For further information on D1c. Status of pollinating insects

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UK Biodiversity Indicators
2015
This documents supports
D1c. Status of pollinating Insects
Technical background document:
Gary D. Powney, Tom A. August, Colin A. Harrower, Charlotte Outhwaite, Nick J.B. Isaac
For further information on D1c. Status of pollinating insects
visit http://jncc.defra.gov.uk/page-6851
For further information on the UK Biodiversity Indicators visit
http://www.jncc.gov.uk/page-1824
D1c. Biodiversity and Ecosystem Services – Status of pollinating
insects – technical background document
Gary D. Powney, Tom A. August, Colin A. Harrower, Charlotte Outhwaite, Nick J. B. Isaac
INTRODUCTION
Pollination is a vital ecosystem service that benefits agricultural and horticultural production, and is
essential for maintaining wild flower biodiversity. By improving the yield, quality and resilience of
crops, insect pollination has been valued at £400 million per year to the UK economy (POST,
2010). 35 per cent of the World’s agricultural output, by volume, consists of 87 crop types that
benefit from pollination by animals (insects, birds and mammals), but because most of these crops
are not entirely dependent on animal pollination, the amount of production directly attributable to
animals is lower than this value (Klein et al. 2007). There is growing concern regarding the
population status of insect pollinators, and in turn the pollination service they provide (Potts et al.
2010; Garratt et al. 2014). As with most other areas of biodiversity, the main threats to pollinators
include habitat loss, environmental pollution, climate change and the spread of alien species (Klein
et al. 2007; Potts et al. 2010; Vanbergen & The Insect Pollinators Initiative 2013). The widespread
application of pesticides is also perceived as a major threat to pollinator diversity (Brittain et al.
2010). In order for governments to act upon these threats they need robust metrics on the
national-scale status of pollinators and pollination. Deriving such a metric has previously been
limited by the availability of suitable data and analytical techniques. With the increase in citizen
science, the availability of large-scale biological record data has increased (Silvertown 2009).
Such data are collected without a standardized survey protocol and therefore extracting reliable
trends from them can be difficult. However, with recent analytical advances it is now possible to
estimate reliable trends from such data (van Strien et al. 2013; Isaac et al. 2014).
METHODS
Data sources
Occurrence records of bee and hoverfly species within 1km grid squares in the UK were extracted
from the Bees, Wasps and Ants Recording Society (BWARS) and the Hoverfly Recording Scheme
biological records databases. The time-period used for the indicator was 1980 to 2010, as this
represents a core period of recording for these taxa in the UK. A lag in submission and collation of
records means that after 2010 the number of records per year tended to drop off. Bee species
were filtered (following expert guidance from BWARS) so that only species considered to be wild
pollinators were included. Species that had undergone taxonomic changes or had taxonomic
issues during the time frame of the indicator were excluded from the analysis. The final composite
indicator was based on 213 species of wild pollinator, see Appendix 1 for a list of species covered.
Generating species’ trends and the composite indicator
The data used to produce the indicator were not collected using a standardised protocol, but
instead are a collation of unstructured biological observations collected by a large network of
volunteer recorders. Such data tend to contain many forms of sampling bias and noise, making it
hard to detect genuine signals of change (Tingley & Beissinger 2009; Hassall & Thompson 2010;
Isaac et al. 2014). Recent studies have highlighted the value of Bayesian occupancy models for
estimating species occurrence in the presence of imperfect detection (van Strien et al. 2013; Isaac
et al. 2014). This approach uses two hierarchically coupled sub-models: an occupancy sub-model
(i.e. presence verses absence), and a detection sub-model (i.e. detection verses non-detection).
Together these sub-models estimate the conditional probability that a species is detected when
present. A Bayesian occupancy model was applied to the data for each species, following van
Strien et al. (2013) and Isaac et al. (2014). For each site-year combination the model estimates
1
presence or absence for the species in question given variation in detection probability: from this
the proportion of occupied sites (‘occupancy’) was estimated for each year. These annual
occupancy estimates were scaled so the value in 1980 was set to 100. The annual values of the
composite indicator were calculated as the arithmetic mean of scaled species-specific occupancy
estimates, and uncertainty in the species-specific annual occupancy estimates was propagated
through to the final indicator. A detailed description of the occupancy model, and the creation of
the composite indicator, can be found in the technical document on Bayesian indicator
development.
Species-specific trends
Species were grouped into one of five categories based on both their short-term (over the most
recent five years of data) and long-term (all years) mean annual change in occupancy (Table 1).
Table 1. Thresholds used to define individual species trends.
Category
Thresholds
Threshold – equivalent
Strong increase
Above +2.81% per annum
+100% over 25 years
Weak increase
Between +1.16% and +2.81% p.a.
+33% to +100% over 25 years
Stable
Between -1.14 % and +1.16% p.a.
-25% to +33% over 25 years
Weak decrease
Between -2.73% and -1.14% p.a.
-50% to -25% over 25 years
Strong decrease
Below -2.73% p.a.
-50% over 25 years
Asymmetric percentage change thresholds are used to define these classes as they refer to
proportional change, where a doubling of a species index (an increase of 100%) is
counterbalanced by a halving (a decrease of 50%).
The threshold values for each category were based on those of the wild bird indicator; whether an
individual species is increasing or decreasing has been decided by its rate of annual change over
the time period (long or short) of interest. If the rate of annual change would lead to an occupancy
increase or decrease of between 25 per cent and 49 per cent over 25 years, the species is said to
have shown a ‘weak increase’ or a ‘weak decline’ respectively. If the rate of annual change would
lead to a population increase or decrease of 50 per cent or more over 25 years, the species is said
to have shown a ‘strong increase’ or a ‘strong decline’ respectively. These thresholds are used in
the Birds of Conservation Concern status assessment for birds in the UK. See the technical
document on the Bayesian indicator development for further detail on the calculation of the
species-specific trends.
RESULTS
 The indicator shows the average relative change in distribution of 213 species of pollinator, as
measured by the number of 1km grid squares across the UK in which they were recorded –
this is referred to as the ‘occupancy index’.

Based on the unsmoothed data, there was an overall decrease in the indicator from 1987
onwards. In 2010, the occupancy indicator had declined to 68 per cent of the value in 1980.

Between 1980 and 2010, 27 per cent of pollinator species became more widespread (14 per
cent showed a strong increase), and 51 per cent became less widespread (36 per cent
showed a strong decrease). Similar patterns occurred between 2005 and 2010, but with a
greater proportion increasing and decreasing strongly.

As individual pollinator species become more or less widespread, the communities in any
given area become more or less diverse, and this may have implications for pollination as
2
more diverse communities are, in broad terms, more effective in pollinating a wide range of
crops and wild flowers.
The occupancy index was also produced for the bee (Figure 2) and hoverfly (Figure 3) species
separately. The wild bee index was relatively stable up to 2005, it then increased before a sharp
decline. In 2010, the wild bee index had declined to 62 per cent of the original value in 1980. The
occupancy index was declining for a greater number of wild bee species than were increasing over
both the long- and short-term. The sharp decline in the occupancy index in the three years up to
2010 of the indicator plot is reflected in the large (70 per cent) proportion of wild bee species
showing strong declines in occupancy over the short-term.
In contrast to the bees, the hoverfly index (Figure 3) shows a gradual decline from 1987 to 2007
onwards, reaching a low of 59 per cent of the value in 1980 in 2007. This trend was reversed in
the last three years to 2010, ending at 76 per cent. A greater proportion of hoverflies have
declined in occupancy over the long-term than have increased, but in the short-term 59 per cent of
hoverflies show strong increases in occupancy between 2005 and 2010.
The annual variability in the data is likely to be partly explained by annual variation in weather
conditions. Pollinators tend to respond positively to temperature but negatively to rainfall. Hot dry
periods are likely to have a greater negative impact on hoverflies than bees, as the exposed larvae
of hoverflies are more vulnerable to desiccation compared to the larvae of bees that tend to be
protected within an enclosed nest. The recent decline in bees from 2007–2010 is striking. A
number of pressures are known to impact on local pollinator behaviour, distribution and
abundance: weather, climate, land use change and pesticide use, for example (Vanbergen et al.
2014; Stanley et al. 2015). There was a decline in the indicator between 2007 and 2010. It is not
known whether this change in distribution is the start of a longer term trend or short term
fluctuation, and if the former, whether it is linked to one particular pressure or to a combination of
pressures. Despite the inter-annual variation, the overall trend for pollinators remains downward.
This indicator is a composite measure across 213 species (Appendix 1) and therefore covers a
large proportion of the pollinator species within the UK. Not all species contribute to all years (see
No. spp. column in Tables 2, 3 and 4 for the overall, bee and hoverfly indices respectively).
3
Figure 1. Change in the distribution of pollinators in the UK between 1980 and 2010. The shaded
region is the 90 per cent credible intervals of the annual occupancy estimates and represents the
uncertainty surrounding the annual estimates. The solid line illustrates a smoothed trend
estimated from a GAM fitted to the rescaled indicator values (dashed line). The proportion of
pollinator species in each trend category is based on mean change in occupancy over both a) the
long term (all years) and b) the short term (the most recent five years).
4
Table 2. Change in the distribution of pollinators in the UK between 1980 and 2010. The indicator
values per year are presented alongside their uncertainty (upper and lower 90 per cent credible
intervals), and the number of species contributing to the annual index value. The number of
species contributing has been split into those with an interpolated estimate and those with an
actual occupancy estimate.
Year
Indicator
Lower CI
Upper CI
1980
1981
1982
1983
1984
1985
1986
1987
1988
1989
1990
1991
1992
1993
1994
1995
1996
1997
1998
1999
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
2010
100
100
100
100.76
95.78
92.44
97.92
99.80
104.36
106.19
99.17
94.72
94.74
86.48
92.46
85.13
95.40
91.47
93.58
86.59
85.31
86.04
84.89
76.93
83.33
87.99
85.50
77.29
82.45
84.40
89.14
84.65
68.49
90.24
86.24
82.89
87.18
89.09
93.86
95.51
89.33
84.23
84.91
77.85
82.70
76.73
85.80
82.15
84.63
78.27
77.16
77.71
76.70
69.47
75.30
79.73
77.82
69.89
73.98
75.83
80.21
76.13
60.56
112.37
106.87
102.86
109.43
111.00
116.07
117.92
109.58
105.40
104.94
96.41
102.92
94.17
105.39
101.22
103.78
95.88
94.26
95.20
93.55
84.72
91.61
96.84
94.26
85.35
91.54
93.35
98.92
94.01
76.50
No. Sp.
Estimated
184
180
192
189
195
190
194
197
197
193
198
188
203
202
197
204
199
202
201
202
201
202
210
201
202
190
196
203
200
199
193
5
No. Sp.
Interpolated
0
4
12
20
15
21
18
16
16
20
15
25
10
11
16
9
14
11
12
11
12
11
3
12
11
23
17
10
12
10
0
Figure 2. Change in the distribution of pollinating wild bee species in the UK between 1980 and
2010. The shaded region is the 90 per cent credible intervals of the annual occupancy estimates
and represents the uncertainty surrounding the annual estimates. The solid line illustrates a
smoothed line from a GAM fitted to the rescaled indicator values (dashed line). The proportion of
pollinating bee species in each trend category is based on mean change in occupancy over both a)
the long term (all years) and b) the short term (the most recent five years).
6
Table 3. Change in the distribution of pollinating wild bee species in the UK between 1980 and
2010. The indicator values per year are presented alongside their uncertainty (upper and lower 90
per cent credible intervals), and the number of species contributing to the annual index value. The
number of species contributing has been split into those with an interpolated estimate and those
with an actual occupancy estimate.
Year
Indicator
Lower CI
Upper CI
1980
1981
1982
1983
1984
1985
1986
1987
1988
1989
1990
1991
1992
1993
1994
1995
1996
1997
1998
1999
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
2010
100
107.09
94.65
94.36
105.81
105.30
104.52
107.04
98.74
99.24
100.08
93.53
90.64
93.49
104.70
103.72
107.36
108.69
99.52
95.27
109.97
87.09
92.83
98.91
107.53
102.81
115.17
121.05
109.38
94.38
61.87
100
91.19
80.18
80.06
90.63
89.75
89.05
91.20
84.12
84.07
84.86
79.50
77.37
79.89
89.30
89.64
92.68
93.47
85.94
82.34
95.17
75.15
80.49
85.49
92.62
87.98
98.81
104.93
93.36
80.81
51.85
100
123.68
110.10
109.78
121.26
121.60
121.05
125.26
115.26
116.09
117.04
109.42
105.33
108.84
120.18
119.55
123.05
124.25
114.35
109.01
125.87
99.57
105.45
112.43
123.15
117.75
132.10
137.80
125.21
107.84
72.81
No. Sp.
Estimated
97
90
91
93
98
97
95
92
95
91
101
92
103
103
98
102
100
105
103
100
100
101
104
99
100
93
93
102
103
101
97
7
No. Sp.
Interpolated
0
7
10
9
4
6
9
13
10
14
4
13
2
2
7
3
5
0
2
5
5
4
1
6
5
12
12
3
2
4
0
Figure 3. Change in the distribution of hoverfly species in the UK between 1980 and 2010. The
shaded region is the 90 per cent credible intervals of the annual occupancy estimates and
represents the uncertainty surrounding the annual estimates. The solid line illustrates a smoothed
line from a GAM fitted to the rescaled indicator values (dashed line). The proportion of hoverfly
species in each trend category is based on mean change in occupancy over both a) the long term
(all years) and b) the short term (the most recent five years).
8
Table 4. Change in the distribution of hoverfly species in the UK between 1980 and 2010. The
indicator values per year are presented alongside their uncertainty (upper and lower 90 per cent
credible intervals), and the number of species contributing to the annual index value. The number
of species contributing has been split into those with an interpolated estimate and those with an
actual occupancy estimate.
Year
Indicator
Lower CI
Upper CI
1980
1981
1982
1983
1984
1985
1986
1987
1988
1989
1990
1991
1992
1993
1994
1995
1996
1997
1998
1999
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
2010
100
94.29
95.85
90.08
89.79
93.84
103.14
104.36
98.77
89.73
88.62
79.58
93.64
76.75
86.04
80.37
81.29
68.67
72.57
77.25
65.44
67.46
74.47
77.85
67.69
57.84
59.01
58.89
72.45
75.87
76.23
100
79.14
81.02
75.51
74.82
77.98
86.13
87.60
82.87
75.70
74.37
66.88
78.82
64.40
72.23
67.72
67.58
57.79
60.73
65.03
54.92
56.87
62.58
65.91
56.65
48.83
49.24
49.55
60.93
64.02
64.71
100
110.15
112.67
106.28
107.62
110.52
122.77
122.61
115.51
106.25
103.87
93.84
110.44
90.44
100.81
95.28
95.33
80.92
85.27
91.47
76.68
78.82
87.92
91.21
79.41
67.81
69.93
69.41
85.53
88.90
89.51
No. Sp.
Estimated
87
87
101
96
97
93
99
105
102
102
97
96
100
99
99
102
99
97
98
102
101
101
106
102
102
97
103
101
97
98
96
9
No. Sp.
Interpolated
0
0
2
11
11
15
9
3
6
6
11
12
8
9
9
6
9
11
10
6
7
7
2
6
6
11
5
7
10
6
0
FUTURE WORK
Bees and hoverflies are key pollinators in the UK and are presented here as an indicator of the
overall trend in pollinators. Other taxonomic groups (e.g. some butterflies and moths) can provide
pollination services but are not yet included in the indicator. Future updates of the pollinator
indicator could include trends from other taxonomic groups known to provide pollination services.
All species were given equal weight in the pollinator indicator – effectively the indicator assumes all
species are equally valuable in terms of their contribution to pollination services. However,
contribution to pollination is known to vary between species and is dependent on inherent life
history and ecological characteristics of the species, but also on total population abundance
(Breeze et al. 2011; Woodcock et al. 2013). Future work could examine the feasibility of weighting
the indicator to take account of this variation in species importance as pollinators.
REFERENCES
Breeze, T.D., Bailey, A.P., Balcombe, K.G. & Potts, S.G. (2011) Pollination services in the UK:
How important are honeybees? Agriculture, Ecosystems & Environment, 142, 137–143.
Brittain, C. A., Vighi, M., Bommarco, R., Settele, J. & Potts, S.G. (2010) Impacts of a pesticide on
pollinator species richness at different spatial scales. Basic and Applied Ecology, 11, 106–
115.
Garratt, M.P.D., Truslove, C.L., Coston, D.J., Evans, R.L., Moss, E.D., Dodson, C., Jenner, N.,
Biesmeijer, J.C. & Potts, S.G. (2014) Pollination deficits in UK apple orchards. Journal of
Pollination Ecology, 12, 9–14.
Hassall, C. & Thompson, D.J. (2010) Accounting for recorder effort in the detection of range shifts
from historical data. Methods in Ecology and Evolution, 1, 343–350.
Isaac, N.J.B., van Strien, A.J., August, T.A., de Zeeuw, M.P. & Roy, D.B. (2014) Statistics for
citizen science: extracting signals of change from noisy ecological data. Methods in Ecology
and Evolution, 5, 1052–1060.
Klein, A.-M., Vaissière, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A, Kremen, C. &
Tscharntke, T. (2007) Importance of pollinators in changing landscapes for world crops.
Proceedings. Biological sciences / The Royal Society, 274, 303–13.
POST (2010) Insect Pollination, London.
Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O. & Kunin, W.E. (2010)
Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution, 25,
345–53.
Silvertown, J. (2009) A new dawn for citizen science. Trends in Ecology & Evolution, 24, 467–471.
Stanley, D.A. Garratt, M.P.D., Wickens, J.B., Wickens, V.J., Potts, S.G. & Raine, N.E. (2015)
Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees.
Nature, online early.
Van Strien, A.J., van Swaay, C.A.M. & Termaat, T. (2013) Opportunistic citizen science data of
animal species produce reliable estimates of distribution trends if analysed with occupancy
models. Journal of Applied Ecology, 50, 1450–1458.
Tingley, M.W. & Beissinger, S.R. (2009) Detecting range shifts from historical species occurrences:
new perspectives on old data. Trends in Ecology & Evolution, 24, 625–633.
Vanbergen, A.J. & The Insect Pollinators Initiative. (2013) Threats to an ecosystem service:
pressures on pollinators. Frontiers in Ecology and the Environment, 11, 251–259.
Woodcock, B.A., Edwards, M., Redhead, J., Meek, W.R., Nuttall, P., Falk, S., Nowakowski, M. &
Pywell, R.F. (2013) Crop flower visitation by honeybees, bumblebees and solitary bees:
Behavioural differences and diversity responses to landscape. Agriculture, Ecosystems &
Environment, 171, 1–8.
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APPENDICES
Appendix 1. The list of 213 species included in the pollinator indicator.
Species
Anasimyia contracta
Anasimyia lineata
Anasimyia transfuga
Andrena apicata
Andrena argentata
Andrena barbilabris
Andrena bicolor
Andrena bimaculata
Andrena bucephala
Andrena carantonica
Andrena chrysosceles
Andrena cineraria
Andrena clarkella
Andrena dorsata
Andrena flavipes
Andrena florea
Andrena fucata
Andrena fulva
Andrena fuscipes
Andrena haemorrhoa
Andrena hattorfiana
Andrena helvola
Andrena humilis
Andrena labialis
Andrena lapponica
Andrena marginata
Andrena minutula
Andrena nigroaenea
Andrena nitida
Andrena nitidiuscula
Andrena ovatula
Andrena praecox
Andrena semilaevis
Andrena subopaca
Andrena synadelpha
Andrena tarsata
Andrena thoracica
Andrena tibialis
Andrena trimmerana
Anthidium manicatum
Anthophora bimaculata
Anthophora plumipes
Anthophora quadrimaculata
Arctophila superbiens
Baccha elongata
Bombus distinguendus
Bombus hortorum
Bombus humilis
Bombus jonellus
Bombus lapidarius
Bombus muscorum
Bombus pascuorum
Bombus pratorum
Bombus ruderarius
Bombus soroeensis
Bombus sylvarum
Bombus terrestris
Brachyopa scutellaris
Brachypalpoides lentus
Brachypalpus laphriformis
Caliprobola speciosa
Ceratina cyanea
Chalcosyrphus nemorum
Cheilosia albitarsis
Cheilosia antiqua
Cheilosia bergenstammi
Cheilosia fraterna
Cheilosia illustrata
Cheilosia impressa
Cheilosia longula
Cheilosia pagana
Cheilosia proxima
Cheilosia scutellata
Cheilosia soror
Cheilosia variabilis
Cheilosia vernalis
Cheilosia vulpina
Chelostoma campanularum
Chelostoma florisomne
Chrysogaster cemiteriorum
Chrysogaster solstitialis
Chrysogaster virescens
Chrysotoxum arcuatum
Chrysotoxum bicinctum
Chrysotoxum cautum
Chrysotoxum elegans
Chrysotoxum festivum
Colletes cunicularius
Colletes daviesanus
11
Colletes fodiens
Colletes halophilus
Colletes marginatus
Colletes similis
Colletes succinctus
Criorhina asilica
Criorhina berberina
Criorhina floccosa
Criorhina ranunculi
Dasypoda hirtipes
Dasysyrphus albostriatus
Dasysyrphus tricinctus
Dasysyrphus venustus
Didea fasciata
Epistrophe eligans
Epistrophe grossulariae
Episyrphus balteatus
Eristalinus aeneus
Eristalinus sepulchralis
Eristalis abusivus
Eristalis arbustorum
Eristalis horticola
Eristalis interruptus
Eristalis intricarius
Eristalis pertinax
Eristalis rupium
Eristalis tenax
Eucera longicornis
Eumerus funeralis
Eumerus ornatus
Eumerus strigatus
Eupeodes corollae
Eupeodes latifasciatus
Eupeodes luniger
Halictus confusus
Halictus rubicundus
Halictus tumulorum
Heriades truncorum
Lasioglossum albipes
Lasioglossum calceatum
Lasioglossum cupromicans
Lasioglossum fratellum
Lasioglossum fulvicorne
Lasioglossum laevigatum
Lasioglossum lativentre
Lasioglossum leucopus
Lasioglossum leucozonium
Lasioglossum malachurum
Lasioglossum minutissimum
Lasioglossum morio
Lasioglossum parvulum
Lasioglossum pauxillum
Lasioglossum prasinum
Lasioglossum
punctatissimum
Lasioglossum puncticolle
Lasioglossum rufitarse
Lasioglossum
smeathmanellum
Lasioglossum villosulum
Lasioglossum zonulum
Lejogaster metallina
Leucozona glaucia
Leucozona laternaria
Leucozona lucorum
Macropis europaea
Megachile leachella
Megachile maritima
Megachile versicolor
Megachile willughbiella
Melangyna arctica
Melangyna lasiophthalma
Melanogaster hirtella
Melanostoma mellinum
Melanostoma scalare
Meliscaeva auricollis
Meliscaeva cinctella
Melitta haemorrhoidalis
Melitta leporina
Melitta tricincta
Merodon equestris
Microdon analis
Myathropa florea
Neoascia geniculata
Neoascia interrupta
Neoascia meticulosa
Neoascia obliqua
Neoascia podagrica
Neoascia tenur
Orthonevra geniculata
Orthonevra nobilis
Osmia aurulenta
Osmia bicolor
Osmia bicornis
Osmia caerulescens
Osmia leaiana
Osmia spinulosa
Panurgus banksianus
Panurgus calcaratus
Paragus haemorrhous
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Parasyrphus punctulatus
Parasyrphus vittiger
Parhelophilus frutetorum
Parhelophilus versicolor
Pelecocera tricincta
Pipiza noctiluca
Pipizella viduata
Platycheirus albimanus
Platycheirus angustatus
Platycheirus clypeatus
Platycheirus fulviventris
Platycheirus granditarsus
Platycheirus manicatus
Platycheirus peltatus
Platycheirus rosarum
Platycheirus scambus
Platycheirus tarsalis
Portevinia maculata
Rhingia campestris
Riponnensia splendens
Scaeva pyrastri
Sericomyia lappona
Sericomyia silentis
Sphaerophoria batava
Sphaerophoria interrupta
Sphaerophoria philanthus
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