019; Stange et al., 2017).
Wild bees fly shorter distances
whilst foraging than managed honeybees does (Linkowski et al.,
2004), thus island effect can
occur in cities where green areas are located in-between concrete
and tall buildings, making it
harder for wild bees to escape competition pressure (Stange et al.,
2017). A recent study
conducted in Paris (Ropars et al. 2019) found that managed
honeybee-colony densities within
a 500-meter radius from the study site, was negatively correlated
with wild bee activity
(especially for big solitary bees).
1.2 The western honeybee (Apis mellifera)
The western honeybee (Apis mellifera) has a wide native range
stretching from Scandinavia to
Asia and the African continent (Franck et al., 1998). The species
mainly exists in domestic
colonies and is now spread all over the world, mainly due to
beekeeping activities (Han et al.,
2012). As a social species, the western honeybee lives in big
colonies consisting of one fertile
female (the queen), workers and drones. A full-grown colony often
holds 20 000 – 60 000
honeybees (Geslin et al., 2017). The species is highly polylectic,
foraging pollen and nectar
from a wide range of plant families (Goulson, 2003). In contrast to
many other bee-species, the
managed honeybee has the ability to fly very long distances while
foraging. On average, the
species flies 1.5 km but has been reported to fly as long as 10 km
(Geslin et al., 2013). Managed
honeybees also forage pollen earlier and later and during colder
weather, than smaller solitary
bee-species. Managed honeybees are equipped with semi-long tongues
enabling them to forage
from both deep and shallow flowers, thus making them a highly
adaptable and adjusting species
(Goulson, 2003).
1.2 Solitary bees
Most wild bee species, excluding bumblebees (Bombus sp.) who are
social bees, live solitarily
(Westrich, 2018). In contrast to social bee-species, all female
solitary bees are fertile. Each
solitary-female builds her own nest, collects pollen and lays eggs
without help from other
female bees (Westrich, 2018). Solitary bee-species can build large
colonies by building their
nests close together, but they never interact. On average the
female solitary bee lays six eggs in
separate nesting cells, each provided with a pollen provision
(Larsson & Franzèn, 2007;
Westrich, 2018). Pollen is therefore a constraining factor for
solitary bees, and their diet breadth
varies amongst species (Larsson & Franzèn, 2007). Some solitary
bees are generalists
(polylectic) and can utilize pollen from a wide range of plants
from different plant-families.
Their foraging ability then resembles that of honeybees and
bumblebees, but their diet breadths
6
are usually not as wide (Westrich, 2018; Larkin et al., 2007).
Other solitary species, the true
oligoleges, are highly specialized and forages pollen only from one
plant genus or plant species
(Stenmark, 2013; Larsson & Franzèn, 2007; Westrich, 2018).
Larsson and Franzèn (2007)
found that ten females of the strictly oligolectic species Andrena
hattorfiana needs to have
access to 780 inflorescences which translates to 156
plant-individuals from their host plant
Knautia arvensis, to provide enough food for their offspring. The
single female uses about 10.3
days with suitable weather to collect the pollen needed to brood
six eggs (Larsson & Franzèn,
2007).
In addition to narrow diets, solitary bees are known to fly shorter
distances than managed
honeybees and bumblebees. Average foraging distance for solitary
bees is usually 200-300
meters, but most prefer to fly as short as possible (Linkowski et
al., 2004; Westrich, 2018).
Solitary bee-species often have short active periods, varying from
one to two months, that
matches the active period of their host plants (Westrich, 2018).
Specialized species are thought
to be more vulnerable against competition and changes in their
habitats (Larsson & Franzèn,
2007; Wood & Roberts, 2017) However, vulnerability depends on
resource availability.
Oligolectic species can be common if their host plants also are
common and abundant (Wood
& Roberts, 2017).
1.4 Study site
In Sweden 274 wild bee species (bumblebees included) currently live
and reproduce, (Svensk
taxonomisk databas, n.d.b) of which about one third are red-listed
(ArtDatabanken, 2015). The
number of managed honeybee-colonies in the country has increased
with approximately 40 000
colonies the last ten years (Jordburksverket, 2020). There is a big
interest for pollinators from
both authorities and citizens and campaigns to save the bees have
proven very successful
(Naturskyddsföreningen, 2020). Gothenburg is Sweden’s second
largest city and is located on
the Swedish west coast. The city has a total of 571 868 inhabitants
and is known for its many
parks and gardens. A large percent (38 %) of the city area consists
of green areas
(Göteborgsposten, 2018) and Gothenburg has one of Europe’s biggest
and most spectacular
botanical gardens with about 16 000 plant-species (Botaniska
trädgården, n. d. a). Considering
the city’s many green areas and flower resources, Gothenburg has a
good potential to host many
native bee-species (Gunnarsson & Federsel, 2014). However, as
beekeeping has become more
popular and densities of honeybee colonies are also increasing, it
is important to know if this
can affect the native bee fauna in the city.
1.5 Aim and hypothesis
The aim of the study is to investigate if patterns of possible
competition can be seen between
managed honeybees and wild bees in the city of Gothenburg. The
study is inspired by the study
conducted in Paris by Ropars et al. (2019). I aim to investigate if
wild bee activity decreases as
the density of managed honeybee-colonies increases; if wild bee
visitation-rates are affected by
seasonal effects: and to analyze which plant species wild bees and
managed honeybees collect
pollen from in an urban context. By knowing if their food-resources
and living spaces overlap
within certain areas, one can direct the distribution of
honeybee-colonies to release the
competition pressure on wild bees. Based on the results from the
study of Ropars et al. (2019),
my hypothesis is that there is a negative correlation between the
density of managed honeybees
and the activity of wild bees in urban areas where their foraging
distances overlap.
7
2.0 METHODS
The method for this project was based on the study of Ropars et al.
(2019), to enable a
comparison of results. To investigate the activity of wild bees in
relation to honeybee density,
different green areas with abundant flower resources in the city of
Gothenburg, were
investigated by observing bee-activity per time unit.
2.1 Observation sites
colonies within a 500-meter buffer zone
(Figure 2), as well as available flower
resources and accessibility. The 500-
meter buffer zone reflects the average
flight distance for many solitary bees
(Linkowski et al., 2014; Westrich, 2004)
and was used in the study of Ropars et al.
(2019). All study areas were open for the
public. They were spread over
Gothenburg, with 1170 meters between
the closest sites and 10390 meters
between the furthest.
County Administrative Board in Västra
Götaland. Beekeepers in the city of
Gothenburg are obligated to register their
apiaries, but not all of them do. However,
this was the most accurate data that could
be derived within the scope of the project.
The number of colonies on each registered
location was controlled in field, as this was
not included in the registration data. Using
honeybee-colony density as a measure of a
constant pressure on wild bee communities is a method acknowledged
in several studies (Torné-
Noguera et al., 2015; Mallinger et al., 2017; Geslin et al., 2017;
Ropars et al., 2019).
Lastly, the map service eniro.se was used to measure how many
colonies were situated within
the 500-meter radius of each site. The number of honeybee-colonies
within each site (500-
meters buffer-zone) varied from 3 to 23 honeybee-colonies (Site
1(19), site 2(23), site 3(3), site
4(3), site 5(7) & site 6(11)). There has been a lot of damage
and thefts of honeybee colonies in
Gothenburg during the last years. I will therefore not be allowed
by the County Administrative
Board to reveal where my study sites are located.
2.2 DATA COLLECTION
Wild bee activity was monitored by conducting field observations
every week from May 29th
to September 1st. Field observations were performed at minimum
seven days apart during
9.a.m. and 5.p.m., and days with low wind speed and temperatures at
least exceeding 15°C,
were chosen. Observations of all sites could not always be
conducted on the same day, due to
Figure 2
A study of possible competition between wild bees and managed
honeybees in the city of Gothenburg, Sweden. Model of the study
design on a random site showing three observation squares in the
center of the site and the surrounding honeybee colonies within the
500-meter radius.
8
changed as much as possible between different occasions.
Foraging activity was investigated by observing a 1 m2 square,
placed on a patch of flowering
plants, for 10 minutes. Plant species richness and number of
visited plant species within the
square were noted for each observation. All bees (including
domestic honeybees) that visited
the square for foraging, were noted and speciated to the nearest
genus possible. In addition, the
plant species within the square visited by bees were also noted for
the plant-pollinator analysis.
A visit was defined as the first time one individual bee entered
the square for foraging purposes.
The 10-minute observation session was repeated three times within
each site and each occasion.
In total, wild bee foraging activity was investigated at 12
different occasions, which means that
216 squares were observed for 1260 minutes
2.2.1 Honeybee-pollen collection
Honeybees are broadly polylectic bees. It is therefore interesting
to know which pollen-sources
they prefer. This information can also be used to assess the level
of diet overlap between
managed and wild bees. To get an overview of what pollen the
managed honeybees collected
within the investigated buffer-zones, pollen-traps were set out on
four occasions on four
different honeybee-colonies within the buffer-zone of site 1, 4, 5
and 6. The traps remained
mounted during one day during week 21, 25, 30 and 36. Due to
technical issues, no pollen was
collected during week 36 on site 1 and site 6 (postponed until week
39). All pollen collected in
the traps were collected and marked with ID and date. The fresh
pollen-pellets were stored in a
freezer before preparation of pollen samples (see section
2.4).
2.3 STATISTICAL METHODS
The data could not be collected in a randomized way, as it proved
very difficult to randomly
select observation-squares on a small area and assure that there
were flowering plants within
the square. As a result, traditional statistical methods built on
the presumption that the data had
been collected in a random manner could not be used. Instead,
non-parametric tests such as
Spearman rank correlation (using ranks instead of true values) were
chosen to perform the
statistical analyses. All statistical analyses were conducted in
RStudio version 3. 6. 1.
2.3.1 Spearman rank correlation
A Spearman rank correlation was calculated using wild bee
visitation rates and abundance of
honeybee-colonies, to test if honeybee-colony density (within a
500-meter radius) and wild bee
activity were negatively correlated. The Spearman rank correlation
was calculated for all
subsamples (n=216) and the for the mean of subsamples (n=6). Before
conducting the
Spearman correlation, all datapoints for wild bee visitation rates,
excluding those for
honeybees, within the six sites were checked for dependents. All
subsamples within each site
were randomly paired, and correlation coefficients were calculated.
A strong correlation
indicates that there are dependents, and little or no correlation
indicates that there are no
dependents among subsamples. Before calculations, visitation rates
were converted to rate per
square meter and minute, to make the outcome comparable to that of
the study of Ropars et al.
(2019) – even though this study used different statistical
methods.
2.3.2 Friedman’s two-way ANOVA and Kendall’s W
To cover the change in wild bee species and plant species during
the season, the field study
lasted for several months. A Friedman’s two-way analysis of
variance was conducted with the
rstatix package and the function firedman_test, using visitation
rate as the variable, and week
9
and site ID as factors (Kassambara, 2018). As data was resampled
every week, the visitation
rates were calculated as the average number of visits of wild bees
per minute and per site and
week(n=6). In order to be able to perform the Friedman’s test, the
results from May 29th and
June 1st were named week 23 although they technically were sampled
in week 22 respectively
week 23.
A Kendall’s coefficient of concordance (W) was also calculated with
the friedmans_effectsize
function, to assess the Friedman’s test (X2) effect size.
= 2/( − 1)
where n is the sample size and k are the number of measurements per
subject. The Kendall’s W
test computes a value between 0 (indicating no relationship) and
1(indicating full relationship,
Tomczak, 2014). Effect size can be helpful to tell more about the
results as the test assesses
how much of the variation of the visitation rate (in this case) can
be explained by the seasonal
effect. The R-function uses Cohens interpretation coefficient
(Small (0.1 - <0.3), moderate (0.3
- <0.5) and large (>= 0.5)).
2.3.3 Plant-pollinator network analysis
A plant-pollinator network analysis was conducted with the
bipartite package (Dorman et al.,
2020) to visualize and assess the interaction evenness between
pollinator genera and plant
species within the six different sites. Visitation frequencies for
the whole period was used. In
some cases, small solitary bees were hard to distinguish and were
therefore put in a group called
“other small solitary bees”. The interaction evenness index was
calculated as a complement to
the visual presentation. This index reflects how balanced the
network interactions are,
computing a number between 0 and 1. If the network consists of few
and dominant species, the
index will go towards zero and if the network consists of many
species with equally distributed
interactions the index will go towards one (Blüthgen et al., 2009;
Ropars et al, 2019).
The interaction evenness index (IE) is based on the Shannon
diversity, and is calculated:
= ∑
ln
where ln I is the total number of plant-pollinator interactions in
the matrix and pi is the
proportion of interactions involving species i, of all interactions
(Blüthgen et al., 2009; Ropars
et al., 2019).
2.4 HONEYBEE-POLLEN ANALYSIS
2.4.1 Preparation of samples
Following the method of Barth et al. (2010), two grams of frozen
non-dried bee-pollen was
subsampled from each sample and put into 15 ml tubes. 70 % ethanol
was added just to
complete 13 ml and left to set for 30 minutes. The samples were
shaken repeatedly to dissolve
all pollen pellets and then centrifuged for 5 minutes at 2500 rpm
to create a pellet. The
supernatant was removed, and the samples were resuspended with a
distilled water/glycerol 1:1
mixture to finish 13 ml. The samples were stirred with a glass wand
and rested for 30 minutes.
2.4.2 Preparation on microscope slides
One drop of the well mixed pollen solution (pollen grains and 1:1
distilled water/glycerol
mixture) was placed on a microscope slide and painted out with the
pipette tip to match the
10
dimensions of a 24x24 mm cover slip. The solution was evenly spread
within the square and
set to dry for a few minutes. The samples were sealed with a 24x24
mm cover slip covered with
a drop of glycerol-gelatin containing safranin and a bactericide
(phenol). The safranin stains
the pollen exine into a pink color, making it easier to distinguish
the pollen grains from spores
and other organic material and to discern their specific surface
patterns.
Following the method of Lau et al. (2018), five slides (subsamples)
were made from each
sample. 500 pollen grains were counted and identified from each
slide (in total 2500 pollen
grains per sample) in a light microscope with 400 x magnification.
The grains were counted by
starting in the upper middle of the slide and moving downwards
counting all grains within a
320 µm scale. Pollen grains were identified to the lowest taxonomic
level possible. The mean
proportion of collected pollen species was calculated per sample
and presented in percent.
Pollen species below 1 percent were not presented in the results as
they can be considered as
contamination (Ritchie et al., 2016; Wood & Roberts., 2017;
Wood et al., 2018).
3.0 RESULTS
In total 1847 bees were counted and observed, of which 8.3% were
big solitary bees, 9.5%
small solitary bees, 26.6% bumblebees and 55.6% honeybees (Table
1). Mean visitation rate
per minute and square meter for all sites were as following; site 1
(0.18±0.17), site 2
(0.21±0.25), site 3 (0.69±0.57), site 4 (0.72±0.56), site 5
(0.32±0.34) and site 6( 0.27±0.24).
Tabell 1 A study of possible competition between wild bees and
managed honeybees in the city of Gothenburg, Sweden. Total numbers
of bee-individuals observed during the field observations.
Colonies=managed honeybee-colonies.
ID Colonie
11
Correlation coefficients for the
random pairwise testing of
varied with relatively low
values from 0.009 to
datapoints of
value of subsamples within
observed visitation rate per
minute and square meter
occasional observed visitation
rates of zero.
bee visitation rate
(Figure 4) showed that
changed significantly during
effect size (W) 0.346.
different sites varied between
(Appendix 2). Site 1 had the
lowest mean number of plant
species visited per square
mean number (2.19) (Appendix
2).
Site 3 and 4 had the highest number of observed bee-genera (11).
Site 4 also had the highest
total number of visiting wild bees with 249 individuals (Table 1)
and the highest number of
visited plant species (40) (Figure 5). Site 5 had the lowest number
of bee-genera (6) whereas
site 1 had the lowest number of visited plant species (10) and the
lowest number of visiting wild
Figure 3 A study of possible competition between wild bees and
managed honeybees in the city of Gothenburg, Sweden. Visitation
rates shown as rate/ m2 /min for all data points (n=216) for the
six investigated sites. Two sites had the density of 3
honeybee-colonies (Site 3 and 4), thus overlapping on the
plot.
Figure 4 A study of possible competition between wild bees and
managed honeybees in
the city of Gothenburg, Sweden. Results from Friedman’s test and
visualization of the data-distribution. Wild bee visitation rate
presented as mean visitation rate/ m2 /min, per week for each
site(n=6).
12
bees, with 61 individuals. All sites had similar interaction
evenness indices, with values ranging
from 0.657 to 0.503(Figure 5).
3.4 Honeybee-pollen analysis
In total 27 500 pollen grains were counted and identified to the
lowest taxonomic level possible.
Total counts can be found in appendix 3. All samples from Week 21
were dominated by pollen
belonging to tree species (Appendix 3). The samples from week 25
were dominated by pollen
from Trifolium repens, Aegopodium podagraria and pollen belonging
to the genus Spiraea.
Filipendula ulmaria was present in all samples in week 30. Samples
from week 36-39 contained
late-flowering plants such as Calluna vulgaris, Bistorta sp. and
Lotus corniculatus.
4.0 DISCUSSION
A negative correlation was found between wild bee visitation rate
and density of managed
honeybee-colonies on the investigated sites. The visitation rate of
wild bees was significantly
different over time, indicating a seasonal effect. In total,
polylectic bee-species such as
honeybees and bumblebees were dominant on the investigated sites.
Pollen analyses and field
observations showed that wild bees and managed honeybees mostly
foraged on native plant
species, thus diets did overlap to some extent. The honeybee-pollen
analyses revealed that the
four different honeybee-colonies investigated, collected roughly
the same pollen-species. In
Figure 5 A study of possible competition between wild bees and
managed honeybees in the city of Gothenburg, Sweden. Plant-
pollinator networks of the six sites investigated. Pollinator
generas on the top and plant species on the bottom. Thickness of
lines represents how many times a bee-genus visited a certain plant
species IE is the interaction evenness index. Color description:
Andrena(black), Anthidium(pink), Apis(orange), Bombus(yellow),
Colletes(mustard), Eucera(purple),
Hallictus(brown), Hylaeus(darkgreen), Lassioglossum(grey),
Macropis(red), Megachile(green), Melitta(darkblue)
Micraandrena(blue), Nomada(darkmagenta), Osmia(darkgrey), Other
small solitary bees(Pale).
addition, the investigated colonies seemed to prefer pollen from
plant-species that often grow
in big aggregations.
4.1 Negative correlation between wild bee activity and
honeybee-colony density
When testing the correlation coefficients of the random pairing of
subsamples within the
different sites, the coefficients were relatively low (Appendix 5),
which could indicate no
dependents among subsamples. Therefore, one could argue that it is
justifiable to use values
from all subsamples, rather than their mean values, in the Spearman
correlation analysis. When
all datapoints were used, the result was a Spearman correlation
coefficient of -0.42, which can
be considered a relatively strong negative correlation, given the
big sample size (n=216). The
same calculations for the mean visitation on each site(n=6)
resulted in a correlation coefficient
of -0.93. This is a very strong correlation coefficient, but on the
other hand, the sample size is
very low. As both tests resulted in strong negative correlation
coefficients, I would dare to state
that I found a negative correlation between wild bee visitation
rate and density of managed
honeybee-colonies, in the areas investigated. My results are
therefore in agreement with the
results from Ropars et al. (2019), keeping in mind that our studies
were conducted in different
manners.
P-values were not calculated for the two Spearman correlation
analyses. Even though the data
was tested for dependents, there could be a risk that some of the
data within sites are dependent.
A p-value calculated on dependent data would be biased, and the
possibility of a significant
result enhanced. The same problem arises when calculating the mean
visitation rate for all sites.
A sample size of n=6 with a correlation coefficient of -0.93 will
most likely be significant
(Wagenmakers, 2007; Tomczak, 2014). Considering this, I argue that
a calculation of the p-
value would not provide any statistical evidence or reassurance to
my correlation analyses.
An observation study does not result in clear evidence or
causation. As the factors affecting the
outcome are not controlled, it is impossible to draw strict
conclusions about the causes of the
result. The field observations in my study were all conducted in
different green areas. The two
sites with the lowest number of honeybee-colonies (site 3 and 4)
had the highest number of
plant species (Appendix 6). In addition, these two sites also had
an overall higher resource
availability and more park-like structure than the other sites.
Thus, high visitation rates of wild
bees on these sites could be caused by high plant diversity and
abundance. Ideally, floral
resources should have been accounted for in the analysis, but due
to the fact that the data were
collected in a non-random manner, a multiple regression could not
be conducted. Another bias
is that two sites (site 1 and 5), were unexpectedly mowed on two
occasions, leaving very few
plants in flower. The low visitation rates observed on site
1(Figure 3) could be affected by the
fact that the green area never fully recovered after being mowed
during a very hot period in the
end of June (observed 26. June).
4.2 Seasonal effect on wild bee visitation rate
The Friedman’s ANOVA showed that there was a significant difference
(p=0.0186) in wild bee
visitation rate over time. The week 23 stands out from the rest
(Figure 4). This difference can
be due to errors in data-sampling, as week 23 was the first
sampling-occasion. Interestingly, the
pollen collected from honeybees during week 21(Appendix 3) mostly
belonged to tree-species,
such as Salix sp., Malus sp. and Prunus sp. It is also known from
the literature (Westrich, 2018)
and studies (Wood et al., 2018) of pollen-foraging by wild bees,
that early wild bee-species
depend on early-flowering tree-species for pollen foraging. Due to
practical reasons, my field-
observations were conducted on ground-level. The low observed
visitation-rates of week 23 as
14
compared to later parts of the season, could therefore reflect this
early preference for tree pollen,
and that later, there was a shift in pollen hosts to herbaceous
plant species.
The effect size of the Friedman’s test was 0.346, just reaching a
moderate effect size (according
to the Cohens interpretation coefficient). This effect size
combined with the data distribution
(Figure 4), reveals that the relationship between wild bee
visitation rate and the seasonal effect
is quite weak. I can therefore not argue that there is a clear
seasonal effect on the wild bee
visitation rate. The effect could have been stronger if the field
observations were started earlier,
capturing the early species relying on other pollen-sources.
However, this is only speculation.
4.3 Plant-pollinator networks and foraging preferences
Plant -pollinator networks have been reported to differ greatly
between seasons (Chacoff et al.,
2017). Thus, an interpretation of results that are based on data
from one season is precarious.
However, the visual presentation of the plant-pollinator networks
shows that the two sites with
low abundance of honeybee colonies have more cross-over
interactions (Figure 5). As discussed
above (section 4.1), site 3 and site 4 had very abundant
flower-resources which could have
affected the results. Both honeybees and bumblebees, which were the
most abundant species
on site 3 and 4, are polylectic. One would therefore expect more
interactions with these species
present. The interaction-evenness-indices calculated for the
networks were very similar and did
not strictly decline as the honeybee-colony density increased.
Interestingly, the two sites that
were mowed during the field-season (Site 1 and 5) had the lowest
interaction evenness indices
(Figure 5). Site 1 also had few plant species and few
bee-individuals, which could explain the
few interactions observed (Figure 5).
Bombus(bumblebees) were the most abundant wild bees on all sites
except on site 2, where
Colletes was the most abundant genus. It is not surprising to find
high abundances of
bumblebees in urban environments, as they are social, polylectic
and tough bees, much like
managed honeybees (Gunnarsson & Federsel, 2014). However, to
find high abundances of
oligolectic bees, was more unexpected. Site 2 and Site 6, who had
high abundances of honeybee
colonies, also hosted a fair amount of bees from the Colletes
genus. The Colletes bees were
mostly observed (Appendix 6) on Leucanthemum vulgare,
Tripleurospermum inodorum and
Tanacetum vulgare, plants that often grow abundantly in SLOAP’s
(space left over in
planning). Based on the plants visited (Appendix 6) the bees most
likely belonged to Colletes
similis, which are oligolectic for the Asteraceae family (Westrich,
2018). Even though managed
honeybees also visited these plant-species, they seemed to be
abundant enough to host both
wild and managed species. Again, this indicates that
resource-abundance is important to prevent
exploitative competition (Cane & Tepedino, 2016; Tornè-Noguera
et al., 2015).
4.3.1 Did honeybees collect the same pollen as observed in
field?
Some of the plant species that honeybees visited in field, were
indeed found in the pollen
samples. For instance: Trifolium repens, Cirsium arvense, Tanacetum
vulgare and Aegopodium
podagraria. However, most of the pollen collected, belonged to
plant species that were not
observed in field. Beginning with the first week, pollen collected
from honeybees belonged to
different tree-species. I did not have the opportunity to observe
tree-species, due to my study
design. I was however aware that plants like Salix sp. are very
important as they provide an
early and abundant pollen-source for many bee-species (Westrich,
2018). Many of the
oligolectic bees from the Andrena genera are active during the
spring or late summer, foraging
on Salix and Calluna vulgaris (Westrich, 2018). As they are
specialists, they are more exposed
to competition (Cane & Tepedino, 2016; Larsson & Franzèn,
2007). To avoid competition from
15
managed honeybees, who also seem to collect from these species,
plantation and conservation
of both Salix and Calluna vulgaris should be encouraged.
The following weeks (25, 30 and 36), most species from which the
managed honeybees
collected pollen were not present on the observation sites
(Appendix 6). As honeybees are
known to fly long distances (Geslin et al., 2013), the bees
foraging on my sites could have come
from other apiaries nearby. However, since I only had one
pollen-trap in each buffer zone, the
chances are big that the remaining colonies within my zones were
indeed foraging on the
selected sites. Interestingly, I did not to find any pollen grains
from Origanum vulgare or
Nepeta sp. These plants were very well visited in field (Appendix
6) and are known as bee-
friendly plants. This could indicate that managed bees mainly use
the species mentioned above
as nectar-sources. Except for some pollen-species, honeybees in my
study mainly collected
pollen from common plants or weeds, even grass (Poaceae, appendix
3). This was not expected
as Ropars et al. (2019) found that managed honeybees significantly
preferred foraging from
managed plant species. However, their study was based on field
observations and could
therefore reflect both nectar and pollen foraging (Ropars et al.,
2019). My data is inadequate to
prove any hypothesis, but it can indicate that managed honeybees
prefer to forage pollen from
wild plant species.
4.4 Exploitative competition and suggested thresholds
One cannot exclude that the wild bee visitation rates observed in
my study are affected by
environmental factors such as resource availability, lack of
suitable areas to build nests and
possibly high emissions and poor air quality. However, my results
agree with previous studies
done in different environments and countries. High density
beekeeping has been related to
decreased wild bee visitation rates and foraging success (Ropars et
al., 2019; Henry & Rodet,
2018), decrease in wild bee biomass and resource availability
(Tornè-Noguera et al., 2015), and
decrease in bumblebee-body mass (which could ultimately affect
bumblebee-colony success)
(Goulson & Sparrow, 2009). Negative effects of high-density
beekeeping on wild pollinators
has even been found in experimental studies, conducted in Swedish
oil-seed-rape fields
(Lindström et al., 2016). Further, Cane & Tepedino (2016) found
that one colony of managed
honeybees during three months, collected the amount of pollen
needed to breed 110 000
progenies of an average sized solitary bee. This can become very
problematic if resources are
scarce and diets overlap (Cane & Tepedino 2016; Larsson &
Franzèn 2007). My study results,
together with previous studies therefore strengthens the hypothesis
that high density beekeeping
can cause negative effects on wild bee communities. However, not
all studies support the
exploitative competition hypothesis (City of Oslo, Stange et al.,
2017; Grasslands, Germany,
Steffan-Dewenter & Tscharntke, 2000).
An earlier study also conducted in Gothenburg, that investigated
species richness and
abundance of bumblebees in an urban context, found a positive
co-variation between
bumblebee- and honeybee-abundance (Gunnarsson & Federsel,
2014). The authors concluded
that resource availability was sufficient to avoid exploitative
competition. Bumblebee-species
and managed honeybees are both polylectic and can fly long
distances in tough conditions
(Westrich, 2018), which could make them more successful than
solitary bees. Honeybees and
bumblebee-species were also the most abundant bees observed in my
study (Table 1 & Figure
5). However, abundance of bumblebees did not completely follow that
of honeybees on the
sites investigated (Table 1). Further, Gunnarsson & Federsel
(2014) used the observed
abundance of foraging honeybees, whereas I used the density of
colonies. It can be argued
which method is more correct, but density of managed
honeybee-colonies has been regarded as
a good measure for competition pressure in previous studies
(Torné-Noguera et al., 2015;
16
Mallinger et al., 2017; Geslin et al., 2017; Ropars et al., 2019)
as it reflects a constant pressure
on the wild bee communities, rather than a temporary one.
4.4.1 Suggested thresholds and conservation efforts
As the nature of plant-pollinator networks are ever-changing and
highly variable, it is hard to
assess the thresholds needed for managed honeybee-density to avoid
exploitative competition.
Depending on environment and resource availability, the thresholds
might differ greatly. As a
guideline, studies have suggested that thresholds should be set to
3.1-3.9 colonies/km2 (Steffan-
Dewenter & Tscharntke 2000; Tornè-Noguera et al. 2015; Henry
& Rodet 2018). If using 3.5
colonies/ km2, no more than 4.5 colonies should be within the
500-meter buffer zone. Only two
of the sites that I investigated were bellow the suggested
thresholds (Figure 3).
Henry & Rodet (2018) argued that distance-based thresholds
could be more feasible and
suggested that thresholds should be set to approximately 1-2 km
between the apiaries. Further,
thresholds should be re-evaluated and based on the resource
availability of the area in question
(Henry & Rodet, 2018). Lowering the resource pressure is not
only desirable for wild bee
conservation, but can even decrease intraspecific competitions
amongst managed honeybees
leading to increases in honey-yield (Henry & Rodet, 2018).
Sørensen et al. (2020) has purposed
a model assessing the risk of negative effects on wild bee
communities in relation to managed
honeybee-density. Taking different factors into account, the model
follows the same line of
thoughts as Henry & Rodet (2020), suggesting regulation of the
distance from apiaries, rather
than number of colonies, to avoid negative effects on wild bees
(Sørensen et al., 2020).
5.0 CONCLUSIONS
A negative correlation was found between the activity of wild bees
and the density of managed
honeybees, within the investigated areas. A weak seasonal effect
was found on wild bee
visitation rates. Plant-pollinator networks were less balanced on
sites with a high number of
managed honeybees and limited plant-resources. Diet overlap between
wild and managed bees
could be higher during spring and late summer, when pollen-sources
are scarcer than later in
the season. Wild bee visitation rates were extremely variable and
should therefore be analyzed
with caution. The results of this study agree with previous studies
done in other countries and
environments and support the hypothesis that high density
beekeeping could negatively affect
native wild bee communities. The introduction of threshold numbers
for managed honeybee
colonies could be an effective conservation measure. In addition,
thresholds can result in
increased honey-yields and less intraspecific competition amongst
honeybees.
ACKNOWLEGDEMENTS
I would like to express my sincere gratitude to my supervisor Åslög
Dahl, who has guided me
through the project and helped me improve my thesis and scientific
content. Also, her special
skills in pollen analysis and speciation has been invaluable in
this project. I would also like to
thank Mattias Lindholm, who came up with the project idea and for
providing equipment and
contact information to the park-managers in Gothenburg. A special
thanks to Donald
Blomquist, who helped me with the statistics. Thanks to the
beekeepers, Mikael Lagerman,
Ingemar Widheden, Janne Petterson and Leif Andersson, who helped me
collect honeybee-
pollen and lend me equipment. Lastly, I would like to thank Rasmus
Lindblad for helping me
with data collection, problem solving and having long discussions
about statistics.
17
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BUZZY IN THE CITY
setting
been directed towards how managed
honeybees interfere with our native wild
bees. Results from different studies in
different environments, reveal that large
number of honeybees can be a
constraining factor on wild bees, thus
leading to indirect resource competition.
The interest in pollinators has increased
rapidly the last decade. Besides the well-
known managed honeybee, there are many
wild bee species that play a very important
role in pollination of wild and managed plant species. For
instance, tomato-flowers require a
special frequency of vibration to release pollen, that mainly
bumblebees can produce. To
maintain a high biodiversity of wild bees should be in our
strongest interest, as many species
with different niches can function as a buffer during climate
changes. Sadly, many important
habitats and food sources for wild bees are disappearing as the
agriculture is modernizing.
Controversially, studies have shown that cities can provide both
high diversity of flowers and
long flower-seasons, which can benefit both wild and managed
bees.
Managed honeybees risk outcompeting native bees
At the same time as wild bees decrease, the number of managed
honeybees increases in many
European cities. The increase is linked to the public interest in
pollinators, and people wanting
to save the bees. However, as only one colony of managed honeybees
can contain 40 000 –
60 000 working-bees, they risk outcompeting other species. Both
managed and wild bees feed
their offspring with pollen, which becomes essential for the
bee-populations to survive. When
plant resources become low, indirect competition for
pollen-resources amongst wild bees and
managed honeybees can occur. Wild or solitary bees (excluding
bumblebees) usually don’t live
in colonies. Solitary-bee females live as single moms, building the
nest, foraging pollen and
laying eggs, all by themselves. Wild bees are therefore fewer in
number, more stationary and
often utilizes pollen from fewer plant species, which makes them
more exposed to competition.
In Sweden, one third of the wild bee species are red listed.
Increasing our knowledge is therefore
crucial to do the right conservational efforts. In this
master-project, I studied if activity and
structure of wild bees changed as number of honeybee-colonies
increased in certain areas in the
city of Gothenburg. Activity was observed by counting the number of
bees foraging pollen and
nectar on different plant species, during a fixed time and area
unit. After observing wild bee
activity on six different locations during the summer, I could see
that there was a negative
correlation between the activity of wild bees and the number of
honeybee-colonies. Further,
areas with high plant biodiversity and few honeybee-colonies,
hosted more bee-genera’s and
had more balanced plant-pollinator networks, than those with little
plant diversity and many
honeybee-colonies. Wild and managed bee-diets seemed to overlap to
some extent, especially
during spring. Similar studies have been done in other European
cities with similar outcome.
22
Coexistence of wild and managed bees
As the European honeybee is such a widespread species, it becomes
crucial that we learn how
to balance its use with the survival of wild bee species. The
results of this study suggest that
there is a pattern between decreasing activity of wild bees and
high numbers of honeybee-
colonies combined with little resource, on the investigated sites.
With broader knowledge about
the indirect resource competition, we can avoid high aggregations
of honeybee-colonies in areas
that are especially fragile, such as nature reserves. Maintaining
and creating more green areas
with high plant species-diversity also becomes more important to
decrease the pressure of
resource competition amongst all pollinators. At last, it is
important not to blame beekeepers,
but rather address the problem and spread awareness.
APPENDIX 2
A study of possible competition between wild bees and managed
honeybees in the city of Gothenburg, Sweden. Total data of number
of visited plant species and mean plant species per observed square
and site.
Table 3
APPENDIX 3
A study of possible competition between wild bees and managed
honeybees in the city of Gothenburg, Sweden. Honeybee- pollen total
result for all sites and weeks. Presenting the mean amount (%) of
all pollen species within each sample collected. Pollen species
that were less than one present are not shown, as they are
considered as contamination (Ritchie et al., 2016;
Wood & Roberts., 2017; Wood et al., 2018).
Week 21
Site ID Pollen content
1 Salix sp. (62.3), Malus sp. (17.), Prunus sp. (6.6), Taraxacum
coll. (4.1), Quercus robur (3.6), Aescelus hippocastanum
(1.9)
4 Malus sp. (32.9), Prunus sp. (31.2), Salix sp. (14.), Quercus
robur (8.3), Aescelus hippocastanum (8.1)
5 Malus sp. (5.1), Salix sp. (23.4), Aescelus hippocastanum (15.),
Prunus sp. (7.7), Quercus robur (1.6)
6 Quercus robur (4.8), Salix sp. (19.2), Malus sp. (15.5), Prunus
sp. (15.), Aescelus hippocastanum (4.4)
Week 25
1 Spirea sp. (55.4), Filipendula ulmaria (12.1), Poaceae (11.2),
Trifolium repens (8.1), Ig. 8 (3.1), Polemonium sp. (1.5),
Aegopodium podagraria (1.)
4 Spirea sp. (6.9), Aegopodium podagraria (18.6), Trifolium repens
(4.8), Poaceae (2.5), Ig. 12 (1.7), Ig. 7 (1.5)
23
5 Spirea sp. (48.3), Trifolium repens (16.1), Aegopodium podagraria
(7.4), Ig. 12 (5,2), Ig. 22 (3.7), I.g 19 (3.1), Poaceae (2.6), Ig.
21 (1.4)
6 Trifolium repens (41.) Spirea sp. (37.3), Poaceae (6.3), Ig. 29
(3.6), Filipendula ulmaria (1.4), Ig. 17 (1.1)
Week 30
1 Cirsium pratense (28.6), Filipendula ulmaria (18.4), Heracleum
mantegazzianum (11.9), Tanacetum vulgare (1.), Trifolium repens
(9.6), Hieracium sp. (5.9), Tilia sp. (5.7), Ig. 38 (4.4), Bistorta
sp. (4.2)
4 Filipendula ulmaria (94.8), Trifolium repens (3.)
5 Filipendula ulmaria (76.), Bistorta sp. (8.7), Ig. 33 (6.5),
Cirsium arvense (3.), Trifolium repens (1.6), Caryophyllaceae
(1.3)
6 Filipendula ulmaria (42.6), Tanacetum vulgare (36.1), Tilia sp.
(13.6), Trifolium repens (5.8)
Week 36. *Week 39
Site ID Pollen content
1 No pollen was collected
4 Calluna vulgaris (32.2), Ig. 41 (26.8), Ig. 44 (19.9), Impatiens
glandulifera (5.6), Trifolium repens (4.3), Ig. 4 (2.6), Ig. 34
(1.7), Hieracium sp. (1.4), Ig. 42 (1.4), Filipendula ulmaria
(1.)
5 Bistorta sp. (66.), Ig. 45 (23.4), Ig. 46 (5.9), Hieracium sp.
(1.9), Calluna vulgaris (1.6)
6 * Lotus corniculatus (72.5), Calluna vulgaris (15.2), Ig. 49
(6.4), Trifolium pratense (2.9), Ig. 45 (1.3)
APPENDIX 4
A study of possible competition between wild bees and managed
honeybees in the city of Gothenburg, Sweden. Weather conditions
recorded by SMHI for all dates that field observations were done.
Wind and temperature are presented as averages of the hours the
observations were made in field (9.a.m. and 5.p.m.)
Week Date Min temp Max temp Wind average Gust average
22 29.mai 7,20 2,50 4,70 6,60
23 1.jun 11,5 26,0 4,90 7,30
24 9.jun 9,70 19,0 3,67 5,90
24 11.jun 15,7 25,2 7,20 12,5
25 17.jun 16,2 23,9 4,30 6,50
25 18.jun 14,7 26,8 3,90 5,70
25 19.jun 17,7 27,5 4,12 5,90
26 25.jun 15,1 29,1 3,00 5,00
26 26.jun 17,3 29,6 4,10 6,60
28 8.jul 12,6 18,8 5,70 8,60
29 16.jul 11,0 21,7 3,10 4,90
29 17.jul 12,3 22,5 4,10 5,90
30 22.jul 10,7 20,6 6,20 9,40
30 23.jul 14,5 20,6 6,00 9,00
31 31.jul 14,5 25,7 3,50 5,70
32 6.aug 16,0 26,6 3,30 5,00
32 7.aug 20,2 30,5 3,90 5,90
33 13.aug 14,9 26,3 3,50 5,00
35 25.aug 13,6 19,1 4,70 6,70
24
APPENDIX 5
Table 1 A study of possible competition between wild bees and
managed honeybees in the city of Gothenburg, Sweden. Correlation
coefficients derived from testing for dependents amoung samples
within each site. Sampels were randomly paired and tested.
ID Correlation coff
Site 1 0.1547
Site 2 0.2411
Site 3 -0.1672
Site 4 0.1198
Site 5 -0.1368
Site 6 0.0096
APPENDIX 6
Total data of all plant-visits by bees within the
observation-squares during the ten minutes of observation from May
29th and
September 1st. O.s.s = Other small solitary bees.
Site 1
Plant species Apis Bombus Eucera Hallictus Hylaeus Macropis Osmia
O.s.s
Calystegia sepium - 1 - - - - - -
Solidago canadensis 17 - - - - - - -
Trifolium repens 9 1 - - - - - 1
Vicia cracca - 2 - - - - - -
Barbarea vulgaris - 2 - - - 1 - -
Epilobium angustifolium - 15 1 - - - - -
25
Vicia cracca - 4 2 - - - - -
Aster sp. 3 - - - - - - - - - - 1
Campanula
poscharskyan
Echinacea sp. - - - 1 - - - - - - - -
Geranium
Geranium
Hylotelephiu
Hypericum sp. - - 1 8 - - 1 - - - - 1
Lavendula sp. - 1 19 1 - - - - - - - 1
Lysimachia
Origanum
Rosa
Thymus sp. - - 6 - - - - - - - - -
Alyssum stribrnyi - - 12 - - - 1 - - - -
Aquilegia olympica - - 1 3 - - - - - - -
Asclepias incarnata - - 11 6 - - - - - - -
Aster tataricus - - - 1 - - - 1 - - -
Calluna vulgaris - - 6 - - - - - - - 1
Campanula sp - - - 12 - - - 6 - - -
Centaurea jacea - - 2 3 - - - - - - -
Cotoneaster adpressus - - 4 - - - - 3 - - -
Echinacea tennesseensis - - 3 - - - - - - - -
Geranium gracile - - - - - - - 3 - - -
Helichrysum arenarium - - - 3 6 - - - - - -
Lotus corniculatus - - - - - - - - 1 - -
Phedimus selskinanus - - - 4 - 2 - - - - -
Polemonium vanbruntiae - - 14 4 - - - - - - -
Sempervivum montanum - - - 1 - - - - - - -
Solidago bicolor - - 2 - - - - - - - -
Succisa pratensis 3 - 5 18 - - - 1 - - -
Thymus serphyllum ssp
serphyllum - - 2 6 - - - - - - -
Thymus serpyllum - - 1 - - - - - - - -
Aegopodium podagraria - - - - - - 5
Nepeta sp - 9 40 2 2 - 1
Origanum vulgare - 60 12 - - - -
Achillea.millefolium - 15 - 2 1 - - - 2
Anaphalis.triplinervis - 11 - - 3 - - 1 -
Centaurea.jacea - 2 3 - - 1 - - -
Geum.boreale - - - - - - - - 1
Lathyrus.pratensis - - 9 - - - - - -
Sinapsis.arvensis - 3 - - - - - - -