# Spatial distribution of Vespa velutina-mediated beekeeping risk in France and Germany

Fabrice Requier, Fabian Nürnberger, Sandra V Rojas-Nossa, Quentin Rome

► To cite this version:

Fabrice Requier, Fabian Nürnberger, Sandra V Rojas-Nossa, Quentin Rome. Spatial distribution of Vespa velutina-mediated beekeeping risk in France and Germany. Journal of Pest Science, 2024, 10.1007/s10340-024-01782-1. mnhn-04552279

HAL Id: mnhn-04552279

https://mnhn.hal.science/mnhn-04552279

Submitted on 25 Apr 2024

HAL is a multi-disciplinary open access
archive for the deposit and dissemination of sci-
entific research documents, whether they are pub-
lished or not. The documents may come from
teaching and research institutions in France or
abroad, or from public or private research centers.

L'archive ouverte pluridisciplinaire HAL, est
destinée au dépôt et à la diffusion de documents
scientifiques de niveau recherche, publiés ou non,
émanant des établissements d'enseignement et de
recherche français ou étrangers, des laboratoires
publics ou privés.

<figure><img src="image_1.png" /></figure>

Distributed under a Creative Commons Attribution 4.0 International License
1 **Spatial distribution of *Vespa velutina*-mediated beekeeping risk in**
2 **France and Germany**

3

4 Fabrice Requier¹*, Fabian Nürnberger², Sandra V. Rojas-Nossa³, Quentin Rome⁴

5 ¹Université Paris-Saclay, CNRS, IRD, UMR Évolution, Génomes, Comportement et Écologie, 91198, Gif-sur-Yvette, France

7 ²Thünen Institute of Biodiversity, 38116, Brauschnweig, Germany

8 ³Department of Ecology and Animal Biology, Faculty of Sciences, University of Vigo,
9 36310, Vigo, Pontevedra, Spain.

10 ⁴PatriNat (OFB, MNHN), 75005 Paris, France

11 * Corresponding author: Fabrice Requier, fabrice.requier@ird.fr

12

13 **ORCID**

14 Fabrice Requier [https://orcid.org/0000-0003-1638-3141](https://orcid.org/0000-0003-1638-3141)

15 Fabian Nürnberger [https://orcid.org/0000-0002-7360-3617](https://orcid.org/0000-0002-7360-3617)

16 Sandra V. Rojas-Nossa [https://orcid.org/0000-0003-2027-0123](https://orcid.org/0000-0003-2027-0123)

17 Quentin Rome [https://orcid.org/0000-0002-7055-8064](https://orcid.org/0000-0002-7055-8064)

18

19 **Word count (for a Brief Communication in Journal of Pest Science):**

20 Abstract: 225 words (150 to 250 words)

21 Keywords: 6 words (suggested 4 to 6)

22 Key message: 67 (max. 80 words)

23 Main text: 3,801 words (max. 4000 words)

24 Figure legends: 226 words

25 Tables: 200 words

26 Artwork: 4 figures and 2 tables

27 Number of references: 48 references

28
1 **Spatial distribution of *Vespa velutina*-mediated beekeeping risk in**
2 **France and Germany**

3

4 Fabrice Requier¹*, Fabian Nürnberger², Sandra V. Rojas-Nossa³, Quentin Rome⁴

5 ¹Université Paris-Saclay, CNRS, IRD, UMR Évolution, Génomes, Comportement et Écologie, 91198, Gif-sur-Yvette, France

7 ²Thünen Institute of Biodiversity, 38116, Brauschnweig, Germany

8 ³Department of Ecology and Animal Biology, Faculty of Sciences, University of Vigo,
36310, Vigo, Pontevedra, Spain.

10 ⁴PatriNat (OFB, MNHN), 75005 Paris, France

11 * Corresponding author: Fabrice Requier, fabrice.requier@ird.fr

12

13 **ORCID**

14 Fabrice Requier https://orcid.org/0000-0003-1638-3141

15 Fabian Nürnberger https://orcid.org/0000-0002-7360-3617

16 Sandra V. Rojas-Nossa https://orcid.org/0000-0003-2027-0123

17 Quentin Rome https://orcid.org/0000-0002-7055-8064

18

19 **Word count (for a Brief Communication in Journal of Pest Science):**

20 Abstract: 225 words (150 to 250 words)

21 Keywords: 6 words (suggested 4 to 6)

22 Key message: 67 (max. 80 words)

23 Main text: 3,801 words (max. 4000 words)

24 Figure legends: 226 words

25 Tables: 200 words

26 Artwork: 4 figures and 2 tables

27 Number of references: 48 references

28
29

**Abstract**

30

31

32

33

34

35

36

37

38

39

40

41

42

43

44

45

46

47

48

49

50

The Yellow-legged hornet (Vespa velutina nigrithorax) was accidentally brought to south-western of France in 2004 and rapidly spread throughout France and neighbouring countries. This predator of insect hunts honey bees leading to a hornet-mediated beekeeping risk (HBR) with potential mortality of honey bee colonies and important economic costs.

However, the spatial distribution of HBR is not yet assessed and is urgently required to formulate suitable management plans in Western Europe. We carried out a two-year citizen science survey in France and Germany in order to assess the spatial distribution of (1) the hornet and (2) HBR, and to (3) determine the environmental factors involved. A total of 1697 beekeepers responded to the survey. The hornet was established throughout the French territory as expected, and mostly detected near the French border in Germany. We found that HBR was substantially lower in Germany than in France. Temperature had a positive effect on both the hornet presence and HBR whereas the distance to the introduction point had a negative effect, both in France and Germany. These results suggest that the impact of *V. velutina* on beekeeping is not homogeneous throughout the invasion range and could be reduced on the eastern front due to continental climate. Considering HBR spatial variability could help formulating regionally adapted management plans to limit *V. velutina* impacts on biodiversity, human health and economic sectors.

**Keywords:** *Apis mellifera*, expansion range, invasive species, risk assessment, *Vespa velutina*, Yellow-legged hornet
29

**Abstract**

30

31

32

33

34

35

36

37

38

39

40

41

42

43

44

45

46

47

48

49

50

The Yellow-legged hornet (Vespa velutina nigrithorax) was accidentally brought to south-western of France in 2004 and rapidly spread throughout France and neighbouring countries. This predator of insect hunts honey bees leading to a hornet-mediated beekeeping risk (HBR) with potential mortality of honey bee colonies and important economic costs.

However, the spatial distribution of HBR is not yet assessed and is urgently required to formulate suitable management plans in Western Europe. We carried out a two-year citizen science survey in France and Germany in order to assess the spatial distribution of (1) the hornet and (2) HBR, and to (3) determine the environmental factors involved. A total of 1697 beekeepers responded to the survey. The hornet was established throughout the French territory as expected, and mostly detected near the French border in Germany. We found that HBR was substantially lower in Germany than in France. Temperature had a positive effect on both the hornet presence and HBR whereas the distance to the introduction point had a negative effect, both in France and Germany. These results suggest that the impact of *V. velutina* on beekeeping is not homogeneous throughout the invasion range and could be reduced on the eastern front due to continental climate. Considering HBR spatial variability could help formulating regionally adapted management plans to limit *V. velutina* impacts on biodiversity, human health and economic sectors.

**Keywords:** *Apis mellifera*, expansion range, invasive species, risk assessment, *Vespa velutina*, Yellow-legged hornet
51 **Key message**

52 • The Yellow-legged hornet impacts honey bee survival and beekeeping activity in
53 Western Europe

54 • Little is known on the spatial distribution of the hornet-mediated beekeeping risk
55 (HBR)

56 • We assessed HBR across France and Germany over two years

57 • HBR was substantially lower in Germany than in France and negatively affected by
58 temperature and distance to the introduction point

59 • Considering HBR spatial variability could help formulating regionally adapted man-
60 agement plans

61

62 **Author Contribution Statement**

63 F.R. and Q.R. conceived the ideas and designed methodology; F.R., F.N. and Q.R. col-
64 lected the data; F.R. analysed the data; F.R. and S.R.N. wrote the paper and all authors
65 contributed significantly to the drafts and gave their final approval for publication.

66
51

## Key message

52

* The Yellow-legged hornet impacts honey bee survival and beekeeping activity in Western Europe

53

54

* Little is known on the spatial distribution of the hornet-mediated beekeeping risk (HBR)

55

56

* We assessed HBR across France and Germany over two years

57

* HBR was substantially lower in Germany than in France and negatively affected by temperature and distance to the introduction point

58

59

* Considering HBR spatial variability could help formulating regionally adapted management plans

60

61

62

## Author Contribution Statement

63

64

65

F.R. and Q.R. conceived the ideas and designed methodology; F.R., F.N. and Q.R. collected the data; F.R. analysed the data; F.R. and S.R.N. wrote the paper and all authors contributed significantly to the drafts and gave their final approval for publication.

66
67 **Introduction**

68 Wild and managed pollinators are suffering a combination of pressures including environ-
69 mental factors (e.g. pesticides and lack of flowers), biotic factors (e.g. parasites, patho-
70 gens and predators) and a lack of genetic diversity that affects populations, ecosystem
71 services and related food security (Potts et al. 2010, 2016). In addition, the interaction be-
72 tween these pressures can generate synergistic effects increasing their impacts (Goulson
73 et al. 2015, Henry et al. 2017). Among these pressures, the Yellow-legged hornet, *Vespa
74 velutina nigrithorax* represents a relatively new biotic pressure upon the Western honey
75 bee, *Apis mellifera* in Western Europe. *V. velutina* is native to China and was accidentally
76 introduced to southwestern France in 2004 (Arca et al. 2015). This species quickly spread
77 throughout France and beyond (Rome and Villemant 2023). As early as 2010, sightings of
78 the species were recorded successively in Spain (Lopez et al. 2011), Portugal (Grosso-
79 Silva and Maia 2012), Belgium (Rome et al. 2013), Italy (Bertolino et al. 2016), Germany
80 (Witt 2015), Great Britain (Budge et al. 2017), Switzerland (Sciences Switzerland 2017),
81 the Netherlands (Smit et al. 2017), and Luxembourg (Ries et al. 2021). Currently, *V. ve-
82 lutina nigrithorax* is a subspecies of Union Concern included in the EU list of invasive alien
83 species (Regulation EU No 1143/2014 of the European Parliament and of the Council).

84 Its expansion in Western and Central Europe is explained both by natural disper-
85 sal mechanisms of *V. velutina* but also by the effects of anthropogenic facilitation of long-
86 distance dispersal via the transport of goods (trucks, trains, etc.) creating new queen intro-
87 duction areas (Robinet et al. 2018; Husemann et al. 2020). Previous studies assessed the
88 dispersion range of this invasion and defined climate (e.g. temperature or precipitation;
89 Villemant et al. 2011, Barbet-Massin et al. 2013), habitat (e.g. artificial surfaces such as
90 urban areas; Fournier et al. 2017) and distance to the introduction place (located in the
67 **Introduction**

68 Wild and managed pollinators are suffering a combination of pressures including environ-
69 mental factors (e.g. pesticides and lack of flowers), biotic factors (e.g. parasites, patho-
70 gens and predators) and a lack of genetic diversity that affects populations, ecosystem
71 services and related food security (Potts et al. 2010, 2016). In addition, the interaction be-
72 tween these pressures can generate synergistic effects increasing their impacts (Goulson
73 et al. 2015, Henry et al. 2017). Among these pressures, the Yellow-legged hornet, *Vespa
74 velutina nigrithorax* represents a relatively new biotic pressure upon the Western honey
75 bee, *Apis mellifera* in Western Europe. *V. velutina* is native to China and was accidentally
76 introduced to southwestern France in 2004 (Arca et al. 2015). This species quickly spread
77 throughout France and beyond (Rome and Villemant 2023). As early as 2010, sightings of
78 the species were recorded successively in Spain (Lopez et al. 2011), Portugal (Grosso-
79 Silva and Maia 2012), Belgium (Rome et al. 2013), Italy (Bertolino et al. 2016), Germany
80 (Witt 2015), Great Britain (Budge et al. 2017), Switzerland (Sciences Switzerland 2017),
81 the Netherlands (Smit et al. 2017), and Luxembourg (Ries et al. 2021). Currently, *V. ve-
82 lutina nigrithorax* is a subspecies of Union Concern included in the EU list of invasive alien
83 species (Regulation EU No 1143/2014 of the European Parliament and of the Council).

84 Its expansion in Western and Central Europe is explained both by natural disper-
85 sal mechanisms of *V. velutina* but also by the effects of anthropogenic facilitation of long-
86 distance dispersal via the transport of goods (trucks, trains, etc.) creating new queen intro-
87 duction areas (Robinet et al. 2018; Husemann et al. 2020). Previous studies assessed the
88 dispersion range of this invasion and defined climate (e.g. temperature or precipitation;
89 Villemant et al. 2011, Barbet-Massin et al. 2013), habitat (e.g. artificial surfaces such as
90 urban areas; Fournier et al. 2017) and distance to the introduction place (located in the
south-west, in the Lot et Garonne department; Robinet et al. 2018) as robust predictors of *V. velutina* invasion range. Moreover, scientific projections estimate that the expansion of *V. velutina* could continue, or even accelerate under the impulse of climate change (Barbet-Massin et al. 2013). In this sense, studies have reported other areas of introduction around the world, such as South Korea (Kim et al. 2006) and Japan (Ueno et al. 2014).

*V. velutina* is an important predator of honey bees in Western Europe. The predation activity of *V. velutina* on honey bees increases during the summer and reaches its peak between September and October (Requier et al. 2019). At this period, honey bees can constitute 38% of the diet of *V. velutina* in average (Rome et al. 2021). This period also corresponds to a critical time for honey bees as they prepare for overwintering (Requier et al. 2019). Field observations show that honey bees are not yet able to defend itself against *V. velutina* attacks and/or has not developed an effective defense mechanism against *V. velutina* attacks (Monceau et al. 2018) comparatively to defense ability of *Apis cerana* in *V. velutina*'s native range (Monceau et al. 2013; Arca et al. 2015). Thus, *V. velutina* predation poses an additional threat to honey bees that already face multiple pressures and significant colony mortalities (Brodschneider et al. 2018).

*V. velutina* predation of worker honey bees at the entrance of the beehive, in particular on foragers returning to the beehive, can have a noticeable effect on the demography of honey bee colonies (Monceau et al. 2013; Requier et al. 2019). More alarmingly, the presence of hornets hovering in front of the beehive has the effect of paralyzing beehive activity when the number of hornets is too high (Requier et al. 2019). When the number of hornets in front of a beehive exceeds a certain threshold, established at 12 individuals (Requier et al. 2019), honey bees no longer leave the hive and therefore no longer bring back the resources necessary for the overwintering of the colony. This maladaptive
south-west, in the Lot et Garonne department; Robinet et al. 2018) as robust predictors of *V. velutina* invasion range. Moreover, scientific projections estimate that the expansion of *V. velutina* could continue, or even accelerate under the impulse of climate change (Barbet-Massin et al. 2013). In this sense, studies have reported other areas of introduction around the world, such as South Korea (Kim et al. 2006) and Japan (Ueno et al. 2014).

*V. velutina* is an important predator of honey bees in Western Europe. The predation activity of *V. velutina* on honey bees increases during the summer and reaches its peak between September and October (Requier et al. 2019). At this period, honey bees can constitute 38% of the diet of *V. velutina* in average (Rome et al. 2021). This period also corresponds to a critical time for honey bees as they prepare for overwintering (Requier et al. 2019). Field observations show that honey bees are not yet able to defend itself against *V. velutina* attacks and/or has not developed an effective defense mechanism against *V. velutina* attacks (Monceau et al. 2018) comparatively to defense ability of *Apis cerana* in *V. velutina*'s native range (Monceau et al. 2013; Arca et al. 2015). Thus, *V. velutina* predation poses an additional threat to honey bees that already face multiple pressures and significant colony mortalities (Brodschneider et al. 2018).

*V. velutina* predation of worker honey bees at the entrance of the beehive, in particular on foragers returning to the beehive, can have a noticeable effect on the demography of honey bee colonies (Monceau et al. 2013; Requier et al. 2019). More alarmingly, the presence of hornets hovering in front of the beehive has the effect of paralyzing beehive activity when the number of hornets is too high (Requier et al. 2019). When the number of hornets in front of a beehive exceeds a certain threshold, established at 12 individuals (Requier et al. 2019), honey bees no longer leave the hive and therefore no longer bring back the resources necessary for the overwintering of the colony. This maladaptive
defensive behavior leads to the consumption of honey provisions planned for the winter and significantly increases the risk of collapse of bee colonies during the winter (Requier et al. 2019; Rojas-Nossa et al. 2022). Thus, the predation of honey bees leads to a hornet-mediated beekeeping risk (HBR) that can provide mortality of honey bee colonies with important economic costs estimated reach as much as € 30.8 million per year due to colony loss in France (Requier et al. 2023a).

Although the current and potential spatial distribution of *V. velutina* is well documented, the spatial distribution of the risk that this invasive species represents for beekeeping (i.e. HBR) is not yet assessed. Information of the spatial distribution, however, is urgently required to formulate suitable management plans. In this study, we carried out a large-scale citizen science program aimed at accurately mapping the distribution of *V. velutina* in apiaries across France and Germany, where uncertainty persists concerning the eastern limit of the invasion front. Moreover, we mapped HBR in these two countries in order to perform a spatial risk assessment that can help recommending management measures for the species. Finally, we explored whether the spatial distributions of *V. velutina* and HBR can be determined by environmental variables (i.e. climate, habitat and distance to the introduction place) in order to help formulating regionally adapted management plans.

## Materials and Methods

### Franco-German citizen science program

This study is based on two-year citizen-science program involving beekeepers in France and Germany over the years 2018 and 2019. A standardized questionnaire was designed
defensive behavior leads to the consumption of honey provisions planned for the winter and significantly increases the risk of collapse of bee colonies during the winter (Requier et al. 2019; Rojas-Nossa et al. 2022). Thus, the predation of honey bees leads to a hornet-mediated beekeeping risk (HBR) that can provide mortality of honey bee colonies with important economic costs estimated reach as much as € 30.8 million per year due to colony loss in France (Requier et al. 2023a).

Although the current and potential spatial distribution of *V. velutina* is well documented, the spatial distribution of the risk that this invasive species represents for beekeeping (i.e. HBR) is not yet assessed. Information of the spatial distribution, however, is urgently required to formulate suitable management plans. In this study, we carried out a large-scale citizen science program aimed at accurately mapping the distribution of *V. velutina* in apiaries across France and Germany, where uncertainty persists concerning the eastern limit of the invasion front. Moreover, we mapped HBR in these two countries in order to perform a spatial risk assessment that can help recommending management measures for the species. Finally, we explored whether the spatial distributions of *V. velutina* and HBR can be determined by environmental variables (i.e. climate, habitat and distance to the introduction place) in order to help formulating regionally adapted management plans.

## Materials and Methods

### Franco-German citizen science program

This study is based on two-year citizen-science program involving beekeepers in France and Germany over the years 2018 and 2019. A standardized questionnaire was designed
to record the distribution and predation behavior of *V. velutina* at the country level. The consideration of two countries resulted from the lack of information on the expansion of *V. velutina* at the eastern distribution boundary (Germany) following the first records in 2014 in southern Germany ("Rheinland-Pfalz" region) (Witt 2015). The beekeepers were invited to record their observations in front of the beehives through a questionnaire (**Supporting Information, Table S1**). The questionnaire was distributed across Germany via the solicited publication in two major national beekeeping journals (Requier et al. 2018a, b). Additionally, the survey was advertised in a beekeeping newsletter published by the German bee institutes. The survey was disseminated via beekeeping social networks in France, on the website of the National Museum of Natural History of Paris, and promoted by a beekeeper on Youtube. The call to participate at the survey started in the fall (i.e. September 2018 for the first year and September 2019 for the second year) and the survey was open until the end of the year studied, i.e. until December 2018 for the first year and December 2019 for the second year. This period of time represents the most likely time window to observe *V. velutina* predating at the apiary (Requier et al. 2019).

## Record of *V. velutina* presence and hornet-mediated beekeeping risk (HBR)

Volunteer beekeepers were asked to fill in their apiary location (city/region/country), if they observed predation behavior of *V. velutina* in front of the beehives between September 1st and October 31st (the most likely time window to observe *V. velutina* predating at the apiary and potentially leading to detrimental effect on colony survival; Requier et al. 2019), and the maximum number of hornet individuals observed hunting simultaneously at each beehive between September 1st and October 31st. Based on the answers to the survey, the GPS data of all sightings was populated using the postal code recorded by the bee-
to record the distribution and predation behavior of *V. velutina* at the country level. The consideration of two countries resulted from the lack of information on the expansion of *V. velutina* at the eastern distribution boundary (Germany) following the first records in 2014 in southern Germany (“Rheinland-Pfalz” region) (Witt 2015). The beekeepers were invited to record their observations in front of the beehives through a questionnaire (**Supporting Information, Table S1**). The questionnaire was distributed across Germany via the solicited publication in two major national beekeeping journals (Requier et al. 2018a, b). Additionally, the survey was advertised in a beekeeping newsletter published by the German bee institutes. The survey was disseminated via beekeeping social networks in France, on the website of the National Museum of Natural History of Paris, and promoted by a beekeeper on Youtube. The call to participate at the survey started in the fall (i.e. September 2018 for the first year and September 2019 for the second year) and the survey was open until the end of the year studied, i.e. until December 2018 for the first year and December 2019 for the second year. This period of time represents the most likely time window to observe *V. velutina* predating at the apiary (Requier et al. 2019).

## Record of *V. velutina* presence and hornet-mediated beekeeping risk (HBR)

Volunteer beekeepers were asked to fill in their apiary location (city/region/country), if they observed predation behavior of *V. velutina* in front of the beehives between September 1st and October 31st (the most likely time window to observe *V. velutina* predating at the apiary and potentially leading to detrimental effect on colony survival; Requier et al. 2019), and the maximum number of hornet individuals observed hunting simultaneously at each beehive between September 1st and October 31st. Based on the answers to the survey, the GPS data of all sightings was populated using the postal code recorded by the bee-
keeper and considering the center of the municipality. Whenever beekeepers observed hornet predation on beehives, they were asked to report the maximum number of hornet individuals observed simultaneously in front of a beehive. However, a few answers were given in text form (less than 1% of answers), and these were quantitatively transformed as follows. For closed intervals such as "1 to 6 hornets observed", we considered the high interval as (maximum number requested in the question), namely "6" in this example. In the case of open intervals, for example "more than 10 hornets observed", at least 10 hornets have been observed, so this is the information that has been retained. Finally, in the case of adjectives (e.g. "few", "too many") a binary reasoning was adopted, considering that at least 1 hornet was observed. The answer was changed to "1". This recorded maximum number of hornet individuals observed at the same time predating in front of a beehive was used to establish whether each apiary was over or below the hornet-mediated beekeeping risk (HBR). According to the literature, more than 12 hornets observed at the same time predating in front of a beehive induce bee foraging paralysis and can lead to colony collapse (Requier et al. 2019). Therefore, we considered that reaching (or exceeding) the critical threshold of 12 hornet individuals lead to HBR.

179

## Expert-based validation

Given that *V. velutina* is a new invasive species in Western Europe, we carried out a validation by experts of the identifications (Q. Rome and F. Requier). To perform the confirmation, beekeepers were invited to send pictures of the recorded insects. When validating the detections, particular attention was paid to German regions for which little positive detection had been recorded to date. This validation was only carried out for the German data
keeper and considering the center of the municipality. Whenever beekeepers observed hornet predation on beehives, they were asked to report the maximum number of hornet individuals observed simultaneously in front of a beehive. However, a few answers were given in text form (less than 1% of answers), and these were quantitatively transformed as follows. For closed intervals such as "1 to 6 hornets observed", we considered the high interval as (maximum number requested in the question), namely "6" in this example. In the case of open intervals, for example "more than 10 hornets observed", at least 10 hornets have been observed, so this is the information that has been retained. Finally, in the case of adjectives (e.g. "few", "too many") a binary reasoning was adopted, considering that at least 1 hornet was observed. The answer was changed to "1". This recorded maximum number of hornet individuals observed at the same time predating in front of a beehive was used to establish whether each apiary was over or below the hornet-mediated beekeeping risk (HBR). According to the literature, more than 12 hornets observed at the same time predating in front of a beehive induce bee foraging paralysis and can lead to colony collapse (Requier et al. 2019). Therefore, we considered that reaching (or exceeding) the critical threshold of 12 hornet individuals lead to HBR.

179

## Expert-based validation

Given that *V. velutina* is a new invasive species in Western Europe, we carried out a validation by experts of the identifications (Q. Rome and F. Requier). To perform the confirmation, beekeepers were invited to send pictures of the recorded insects. When validating the detections, particular attention was paid to German regions for which little positive detection had been recorded to date. This validation was only carried out for the German data

163

164

165

166

167

168

169

170

171

172

173

174

175

176

177

178

179

180

181

182

183

184

185
because we followed the hypothesis that French beekeepers have knowledge of *V. ve-
lutina*.

188

189 Environmental variables

190 Based on the GPS data, the environmental parameters of each record were extracted from
191 Open Source databases to inform the climate of the site, habitat within a radius of 10 km²,
192 and distance to the introduction place. Habitat was extracted via the GlobCover2009 land
193 cover map database (http://due.esrin.esa.int/page_globcover.php) for the years 2018 and
194 2019. Given that the urbanization is the most likely landscape factor that affects the distri-
195 bution of *V. velutina* (Fournier et al. 2017), we calculated the proportion of urbanized areas
196 around the observation points in an area of 10 km² around the GPS coordinates (square of
197 about 3 km on each side, **Figure S1**). This distance was chosen because the average for-
198 aging distance of honey bees is about 1.5 km (Steffan-Dewenter and Kuhn 2003) and the
199 average foraging distance of *V. velutina* is about 2 km (Budge et al. 2017; Sauvard et al.
200 2018; Kennedy et al. 2018; Rome et al. 2021). Similarly, we selected the temperature
201 among the climatic factors, which is known to affect the distribution of the species (Barbet-
202 Massin et al. 2013). Temperature data were obtained from the WorldClim database ver-
203 sion 2.0 Beta (https://www.worldclim.org/). The 1970-2000 monthly mean temperatures at
204 each observation site were used to estimate the annual mean temperature (in °C, **Figure
205 S2**). Finally, we computed the distance to the introduction site as an euclidean distance in
206 kilometers considering the location of accidental introduction in 2004 in the south-western
207 France in the Lot et Garonne department (Robinet et al. 2018, **Figure S3**). We performed
208 Pearson's correlation tests to assess colinearity among environmental variables, showing
209 few colinearity (**Figure S4**).
because we followed the hypothesis that French beekeepers have knowledge of *V. ve-
lutina*.

188

189 Environmental variables

190 Based on the GPS data, the environmental parameters of each record were extracted from
191 Open Source databases to inform the climate of the site, habitat within a radius of 10 km²,
192 and distance to the introduction place. Habitat was extracted via the GlobCover2009 land
193 cover map database (http://due.esrin.esa.int/page_globcover.php) for the years 2018 and
194 2019. Given that the urbanization is the most likely landscape factor that affects the distri-
195 bution of *V. velutina* (Fournier et al. 2017), we calculated the proportion of urbanized areas
196 around the observation points in an area of 10 km² around the GPS coordinates (square of
197 about 3 km on each side, **Figure S1**). This distance was chosen because the average for-
198 aging distance of honey bees is about 1.5 km (Steffan-Dewenter and Kuhn 2003) and the
199 average foraging distance of *V. velutina* is about 2 km (Budge et al. 2017; Sauvard et al.
200 2018; Kennedy et al. 2018; Rome et al. 2021). Similarly, we selected the temperature
201 among the climatic factors, which is known to affect the distribution of the species (Barbet-
202 Massin et al. 2013). Temperature data were obtained from the WorldClim database ver-
203 sion 2.0 Beta (https://www.worldclim.org/). The 1970-2000 monthly mean temperatures at
204 each observation site were used to estimate the annual mean temperature (in °C, **Figure
205 S2**). Finally, we computed the distance to the introduction site as an euclidean distance in
206 kilometers considering the location of accidental introduction in 2004 in the south-western
207 France in the Lot et Garonne department (Robinet et al. 2018, **Figure S3**). We performed
208 Pearson's correlation tests to assess colinearity among environmental variables, showing
209 few colinearity (**Figure S4**).
210

## 211 Statistical analyses

212 The statistical analyses were performed with the R software, version 3.6.3 (R Develop-
213 ment Core Team, 2023).

214 *Spatial drivers of V. velutina presence.* A Generalized Linear Models with a bino-
215 mial distribution of errors (binomial GLM) was used to analyze whether the presence of the
216 *V. velutina* in apiaries (response variable) is affected by (1) the distance to the point of in-
217 troduction, (2) the temperature and (3) the percentage of urbanization (explainatory vari-
218 ables). The presence of *V. velutina* was considered in a binary way, with 0 for absence
219 and 1 for presence.

220 *Spatial drivers of HBR.* A Generalized Linear Model with a Poisson distribution of
221 errors (Poisson GLM) was used to analyze whether HBR (response variable) is affected by
222 (1) the distance to the point of introduction, (2) the temperature and (3) the percentage of
223 urbanization explainatory variables.

224 For all the statistics, model residuals were extracted and inspected against fitted
225 values (residuals versus fitted plot and normal Q-Q plot) to ensure residual normality and
226 homoscedasticity assumptions were fulfilled. The significance level for the statistical tests
227 was set at 5% for the probability of rejecting the true null hypothesis.

228

## 229 Results

230

## 231 Spatial drivers of *V. velutina* presence

232 We collected a total of 1697 responses from beekeepers on the presence or absence of *V.
233 velutina* predating in the apiaries across France (n=1368 responses) and Germany (n=329
210

## 211 Statistical analyses

The statistical analyses were performed with the R software, version 3.6.3 (R Develop-ment Core Team, 2023).

214 *Spatial drivers of V. velutina presence.* A Generalized Linear Models with a bino-mial distribution of errors (binomial GLM) was used to analyze whether the presence of the V. velutina in apiaries (response variable) is affected by (1) the distance to the point of in-troduction, (2) the temperature and (3) the percentage of urbanization (explainatory vari-ables). The presence of V. velutina was considered in a binary way, with 0 for absence and 1 for presence.

220 *Spatial drivers of HBR.* A Generalized Linear Model with a Poisson distribution of errors (Poisson GLM) was used to analyze whether HBR (response variable) is affected by (1) the distance to the point of introduction, (2) the temperature and (3) the percentage of urbanization explainatory variables.

224 For all the statistics, model residuals were extracted and inspected against fitted values (residuals versus fitted plot and normal Q-Q plot) to ensure residual normality and homoscedasticity assumptions were fulfilled. The significance level for the statistical tests was set at 5% for the probability of rejecting the true null hypothesis.

228

## 229 Results

230

## 231 Spatial drivers of V. velutina presence

We collected a total of 1697 responses from beekeepers on the presence or absence of V. velutina predating in the apiaries across France (n=1368 responses) and Germany (n=329
234 responses). The responses were widely distributed throughout France and Germany (Fig-
235 ure 1). A large majority of French beekeepers observed the presence of *V. velutina* hunt-
236 ing in front of their beehives (72.9% of observations were positive). The frequency of ob-
237 servation of *V. velutina* presence in front of the beehives in Germany was lower than in
238 France (5.5% of positive records in Germany), with concentration of positive observation in
239 the Rhine valley, and in the south-west of Germany and in the north (Hamburg) with less
240 frequency (Figure 1).

241 We found that temperature, the distance to the point of introduction and the per-
242 centage of urbanization significantly explained the presence of *V. velutina* predating in the
243 apiaries across France and Germany (Table 1), with temperature and distance to the point
244 of introduction as the best explanatory variables (higher z values; Table 1). Therefore, the
245 distribution of *V. velutina* presence in France and Germany is strongly determined by the
246 temperature and the distance to the point of introduction, and in lesser extent on the ur-
247 banization rate. The temperature has a positive effect on the presence of *V. velutina* pre-
248 dating in the front of the beehives (Figure 2A), and the distance to the point of introduction
249 has a negative effect (Figure 2B). The presence of *V. velutina* increases slightly with the
250 percentage of urbanization (Figure 2C).

251

252 Spatial drivers of HBR

253 In total, 1015 validated positive observations of *V. velutina* in France and Germany were
254 collected over the years 2018 and 2019 (Figure 3). In France, the 3.5% of apiaries with
255 presence of *V. velutina* exceeded the HBR risk threshold of 12 hornet individuals observed
256 at the same time predating in front of a beehive, whereas in Germany this threshold was
257 never reached. The apiaries at risk of HBR (i.e. a minimum of 12 hornet individuals ob-
234 responses). The responses were widely distributed throughout France and Germany (Fig-
235 ure 1). A large majority of French beekeepers observed the presence of *V. velutina* hunt-
236 ing in front of their beehives (72.9% of observations were positive). The frequency of ob-
237 servation of *V. velutina* presence in front of the beehives in Germany was lower than in
238 France (5.5% of positive records in Germany), with concentration of positive observation in
239 the Rhine valley, and in the south-west of Germany and in the north (Hamburg) with less
240 frequency (Figure 1).

241 We found that temperature, the distance to the point of introduction and the per-
242 centage of urbanization significantly explained the presence of *V. velutina* predating in the
243 apiaries across France and Germany (Table 1), with temperature and distance to the point
244 of introduction as the best explanatory variables (higher z values; Table 1). Therefore, the
245 distribution of *V. velutina* presence in France and Germany is strongly determined by the
246 temperature and the distance to the point of introduction, and in lesser extent on the ur-
247 banization rate. The temperature has a positive effect on the presence of *V. velutina* pre-
248 dating in the front of the beehives (Figure 2A), and the distance to the point of introduction
249 has a negative effect (Figure 2B). The presence of *V. velutina* increases slightly with the
250 percentage of urbanization (Figure 2C).

251
252
**Spatial drivers of HBR**

253 In total, 1015 validated positive observations of *V. velutina* in France and Germany were
254 collected over the years 2018 and 2019 (Figure 3). In France, the 3.5% of apiaries with
255 presence of *V. velutina* exceeded the HBR risk threshold of 12 hornet individuals observed
256 at the same time predating in front of a beehive, whereas in Germany this threshold was
257 never reached. The apiaries at risk of HBR (i.e. a minimum of 12 hornet individuals ob-
served simultaneously predating in front of a beehive) were located in south-western France, in the region of the accidental introduction of the invasive species (Figure 3).

Temperature and the distance to the point of introduction significantly affect the distribution of HBR (Table 2). The percentage of urbanization did not explain the spatial variability in HBR (Table 2). The temperature had a positive effect on HBR (Figure 4A), while the distance to the point of introduction had a negative effect on HBR (Figure 4B). HBR increases slightly with the percentage of urbanization, but not significantly (Figure 3C).

## Discussion

The first objective of this study was to assess the distribution boundary of *V. velutina* in Germany, as the maximum front of the invasion of the species in Western Europe. The results showed that the majority of sightings of *V. velutina* in Germany were in the already known presence area, in the Rhine Valley (Witt 2015). These first results therefore confirm the establishment of the species in the Rhine valley, in continuity of the French invasion front. This valley has a microclimate in which the temperatures are slightly higher than the surrounding region and therefore potentially more favorable to *V. velutina* (Villemant et al. 2011; Barbet-Massin et al. 2013). The results of this study support this hypothesis, showing that the annual mean ambient temperature has a positive effect on the probability of the presence of *V. velutina* in front of the beehives, in France and in Germany. However, new observations have also been noted, such as in Hamburg (Husemann et al. 2020b), and in other sites not connected to this first zone. These are indicators of secondary invasions. The presence of the species in these areas suggests that the spread of *V. velutina* is, as probably all other invasive species (e.g. Suarez et al. 2001), not only natural but is
served simultaneously predating in front of a beehive) were located in south-western France, in the region of the accidental introduction of the invasive species (Figure 3).

Temperature and the distance to the point of introduction significantly affect the distribution of HBR (Table 2). The percentage of urbanization did not explain the spatial variability in HBR (Table 2). The temperature had a positive effect on HBR (Figure 4A), while the distance to the point of introduction had a negative effect on HBR (Figure 4B). HBR increases slightly with the percentage of urbanization, but not significantly (Figure 3C).

## Discussion

The first objective of this study was to assess the distribution boundary of *V. velutina* in Germany, as the maximum front of the invasion of the species in Western Europe. The results showed that the majority of sightings of *V. velutina* in Germany were in the already known presence area, in the Rhine Valley (Witt 2015). These first results therefore confirm the establishment of the species in the Rhine valley, in continuity of the French invasion front. This valley has a microclimate in which the temperatures are slightly higher than the surrounding region and therefore potentially more favorable to *V. velutina* (Villemant et al. 2011; Barbet-Massin et al. 2013). The results of this study support this hypothesis, showing that the annual mean ambient temperature has a positive effect on the probability of the presence of *V. velutina* in front of the beehives, in France and in Germany. However, new observations have also been noted, such as in Hamburg (Husemann et al. 2020b), and in other sites not connected to this first zone. These are indicators of secondary invasions. The presence of the species in these areas suggests that the spread of *V. velutina* is, as probably all other invasive species (e.g. Suarez et al. 2001), not only natural but is
282 also largely facilitated by the transport of goods (Rome et al. 2011; Robinet et al. 2018).

283 Indeed, the queens can be transported, in convoys of wood for example, thus favoring the
284 establishment of the species in areas not yet colonized (Robinet et al. 2018).

285 This study also shows the establishment of *V. velutina* in the whole metropolitan
286 French territory, and that the species is not yet present in Corsica (see also Rome and
287 Villemant 2023). However, the species density is not homogeneous across France. We
288 detected a lower density of *V. velutina* sightings in the Grand-Est region and in the Alps
289 and Massif Central mountains in France. The temperature effect explains this heterogene-
290 ity, as these two French regions have colder climates than the rest of France. The lower
291 annual mean ambient temperature can also explain the observation of fewer hornet indi-
292 viduals in the Alps. Indeed, we found that temperature is the predominant environmental
293 factor explaining the presence of the species in France and Germany. This result is in
294 agreement with previous studies that observed a positive effect of temperature on the dis-
295 tribution of the invasive species (Barbet-Massin et al. 2013; Rodríguez-Flores et al. 2019).

296 The distance to the point of introduction has a negative effect on the presence of *V. velutina*, which is also in agreement with previous studies (Robinet et al. 2018). Finally, we 297 showed that urbanization had a positive effect on the presence of the species. A previous 298 study (Fournier et al. 2017) found that urbanization was one of the landscape elements 299 determining the rank of *V. velutina* invasion. Although *V. velutina* has established itself in 300 Germany through expansion by the French territory, climatic barriers seem to restrict its 301 natural expansion in the eastern front. Indeed, since its introduction in 2014 in Germany, 302 the species has made little progress, depending of more favourable years. However, cli- 303 mate change and rising temperatures could allow *V. velutina* to continue its expansion on 304 the eastern front of Europe in the years to come (Barbet-Massin et al. 2013). 305
282 also largely facilitated by the transport of goods (Rome et al. 2011; Robinet et al. 2018).

283 Indeed, the queens can be transported, in convoys of wood for example, thus favoring the
284 establishment of the species in areas not yet colonized (Robinet et al. 2018).

285 This study also shows the establishment of *V. velutina* in the whole metropolitan
286 French territory, and that the species is not yet present in Corsica (see also Rome and
287 Villemant 2023). However, the species density is not homogeneous across France. We
288 detected a lower density of *V. velutina* sightings in the Grand-Est region and in the Alps
289 and Massif Central mountains in France. The temperature effect explains this heterogene-
290 ity, as these two French regions have colder climates than the rest of France. The lower
291 annual mean ambient temperature can also explain the observation of fewer hornet indi-
292 viduals in the Alps. Indeed, we found that temperature is the predominant environmental
293 factor explaining the presence of the species in France and Germany. This result is in
294 agreement with previous studies that observed a positive effect of temperature on the dis-
295 tribution of the invasive species (Barbet-Massin et al. 2013; Rodríguez-Flores et al. 2019).

296 The distance to the point of introduction has a negative effect on the presence of *V. velutina*, which is also in agreement with previous studies (Robinet et al. 2018). Finally, we 297 showed that urbanization had a positive effect on the presence of the species. A previous 298 study (Fournier et al. 2017) found that urbanization was one of the landscape elements 299 determining the rank of *V. velutina* invasion. Although *V. velutina* has established itself in 300 Germany through expansion by the French territory, climatic barriers seem to restrict its 301 natural expansion in the eastern front. Indeed, since its introduction in 2014 in Germany, 302 the species has made little progress, depending of more favourable years. However, cli- 303 mate change and rising temperatures could allow *V. velutina* to continue its expansion on 304 the eastern front of Europe in the years to come (Barbet-Massin et al. 2013). 305
Beyond the presence of the species, this study also aimed to study the spatial distribution of the hornet-mediated beekeeping risk (HBR) in France and Germany. The HBR threshold was set at 12 individuals observed simultaneously in front of a beehive (Requier et al. 2019). Once we reach or exceed this threshold, the bee colony is often paralyzed, which leads to its collapse. This study confirms that this threshold is reached in France, which can lead to a risk of losing colonies (Requier et al. 2019). In Germany, this risk does not occur because the number of hornet individuals observed simultaneously in front of a beehive never exceeds the risk threshold. However, there is evidence revealing that lower predation pressure maintained over several weeks can also lead to the paralysis of the colony (Rojas-Nossa et al. 2022). Therefore, further studies are needed to understand the triggering factors for this antipredator behaviour, and it is important the awareness of keepers about monitoring colonies' behaviour even in regions that have not a high HBR. Temperature and distance to the point of introduction were identified as predictive variables of HBR in France and Germany. Overall, temperature appears to be a critical factor of both the presence of the species and HBR in France and Germany. Temperature has a positive effect on HBR. The annual mean ambient temperature is lower in Germany than in France, potentially explaining the fact that HBR is lower in Germany than in France. The distance to the point of introduction is also a determining factor of *V. velutina* presence and the pressure, unlike urbanization which is a predictive factor of the presence of the species (in comparison with the temperature and the distance to the point of introduction), and which does not explain the spatial variability of HBR. Thus, if a beekeeper is located in an area where the temperature is conducive to the implementation of *V. velutina*, the risk of observing hornets and that they are a threat to bee colonies could increase.
Beyond the presence of the species, this study also aimed to study the spatial distribution of the hornet-mediated beekeeping risk (HBR) in France and Germany. The HBR threshold was set at 12 individuals observed simultaneously in front of a beehive (Requier et al. 2019). Once we reach or exceed this threshold, the bee colony is often paralyzed, which leads to its collapse. This study confirms that this threshold is reached in France, which can lead to a risk of losing colonies (Requier et al. 2019). In Germany, this risk does not occur because the number of hornet individuals observed simultaneously in front of a beehive never exceeds the risk threshold. However, there is evidence revealing that lower predation pressure maintained over several weeks can also lead to the paralysis of the colony (Rojas-Nossa et al. 2022). Therefore, further studies are needed to understand the triggering factors for this antipredator behaviour, and it is important the awareness of bekeepers about monitoring colonies' behaviour even in regions that have not a high HBR. Temperature and distance to the point of introduction were identified as predictive variables of HBR in France and Germany. Overall, temperature appears to be a critical factor of both the presence of the species and HBR in France and Germany. Temperature has a positive effect on HBR. The annual mean ambient temperature is lower in Germany than in France, potentially explaining the fact that HBR is lower in Germany than in France. The distance to the point of introduction is also a determining factor of *V. velutina* presence and the pressure, unlike urbanization which is a predictive factor of the presence of the species (in comparison with the temperature and the distance to the point of introduction), and which does not explain the spatial variability of HBR. Thus, if a beekeeper is located in an area where the temperature is conducive to the implementation of *V. velutina*, the risk of observing hornets and that they are a threat to bee colonies could increase.
The risk of bee colony mortality linked to *V. velutina* predation is likely to occur in France (i.e. number of hornet individuals observed simultaneously in front of a beehive above the HBR threshold) but not in Germany (i.e. number of hornet individuals never exceeding the HBR threshold). Species control measures should be considered accordingly.

An important point to consider along with the limited risk to beekeeping is the conservation status of the European hornet (*Vespa crabro*) in Germany. Indeed, the European hornet is a species with a special protection category in Germany (the species is not protected in France), and its capture is therefore illegal in Germany. All traps traditionally used to control the invasion of the hornet in France also have lethal effects on other parts of the entomofauna including the European hornet (Rojas-Nossa et al. 2018; Requier et al. 2020a).

Therefore, baited traps are not suitable as a control method in Germany. Nevertheless, the threat of *V. velutina* on beekeeping could increase in the future in Germany with climate change and its impetus on the establishment of the species in Europe (Barbet-Massin et al. 2013). We urge beekeepers and the public authorities to implement prevention and management plans that involve biodiversity-friendly techniques (e.g. non-lethal techniques) in order to control the potential impact of *V. velutina* on beekeeping.

346

## Conclusion

Faced with the concern that represent *V. velutina* invasion and the risk it represents for beekeeping (Laurino et al. 2019), a large diversity of methods of controlling hornet populations are put in place but are not always effective or even dangerous for other non-target insect species (Rojas-Nossa et al 2018; Turchi and Derijard 2018; Requier et al. 2020b).

Beehive muzzles could be recommended to beekeepers since they reduce the risk of colony mortality without causing adverse effects on biodiversity (Requier et al. 2020b). In addition
The risk of bee colony mortality linked to *V. velutina* predation is likely to occur in France (i.e. number of hornet individuals observed simultaneously in front of a beehive above the HBR threshold) but not in Germany (i.e. number of hornet individuals never exceeding the HBR threshold). Species control measures should be considered accordingly.

An important point to consider along with the limited risk to beekeeping is the conservation status of the European hornet (*Vespa crabro*) in Germany. Indeed, the European hornet is a species with a special protection category in Germany (the species is not protected in France), and its capture is therefore illegal in Germany. All traps traditionally used to control the invasion of the hornet in France also have lethal effects on other parts of the entomofauna including the European hornet (Rojas-Nossa et al. 2018; Requier et al. 2020a).

Therefore, baited traps are not suitable as a control method in Germany. Nevertheless, the threat of *V. velutina* on beekeeping could increase in the future in Germany with climate change and its impetus on the establishment of the species in Europe (Barbet-Massin et al. 2013). We urge beekeepers and the public authorities to implement prevention and management plans that involve biodiversity-friendly techniques (e.g. non-lethal techniques) in order to control the potential impact of *V. velutina* on beekeeping.

346

## Conclusion

Faced with the concern that represent *V. velutina* invasion and the risk it represents for beekeeping (Laurino et al. 2019), a large diversity of methods of controlling hornet populations are put in place but are not always effective or even dangerous for other non-target insect species (Rojas-Nossa et al 2018; Turchi and Derijard 2018; Requier et al. 2020b).

Beehive muzzles could be recommended to beekeepers since they reduce the risk of colony mortality without causing adverse effects on biodiversity (Requier et al. 2020b). In addition
dition, implementing effective measures to mitigate long-distance transport of hornets
should be considered (Robinet et al. 2018). The invasion of *V. velutina* places in a context
of increasing new species invasions leading to numerous ecological and socio-economic
impacts worldwide. These impacts include biodiversity loss and species extinction (Bellard
et al. 2016), health impacts (Mazza et al. 2014) and very significant economic costs (Brad-
shaw et al. 2016; Requier et al. 2023a). We suggest that considering the spatial variability
of the hornet-mediated beekeeping risk could help formulating regionally adapted man-
agement plans to limit *V. velutina* impacts on biodiversity, human health and economic
sectors.

363

364 Acknowledgements

We want to thank all the beekeepers that participated in this survey. We also thank
Margaux Goulard for assistance in data cleaning, Léandre Goydadin
\#UneSaisonAuxAbeilles and Christoph Otten for the help in the diffusion of the survey.

368

369 Funding

This research did not receive any specific grant from funding agencies in the public,
commercial, or not-for-profit sectors.

372

373 Competing Interests

The authors declare that the research was conducted in the absence of any commercial or
financial relationships that could be construed as a potential conflict of interest.

376

377 Data Availability
dition, implementing effective measures to mitigate long-distance transport of hornets should be considered (Robinet et al. 2018). The invasion of *V. velutina* places in a context of increasing new species invasions leading to numerous ecological and socio-economic impacts worldwide. These impacts include biodiversity loss and species extinction (Bellard et al. 2016), health impacts (Mazza et al. 2014) and very significant economic costs (Bradshaw et al. 2016; Requier et al. 2023a). We suggest that considering the spatial variability of the hornet-mediated beekeeping risk could help formulating regionally adapted management plans to limit *V. velutina* impacts on biodiversity, human health and economic sectors.

363

### Acknowledgements

We want to thank all the beekeepers that participated in this survey. We also thank Margaux Goulard for assistance in data cleaning, Léandre Goydadin \#UneSaisonAuxAbeilles and Christoph Otten for the help in the diffusion of the survey.

368

### Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

372

### Competing Interests

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

376

### Data Availability
378 Data available from the figshare repository https://doi.org/10.6084/m9 figshare.24182721
379 (Requier et al. 2023b).

380

381 References

382 Arca M, Mougel F, Guillemaud T, Dupas S, Rome Q, Perrard A, et al. (2015) Reconstructing the invasion and the demographic history of the yellow-legged hornet, *Vespa velutina*, in Europe. Biological Invasions 17: 2357–2371.

385 Barbet-Massin M, Rome Q, Muller F, Perrard A, Villemant C, Jiguet F (2013) Climate change increase the risk of invasion by the Yellow-legged hornet. Biological Conservation 157: 4–10.

388 Bellard C, Cassey P., Blackburn TM (2016) Alien species as a driver of recent extinctions. Biology Letters 12: 20150623.

390 Bertolino S, Lioy S, Laurino D, Manino A, Porporato M (2016) Spread of the invasive yellow-legged hornet *Vespa velutina* (Hymenoptera : Vespidae) in Italy. Applied Entomology and Zoology 51: 589–597.

393 Bradshaw CJA, Leroy B, Bellard C, et al (2016) Massive yet grossly underestimated global costs of invasive insects. Nature Communications 7: 12986.

395 Brodschneider R, Gray A, Adjlane N et al (2018) Multi-country loss rates of honey bee colonies during winter 2016/2017 from the COLOSS survey. Journal of Apicultural Research 57: 452–457.

398 Budge GE, Hodgetts J, Jones EP, et al (2017) The invasion, provenance and diversity of *Vespa velutina* Lepeletier (Hymenoptera: Vespidae) in Great Britain. PLoS ONE 12: e0185172.

401 European Parliament, Council of the European Union (2014) Regulation (EU) No
378 Data available from the figshare repository https://doi.org/10.6084/m9 figshare.24182721
379 (Requier et al. 2023b).

380

381 References

382 Arca M, Mougel F, Guillemaud T, Dupas S, Rome Q, Perrard A, et al. (2015) Reconstructing the invasion and the demographic history of the yellow-legged hornet, *Vespa velutina*, in Europe. Biological Invasions 17: 2357–2371.

385 Barbet-Massin M, Rome Q, Muller F, Perrard A, Villemant C, Jiguet F (2013) Climate change increase the risk of invasion by the Yellow-legged hornet. Biological Conservation 157: 4–10.

388 Bellard C, Cassey P., Blackburn TM (2016) Alien species as a driver of recent extinctions. Biology Letters 12: 20150623.

390 Bertolino S, Lioy S, Laurino D, Manino A, Porporato M (2016) Spread of the invasive yellow-legged hornet *Vespa velutina* (Hymenoptera : Vespidae) in Italy. Applied Entomology and Zoology 51: 589–597.

393 Bradshaw CJA, Leroy B, Bellard C, et al (2016) Massive yet grossly underestimated global costs of invasive insects. Nature Communications 7: 12986.

395 Brodschneider R, Gray A, Adjlane N et al (2018) Multi-country loss rates of honey bee colonies during winter 2016/2017 from the COLOSS survey. Journal of Apicultural Research 57: 452–457.

398 Budge GE, Hodgetts J, Jones EP, et al (2017) The invasion, provenance and diversity of *Vespa velutina* Lepeletier (Hymenoptera: Vespidae) in Great Britain. PLoS ONE 12: e0185172.

401 European Parliament, Council of the European Union (2014) Regulation (EU) No
402 1143/2014 of the European Parliament and of the Council of 22 October 2014 on
403 the prevention and management of the introduction and spread of invasive alien
404 species

405 Fournier A, Barbet-Massin M, Rome Q, Courchamp F (2017) Predicting species distribu-
tion combining multi-scale drivers. Global Ecology and Conservation 12: 215–226.

407 Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined
408 stress from parasites, pesticides, and lack of flowers. Science 347:1255957.Grosso-
409 Silva JM, Maia M (2012) *Vespa velutina* Lepeletier, 1836 (Hymenoptera, Vespidae),
410 new species for Portugal. Arq Entomol 6:53–54.Henry M, Becher MA, Osborne JL
411 et al (2017) Predictive systems models can help elucidate bee declines driven by
412 multiple combined stressors. Apidologie 48: 328–339.

413 Husemann M, Dey LS, Hawlitschek O (2020a) *Vespa velutina nigrithorax* Lepeltier, 1836
414 from Hamburg (Northern Germany) shares the same COI haplotype with other
415 European populations. Journal of Hymenoptera Research 79: 111–115.

416 Husemann M, Sterr A, Maack S, Abraham R (2020b) The northernmost record of the
417 Asian hornet *Vespa velutina nigrithorax* (Hymenoptera, Vespidae). Evolutionary
418 Systematics 4:1-4.

419 Kennedy PJ, Ford SM, Poidatz J, Thiéry D, Osborne JL (2018) Searching for nests of the
420 invasive Asian hornet (Vespa velutina) using radio-telemetry. Communications Bio-
421 logy 1: 1-8.

422 Kim J, Choi M, Moon T (2006) Occurrence of *Vespa velutina* Lepeletier from Korea, and a
423 revised key for Korean *Vespa species* (Hymenoptera: Vespidae). Entomological
424 Research 36: 112–115.
402 1143/2014 of the European Parliament and of the Council of 22 October 2014 on
403 the prevention and management of the introduction and spread of invasive alien
404 species

405 Fournier A, Barbet-Massin M, Rome Q, Courchamp F (2017) Predicting species distribu-
tion combining multi-scale drivers. Global Ecology and Conservation 12: 215–226.

407 Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1255957. Grosso-Silva JM, Maia M (2012) *Vespa velutina* Lepeletier, 1836 (Hymenoptera, Vespidae), new species for Portugal. Arq Entomol 6:53–54. Henry M, Becher MA, Osborne JL et al (2017) Predictive systems models can help elucidate bee declines driven by multiple combined stressors. Apidologie 48: 328–339.

413 Husemann M, Dey LS, Hawlitschek O (2020a) *Vespa velutina nigrithorax* Lepeltier, 1836 from Hamburg (Northern Germany) shares the same COI haplotype with other European populations. Journal of Hymenoptera Research 79: 111–115.

416 Husemann M, Sterr A, Maack S, Abraham R (2020b) The northernmost record of the
417 Asian hornet *Vespa velutina nigrithorax* (Hymenoptera, Vespidae). Evolutionary
418 Systematics 4:1-4.

419 Kennedy PJ, Ford SM, Poidatz J, Thiéry D, Osborne JL (2018) Searching for nests of the
420 invasive Asian hornet (Vespa velutina) using radio-telemetry. Communications Bio-
421 logy 1: 1-8.

422 Kim J, Choi M, Moon T (2006) Occurrence of *Vespa velutina* Lepeletier from Korea, and a
423 revised key for Korean *Vespa species* (Hymenoptera: Vespidae). Entomological
424 Research 36: 112–115.
425 Laurino D, Lioy S, Carisio L, Manino A, Porporato M (2019) *Vespa velutina*: An alien driver of honey bee colony losses. Diversity 12: 5.

427 López S, González Mm Goldarazena A (2011) *Vespa velutina* Lepeletier, 1836 (Hymenoptera: Vespidae): first records in Iberian Peninsula. EPPO Bulletin 41: 439-441.

429 Mazza G, Tricarico E, Genovesi P, Gherardi F (2014) Biological invaders are threat to human health: an overview. Ethology Ecology and Evolution 26: 112-129.

431 Monceau K, Arca M, Leprêtre L et al. (2013) Native prey and invasive predator patterns of foraging activity: the case of the yellow-legged hornet predation at European honeybee hives. PLoS ONE 8: e66492.

434 Monceau K, Arca M, Leprêtre L, Bonnard O, Arnold G, Thiéry D (2018) How *Apis mellifera* behaves with its invasive hornet predator *Vespa velutina?*. Journal of Insect Behavior 31: 1-11.

437 National Museum of Natural History of Paris (2019) http://frelonasiatique.mnhn.fr/enquete-le-frelon-asiatique-vespa-velutina-menace-t-il-lapiculture-en-france/

439 Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends in Ecology and Evolution 25: 345-353

442 Potts SG, et al. (2016) Safeguarding pollinators and their values to human well-being. Nature 540: 220-229.

444 R Development Core Team (2023) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

446 Requier F, Nürnberger F, Rome Q, Steffan-Dewenter I (2018a) Gefürchtete Einwanderin: Breitet sich die Asiatische Hornisse in Deutschland aus? Bienen&Natur.
425 Laurino D, Lioy S, Carisio L, Manino A, Porporato M (2019) *Vespa velutina*: An alien driver of honey bee colony losses. Diversity 12: 5.

427 López S, González Mm Goldarazena A (2011) *Vespa velutina* Lepeletier, 1836 (Hymenoptera: Vespidae): first records in Iberian Peninsula. EPPO Bulletin 41: 439-441.

429 Mazza G, Tricarico E, Genovesi P, Gherardi F (2014) Biological invaders are threat to human health: an overview. Ethology Ecology and Evolution 26: 112-129.

431 Monceau K, Arca M, Leprêtre L et al. (2013) Native prey and invasive predator patterns of foraging activity: the case of the yellow-legged hornet predation at European honeybee hives. PLoS ONE 8: e66492.

434 Monceau K, Arca M, Leprêtre L, Bonnard O, Arnold G, Thiéry D (2018) How *Apis mellifera* behaves with its invasive hornet predator *Vespa velutina?*. Journal of Insect Behavior 31: 1-11.

437 National Museum of Natural History of Paris (2019) http://frelonasiatique.mnhn.fr/enquete-le-frelon-asiatique-vespa-velutina-menace-t-il-lapiculture-en-france/

439 Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends in Ecology and Evolution 25: 345-353

442 Potts SG, et al. (2016) Safeguarding pollinators and their values to human well-being. Nature 540: 220-229.

444 R Development Core Team (2023) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

446 Requier F, Nürnberger F, Rome Q, Steffan-Dewenter I (2018a) Gefürchtete Einwanderin: Breitet sich die Asiatische Hornisse in Deutschland aus? Bienen&Natur.
448 Requier F, Nürnberger F, Rome Q, Steffan-Dewenter I (2018b) Haben Sie mich gesehen?

449 Deutsches Bienen-Journal. https://www.bienenjournal.de/

450 Requier F, Rome Q, Chiron G et al (2019) Predation of the invasive Asian hornet affects
451 foraging activity and survival probability of honey bees in Western Europe. Journal
452 of Pest Science 92: 567–578.

453 Requier, F., Fournier, A., Rome, Q., Darrouzet, E. (2020a) Science communication is
454 needed to inform risk perception and actions of stakeholders. Journal of Environ-
455 mental Management 257: 109983.

456 Requier F, Rome Q, Villemant C, Henry M (2020b) A biodiversity-friendly method to miti-
457 gate the invasive Asian hornet impact on European honey bees. Journal of Pest
458 Science 93: 1–9

459 Requier F, Fournier A, Poiteau S, Rome Q, Courchamp F (2023a) Economic costs of the
460 invasive Yellow-legged hornet on honey bees. Science of the Total Environment,
461 898: 165576.

462 Requier F, Nürnberger F, Rojas-Nossa S, Rome Q (2023b) Data from: Expansion limits of
463 the Yellow-legged hornet-mediated beekeeping risk in Western Europe. figshare
464 Dataset.

465 Ries C, Schneider N, Vitali F, Weigand A (2021) First records and distribution of the inva-
466 sive alien hornet *Vespa velutina nigrithorax* du Buysson, 1905 (Hymenoptera:
467 Vespidae) in Luxembourg. Bulletins mensuels - Société des naturalistes luxem-
468 bourgeois 123: 181–193.

469 Robinet C, Darrouzet E, Suppo C (2018) Spread modelling: A suitable tool to explore the
470 rôle of human-mediated dispersal in the range of expansion of the yellow-legged
471 hornet in Europe. Journal of Pest Management 65: 258–267.
448 Requier F, Nürnberger F, Rome Q, Steffan-Dewenter I (2018b) Haben Sie mich gesehen?

449 Deutsches Bienen-Journal. https://www.bienenjournal.de/

450 Requier F, Rome Q, Chiron G et al (2019) Predation of the invasive Asian hornet affects
451 foraging activity and survival probability of honey bees in Western Europe. Journal
452 of Pest Science 92: 567–578.

453 Requier, F., Fournier, A., Rome, Q., Darrouzet, E. (2020a) Science communication is
454 needed to inform risk perception and actions of stakeholders. Journal of Environ-
455 mental Management 257: 109983.

456 Requier F, Rome Q, Villemant C, Henry M (2020b) A biodiversity-friendly method to miti-
457 gate the invasive Asian hornet impact on European honey bees. Journal of Pest
458 Science 93: 1–9

459 Requier F, Fournier A, Poiteau S, Rome Q, Courchamp F (2023a) Economic costs of the
460 invasive Yellow-legged hornet on honey bees. Science of the Total Environment,
461 898:165576.

462 Requier F, Nürnberger F, Rojas-Nossa S, Rome Q (2023b) Data from: Expansion limits of
463 the Yellow-legged hornet-mediated beekeeping risk in Western Europe. figshare
464 Dataset.

465 Ries C, Schneider N, Vitali F, Weigand A (2021) First records and distribution of the inva-
466 sive alien hornet *Vespa velutina nigrithorax* du Buysson, 1905 (Hymenoptera:
467 Vespidae) in Luxembourg. Bulletins mensuels - Société des naturalistes luxem-
468 bourgeois 123: 181–193.

469 Robinet C, Darrouzet E, Suppo C (2018) Spread modelling: A suitable tool to explore the
470 rôle of human-mediated dispersal in the range of expansion of the yellow-legged
471 hornet in Europe. Journal of Pest Management 65: 258–267.
472 Rodríguez-Flores M, Seijo-Rodríguez A, Escuredo O, Seijo-Coello M (2019) Spreading of
473 *Vespa velutina* in northwestern Spain: influence of elevation and meteorological fac-
tors and effect of bait trapping on target and non-target living organisms. *Journal of
474 Pest Science* 92: 557–565.

476 Rojas-Nossa SV, Novoa N, Serrano A, Calviño-Cancela M (2018). Performance of baited
477 traps used as control tools for the invasive hornet *Vespa velutina* and their impact
478 on non-target insects. *Apidologie* 49: 872–885.

479 Rojas-Nossa SV, Dasilva-Martins D, Mato S, Bartolomé C, Maside X, Garrido J (2022)
480 Effectiveness of electric harps in reducing *Vespa velutina* predation pressure and
481 consequences for honey bee colony development. *Pest Management Science* 78:
482 5142–5149.

483 Rome Q, Villemant C (2023) Le frelon asiatique *Vespa velutina*. In: INPN - MNHN. Avail-
able at https://frelonasiatique.mnhn.fr. Last access in May 2023.

485 Rome Q, Perrard A, Muller F, Fontaine C, Quilès A, Zuccon D, Villemant C (2021) Not just
486 honeybees: predatory habits of *Vespa velutina* (Hymenoptera: Vespidae) in France.
487 Annales de la Société Entomologique de France 57: 12.

488 Rome Q, Dambrine L, Onate C et al (2013) Spread of the invasive hornet *Vespa velutina*
489 Lepeletier, 1836, in Europe in 2012 (Hym., Vespidae). *Bulletin de la Société ento-
mologique de France* 118: 21–22.

491 Rome Q, Perrard A, Muller F, Villemant C (2011) Monitoring and control modalities of a
492 honeybee predator, the yellow-legged hornet *Vespa velutina nigrithorax* (Hymenop-
tera: Vespidae). *Aliens: The Invasive Species Bulletin* 31: 7–15.

494 Sauvard D, Imbault V, Darrouzet É (2018) Flight capacities of yellow-legged hornet (Vespa
495 velutina nigrithorax, Hymenoptera: Vespidae) workers from an invasive population
472 Rodríguez-Flores M, Seijo-Rodríguez A, Escuredo O, Seijo-Coello M (2019) Spreading of
473 *Vespa velutina* in northwestern Spain: influence of elevation and meteorological fac-
474 tors and effect of bait trapping on target and non-target living organisms. Journal of
475 Pest Science 92: 557–565.

476 Rojas-Nossa SV, Novoa N, Serrano A, Calviño-Cancela M (2018). Performance of baited
477 traps used as control tools for the invasive hornet *Vespa velutina* and their impact
478 on non-target insects. *Apidologie* 49: 872–885.

479 Rojas-Nossa SV, Dasilva-Martins D, Mato S, Bartolomé C, Maside X, Garrido J (2022)
480 Effectiveness of electric harps in reducing *Vespa velutina* predation pressure and
481 consequences for honey bee colony development. *Pest Management Science* 78:
482 5142–5149.

483 Rome Q, Villemant C (2023) Le frelon asiatique *Vespa velutina*. In: INPN - MNHN. Avail-
484 able at https://frelonasiatique.mnhn.fr. Last access in May 2023.

485 Rome Q, Perrard A, Muller F, Fontaine C, Quilès A, Zuccon D, Villemant C (2021) Not just
486 honeybees: predatory habits of *Vespa velutina* (Hymenoptera: Vespidae) in France.
487 Annales de la Société Entomologique de France 57: 12.

488 Rome Q, Dambrine L, Onate C et al (2013) Spread of the invasive hornet *Vespa velutina*
489 Lepeletier, 1836, in Europe in 2012 (Hym., Vespidae). *Bulletin de la Société ento-
490 mologique de France* 118: 21–22.

491 Rome Q, Perrard A, Muller F, Villemant C (2011) Monitoring and control modalities of a
492 honeybee predator, the yellow-legged hornet *Vespa velutina nigrithorax* (Hymenop-
493 tera: Vespidae). *Aliens: The Invasive Species Bulletin* 31: 7–15.

494 Sauvard D, Imbault V, Darrouzet É (2018) Flight capacities of yellow-legged hornet (Vespa
495 velutina nigrithorax, Hymenoptera: Vespidae) workers from an invasive population
496 in Europe. PLOS ONE 13: e0198597.

497 Sciences Switzerland (2017) The Asian hornet reaches Switzerland.

498 https://naturalsciences.ch/service/news/90430-the-asian-hornet-reaches-

499 switzerland. Accessed 20 March 2023

500 Smit J, van de Roer RC, Fontein R, Wilde A H (2017) Eerste vondst van de Aziatische hoornaar *Vespa velutina nigrithorax* in Nederland (Hymenoptera: Vespidae). Nederlandse Faunistische Mededelingen 49: 1–10.

503 Steffan-Dewenter I, Kuhn A (2003) Honeybee foraging in differentially structured land- scapes. Proceedings of the Royal Society B 270: 569–575.

505 Suarez AV, Holway DA, Case TJ (2001) Patterns of spread in biological invasions domi- nated by long- distance jump dispersal: insights from Argentine ants. Proceedings of the National Academy of Sciences 98: 1095–1100.

508 Turchi L, Derijard B (2018). Options for the biological and physical control of *Vespa ve- lutina nigrithorax* (Hym.:Vespidae) in Europe : A review. Journal of Applied Ento- mology 142: 553–562.

511 Ueno T (2014) Establishment of the invasive hornet *Vespa velutina* (Hymenoptera: Vespi- dae) in Japan. International Journal of Chemical, Environmental and Biological Sciences 2:220–222.

514 Villemant C, Barbet-Massin M, Perrard A, Muller F, Gargominy O, Jiguet F, et al. (2011) Predicting the invasion risk by the alien bee-hawking Yellow-legged hornet *Vespa velutina nigrithorax* across Europe and other continents with niche models. Biological Conservation 144 : 2142–2150.
496 in Europe. PLOS ONE 13: e0198597.

497 Sciences Switzerland (2017) The Asian hornet reaches Switzerland.

498 https://naturalsciences.ch/service/news/90430-the-asian-hornet-reaches-

499 switzerland. Accessed 20 March 2023

500 Smit J, van de Roer RC, Fontein R, Wilde A H (2017) Eerste vondst van de Aziatische
501 hoornaar *Vespa velutina nigrithorax* in Nederland (Hymenoptera: Vespidae). Neder-
502 landse Faunistische Mededelingen 49: 1–10.

503 Steffan-Dewenter I, Kuhn A (2003) Honeybee foraging in differentially structured land-
504 scapes. Proceedings of the Royal Society B 270: 569–575.

505 Suarez AV, Holway DA, Case TJ (2001) Patterns of spread in biological invasions domi-
506 nated by long- distance jump dispersal: insights from Argentine ants. Proceedings
507 of the National Academy of Sciences 98: 1095–1100.

508 Turchi L, Derijard B (2018). Options for the biological and physical control of *Vespa velutina nigrithorax* (Hym.:Vespidae) in Europe : A review. Journal of Applied Ento-
509 mology 142: 553–562.
510

511 Ueno T (2014) Establishment of the invasive hornet *Vespa velutina* (Hymenoptera: Vespi-
512 dae) in Japan. International Journal of Chemical, Environmental and Biological
513 Sciences 2:220–222.

514 Villemant C, Barbet-Massin M, Perrard A, Muller F, Gargominy O, Jiguet F, et al. (2011)
515 Predicting the invasion risk by the alien bee-hawking Yellow-legged hornet *Vespa
516 velutina nigrithorax* across Europe and other continents with niche models. Biologi-
517 cal Conservation 144 : 2142–2150.
518 Witt R (2015) Erstfund eines Nestes der Asiatischen Hornisse *Vespa velutina* Lepeletier,

519 1838 in Deutschland und Details zum Nestbau (Hymenoptera, Vespinae). Ampulex

520 7: 42–53.

521
518 Witt R (2015) Erstfund eines Nestes der Asiatischen Hornisse *Vespa velutina* Lepeletier,

519 1838 in Deutschland und Details zum Nestbau (Hymenoptera, Vespinae). Ampulex

520 7: 42–53.

521
**Table 1.** Summary of the binomial Generalized Linear Model performed to evaluate the effects of temperature (mean annual ambient temperature, in °C), distance to the point of introduction (in km), and percentage of urbanization (proportion of urban habitat within 3km around the site in %) on the presence of *V. velutina* in apiaries (n=1697).

<table><thead><tr><th>Parameters</th><th>Estimate</th><th>Std. Error</th><th>z value</th><th>P value</th></tr></thead><tbody><tr><td>Intercept</td><td>-6.099</td><td>0.924</td><td>-6.601</td><td>&lt;0.001</td></tr><tr><td>Temperature</td><td>0.828</td><td>0.077</td><td>10.684</td><td>&lt;0.001</td></tr><tr><td>% Urbanization</td><td>0.033</td><td>0.007</td><td>4.606</td><td>&lt;0.001</td></tr><tr><td>Distance</td><td>-0.005</td><td>0.001</td><td>-10.685</td><td>&lt;0.001</td></tr></tbody></table>
**Table 1.** Summary of the binomial Generalized Linear Model performed to evaluate the effects of temperature (mean annual ambient temperature, in °C), distance to the point of introduction (in km), and percentage of urbanization (proportion of urban habitat within 3km around the site in %) on the presence of *V. velutina* in apiaries (n=1697).

<table><thead><tr><th>Parameters</th><th>Estimate</th><th>Std. Error</th><th>z value</th><th>P value</th></tr></thead><tbody><tr><td>Intercept</td><td>-6.099</td><td>0.924</td><td>-6.601</td><td>&lt;0.001</td></tr><tr><td>Temperature</td><td>0.828</td><td>0.077</td><td>10.684</td><td>&lt;0.001</td></tr><tr><td>% Urbanization</td><td>0.033</td><td>0.007</td><td>4.606</td><td>&lt;0.001</td></tr><tr><td>Distance</td><td>-0.005</td><td>0.001</td><td>-10.685</td><td>&lt;0.001</td></tr></tbody></table>
**Table 2.** Summary of the Poisson Generalized Linear Model performed to evaluate the effects of temperature (mean annual ambient temperature, in °C), distance to the point of introduction (in km), and percentage of urbanization (proportion of urban habitat within 3km around the site in %) on the number of hornets observed simultaneously preying in front of a beehive (n=1015).

<table><thead><tr><td>Parameters</td><td>Estimate</td><td>Std. Error</td><td>z value</td><td>P value</td></tr></thead><tbody><tr><td>Intercept</td><td>0.340</td><td>0.194</td><td>1.751</td><td>0.080</td></tr><tr><td>Temperature</td><td>0.118</td><td>0.015</td><td>8.123</td><td>&lt;0.001</td></tr><tr><td>% Urbanization</td><td>0.002</td><td>0.001</td><td>1.780</td><td>0.075</td></tr><tr><td>Distance</td><td>-0.001</td><td>0.001</td><td>-11.164</td><td>&lt;0.001</td></tr></tbody></table>
**Table 2.** Summary of the Poisson Generalized Linear Model performed to evaluate the effects of temperature (mean annual ambient temperature, in °C), distance to the point of introduction (in km), and percentage of urbanization (proportion of urban habitat within 3km around the site in %) on the number of hornets observed simultaneously predating in front of a beehive (n=1015).

<table><thead><tr><th>Parameters</th><th>Estimate</th><th>Std. Error</th><th>z value</th><th>P value</th></tr></thead><tbody><tr><td>Intercept</td><td>0.340</td><td>0.194</td><td>1.751</td><td>0.080</td></tr><tr><td>Temperature</td><td>0.118</td><td>0.015</td><td>8.123</td><td>&lt;0.001</td></tr><tr><td>% Urbanization</td><td>0.002</td><td>0.001</td><td>1.780</td><td>0.075</td></tr><tr><td>Distance</td><td>-0.001</td><td>0.001</td><td>-11.164</td><td>&lt;0.001</td></tr></tbody></table>
536 **Figure Captions**

537

538 **Figure 1.** Mapping the spatial distribution of presence of the Yellow-legged hornet (Vespa velutina nigrithorax) in apriaries across France and Germany (n=1697).

540

541 **Figure 2.** Effects of (A) temperature (mean annual ambient temperature, in °C), (B) distance to the point of introduction (in km), and (C) percentage of urbanization (proportion of urban habitat within 3km around the site in %) on the presence of *V. velutina* in apriaries (n=1697). The dots represent the observations; the thick lines represent the binomial GLM predictions with shaded areas indicating the 95% confidence interval.

546

547 **Figure 3.** Mapping the spatial distribution of the hornet-mediated beekeeping risk (HBR) as the maximum number of individual hornets observed simultaneously in predation in front of a beehive across France and Germany (n=1015).

550

551 **Figure 4.** Effects of (A) temperature (mean annual ambient temperature, in °C), (B) distance to the point of introduction (in km), and (C) percentage of urbanization (proportion of urban habitat within 3km around the site in %) on the number of hornets observed simultaneously predating in front of a beehive (n=1015). The dots represent the observations; the thick black lines represent the Poisson GLM predictions with shaded areas indicating the 95% confidence interval. These lines are dashed if they are non-significant. The dotted red lines represent the HBR threshold (i.e. a minimum of 12 hornet individuals observed simultaneously predating in front of a beehive).

559
536 **Figure Captions**

537

538 **Figure 1.** Mapping the spatial distribution of presence of the Yellow-legged hornet (Vespa velutina nigrithorax) in apriaries across France and Germany (n=1697).

540

541 **Figure 2.** Effects of (A) temperature (mean annual ambient temperature, in °C), (B) distance to the point of introduction (in km), and (C) percentage of urbanization (proportion of urban habitat within 3km around the site in %) on the presence of *V. velutina* in apriaries (n=1697). The dots represent the observations; the thick lines represent the binomial GLM predictions with shaded areas indicating the 95% confidence interval.

546

547 **Figure 3.** Mapping the spatial distribution of the hornet-mediated beekeeping risk (HBR) as the maximum number of individual hornets observed simultaneously in predation in front of a beehive across France and Germany (n=1015).

550

551 **Figure 4.** Effects of (A) temperature (mean annual ambient temperature, in °C), (B) distance to the point of introduction (in km), and (C) percentage of urbanization (proportion of urban habitat within 3km around the site in %) on the number of hornets observed simultaneously predating in front of a beehive (n=1015). The dots represent the observations; the thick black lines represent the Poisson GLM predictions with shaded areas indicating the 95% confidence interval. These lines are dashed if they are non-significant. The dotted red lines represent the HBR threshold (i.e. a minimum of 12 hornet individuals observed simultaneously predating in front of a beehive).

559