Distribution of wild bee (Hymenoptera: Anthophila) and hoverfly (Diptera: Syrphidae) communities within farms undergoing ecological transition

Abstract

Background

In Havelange (Belgium), two farms are experiencing an ecological transition. We aimed to evaluate the impact of their agricultural activities on insect pollinator communities. This article depicts the situation at the very early stage of the farm transition. This study supports the fact that the maintenance of farm-level natural habitats provides environmental benefits, such as the conservation of two important pollinator communities: wild bees and hoverflies.

New information

Over two years (2018-2019), by using nets and coloured pan-traps, we collected 6301 bee and hoverfly specimens amongst contrasting habitats within two farmsteads undergoing ecological transition in Havelange (Belgium). We reported 101 bee species and morphospecies from 15 genera within six families and 31 hoverfly species and morphospecies from 18 genera. This list reinforces the national pollinator database by providing new distribution data for extinction-threatened species, such as Andrena schencki Morawitz 1866, Bombus campestris (Panzer 1801), Eucera longicornis (L.) and Halictus maculatus Smith 1848 or for data deficient species, such as A. semilaevis Pérez 1903, A. fulvata (Müller 1766), A. trimmerana (Kirby 1802) and Hylaeus brevicornis Nylander 1852.

Introduction

Nowadays, the greatest challenge faced by agriculture is to provide food for everyone, without altering the agro-biodiversity and the related ecosystem services (Dendoncker et al. 2018, Duru et al. 2015, Muller et al. 2017). Indeed, the worldwide intensification of agricultural systems has led to tragic biodiversity losses. During the last decades, many studies showed a strong impoverishment of insect pollinators in intensively-farmed landscapes. The depletion of these pollinators - and with them the ecosystem service of pollination - could have severe negative impacts on farmers and consumers welfare (Biesmeijer et al. 2006, Carvalheiro et al. 2013, Potts et al. 2016, Woodcock et al. 2019). The decrease in floral resources and the degradation of nesting sites is one of the main factors of decline (Goulson et al. 2015, Potts et al. 2010, Sánchez-Bayo and Wyckhuys 2019). In Belgium, in 2010, the insect-pollination was valuated at around 250 M€ (Jacquemin et al. 2017).

Agroecological farming systems grow crops on small areas, alongside heterogeneous habitats and complex arrangements (e.g. subdivision of plots by hedgerows, fallow areas, flower meadows etc.) that provide shelters and abundant food resources to beneficial insects (Power et al. 2012). Diversified habitats at the plot or at the farm spatial scale help to control pests, weeds and phytopathogens and provide other regulatory ecosystem services, such as pollination and preservation of nutrients and water in soils (Hatt et al. 2018).

The bee community (Hymenoptera: Anthophila) is amongst the most efficient pollinator groups in temperate agriculture landscapes. In Belgium, the latest inventory recorded 403 bee species, which represents almost one quarter of the European bee diversity (Drossart et al. 2019, Rasmont et al. 2017). Their morphological and behavioural traits co-evolved with flowering plants, allowing them to secure pollination (Michener 2007). The richness of bee morphologies, specialisation in pollen and nectar diets and sizes greatly supports an increase in yields in small-scale agricultural farms (Garibaldi et al. 2016). Since the end of the 19th Century, Belgium has had great expertise in the monitoring of bees. Since the 70s, this survey has particularly accelerated through mapping, preservation and management of historical collections, taxonomic keys and revision of the Belgian fauna (Drossart et al. 2019).

Besides, the Diptera order represents one of the largest and most diverse groups in the pollinator community (Skevington and Dang 2002). Too often neglected, dipteran pollinators ensure the reproduction of many flowering plants (Rader et al. 2015, Ssymank et al. 2008). By consuming pollen and nectar, adult hoverflies (Syrphidae) play a pivotal role in the pollen transmission of over 70% of wildflowers (Doyle et al. 2020, Inouye et al. 2015). Hoverfly larvae exhibit a wide variety of feeding habits, including phytophagy, zoophagy, aphidophagy, saprophagy and mycophagy (Sommaggio 1999). As they cover a large spectrum of microhabitats (e.g. roots layer, herbs layer, dead wood, ponds...) (Speight et al. 2000), hoverfly larvae can be used as biological indicators to evaluate the conservation status of ecosystems (Burgio and Sommaggio 2007, Sommaggio 1999). The widespread distribution of syrphids in temperate landscapes and the availability of excellent taxonomic keys for European species identification are also characteristics that promote syrphids as bio-indicators. Syrphids are very interesting organisms for studying the effects of agriculture intensification on biodiversity because they are particularly mobile (Gao et al. 2020). Moreover, hoverfly communities are strongly affected by the standardisation in landscape structures and by intensive agricultural practices (Dormann et al. 2007). In Belgium, 357 syrphid species were recorded according to the latest survey (Frank Van de Meutter, personal communication).

The impacts of agroecological transition on pollinator communities remain poorly documented. Such evaluation needs standardised and fine-scaled sampling efforts. Thus, the goal of this study is to provide a local and robust inventory of the bee and hoverfly fauna in two farms undergoing ecological transtion in Havelange County (Belgium). The general impacts of farm-scale landscape diversification on bee and hoverfly fauna are discussed. In future research, such inventory will allow an assessment of the impacts of regenerating agricultural landscapes on the pollinator community structure. Moreover, this study feeds in new records and new locations for the national repository of the wild bee and hoverfly communities, owned by the Laboratory of Functional and Evolutionary Entomology (Prof. Frédéric Francis), Gembloux Agro-Bio Tech and the Laboratory of Zoology (Prof. Pierre Rasmont), University of Mons.

Materials and methods

Study site and habitats description

The study was conducted in two neighbouring agricultural sites, located in the Municipality of Havelange (Fig. 1A): the Froidefontaine and Emeville farmsteads (Fig. 1B). They are located at 2 km away from each other, in the geological region of Condroz, in Wallonia (Belgium), as defined by Dufrene and Legendre (1991).

Figure 1.

A. Location of Havelange Municipality in Belgium; B. The location of the two farmsteads in Havelange.

The Froidefontaine farmstead

The Froidefontaine farm (50°23'6''N, 5°8'34.799''E) covers an area of 55 hectares, with a mosaic of varied habitats. One of the management objectives is diversifying the land use by conserving natural areas (mesophilic and wet meadows, limestone slopes, ponds...) and hosting different farming projects in a collaborative way on farming areas. Thus, the farm aims at creating a rich and welcoming landscape for diversity, including biodiversity.

Within the farm, we defined four adjacent habitats (Fig. 2A; Table 1) covering about 10 ha each: a parcel of crops (GC) including a third of the surface with vegetable crops (GC1), a meadow zone (PAT), a young apple orchard (VER) and a wetland (ZH). The parcels were surrounded by hedges principally composed of hornbeam, elderberry, dogwood, hawthorn, maple and European charcoal.

Figure 2.

A. Froidefontaine farmstead map. GC, PAT, VER and ZH correspond to the sampled parcels, whose details are given in Table 1. Each numbered red dot corresponds to the position of a trio of coloured (white, yellow, blue) pantraps; B. Emeville farmstead map. PAV, FRE, EPI and DIK correspond to the sampled parcels, whose details are given in Table 1. Each numbered red dot corresponds to the position of a trio of coloured (white, yellow, blue) pantraps. BF1, BF2 and BF3 correspond to the sampled flower strips. Each blue or green numbered dot corresponds to the position of a trio of coloured (white, yellow, blue) pantraps for the "feeder" flower patch or the "pollinator" flower patch, respectively.

Table 1.

Habitats description of the sampled parcels and flower strips.

Parcel Name	Parcel Code	Farmstead	Sampling Year	Parcel description
Pavillon	PAV	Emeville	2019	Pastures combined with apple orchard. Flowering fields under young apple trees (many rustic varieties). There are dandelions, shamrocks, meadow cardamine etc. This parcel is mainly surrounded by woods and hedges. A herd of Angus was grazing most of the time, from May.
Frere	FRE	Emeville	2019	Mainly alfalfa, some other fabaceae (red and white clovers). There are dandelions and speedwells at the start of the season. A hedge borders the parcel to the East. A flowery strip runs on the South face (BF 2; Fig. 2B). Harvested during the month of June and after recovery in mid-July.
Epicurien	EPI	Emeville	2019	Divided parcel along the East to the West, composed equally of small and large spelts. Hedgerows border the parcel to the East face.
Dikkekip	DIK	Emeville	2019	The parcel is at the bottom of the slope. Left without plant cover until May, when pea crop was sown. There are some rumex and a lot of chamomile too.
Flower strips	BF	Emeville	2019	Composed of a mix of cover crops and flower crops. See the site description for more details.
Crops	GC	Froidefontaine	2018-2019	Vegetable crops occupy a third of the surface of the cultivated parcel.
Pasture	PAT	Froidefontaine	2018-2019	A hay meadow composed of Poaceae, clovers, dandelions etc. Bordered by hedgerows, except to the South face (sheep fence).
Orchard	VER	Froidefontaine	2018-2019	Flowering fields under young apple trees (many rustic varieties). This parcel is grazed by sheep in April and May. The parcel is bordered by hedges, except to its North face (sheep fence).
Wetland	ZH	Froidefontaine	2018-2019	The vegetation is mainly composed of plants from wetlands: buttercups, nettles, thistles, cradles etc. The meadow is bordered by a brook to the South and a hedge to the North.

The Emeville farmstead

The Emeville farm (50°23'2.4''N 5°10'1.199''E) covers an area of just over 40 ha. In 2016, the farm managers and a committee of various partners converted conventionally-managed fields to agroecological farming methods. To allow a complexification of the ecological network and creating an agricultural landscape enriched with biodiversity, the first actions were: laying hedges and grass strips; planting rustic apple trees; breeding Angus cattle (Bos taurus taurus L.) in an orchard; alternating temporary and permanent meadows; arranging of flowered grass strips; using no pesticides and amendments.

The sampling zone covered 15 ha and was divided into seven parcels (Fig. 2B; Table 1), which included six parcels of crops separated by flower strips and one parcel of orchard. Each flower strip (BF1, BF2 and BF3; Fig. 2B) was composed of three plant mix sequences, including a combination of one "feeder" flower patch (BFV) and one "pollinator" flower patch (BFB), separated by the cover crop patch. The cover crop patch was composed of a grass mix of Festuca arundinacea Schreb 1771 and Dactylis glomerata L. 1753 sown at 20 kg/ha. The feeder flower patch was composed of a mix of 40% of clover (Trifolium pratense L. 1753) and 60% of alfalfa (Medicago sativa L. 1753) sown at 25 kg/ha. In order to match Agri-Environmental and Climate Measures (AECM) specifications, the pollinator flower patch was sown at 30 kg/ha and was composed of a mix including 85% of grasses (Poa pratensis L., 1753 Festuca rubra L. 1753 and Agrostis capillaris L. 1753), 2% of leguminous species (Lotus corniculatus L. 1753, Medicago lupulina L. 1753 and T. pratense), 3% of annual flower (Papaver rhoeas L. 1753, Glebionis segetum Fourr. 1869 and Cyanus segetum Hill 1762) and 10% of other flower species (Achillea millefolium L. 1753, Centaurea jacea L. 1753, Daucus carota L. 1753, Leucanthemum vulgare Lam. 1779, Malva moschata L. 1753, Silene latifolia Poir. 1789, Melilotus sp. Mill. 1754, Knautia arvensis Coult. 1828 and Echium vulgare L. 1753).

Collection methods

To assess wild bee and hoverfly diversity, we conducted standardised sampling methods by combining coloured pantraps and netting transects (Földesi and Kovács-Hostyánszki 2014, Westphal et al. 2008, Grundel et al. 2011). Sampling was performed in 2018 and 2019, from April to July. At each collection site (Fig. 2A & B), we positioned a triplet of pantraps (FLORA model with a diameter of 26.5 cm, RINGOT, France) coloured with UV reflecting sprays in white, blue and yellow (ROCOL top tracer model, UK). The pantraps were set-up in line and spaced 3 to 5 metres apart, in order to avoid the attraction coverage bias and to reach the same probabilities of insect capture between the pantraps (Amy et al. 2018, Droege et al. 2010). The pantrap triplets were separated by a minimum of 20 metres, in order to cover each parcel as homogeneously as possible (Carboni and Lebuhn 2003, Eeraerts et al. 2017). Each pantrap was filled with odourless and colourless soapy water every two weeks during one day (from 9:00 AM to 5:00 PM). Every two weeks, we also conducted variable transects with an insect net for one hour in the morning and one hour in the afternoon, for each habitat in Froidefontaine and each flower strip in Emeville (Table 1; Fig. 2). We selected the sampling dates according to the following climatic conditions: temperature higher than 7°C, calm wind (< 12 km/h) and sunny and cloudless day (Westphal et al. 2008). We stocked insects in 70% ethanol for their conservation.

We followed the protocol of Mouret et al. (2007) to prepare, pin and label our collected specimens.

In 2019, we decided to let the yellow pantraps to be continuously activated from mid-May to the end of July with sampling every 10 days to maximise the capture of syrphids and considering that hoverflies have a predilection for the yellow colour (An et al. 2018, Lunau et al. 2018, Wäckers and van Rijn 2012).

Species identification

Bee specimens were identified at the species level following identification keys of Pauly (2019) for Halictidae, Patiny and Terzo (2010) for Andrenidae and Falk (2015) for the other bee families (Apidae, Colletidae, Megachilidae and Melittidae). All Halicitidae and Andrenidae specimens were confirmed by Alain Pauly (Royal Belgian Institute of Natural Sciences) and Thomas James Wood (University of Mons), respectively. Other bee specimens were confirmed by the reference collections of Gembloux Agro-Bio Tech. Hoverfly specimens were identified at the species level using the identification key of Verlinden (1994). The specimens were then confirmed by Frédéric Francis (University of Liège) and the reference collections of Gembloux Agro-Bio Tech. We applied Belgian Red List of bees for the conservation status of identified species (Drossart et al. 2019).

Historical data of Havelange Municipality

Thanks to Data Fauna-Flora v.5.1 software (Barbier and Rasmont 2015), we queried the database of Belgian wild bees, on 26 June 2020, for the historical diversity of wild bees in the Havelange Municipality. The selected geographical quadrat was encompassed within latitude from 50°21'14.4''N to 50°24'46.8''N and in longitude from 5°7'12''E to 5°19'26.399''E. The syrphid historical data were not available for Havelange Municipality.

Statistical analysis

We conducted one-way ANOVA tests to compare species richness and abundance of bee and hoverfly fauna between sampled parcels of Froidefontaine and Emeville farmsteads, separately. We also validated normal distribution of residuals of each ANOVA test. Subsequently, Tukey’s post-hoc tests were used to compare each parcel pair. We separated the flower strips of Emeville farm from the parcel comparisons because they were not sampled with the same effort as those of the sampled parcels. We compared the species richness and abundance of bee and hoverfly fauna between the feeder flower patch (BFV; Fig. 2B) and the pollinator flower patch (BFB; Fig. 2B) using the Student t-test. All statistical analysis were performed using R 4.0.2 (R Development Core Team 2020) and the resulting graphs were built using ggplot2 and ggpubr packages (Kassambara 2020, Wickham 2016).

Checklists

Bee Checklist

Andrena (Ptilandrena) angustior

(Kirby 1802)

26086597-4FB4-571F-9533-CDBA94D99EB6

Ecological interactions

Feeds on

Polylectic

Conservation status

Near Threatened

Notes

Table 2

Table 2.

Abundance of each pollinator species according to the habitat of its collection. The habitat details are given in Table 1.

	BF	DIK	EPI	FRE	GC	PAT	PAV	VER	ZH	Total (%)
Bee	285	256	277	244	439	1145	349	685	623	4303 (100)
Andrena angustior		1	2		13	17	1	10	13	57 (1.32)
Andrena apicata		1								1 (0.02)
Andrena bicolor		1		1	7	1		4	10	24 (0.56)
Andrena carantonica				1		5		4	3	13 (0.3)
Andrena chrysosceles		2	5	5	1	2	6	1	4	26 (0.6)
Andrena cineraria		9	25	42	117	409	42	90	109	843 (19.59)
Andrena dorsata		6	4	7		6	6	12	5	46 (1.07)
Andrena flavipes	4	15	16	10	57	54	20	73	63	312 (7.25)
Andrena fulva		1	1	3	4	7	7	8	1	32 (0.74)
Andrena fulvata		6	10	1	7	3	6	9	6	48 (1.12)
Andrena gravida		2	3	3	8	48	4	23	15	106 (2.46)
Andrena haemorrhoa	1	7	5	19	32	145	24	121	107	461 (10.71)
Andrena humilis			1		2	1	1		2	7 (0.16)
Andrena labialis	2									2 (0.05)
Andrena labiata			1					2		3 (0.07)
Andrena minutula	1	3	2	1	2	1	2	3		15 (0.35)
Andrena mitis		2								2 (0.05)
Andrena nigroaenea		5	3	2	13	9	3	6	13	54 (1.25)
Andrena nitida		4	10	8	11	60	24	40	20	177 (4.11)
Andrena ovatula					3			1		4 (0.09)
Andrena praecox									3	3 (0.07)
Andrena schencki								1		1 (0.02)
Andrena semilaevis							1			1 (0.02)
Andrena subopaca	2		1			1			1	5 (0.12)
Andrena trimmerana					1	1				2 (0.05)
Andrena vaga		2	2	3		4	3	1		15 (0.35)
Andrena wilkella	8							6	1	15 (0.35)
Apis mellifera	114	32	33	35	57	63	128	54	41	557 (12.94)
Bombus campestris									1	1 (0.02)
Bombus hortorum	1		2	2		4			1	10 (0.23)
Bombus hypnorum						3			3	6 (0.14)
Bombus lapidarius	35	1	4	5	4	73	7	29	50	208 (4.83)
Bombus pascuorum	58		1	13	7	26	1	7	20	133 (3.09)
Bombus pratorum		1		2	2	9	1	3	4	22 (0.51)
Bombus terrestris	35	2	2	12	19	17	8	12	18	125 (2.9)
Bombus vestalis								1		1 (0.02)
Chelostoma rapunculi						1				1 (0.02)
Colletes cunicularius				1				1		2 (0.05)
Colletes daviesanus					1					1 (0.02)
Eucera longicornis								1		1 (0.02)
Halictus maculatus			1		1	1		3	3	9 (0.21)
Halictus rubicundus						2	1		2	5 (0.12)
Halictus scabiosae								2	2	4 (0.09)
Hylaeus brevicornis								2		2 (0.05)
Hylaeus communis				1			1			2 (0.05)
Hylaeus hyalinatus								1		1 (0.02)
Hylaeus signatus	1									1 (0.02)
Lasioglossum calceatum		38	43	14	9	29	11	24	16	184 (4.28)
Lasioglossum fulvicorne		2					2			4 (0.09)
Lasioglossum laticeps		1	4	1	4	1	1	2	1	15 (0.35)
Lasioglossum lativentre	5	1	16		2	17	4	28	1	74 (1.72)
Lasioglossum leucopus		3	1		1					5 (0.12)
Lasioglossum leucozonium		4	3	1	1	4	1	5	2	21 (0.49)
Lasioglossum malachurum			1		1		1		1	4 (0.09)
Lasioglossum morio		8	1			3	1	2	2	17 (0.4)
Lasioglossum pauxillum	6	93	62	41	19	24	13	16	20	294 (6.83)
Lasioglossum punctatissimum			1	1			1	1	1	5 (0.12)
Lasioglossum sexstrigatum			1							1 (0.02)
Lasioglossum sp.					1		1	2		4 (0.09)
Lasioglossum villosulum		1	1		4	2	1	3		12 (0.28)
Lasioglossum zonulum		1	1	3	4	4	1	2	4	20 (0.46)
Megachile ericetorum	1								1	2 (0.05)
Megachile willughbiella	1							1		2 (0.05)
Melitta tricincta								1		1 (0.02)
Nomada bifasciata						2	1	2	1	6 (0.14)
Nomada fabriciana						1		1	1	3 (0.07)
Nomada flava			1			2		2	2	7 (0.16)
Nomada flavoguttata						1		1	3	5 (0.12)
Nomada fucata	1		2		4	7	5	11	1	31 (0.72)
Nomada fulvicornis			1	2			1			4 (0.09)
Nomada goodeniana			2		5	24	2	13	7	53 (1.23)
Nomada lathburiana					1	9	1	2	2	15 (0.35)
Nomada leucophthalma						2		1	1	4 (0.09)
Nomada marshamella									2	2 (0.05)
Nomada panzeri						2			3	5 (0.12)
Nomada ruficornis			1		1	21		13	17	53 (1.23)
Nomada signata						2		1	1	4 (0.09)
Nomada succincta						1				1 (0.02)
Nomada zonata						1	1	2	1	5 (0.12)
Osmia bicolor									1	1 (0.02)
Osmia bicornis					3	6	1	2	5	17 (0.4)
Osmia cornuta						1		2		3 (0.07)
Osmia leaiana							1	1		2 (0.05)
Osmia leucomelana	1				1			2		4 (0.09)
Osmia tridentata	1									1 (0.02)
Seladonia tumulorum	7	1		3	4	3		6	2	26 (0.6)
Sphecodes ephippius			1	1	3	3		3	1	12 (0.28)
Sphecodes ferruginatus							1			1 (0.02)
Sphecodes gibbus									1	1 (0.02)
Sphecodes monilicornis								1	1	2 (0.05)
Sphecodes puncticeps					1					1 (0.02)
Sphecodes sp.					1			1		2 (0.05)
Hoverfly	907	228	26	91	266	91	86	72	231	1998 (100)
Cheilosia sp.	2				1	15	1	1	55	75 (3.75)
Episyrphus balteatus	124	10	1	36	6	3	5	10	14	209 (10.46)
Eristalis arbustorum	60	10	3	1	5	2	2	5	15	103 (5.16)
Eristalis nemorum	3									3 (0.15)
Eristalis pertinax								1	5	6 (0.3)
Eristalis sepulchralis	1									1 (0.05)
Eristalis similis								1		1 (0.05)
Eristalis tenax	186	13	4	8	37	24	43	4	23	342 (17.12)
Eupeodes luniger	6	9	1	1	3	1	1	1	2	25 (1.25)
Ferdinandea cuprea							2			2 (0.1)
Helophilus trivittatus						1			2	3 (0.15)
Melanostoma mellinum	53	17		13	13	1	3	1	1	102 (5.1)
Metasyrphus corollae	7	15		3	1	1	1	2		30 (1.5)
Metasyrphus latifasciatus						2			4	6 (0.3)
Myathropa florea				1					3	4 (0.2)
Platycheirus albimanus	1	1			1					3 (0.15)
Platycheirus clypeatus									1	1 (0.05)
Platycheirus immarginatus						1		1		2 (0.1)
Platycheirus peltatus						3	1		2	6 (0.3)
Platycheirus scambus					2					2 (0.1)
Rhingia campestris						1				1 (0.05)
Scaeva pyrastri	19	5		3	4	3	1		3	38 (1.9)
Sphaerophoria scripta	401	148	13	23	174	29	17	40	84	929 (46.5)
Syritta pipiens	37		1		13			1	4	56 (2.8)
Syrphus ribesii	3		3	1	3	3	9	1	10	33 (1.65)
Syrphus vitripennis	1				3	1		1	2	8 (0.4)
Volucella bombylans								1		1 (0.05)
Volucella pellucens								1		1 (0.05)
Xanthogramma pedissequum				1					1	2 (0.1)
Xylota segnis	2									2 (0.1)
Xylota sylvarum	1									1 (0.05)
Total of specimens	1192	484	303	335	705	1236	435	757	854	6301

Andrena (Andrena) apicata

Smith 1847

773B4C42-F312-55F1-A798-F2BB489EB06E

Ecological interactions

Feeds on

Oligolectic on Salicaceae

Conservation status

Least Concern

Notes

Table 2

Andrena (Euandrena) bicolor

Fabricius 1775

AD109654-7ACA-53D3-BDCF-F9CDDEC27AC1

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Andrena (Hoplandrena) carantonica

Pérez 1902

87EB1626-D85F-55A6-B7AA-7F30B5637E80

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Andrena (Notandrena) chrysosceles

(Kirby 1802)

6E930963-BB1F-514D-9246-C4CD3A7DC3E5

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Andrena (Melandrena) cineraria

(Linnaeus 1758)

BB080AAB-19F3-50ED-B714-78A2D50B0F24

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Andrena (Andrena) clarkella

(Kirby 1802)

81C96F69-0E63-5D14-8FCE-516BA09F275E

Ecological interactions

Feeds on

Oligolectic on Salicaceae

Conservation status

Least Concern

Notes

Table S1 (Historical data)

Andrena (Simandrena) dorsata

(Kirby 1802)

ED29E1DB-B7AC-5ADC-9E94-9CDE6778C581

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Andrena (Zonandrena) flavipes

Panzer 1799

C4A9DB13-2481-53A0-9C3D-7BB49EB4A3D7

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Andrena (Andrena) fulva

(Müller 1776)

2CEB847B-83E8-5DDF-B29C-2CF8B55F2D79

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2; Table S1 (Historical data)

Andrena (Ptilandrena) fulvata

(Müller 1766)

21981822-F1F5-510D-AFE6-D515BBB463E5

Ecological interactions

Feeds on

Polylectic

Conservation status

Non Applicable

Notes

Table 2

Andrena (Zonandrena) gravida

Imhoff 1832

71CD37F6-AFEF-541A-BE6B-3DF24158A9C7

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Andrena (Trachandrena) haemorrhoa

(Fabricius 1781)

3F1DE46C-C113-5073-A9DF-00F991A6FF82

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Andrena (Chlorandrena) humilis

Imhoff 1832

4BC96DB5-2547-54FA-AC59-5796792FD9F5

Ecological interactions

Feeds on

Oligolectic on Asteraceae

Conservation status

Least Concern

Notes

Table 2

Andrena (Holandrena) labialis

(Kirby 1802)

3F6E04EF-30BC-54E6-A83F-0DC065416A8B

Ecological interactions

Feeds on

Oligolectic on Fabaceae

Conservation status

Near Threatened

Notes

Table 2

Andrena (Poecilandrena) labiata

Fabricius 1781

7FD6F4D7-F0CF-565D-8C12-76B8B4C584B2

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Andrena (Micrandrena) minutula

(Kirby 1802)

0757EFDD-4FFA-5AD3-B208-DDDA0C54DD6A

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Andrena (Andrena) mitis

Schmiedeknecht 1883

EFA73238-883A-51FA-B945-03D97C2A5D10

Ecological interactions

Feeds on

Oligolectic on Salicaceae

Conservation status

Least Concern

Notes

Table 2

Andrena (Melandrena) nigroaenea

(Kirby 1802)

381F5A71-18CB-54ED-80A9-03EEF9D0F6B6

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Andrena (Melandrena) nitida

(Müller 1776)

B7C2E8AB-ECC3-5B86-82A0-D23A612F88C1

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Andrena (Taeniandrena) ovatula

(Kirby 1802)

9605C2AF-A8A2-5C8B-9065-8140A0BD9C3F

Ecological interactions

Feeds on

Polylectic

Conservation status

Near Threatened

Notes

Table 2

Andrena (Andrena) praecox

(Scopoli 1763)

623D6A91-EABB-51EF-AA08-B0CF915AB796

Ecological interactions

Feeds on

Oligolectic on Salicaceae

Conservation status

Least Concern

Notes

Table 2

Andrena (Opandrena) schencki

Morawitz 1866

ADB6FEBD-15C2-53D5-911A-882297C0CBA2

Ecological interactions

Feeds on

Polylectic

Conservation status

Endangered

Notes

Table 2

Andrena (Micrandrena) semilaevis

Pérez 1903

894446EE-D3EC-5DC0-B6DB-607AAAF27820

Ecological interactions

Feeds on

Polylectic

Conservation status

Data Deficient

Notes

Table 2

Andrena (Micrandrena) subopaca

Nylander 1848

05B5B4F5-9688-5D29-B9D4-A4851FD3ED1B

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Andrena (Hoplandrena) trimmerana

(Kirby 1802)

5CBA98DF-9E49-577B-9EB7-5F0D6571780C

Ecological interactions

Feeds on

Polylectic

Conservation status

Data Deficient

Notes

Table 2

Andrena (Melandrena) vaga

Panzer 1799

0167CEF8-A916-5A3E-92F9-50DFACF19429

Ecological interactions

Feeds on

Oligolectic on Salicaceae

Conservation status

Least Concern

Notes

Table 2

Andrena (Taeniandrena) wilkella

(Kirby 1802)

0887060D-D9C4-5E04-8D23-A300E971654F

Ecological interactions

Feeds on

Polylectic

Conservation status

Near Threatened

Notes

Table 2

Anthophora plumipes

(Pallas 1772)

AC896C77-7C6F-5B5F-9E52-93ABED2376D4

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table S1 (Historical data)

Apis mellifera

Linnaeus 1758

05A46C7F-94FE-5EC9-9656-C7D8040B79B1

Ecological interactions

Feeds on

Polylectic

Conservation status

Data Deficient

Notes

Table 2

Bombus (Ashtonipsithyrus) bohemicus

Seidl 1837

E9BB06B7-2300-5E66-8602-C71D1EBFCDB0

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Near Threatened

Notes

Table S1 (Historical data)

Bombus (Psithyrus) campestris

(Panzer 1801)

25C5E9BD-094C-5215-BE6C-BBDD2CFF0872

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Vulnerable

Notes

Table 2

Bombus (Bombus) cryptarum

(Fabricius 1775)

A15CB08A-5268-5E21-A817-536C1D11A458

Ecological interactions

Feeds on

Polylectic

Conservation status

Endangered

Notes

Table S1 (Historical data)

Bombus (Megabombus) hortorum

(Linnaeus 1761)

EC9C9D09-E1D7-5784-990F-B7A98849516C

Ecological interactions

Feeds on

Polylectic

Conservation status

Near Threatened

Notes

Table 2; Table S1 (Historical data)

Bombus (Pyrobombus) hypnorum

(Linnaeus 1758)

FC891598-8EAA-5AE9-8E39-07F7811A92A1

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Bombus (Melanobombus) lapidarius

(Linnaeus 1758)

FD78CC14-D995-5950-9500-12B22441EC65

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2; Table S1 (Historical data)

Bombus (Bombus) lucorum

(Linnaeus 1761)

ED1342B1-7762-5A13-B217-22BE78486F58

Ecological interactions

Feeds on

Polylectic

Conservation status

Near Threatened

Notes

Table S1 (Historical data)

Bombus (Thoracobombus) pascuorum

(Scopoli 1793)

DF277625-98E5-53C1-83DD-FE023E20062E

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2; Table S1 (Historical data)

Bombus (Pyrobombus) pratorum

(Linnaeus 1761)

D29BB35F-A195-5EDD-8913-650982CC35CE

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2; Table S1 (Historical data)

Bombus (Thoracobombus) ruderarius

(Müller, 1776)

FE4DF810-ED84-592D-8885-9EA17CB932BA

Ecological interactions

Feeds on

Polylectic

Conservation status

Endangered

Notes

Table S1 (Historical data)

Bombus (Fernaldaepsithyrus) sylvestris

(Lepeletier 1832)

A6010E96-5C5C-51A8-9ABC-797EA5E12485

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table S1 (Historical data)

Bombus (Bombus) terrestris

(Linnaeus 1758)

BB1DFE9F-B620-52EB-B70F-87252F86243F

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2; Table S1 (Historical data)

Bombus (Psithyrus) vestalis

(Fourcroy 1785)

1E6E660B-A243-58B7-A5CC-6D2EFA69BB3D

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Near Threatened

Notes

Table 2

Chelostoma rapunculi

(Lepeletier 1841)

38ECE448-31C1-5881-ABFB-21B4F172A1EE

Ecological interactions

Feeds on

Oligolectic on Campanulaceae

Conservation status

Least Concern

Notes

Table 2

Colletes cunicularius

(Linnaeus 1758)

705C93B0-B361-57A5-AA37-7BCCD4669F94

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Colletes daviesanus

Smith 1846

70F62270-5245-5F6B-A23B-F94E9500E9F8

Ecological interactions

Feeds on

Oligolectic on Asteraceae

Conservation status

Least Concern

Notes

Table 2

Eucera (Eucera) longicornis

(Linnaeus 1758)

598FC1FF-9AAF-5F2E-AF73-6BEECF404049

Ecological interactions

Feeds on

Oligolectic on Orchidaceae

Conservation status

Vulnerable

Notes

Table 2

Halictus maculatus

Smith 1848

31725763-5194-5955-9C1C-F38B6D1B720F

Ecological interactions

Feeds on

Polylectic

Conservation status

Vulnerable

Notes

Table 2

Halictus rubicundus

(Christ 1791)

873F7A0D-478D-5319-B02F-06192CEE40E6

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Halictus scabiosae

(Rossi 1790)

9805CF81-2787-50D2-BC4B-13A5A9BD6A5F

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Hylaeus brevicornis

Nylander 1852

AD123417-6224-5AD5-9C57-C000FE474C9A

Ecological interactions

Feeds on

Polylectic

Conservation status

Data Deficient

Notes

Table 2

Hylaeus communis

Nylander 1852

DCF6AA3F-43FC-5D8E-A687-281AE90D93A0

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Hylaeus hyalinatus

Smith 1842

90D4646E-40CB-5970-B767-EF525A6E7DA7

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Hylaeus signatus

(Panzer 1798)

17DA14F9-6F8B-55C0-B28B-4D4AA5AFCD21

Ecological interactions

Feeds on

Oligolectic on Resedaceae

Conservation status

Least Concern

Notes

Table 2

Lasioglossum (Evylaeus) calceatum

(Scopoli 1763)

1744D1E1-A2EA-56FA-9526-6D06CD3CB790

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Lasioglossum (Evylaeus) fulvicorne

(Kirby 1802)

B118C370-2825-5A69-82BF-6567D8A808BD

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Lasioglossum (Evylaeus) laticeps

(Schenck 1868)

A7DEA072-A4D9-5DB8-9857-4AA2DE5A6BBE

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Lasioglossum (Lasioglossum) lativentre

(Schenck 1853)

A88DF8F3-10EE-56C5-9AA6-65F265BA0C45

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Lasioglossum (Evylaeus) leucopus

(Kirby 1802)

2573CE7F-7651-5B23-8AE5-FF375F6453CE

Ecological interactions

Feeds on

Polylectic

Conservation status

Near Threatened

Notes

Table 2

Lasioglossum (Lasioglossum) leucozonium

(Schrank 1781)

3DC5D884-DD48-5E14-9D6C-BA11B18FB7AD

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Lasioglossum (Evylaeus) malachurum

(Kirby 1802)

5417ECA7-9629-5D8F-8E10-DEE75FC37A81

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Lasioglossum (Evylaeus) morio

(Fabricius 1793)

16749B48-4DA5-5028-97BE-C1EB97D7E223

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Lasioglossum (Evylaeus) pauxillum

(Schenck 1853)

603F3E27-208A-5D25-853F-8399862F1ECE

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Lasioglossum (Evylaeus) punctatissimum

(Schenck 1853)

B3B32BA7-8805-5918-8FB7-4FDA39BD2C04

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Lasioglossum (Evylaeus) sexstrigatum

(Schenck 1868)

226CB23B-196D-54F9-B303-CA041622F181

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Lasioglossum sp.

3EF7CA5D-A3E8-565A-B100-41D44F98D254

Notes

Table 2

Lasioglossum (Evylaeus) villosulum

(Kirby 1802)

6249CCA0-08DF-5719-8C8F-2B8E01DA95D6

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Lasioglossum (Lasioglossum) zonulum

(Smith 1848)

1D1588AE-FEE5-57F5-9A3B-B6FE878400B8

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Megachile ericetorum

Lepeletier 1841

70278B89-1686-5385-ADEA-6CC72A9FF609

Ecological interactions

Feeds on

Oligolectic on Fabaceae

Conservation status

Least Concern

Notes

Table 2

Megachile willughbiella

(Kirby 1802)

D129DEFE-0678-5879-B31C-7EB786CA440E

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Melitta leporina

(Panzer 1799)

C97B8D1F-79F4-59D6-91D2-B19766E7ADC3

Ecological interactions

Feeds on

Oligolectic on Orobanchaceae

Conservation status

Least Concern

Notes

Table 2

Nomada bifasciata

Olivier 1811

9B1667C8-7517-5CB2-98D0-AF1BAF0B0110

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table 2

Nomada fabriciana

Panzer 1798

B7E531D8-4E55-501A-8291-00D011328259

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table 2

Nomada facilis

Schwarz 1967

D8FC3639-B920-55DD-8C1F-FB7EDDC97407

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table S1 (Historical data)

Nomada flava

(Kirby 1802)

FDD19373-C8B3-594E-AEAE-72C723F678A3

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table 2; Table S1 (Historical data)

Nomada flavoguttata

Panzer 1798

34B6F864-C91E-5EB0-AF52-646D83B27C25

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table 2

Nomada fucata

Fabricius 1793

D4427144-9927-5D2B-82B1-A398030DA9EA

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table 2

Nomada fulvicornis

(Kirby 1802)

39786D32-B140-5908-841B-7F266AB5A941

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table 2

Nomada goodeniana

(Kirby 1802)

93F8F825-D4D8-56F7-AC2B-3E8B9CC82373

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table 2

Nomada integra

Brulé 1832

2C19D6AD-D14C-5E5C-A527-AF76683E2564

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Vulnerable

Notes

Table S1 (Historical data)

Nomada lathburiana

(Kirby 1802)

9F67A09B-2019-5932-AA8C-95F007FD9DE5

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table 2

Nomada leucophthalma

(Kirby 1802)

92AC6EA0-A3BA-51E4-BC86-D60C5CEC225F

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table 2

Nomada marshamella

Lepeletier 1841

55CC1179-8DCE-5C1D-A06E-7A4FD614D928

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table 2; Table S1 (Historical data)

Nomada panzeri

(Linnaeus 1758)

D8D544B6-87EC-5E22-8623-0FED8C8162FF

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table 2

Nomada ruficornis

Fabricius 1793

06000374-DEBA-546D-844E-71E384D5E8FE

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table 2; Table S1 (Historical data)

Nomada signata

Jurine 1807

6BF255D1-42E2-562A-A60F-A1DC7B0CBA32

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table 2

Nomada succincta

Panzer 1798

D6C94E98-8489-5156-B17C-77F5CD03AA46

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table 2

Nomada zonata

Panzer 1798

60709FC6-A497-5FE3-A8C0-E50BC33FF16B

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table 2

Osmia bicolor

(Schrank 1781)

948C4CAF-20AC-5B9F-8FFD-0E90A5FBEA2A

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Osmia bicornis

(Linnaeus 1758)

491182D3-2281-5F9A-8B14-5CB8E9B4720A

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Osmia cornuta

(Latreille 1805)

560596E3-1F94-50A9-B1E4-A9054049D5D8

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Osmia leaiana

(Kirby 1802)

CABA8176-0B1E-55F3-9B7B-72D3C19042B4

Ecological interactions

Feeds on

Oligolectic on Asteraceae

Conservation status

Least Concern

Notes

Table 2

Osmia leucomelana

(Kirby 1802)

23711571-D04D-5663-AB09-638C6B483ADB

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Osmia tridentata

Dufour & Perris 1840

D33C3091-21CA-5E49-B160-C814AC38702D

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Seladonia tumulorum

(Linnaeus 1758)

64AB9D91-37AB-5194-83D8-5A4311AA2ADF

Ecological interactions

Feeds on

Polylectic

Conservation status

Least Concern

Notes

Table 2

Sphecodes ephippius

(Linnaeus 1767)

7F29730F-2965-586C-BFC1-D8CADDB49A3E

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table 2

Sphecodes ferruginatus

Hagens 1882

5CD3E34E-6546-5806-BBD7-4EDD0A124711

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table 2

Sphecodes gibbus

(Linnaeus 1758)

8FC2E3A1-A810-5BC0-BACA-D5C7D2D0E5BD

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table 2

Sphecodes monilicornis

(Kirby 1802)

76A571DE-6A83-59DA-8058-E74BC4176C49

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table 2

Sphecodes puncticeps

Thomson 1870

E9CF53B2-A974-51ED-99DD-168D066F0762

Ecological interactions

Feeds on

Cuckoo bee

Conservation status

Least Concern

Notes

Table 2

Sphecodes sp.

5C8E9C69-5C10-5A06-9F9F-F0600257FC2B

Ecological interactions

Feeds on

Cuckoo bee

Notes

Table 2

Hoverfly Checklist

Cheilosia sp.

Meigen 1822

90050123-9179-5E3F-8E07-2EDAA3F9F3AF

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Episyrphus balteatus

(De Geer 1776)

53CF093A-375A-5B54-AD1B-B8F688A04037

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Eristalis arbustorum

(Linnaeus 1758)

F5FEA349-0334-5849-8ADC-53CC3A9818C9

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Eristalis nemorum

(Linnaeus 1758)

BA3E4C59-DBF8-5529-8093-97F86233CFD4

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Eristalis pertinax

(Scopoli 1763)

BB83C0FB-CBEE-5FD3-9F69-410762CC14A9

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Eristalis sepulchralis

(Linnaeus 1758)

93FF6A50-A0D4-5117-B746-91EE0DD66B8C

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Eristalis similis

(Fallèn 1817)

F89CB51F-CF0A-5D74-9E32-19E1A7A2B421

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Eristalis tenax

(Linnaeus 1758)

38B88F15-9565-5863-A262-EAA792C67AC3

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Eupeodes luniger

(Meigen 1822)

C838CF26-339D-59ED-8A20-93B7FB48C12C

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Ferdinandea cuprea

(Scopoli 1763)

7D8EA026-B075-5EB9-90B5-FE9A80268201

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Helophilus trivittatus

(Fabricius 1805)

EDEACC39-7F2D-53BB-AFA9-4C3ABC0D3CE0

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Melanostoma mellinum

(Linnaeus 1758)

481349F2-DD00-5900-ABDE-5D750AA7A354

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Metasyrphus corollae

(Fabricius 1794)

BF63ABD8-86F0-5ABB-B60D-62979A7E15CB

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Metasyrphus latifasciatus

(Macquart 1829)

61023682-D938-50BD-8BB7-E2E6FC8A5E51

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Myathropa florea

(Linnaeus 1758)

B251790A-E0FA-5E46-935D-612EB37AB9F5

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Platycheirus albimanus

(Fabricius 1781)

290814F9-DC8A-5E26-BA25-ADDCB4733474

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Platycheirus clypeatus

(Meigen 1822)

7F670446-E654-5BA3-9D0D-1EBA9F50B8EB

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Platycheirus immarginatus

(Zetterstedt 1849)

7B152F87-B0F6-562C-A25E-35A4A4C4E6FC

Ecological interactions

Feeds on

Oligolectic on Cyperaceae

Conservation status

Not Applicable

Notes

Table 2

Platycheirus peltatus

(Meigen 1822)

B7F1B06F-01ED-52C0-970D-4F85A42CF4B1

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Platycheirus scambus

(Staeger 1843)

4F178E3D-398F-5E6F-8C92-D1282CA7E6E5

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Rhingia campestris

Meigen 1822

B0EFBFC0-2AC5-515D-B792-F22104462E47

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Scaeva pyrastri

(Linnaeus 1758)

DF7175F0-5E96-5F27-BEF1-7E2AD03539C2

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Sphaerophoria scripta

(Linnaeus 1758)

2B6BC5BE-26CA-50ED-A3CB-0A6837186BBF

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Syritta pipiens

(Linnaeus 1758)

CD7067BB-457C-5FB1-BDFA-12FC949916D4

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Syrphus ribesii

(Linnaeus 1758)

50F55B3F-2078-5B9D-877E-0576C6AA7543

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Syrphus vitripennis

Meigen 1822

EEBD48C0-87E0-5828-99B5-DB19EE78F53D

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Volucella bombylans

(Linnaeus 1758)

A3F2FF42-4B36-58EA-84A0-9CA20C7B2EB1

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Volucella pellucens

(Linnaeus 1758)

3296E90F-34DA-550D-8AC4-22300A23FE44

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Xanthogramma pedissequum

(Harris 1776)

226D97AC-74A4-570F-B298-AFCF80C8226F

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Xylota segnis

(Linnaeus 1758)

F9132A36-B891-5F8F-B53F-492985E4EC15

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Xylota sylvarum

(Linnaeus 1758)

9D5FAD45-007C-5431-B5CD-E6176EFA5110

Ecological interactions

Feeds on

Polylectic

Conservation status

Not Applicable

Notes

Table 2

Analysis

Collection results

Over 2 years (2018-2019) of sampling, we collected 4,303 bees and 1,998 syrphids, representing 92 species and morphospecies from 15 genera and six families for the bees and 31 species and morphospecies from 18 genera for the hoverflies (Table 2). Polylectic, oligolectic and cuckoo bee species correspond to 61%, 14% and 25% of bee richness, respectively. However, the relative proportion of specialised bee (0.9%) was low, with polylectic and cuckoo bees corresponding to 94% and 5.1% in abundance of the total sampled bees, respectively (Table 2). All adult hoverfly species were considered as polylectic species (Frank Van de Meutter, pers. comm.), except for Platycheirus immarginatus (Table 2). In the historical database of Belgian wild bees, we retrieved 18 bee species corresponding to 349 specimens between 1918 and 2007. These data are available in Suppl. material 1. With these historical data of the Havelange Municipality, the bee diversity reached 101 different bee species.

Statistical analysis

For Froidefontaine farmstead, bee richness in VER was significantly higher than in GC (p-value < 0.05; Fig. 3A) and bee abundance in PAT was significantly higher than in GC, VER and ZH (p-values < 0.05; Fig. 3B). Hoverfly diversity in ZH was significantly higher than in VER (p-value < 0.05; Fig. 3C), while hoverfly abundance was homogenous amongst the Froidefontaine parcels (Fig. 3D). For Emeville farmstead, bee and hoverfly richness and bee abundance did not vary amongst parcels (Fig. 4A, B and C), while DIK parcel exhibited significantly greater hoverfly abundance than EPI, FRE and PAV parcels (p-values < 0.05; Fig. 4D). Only for bee richness and hoverfly abundance, the pollinator flower patch BFB showed significantly higher mean values than the feeder flower patch BFV (p-values;Fig. 5A and D).

Figure 3.

Mean values of species richness and abundance for bee and hoverfly fauna amongst Froidefontaine parcels GC, PAT, VER and ZH (see details given in Table 1). A. Bee richness; B. Bee abundance; C. Hoverfly richness; D. Hoverfly abundance. Letters above the boxplots represent Tukey's post-hoc comparisons.

Figure 4.

Mean values of species richness and abundance for bee and hoverfly fauna amongst Emeville parcels DIK, EPI, FRE and PAV (see details given in Table 1). A. Bee richness; B. Bee abundance; C. Hoverfly richness; D. Hoverfly abundance. Letters above the boxplots represent Tukey's post-hoc comparisons.

Figure 5.

Mean values of species richness and abundance for bee and hoverfly fauna amongst flower strips BFB and BFV (see details given in Table 1). A. Bee richness; B. Bee abundance; C. Hoverfly richness; D. Hoverfly abundance. Letters above the boxplots represent Student t-test comparisons.

Discussion

Polylectic bee species

In our study, we identified 101 different bee species, corresponding to almost one quarter of the Belgian bee fauna (Drossart et al. 2019). Depicting 57.32% of the total bee collected material, the top-five bee species in both farms were Andrena cineraria (19.59%), Apis mellifera (12.94%), A. haemorrhoa (10.71%), A. flavipes (7.25%) and Lasioglossum pauxillum (6.83%).

Both farms presented suitable habitats to these polylectic species, including open wooded spaces, fallow land or lawns. The abundance of Taraxacum spp. (Asteraceae), Salix spp. (Salicaceae), Craetegus spp. (Rosaceae) and fruit trees could explain the dominance of A. cineraria, A. haemorrhoa and A. flavipes populations. Moreover, they usually nest in south-exposed sites, in bare soils or in areas with sparse and short vegetation (Falk 2015). The other common polylectic bees were mainly ground-nesting species belonging to Andrena and Lasioglossum genera, such as A. nitida, A. gravida, L. calceatum or L. lativentre (Table 2).

Uncommon polylectic bee species were also collected. For example, Andrena trimmerana and Halictus maculatus (Fig. 6C) are rarely observed in the Condroz Region and more largely in Belgium. H. maculatus is a little more common in Wallonia and this species is considered as "vulnerable" in Belgium, but "least concern" in Europe (Drossart et al. 2019, Nieto et al. 2014). Moreover, this species forages on Achillea millefolium (Asteraceae), Centaurea spp. (Asteraceae) or Daucus carota (Apiaceae) (Pauly 2019), which were naturally present or cultivated in both farms. In 2019, specimens of A. trimmerana were collected only in the Froidefontaine farmstead, where Rubus spp. (Rosaceae), orchards, umbellifers or Cirsium spp. (Asteraceae) were flowering. Two specimens of Colletes cunicularius were sampled from both farms. This species is specialised on Salix spp. (Salicaceae) or Prunus cerasus L., (Rosaceae) (Falk 2015). While Lasioglossum leucopus was observed in both farms - probably because of the presence of several of its preferred host plants, Ranunculus spp. (Ranunculaceae), Taraxacum spp. (Asteraceae) and D. carota - this species is considered as "near threatened" according to the IUCN Red List Criteria in Belgium (Drossart et al. 2019, Pauly 2019).

Figure 6.

Dorsal and lateral side of some rare bees observed within the farmsteads. A. Andrena schencki Morawitz 1866; B. Andrena fulvata (Müller 1766); C. Halictus maculatus Smith 1848; D. Melitta leporina (Panzer 1799); E. Hylaeus brevicornis Nylander 1852.

Rarer species were observed within the farmsteads. Collected in the orchard of Froidefontaine, Andrena schencki (Fig. 6A) had not been observed south of the Sambre and Meuse Furrow for more than 30 years (Rasmont and Haubruge 2002). Andrena semilaevis, a very rare species since 1990 in Belgium (Rasmont and Haubruge 2002), was captured in the orchard of Emeville. This polylectic species is mostly observed on the umbellifers (Falk 2015). Forty-six specimens (1.12% of total sampling) of Andrena fulvata (Fig. 6B) were collected in 2019 in all habitats of both farms, while only one observation was encoded in Atlas Hymenoptera repository for Belgium (Rasmont and Haubruge 2002). That probably means a recent installation of the population on the study sites. However, misidentification due to their morphological resemblance to A. angustior could bias its Belgian rarity (T.J. Wood, personal communication). This species nests in calcareous soils and forages principally on Asteraceae flowers, such as Taraxacum spp. (Falk 2015).

The high diversity of wild bees in the two farms could be linked to the presence of semi-natural habitats around the parcels. Indeed, the implantation of hedgerows, flower strips or shrubby strips between the habitats of both farms provides sufficient floral resources during the foraging activity period of polylectic species (Albrecht et al. 2020).

Oligolectic bee species

Thirteen bee species were characterised as oligolectic (Drossart et al. 2019), which represented 24 specimens (Table 2).

Two common species, A. praecox and A. vaga and two uncommon species, A. apicata and A. mitis, were collected in different parts of both farms (Table 2). In Belgium, they are considered as Salix spp. specialists. Moreover, these last two species had never been observed in Condroz before and not since 1950 in the south of Wallonia. A. humilis is a specialist of Asteraceae plant species, such as Tragopogon dubius Scopoli 1772, Hieracium pilosella Vaillant 1754 (Scheuchl 2002) or Cichorium spp. and A. labialis is a specialist of leguminous plants (Fabaceae) (Rasmont and Haubruge 2002).

A single specimen of Melittidae family, Melitta leporina (Fig. 6D), was sampled. The female is particurlarly related to the flowers of M. sativa and T. pratense species (Fabaceae) (Dellicour and Michez 2010), which were abundantly present around the wetland of Froidefontaine Farm. One species of Colletidae family, Colletes daviesanus, forages pollen entirely from composite flowers such as tansy, mayweeds or oxeye daisy (Asteraceae) (Falk 2015).

In Froidefontaine habitats, we also sampled a few specimens of Chelostoma rapunculi, Eucera longicornis, Hylaeus signatus, Megachile ericertorum and Osmia leaiana, probably because their preferred flowers were partially present:Trifolium sp., Medicago sp., Cirsium sp., Rubus sp., Centaurea sp. and Stachys sylvatica L. 1753.

Cuckoo bee species

We only collected two specimens of cuckoo bumble bees (subgenus Psithyrus Lepeletier), Bombus campestris and B. vestalis, in Froidefontaine wetland and in Froidefontaine orchard (Table 2), respectively. They are considered rare species (Lhomme and Hines 2018) and their presence could be explained by the relative predominance, in the Bombus genus, of their associated host species: B. pascuorum and B. terrestris (Table 2).

Concerning the nomad bees (Nomada spp.), we identified 15 species representing 4.6% of the collected material. They especially parasitise Andrena spp. and their relative abundance is dependent on the proportion of their host bee species (Sheffield et al. 2013). Most of their host species were collected throughout the two years of experiment. For example, we found, in a small proportion, Nomada flavoguttata and N. leucophthalma, which are linked to Micrandrena spp. Ashmead 1899 (Andrena semilaevis, A. subopaca...) and A. apicata, respectively. On the contrary, N. goodeniana and N. ruficornis were largely present due to the strong dominance of A. cineraria and A. haemorrhoa (Rasmont and Haubruge 2002).

All collected Sphecodes spp. are generalist cleptoparasites, except for S. gibbus that parasitises the nests of Halictus species, such as H. maculatus and H. rubicundus. Their relative abundance followed also the abundance of their host species: the most collected S. epphipius is the cuckoo bee of the most collected halictid bee, Lasioglossum pauxillum (Pauly 2019).

Hoverfly species

Within both farmsteads, Sphaerophoria scripta was, by far, the most abundant hoverfly species, followed by Eristalis tenax and Episyrphus balteatus, corresponding together to almost three quarters of the total number of collected specimens (Table 2). These species are the most common syrphids encountered in Central Europe (Alhmedi et al. 2010, Francuski et al. 2013, Nengel and Drescher 1990). Aphidophagous larvae of S. scripta and E. balteatus are important for pest control in agricultural systems, while E. tenax larvae recycle the organic matter in wet manures, muds or ponds (Sommaggio 1999). We also emphasised the presence of Melanostoma mellinum, which occured in almost each habitat and particularly in flower strips. Adults M. mellinum are specialised in the floral visitation of anemophilous plants (Van der Groot and Grabandt 1970).

Beside these ubiquitous species, rarer species were found in only a few habitats: Xanthogramma pedissequum, Myathropa florea and Ferdinandea cuprea (Fig. 7). Unlike S. scripta and E. tenax, these species do not migrate. The larvae of X. pedissequum feed on aphids reared on the anthills of some Lasius sp. Fabricius 1804 (Hymenoptera: Formicidae) (Speight 2020). The species M. florea and F. cuprea present a microphagous larval stage. In intensified agricultural landscapes, it is conceivable that the environmental requirements of such species are scarcely fulfilled. Notably, microphagous species appear to be particularly sensitive to pesticides (Schweiger et al. 2007). On the contrary, agricultural landscapes of Froidefontaine and Emeville Farms are suitable for these specialist species, because they include semi-natural ecosystems and organic orchards where cattle or sheep are grazing. We also identified two specimens of Platycheirus immarginatus that are specialist foragers on Bolboschoenus maritimus (L.) (Table 2) (Speight 2020). We did not find this plant species in Froidefontaine farmstead, meaning that P. immarginatus might forage on other plant species.

Figure 7.

Dorsal and lateral side of some rare hoverfly species observed within the farmsteads. A. Ferdinandea cuprea (Scopoli 1763); B. Xanthogramma pedissequum (Harris 1776); C. Myathropa florea (L.).

Continuous sampling represented only 4.33% of the total hoverfly specimens. However, it allowed us to reveal two more hoverfly species, in Emeville flower strips: Xylota sylvarum and X. segnis, whose larvae are saproxylic and live close to roots and dead wood (Speight et al. 2000).

Impact of agroecological practices on wild bees and hoverflies communities at the farm scale

By in-depth sampling, we documented new occurrences of almost 1/4 of Belgian bee fauna in two farms in ecological transition. For the historical region of the Municipality of Havelange, we have almost quintupled the richness of wild bees community despite high quality monitoring of these populations in Belgium (Drossart et al. 2019). There are few studies of this type in a close environment and with comparable methodology. Therefore, comparing our results with other studies seems to be of little relevance. This study leads us to consider that, on small areas undergoing ecological transition, an important richness of pollinators is easily reached. Moreover, it is possible that the conducted survey underestimates the real diversity per plot, even if the pattern of dominance rarity should be maintained. We also lack data at the end of the season, especially for late summer bees, such as Colletes hederae (Schmidt and Westrich 1993). For hoverflies, we still lack inventory data on the scale of the Belgian territory (Frank Van de Meutter, pers. comm.).

The practices on and around the studied farms seemed favourable to pollinators (Fig. 8) and especially to the polylectic species. In Froidefontaine Farm, the land tenure showed strong impact on bee richness and abundance by an alternation of floral bee-feeding parcels, like the Froidefontaine pasture (PAT; Fig. 3B) and bee-nesting parcels, like the Froidefontaine orchard (VER; Fig. 3A & Fig. 8B). On the one hand, late mowing permits the keeping of abundant floral resources throughout the bee activity period (Meyer et al. 2017) and, on the other hand, sheep grazing permits theconservation of some bare soil sites that favour ground-nesting bees (Cane 1991). Landscape micro-habitats, such as ponds, hedgerows or groves, are important to the survival of many pollinator species, especially by providing habitats for hoverfly larvae (Sommaggio 1999). The wetland of Froidefontaine (ZH) (Fig. 8A) harboured higher hoverfly diversity than the other parcels (Fig. 3C), with species like S. scripta, Cheilosia sp. and E. tenax, whose larvae have different diets (i.e. aphidophagous, phytophagous and microphagous, respectively) (Sommaggio 1999, Speight 2020). The cultivated parcel of Froidefontaine (GC) (Table 2) and the pea crop of Emeville (DIK) (Fig. 4D) showed high abundances of aphidophagous hoverflies, likely caused by the high prevalence of aphids on crops. The flower strips separating the parcels of Emeville Farm consisted of a floral mix especially designed to fill the ecological requirements of bees and hoverflies (Fig. 8D). The floral composition of these flower strips attracted more hoverfly specimens than bees, which were mainly represented by A. mellifera (Table 2). Moreover, they were combined with belatedly-mowed hedges that support floral resources for pollinators throughout their activity season. Similarly, the hedgerows bordering the parcels of Froidefontaine (Fig. 8C), coupled with ecological crop management practices (i.e. no-till, no chemical inputs...), promoted the establishment of wild bee populations (Albrecht et al. 2020). Indeed, hedgerows and other semi-natural habitats usually represent superior floral richness and abundance compared to intensive agricultural land use (Hannon and Sisk 2009).

Figure 8.

Some field pictures in each farm. A. Froidefontaine wetland (ZH); B. Froidefontaine orchard (VER); C. Double hedgerow between Froidefontaine cultivated parcel (GC) and pasture (PAT); D. Emeville flower strip between FRE and EPI parcels (photo credit : I. Van Dorpe); E. Emeville orchard (PAV).

According to the Belgian Red List of bees (Drossart et al. 2019), we have collected several species indexed in threatened categories from diverse habitats of both farms, especially in the orchard and in the wetland of Froidefontaine. These species were represented by one specimen of A. schencki, one specimen of B. campestris, one specimen of E. longicornis and nine specimens of H. maculatus. We also mitigated the data deficiency in Belgium for a few records of bee species, such as A. semilaevis, A. trimmerana and Hylaeus brevicornis (Fig. 6E). Taxonomically recent recognition, split from species complex and morphological similarity with widespread taxa or less studied genera (e.g. Hylaeus sp.) reflect current taxonomic impediments for 9.4% of the Belgian bee richness (Drossart et al. 2019).

Pollinator composition of each farmstead harboured both common and rare species, which indicates that on-farm diversification and organic practices may be an important refuge for rare, Red-Listed or oligolectic pollinator species (Guzman et al. 2019). Restoring or incorporating diverse habitats in agro-ecosystems is therefore a long-term solution for the conservation of pollinating species (Saint Clair et al. 2020).

Supplementary Material

Supplementary material 1

Havelange bee historical data

Grégoire Noël

Data type

occurences

File: oo_472961.xlsm

Author contributions

GN and LS wrote the research project. GN, LS and FF conceived the study. FF provided financial support for the study. CdM and AdL provided the access to their farmstead. GN, LS, JB, AD, SE and AC contributed to the pollinator sampling, insect preparation and identification. GN filtered, curated and analysed the data. JB realised the maps, the field and pollinator pictures, except where mentionned. GN led the manuscript preparation and writing. All authors participated in writing the manuscript, contributed to drafts and gave final approval for publication.