Advertisement

Spreading of Vespa velutina in northwestern Spain: influence of elevation and meteorological factors and effect of bait trapping on target and non-target living organisms

  • María Shantal Rodríguez-Flores
  • Ana Seijo-Rodríguez
  • Olga Escuredo
  • María del Carmen Seijo-Coello
Original Paper
  • 191 Downloads

Abstract

The yellow-legged hornet, Vespa velutina, is a recent invasive species in Galicia (NW Spain). Its invasion has an important socio-economic impact because it preys upon honeybees (Apis mellifera) and other crucial insect pollinators. The dispersal of this species must be monitored to minimise the damage it causes and to take the necessary control actions. The aims of this study were to determine target and nontarget living organisms captured by bait trapping and to compare the distribution patterns of V. velutina and the autochthonous V. crabro. Altitude and weather conditions played important roles in hornet behaviour. The traps placed in low-altitude coastal areas contained the most yellow-legged hornets. In contrast, the autochthonous hornet occurred in relatively greater numbers in the traps hung in high-altitude areas. High minimum temperatures, dew temperature, relative humidity and low maximum temperatures favour the occurrence and spread of V. velutina. These conditions are common in the coastal areas of this territory and promoted the rapid dispersal of this pest. The traps used were not bait-selective, so many other arthropod organisms were captured along with the hornet. Therefore, the use of species-selective baits is required for the ecofriendly effective management of this insect pest.

Keywords

Pest management Invasive insect Vespa velutina Vespa crabro Biodiversity Meteorological conditions Altitude 

Key message

  • Vespa velutina is an invasive pest recently introduced in NW Spain and has had a negative socio-economic impact mainly in primary production as beekeeping and fruticulture.

  • This study investigated the effects of weather and altitude upon the diffusion of the yellow-legged hornet in relation to the autochthonous hornet.

  • High minimum and dew temperatures and relative humidity and low altitude promote the invasion of this insect pest.

Introduction

Invasive alien species are a major cause of biodiversity loss especially because they interact with native species. The Asian yellow-legged hornet, Vespa velutina nigrithorax (Hymenoptera: Vespidae), is currently an invasive exotic species in Europe. It was accidentally introduced in France in 2004–2005 (Monceau et al. 2014a). The rapid dispersal of the yellow-legged hornet brought it to several European regions including the Iberian Peninsula (López et al. 2011; Rome et al. 2011; Villemant et al. 2011). Its expansion in Europe is explained by the fact that it has not enough direct competitors or predators. In addition, it has a high reproduction rate, the regional temperatures and precipitation levels favour its proliferation, it has inexhaustible food sources, and its life cycle is conducive to its introduction and expansion into new habitats (Holway et al. 2002; Barbet-Massin et al. 2013).

The yellow-legged hornet was first reported in Spain in the provinces of Navarra and Guipúzcoa in 2010 (Castro and Pagola-Carte 2010; Neiker-Tecnalia 2010; López et al. 2011). The insects then have spread to Vizcaya, Álava (Atutxa 2012; EFE 2012) and Northern Portugal (Grosso-Silva and Maia 2012). Vespa velutina first entered Galicia (Northwest Iberian Peninsula) at the end of 2012. The dispersal of this species depends mainly on the survival of the foundresses queen (Monceau et al. 2015a). This survival could be strongly correlated with meteorological factors (Villemant et al. 2011; Robinet et al. 2017), food availability (Monceau and Thiéry 2017) and the activity of the colony during its growth, among other factors. Galicia has a heterogeneous climate due to its geographical location and morphology (Martínez-Cortizas and Pérez-Alberti 1999). Most of Galicia is surrounded by the Atlantic Ocean and, therefore, has an oceanic climate. In the inland of the South and Southeast, however, the climate is Mediterranean.

Vespa velutina is a threat to current biodiversity. Its diet consists mainly of Hymenoptera, Diptera, and other insects (López et al. 2011; Monceau et al. 2013a). It directly competes with the autochthonous European hornet V. crabro Linnaeus, 1758 for the same ecological niche and food sources (Monceau et al. 2015a, b; López et al. 2011). One of the most relevant impacts affects the domestic bee (Apis mellifera) since V. velutina feeds on it to obtain a high part of its protein diet. This invasive insect has contributed to the global decline of this crucial pollinator (Monceau et al. 2014a). V. velutina has exterminated entire beehives, thereby reducing the availability and supply of apiculture products and causing substantial losses in this economic sector.

The fast advance of V. velutina makes it nearly impossible to eradicate. The control methods available are not enough to minimise the negative impacts of this species. One of the most widely used control methods is springtime queen trapping (Rome et al. 2011; Monceau et al. 2014a; Islam et al. 2015; Monceau and Thiéry 2017). Bait traps with food attractants are placed at strategic points to capture the largest number of insect individuals. The first objective of this control option is to capture colony-founding queens. In this way, fewer colonies are formed in the summer months when the hornets most frequently attack the beehives. The second objective is to reduce hornet pressure in the vicinity of the apiaries during the summer season when V. velutina workers attack honeybees at the hive entrances.

It is necessary to develop effective V. velutina detection early and control techniques. Monitoring protocols are also required to reduce the spread and negative impact of this species. In this perspective, it is important to identify the dispersion routes of V. velutina and to characterise the landscape and weather conditions favouring its invasion. In parallel, the control method should be tested to check its overall effectiveness. In the present study, V. velutina was monitored by placing bait traps in areas with different landscapes and meteorological conditions. The relationships between the dispersal of V. velutina, altitude, and weather were analysed to determine the conditions this species prefers for colonisation. In addition, the trapping method was tested, analysing its effect on the local entomofauna. The extent of the damage caused by V. velutina is correlated with the number of nests it can establish within the same area. For this reason, the nests located in the periphery of the bait traps were enumerated and correlated with the population densities of V. velutina.

Materials and methods

Sampling area and database

The sampling points were selected according to the various climates and altitudes of Galicia. This territory is located in the northwestern Iberian Peninsula. In the Southeast, there are mountain chains with altitudes > 1600 m located 200 km from the seacoast. In the North, the elevation is ~ 500 m and the coast is 20 km away. Other formations like coastal bays have strong influences on the local weather. During the summer, the regional weather is affected by the Azores high-pressure system which brings northwesterly winds and clear skies. In the wintertime, a low-pressure system over Great Britain brings cold fronts to the region from the Atlantic Ocean. These fronts and the local topography strongly influence precipitation patterns (Souto et al. 2003). The Atlantic climate is characterised by high annual regional precipitation (> 1000 mm). However, the inland climate is continental. It has relatively less precipitation because of the Foehn effect in which the mountains intercept oceanic clouds and humidity. Maximum rainfall occurs in December and January, and a secondary maximum may appear in March and April. Minimum precipitation is observed in July. These seasonal fluctuations may be explained by variations in the atmospheric configuration of the northern hemisphere (Lorenzo and Taboada 2005; de Castro et al. 2006; Lorenzo et al. 2008). Annual temperatures in Galicia vary from 8 °C in winter to ~ 20 °C in summer. The mean annual temperature is ~ 13 °C. The highest wintertime temperatures in the Atlantic provinces are ~ 1–2 °C above the annual mean. In summer, maximum temperatures in the interior of the southern region can exceed 35 °C because of the Mediterranean climate there (Martínez-Cortizas and Pérez-Alberti 1999). Drought frequently occurs in the summertime in this area.

Meteorological data were obtained from the National Weather Service (2017) which has several stations distributed throughout the study area. Bait trap altitude data was calculated using QGIS v. 2.18.9 and Google Earth Pro. The numbers of V. velutina captured individuals were determined according to trap installation altitude range (0–200 m, 201–400 m, 401–600 m, and > 600 m).

Vespa velutina bait and nest data

Yellow-legged hornets were tracked by setting 137 traps throughout the region from early spring to autumn 2017. A total of 418 samples were collected during the study (Fig. 1). The traps were located at an altitude range of 18 m (coastal) to 750 m (mountainous inland). Areas with high V. velutina population densities and those in which the species was just being introduced were considered. Captured samples were classified and organised into the following groups of arthropods: V. velutina, V. crabro, other Vespidae, Diptera, Lepidoptera, Hymenoptera, other insect orders, and arachnids. Results were expressed as percentages of the total content collected in each trap.
Fig. 1

Sampled regions. S: Number of samples collected in each region

Nests of V. velutina identified near the traps the previous year were considered. This information was provided by the Consellería de Medio Rural, Xunta de Galicia. Data are expressed as the numbers of nests detected by the population and are recorded by location.

Statistical analysis

Data were processed using IBM SPSS Statistics® for Windows version 22.0 (IBM Corp., 2013) and Statgraphics Centurion XVI (Statgraphics Technologies, Inc., The Plains, VA, USA). An ANOVA using the post hoc Fisher’s LSD test was performed to analyse the relative differences in the average numbers of V. velutina and V. crabro at various elevation ranges in the territory. Correlations among the numbers of V. velutina, meteorological factors and altitude variables were determined by Spearman’s nonparametric rank correlation analysis because there was no normality in the data. Statistical significance thresholds were set at P < 0.05 and P < 0.001. A stepwise linear regression analysis was performed using V. velutina data as the dependent variable and meteorological factors and altitude as the independent variables.

Results

Insect diversity in the bait traps

During the whole study period, bait trapping allowed the capture of more than 263,307 target and nontarget insect individuals. The most predominant were the Diptera. In addition, 4995 V. velutina, 907 V. crabro, 954 honeybees, 296 Bombus sp., 1744 other Vespidae, and 6562 moths and butterflies were collected along with other insects. The percentage of the different groups collected in the traps is shown in a Box-Cox diagram (Fig. 2). The highest percentage collected in the traps were Dipterans which constituted the 84.5%. Lepidopterans accounted for 3.5% of the total trap content. The mean V. velutina content was 3.3% ranged the number of V. velutina captured from a minimum of zero to a maximum of 190. The group other Vespidae constituted 1.1%. V. crabro was considered separately because it is as an autochthonous species; it accounted 0.9% of the total trap content. Other important pollinator species such as A. mellifera (0.9%) and Bombus sp. (0.2%) were also captured. Arthropods such as arachnids represented 0.1% of all animals identified in the traps. Ants, earwigs, beetles, lacewings, green bugs, and dragonflies were also identified. Together, these accounted for 5.7% of the total trap content.
Fig. 2

Percentages of the arthropod groups collected in the bait traps

Influence of weather and altitude on the average content of V. velutina

The daily mean temperature in the study region was 15 °C. The average minimum and maximum temperatures were 8.5 °C and 22.9 °C, respectively. The absolute minimum and maximum temperatures were 0.4 °C and 30.3 °C, respectively. Rainfall was at a maximum in May. However, precipitation was relatively low throughout most of the experimental period.

Spearman´s correlation analysis showed a positive relationship between the presence of V. velutina and the mean (P < 0.05), minimum (P < 0.01), and dew (P < 0.01) temperatures (Table 1). In contrast, the presence of V. velutina was negatively correlated with the maximum temperature (P < 0.05) and the number of hours in which the temperature was ≤ 7 °C (hours of cold) (P < 0.01). The presence of V. velutina was also positively correlated with relative humidity (mean and minimum, P < 0.01; maximum, P < 0.05) and mean rainfall (P < 0.01). Nevertheless, intense rain events reduced the numbers of insects in the traps. The presence of V. velutina was negatively correlated with wind speed and altitude (P < 0.01) and positively correlated with the number of nests previously recorded (P < 0.01).
Table 1

Spearman correlation coefficients between meteorological variables, altitude and the number of individuals of V. velutina and V. crabro

 

V. velutina

V. crabro

T. mean (°C)

0.248**

− 0.088

T. maximum (°C)

0.054

0.004

T. minimum (°C)

0.360**

− 0.160**

R.H. mean (%)

0.259**

− 0.103

R.H. maximum (%)

0.195**

− 0.024

R.H. minimum (%)

0.335**

− 0.109*

Dew temperature (°C)

0.384**

− 0.116*

Rainfall (L/m2)

0.243**

0.113*

Hours of cold (h)

− 0.261**

0.163**

Wind speed (km/h)

− 0.201**

0.031

Altitude (m)

− 0.484**

0.196**

Nest number

0.572**

− 0.294**

V. crabro

0.090

1.000

**P < 0.01; *P < 0.05

Fisher’s LSD test showed significant differences among altitude ranges at the 95.0% confidence level (Fig. 3a). The average number of V. velutina in the coastal area bait traps (altitude range 0–200 m) was significantly higher (P < 0.05) than those at the other altitudes. At 0–200 m, 21 hornets were captured during the trapping period. Starting at 201 m, the average hornet content in the bait traps decreased. At 201–400 m, three hornets were captured. At 401–600 m and at > 600 m, five and four hornets were captured, respectively. There was a strong negative correlation between the altitude and the number of V. velutina collected in the bait traps studied (r = 0.460; P < 0.001). Far fewer V. crabro than V. velutina were captured. The average numbers of V. crabro trapped at each altitude range were low (Fig. 3b). The average V. crabro content was significantly lower (P < 0.05) in the traps situated at < 200 m than at the other elevations. The highest content of V. crabro was found in the traps at 401–600 m. This finding is corroborated by the positive correlation found between the content of V. crabro and the altitude (r = 0.196; P < 0.001) (Table 1).
Fig. 3

Means and 95% least significant difference (LSD) intervals for average content of V. velutina (a) and V. crabro (b) according to the different altitude ranges of the territory studied

A linear regression model including mean relative humidity, minimum temperature and altitude was applied to predict the appearance of V. velutina in the study area (Table 2). The model explained 42% of the variance in the data and had an F value of 23.76 and a significance of P < 0.01.
Table 2

Results of the stepwise lineal regression analysis for the prediction of V. velutina presence

Model summary

R

R 2

Adjusted R2

Standard error

F

P

 

0.67

0.44

0.42

9.06

23.76

< 0.000

Coefficients

 

B

Standard error for B

Beta

t

P

 

Intercepted

− 39.51

12.96

 

− 3.05

0.003

 

R.H. mean

0.67

0.16

0.35

4.18

<  0.000

 

T. minimum

0.93

0.44

0.23

2.11

0.038

 

Altitude

− 0.02

0.01

− 0.29

− 2.58

0.012

Vespa velutina = − 39.51 + 0.67 R.H. mean + 0.93 T. minimum − 0.02 altitude

Influence of nest vicinity

Vespa velutina began to disperse in our territory at the end of 2012 when the first colonies were detected. By 2017, more than 26,000 nests were detected in the area based on the expansion of this species from coastal to inland locations (Fig. 3). The species have been confirmed at altitudes > 600 m above the sea level. The number of nests in interior areas at higher altitudes has increased over time. Nevertheless, V. velutina still prefers to settle in coastal areas. A strong correlation was found between the number of nests and the altitude (r = 0.572; P < 0.001) (Table 1).

Reported primary nests were found mainly in human habitations. Secondary nests were observed in treetops and represented the highest percentage of nests recorded (Table 3). Vespa velutina prefers to nest in wild deciduous trees like Alnus glutinosa (L.) Gaertn., Populus alba L., Betula sp., Juglans regia L., Castanea sativa Mill., Quercus robur L., and Salix sp., fruit trees such as Pyrus sp, Malus sp., Prunus sp. and Ficus carica L., and ornamentals. However, they also use perennials, especially Eucalyptus globulus Labill., Pinus sp., Cedrus sp., Picea sp, and Cupressus sp.. Vespa velutina nests have also been detected in Laurus nobilis, Ligustrum sp., Olea europaea, Quercus ilex, Quercus suber L., and Citrus sp. Also nests were found in bushes, inside old or abandoned hives and underground.
Table 3

Distribution of the nests (%) according to the year and their habitats

Location

2012

2013

2014

2015

2016

2017

Tree

      

 Deciduous

100.0

0.0

44.7

48.7

40.4

35.6

 Perenne

0.0

10.0

24.5

13.6

8.2

6.7

 Conifer

0.0

10.0

5.7

4.4

3.0

3.2

 Unknown

0.0

0.0

4.0

4.9

6.9

8.4

Underground

0.0

0.0

1.0

1.7

2.3

2.4

Beehive

0.0

0.0

0.1

0.1

0.1

0.2

Building trade

0.0

20.0

15.2

22

27.5

33.9

Vegetation

0.0

0.0

1.3

1.6

2.0

1.7

Other

0.0

60.0

3.5

3.0

9.5

7.9

Discussion

The yellow-legged hornet was introduced into Galicia in the north on the Cantabric coast and the south-west on the Atlantic coast simultaneously (Fig. 4). This spread of two separate and probably different populations at the same time partially explains the rapid dispersal of V. velutina in this territory. The predisposition to install the nest in urban and semi-urban environments makes are easily visible the invasion. These nests can house more than 13,000 individuals (Rome et al. 2015). This species has a substantial negative socio-economic impact on this region, especially in the beekeeping industry, since V. velutina workers attack beehives and use the bees as a source of protein. Some authors reported that the relative impact of V. velutina on honeybee colonies depends on predation pressure (Arca et al. 2014; Monceau et al. 2013b, 2014b). However, little information is actually available. Beekeeping has been practiced in Galicia since antiquity. In recent decades, apiculture has become more technologically advanced. There are more than 150,000 hives in the region. Most of these are organised in small apiaries (< 30 hives) and are located in rural and semi-urban areas where there is an abundance of V. velutina. About 3,000 beekeepers maintain these small apiaries, and they have incurred the greatest economic losses as a consequence of V. velutina invasion.
Fig. 4

Number of nests of V. velutina from 2013 until the end of 2017 and their location in Galicia

The first method used to control this pest was the placement of bait traps to capture colony-founding queens. In this way, the number of nests in the environment will be reduced. However, this type of trap inevitably captures other insect species including Diptera and Hymenoptera which play fundamental roles as pollinators. Bait traps have been set by beekeepers and other groups of the society in Galicia since 2015. Various attractants have been used to capture the yellow-legged hornet. These include homemade attractants and various commercial products used primarily in temperate regions to control invasive social wasp species. According to Landolt and Zhang (2016), the attraction of the wasps to these chemicals is related to their food- or prey-finding behaviours. However, the attractant used in bait traps is not specific to V. velutina since the traps caught a broad array of insects individuals. These latter play key roles in the ecosystems. In general, these individuals develop beneficial functions such as pollination, organic matter removal on soil, are part of the diet of many animals, or can prevent the overpopulation of some species (Hymenoptera (bees, bumblebees, wasps and ants), Diptera (flies and mosquitoes), Lepidoptera (butterflies and moths), Coleoptera (weevils, rose chafer), Neuroptera (lacewing), Odonata (dragonfly)). However, there are species that can be considered pests by changing the current structure of our ecosystems (invasive species (V. velutina) or fruit flies (Ceratitis capitata)). Wide diversity of captured insects has been reported in other V. velutina monitoring studies (Dauphin and Thomas 2009; Haxaire and Villemant 2010; Monceau et al. 2012). An attractant specific to the yellow-legged hornet is needed to minimise the adverse impact of bait traps on pollinator biodiversity. Some studies provide information on the development of food-based attractants (hive products and protein sources), pheromones produced by honeybee, or V. velutina sex pheromones (Couto et al. 2014; Wen et al. 2017). To improve the efficacy of these attractant, it is necessary to account for the variables that enable V. velutina to adapt to the substance and its environment.

The variations in the landscape characteristic of this territory may either promote or inhibit V. velutina dispersal. The results indicated that altitude is highly correlated with the diffusion of this species and with the number of individuals caught in the bait traps. Altitude is one of the first variables considered when monitoring various species in a region because it defines the characteristics of the territory. Several studies have shown that V. velutina rapidly expands through coastal areas, and it prefers lower altitudes for the establishment of its colonies. In these areas, there are valuable resources (seafood) that could be used for the development of their colonies (Monceau and Thiéry 2017). In contrast, the interior mountain areas may actually be a barrier to V. velutina dispersal expansion (Villemant et al. 2011; Porporato et al. 2014; Bertolino et al. 2016; Robinet et al. 2017). Vespa crabro was captured mainly at higher altitudes and seems better adapted to these conditions. On the other hand, V. velutina was more frequently observed in coastal areas. Nevertheless, the speed and intensity of the spreading through the main part of the territory seem to indicate an uncertain future. Both hornets have similar honeybee predation patterns, but the native species, which is well-adapted to the territory, has not had a significantly negative influence on local beekeeping. However, V. velutina despite is recently introduced, is most common in the territory and the impact in honeybee colony could considered very high.

Meteorological conditions can also affect the expansion of this species. Some studies used climatic suitability models to assess the risk of V. velutina invasion (Villemant et al. 2011; Barbet-Massin et al. 2013; Robinet et al. 2017). These models correlated species distributions with climate variables known to delimit niches on a large scale (Luoto et al. 2007). Our study showed that the mean and minimum temperatures were positively correlated with the presence of V. velutina, whereas the maximum temperature and temperatures > 7 °C were negatively correlated with it. Therefore, moderate temperatures favour the presence of the yellow-legged hornet. Dew temperature and relative humidity are also positively correlated with the presence of the hornet. The Asian origin of V. velutina suggests that it prefers temperate to subtropical climates. In Europe, V. velutina would tend to expand along the coastlines of the countries it invades. These include the coasts of the Atlantic, the Mediterranean, and the southern regions of the Black and Caspian seas (Villemant et al. 2011). However, the preference of coastal areas does not imply that climatic conditions are barriers to the expansion of this insect pest. Vespa velutina has proven to be able to invade many more continental areas than initially expected. The intensification of climate change increases the climatic adaptability of this species favouring its further expansion (Barbet-Massin et al. 2013; Bessa et al. 2016).

Galicia is situated in the northwestern Iberian Peninsula and consists of two widely divergent biogeographic areas. The main part has an Atlantic climate and Eurosiberian vegetation. This region has subdued temperatures and abundant rainfall. Its mild winters, cool summers, and low annual thermal oscillation favour V. velutina invasion. The yellow-legged hornet is well adapted to urban environments. Many of its nests have been located in human structures within urban and semi-urban zones, especially during the primary nesting season. By June, when there are very large numbers of workers, a much larger second nest is constructed to accommodate them. Trees are excellent installation sites for these secondary nests especially at altitudes > 15 m. No particular tree species are preferred for nesting. Nevertheless, deciduous forests and wide coastal areas intensively reforested with Eucalyptus globulus Labill. and Pinus pinaster Ait. shelter most of the secondary nests. Nests are common in fruit trees near rivers since water is a fundamental element of nest construction (Monceau et al. 2012). The wide variety of buildings in which primary and secondary nests have been constructed demonstrates the semi-urban preference of V. velutina. Nests are also becoming more common on the ground and in shrubs. The expanding distribution of V. velutina nests in both semi-urban and agricultural areas indicates that their socio-economic threat is increasing with time. Moreover, although the phytosociological Mediterranean region of Galicia has a continental climate which is not particularly conducive to the establishments of V. velutina colonies (wide temperature oscillations, cold winters, hot summers, high thermal amplitude, and scant rainfall), the species continues to spread in this area.

To our knowledge, this is the first study to correlate the weather conditions and altitude favouring the diffusion of this pest into new territories. The relative lack of information on the behaviour of V. velutina in this territory makes long-term monitoring necessary. The spread of V. velutina in Galicia is inevitable. The trapping of foundress queens of V. velutina can estimate its spreading behaviour in an area it recently colonised. Nevertheless, the effect of trapping on target and nontarget living organisms is negative. The elimination of individuals of nontarget species through this method of control also involves the capture of many other species with key roles in biodiversity and ecosystems functioning.

Author contribution

MSRF, ASR, OE and MCSC performed the experiments. MSRF and ASR were involved in acquisition, analysis, and interpretation of data. MSRF, ASR, OE, and MCSC helped in drafting and critical revision of the manuscript.

Notes

Acknowledgements

The authors thank the Agrupación Apícola de Galicia and their beekeepers for their assistance with insect trapping. We also thank the Xunta de Galicia (Consellería de Medio Rural) for the information of the nest location data and the Consellería de Medio Ambiente y Ordenación del Territorio for their financial support.

References

  1. Arca M, Papachristoforou A, Mougel F, Rortais A, Monceau K, Bonnard O et al (2014) Defensive behaviour of Apis mellifera against Vespa velutina in France: testing whether European honeybees can develop an effective collective defence against a new predator. Behav Process 106:122–129.  https://doi.org/10.1016/j.beproc.2014.05.002 CrossRefGoogle Scholar
  2. Atutxa S (2012) Detectan en Bizkaia la presencia de un ejemplar de la avispa asesina, Deia 23 Apr 2012Google Scholar
  3. Barbet-Massin M, Rome Q, Muller F, Perrard A, Villemant C, Jiguet F (2013) Climate change increases the risk of invasion by the yellow-legged hornet. Biol Conserv 157:4–10.  https://doi.org/10.1016/j.biocon.2012.09.015 CrossRefGoogle Scholar
  4. Bertolino S, Lioy S, Laurino D, Manino A, Porporato M (2016) Spread of the invasive yellow-legged hornet Vespa velutina (Hymenoptera: Vespidae) in Italy. Appl Entomol Zool 51(4):589–597.  https://doi.org/10.1007/s13355-016-0435-2 CrossRefGoogle Scholar
  5. Bessa AS, Carvalho J, Gomes A, Santarém F (2016) Climate and land-use drivers of invasion: predicting the expansion of Vespa velutina nigrithorax into the Iberian Peninsula. Insect Conserv Divers 9(1):27–37.  https://doi.org/10.1111/icad.12140 CrossRefGoogle Scholar
  6. Castro L, Pagola-Carte S (2010) Vespa velutina lepeletier, 1836 (Hymenoptera: Vespidae), recolectada en la Península Ibérica. Heteropterus Rev Entomol 10(2):193–196Google Scholar
  7. Couto A, Monceau K, Bonnard O, Thiéry D, Sandoz JC (2014) Olfactory attraction of the hornet Vespa velutina to honeybee colony odors and pheromones. PLoS ONE 9(12):e115943.  https://doi.org/10.1371/journal.pone.0115943 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Dauphin P, Thomas H (2009) Quelques données sur le contenu des pièges à frelons asiatiques posés à Bordeaux (Gironde) en 2009. Bulletin de la Société Linnéenne de Bordeaux 37:287–297Google Scholar
  9. de Castro M, Lorenzo N, Taboada JJ, Sarmiento M, Alvarez I, Gomez-Gesteira M (2006) Influence of teleconnection patterns on precipitation variability and on river flow regimes in the Miño River basin (NW Iberian Peninsula). Clim Res 32(1):63–73CrossRefGoogle Scholar
  10. EFE (2012) Detectan en Aramaio ejemplares de la avispa asiática, Deia 20 Sept 2012Google Scholar
  11. Grosso-Silva JM, Maia M (2012) Vespa velutina Lepeletier, 1836 (Hymenoptera, Vespidae), new species for Portugal. AEGA 6:53–54Google Scholar
  12. Haxaire J, Villemant C (2010) Impact sur l’entomofaune des pièges à frelon asiatique. Insectes 159(4):1–6Google Scholar
  13. Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33(1):181–233.  https://doi.org/10.1146/annurev.ecolsys.33.010802.150444 CrossRefGoogle Scholar
  14. IBM Corp. (2013) IBM SPSS Statistics for Windows, Version 22.0. Armonk, New YorkGoogle Scholar
  15. Islam N, Iftikhar F, Mahmood R (2015) Seasonal variation in hornets spp and efficiency of different traps as a tool for control. Am J Agric Sci 2(6):223–230Google Scholar
  16. Landolt P, Zhang QH (2016) Discovery and development of chemical attractants used to trap pestiferous social wasps (Hymenoptera: Vespidae). J Chem Ecol 42(7):655–665.  https://doi.org/10.1007/s10886-016-0721-z CrossRefPubMedGoogle Scholar
  17. López S, González M, Goldarazena A (2011) Vespa velutina lepeletier, 1836 (Hymenoptera: Vespidae): first records in Iberian Peninsula. Bull OEPP 41(3):439–441CrossRefGoogle Scholar
  18. Lorenzo MN, Taboada JJ (2005) Influences of atmospheric variability on freshwater input in Galician Rias in winter. J Atmos Ocean Sci 10(4):377–387.  https://doi.org/10.1080/17417530601127472 CrossRefGoogle Scholar
  19. Lorenzo MN, Taboada JJ, Gimeno L (2008) Links between circulation weather types and teleconnection patterns and their influence on precipitation patterns in Galicia (NW Spain). Int J Climatol 28(11):1493–1505.  https://doi.org/10.1002/joc.1646 CrossRefGoogle Scholar
  20. Luoto M, Virkkala R, Heikkinen RK (2007) The role of land cover in bioclimatic models depends on spatial resolution. Glob Ecol Biogeogr 16(1):34–42.  https://doi.org/10.1111/j.1466-822x.2006.00262.x CrossRefGoogle Scholar
  21. Martínez-Cortizas A, Pérez-Alberti A (1999) Atlas climático de Galicia. Consellería de Medio Ambiente-Xunta de Galicia, Santiago de CompostelaGoogle Scholar
  22. Monceau K, Thiéry D (2017) Vespa velutina nest distribution at a local scale: an 8-year survey of the invasive honeybee predator. Insect Sci 24(4):663–674.  https://doi.org/10.1111/1744-7917.12331 CrossRefPubMedGoogle Scholar
  23. Monceau K, Bonnard O, Thiéry D (2012) Chasing the queens of the alien predator of honeybees: a water drop in the invasiveness ocean. OJE 2(04):183–191.  https://doi.org/10.4236/oje.2012.24022 CrossRefGoogle Scholar
  24. Monceau K, Maher N, Bonnard O, Thiéry D (2013a) Predation pressure dynamics study of the recently introduced honeybee killer Vespa velutina: learning from the enemy. Apidologie 44(2):209–221.  https://doi.org/10.1007/s13592-012-0172-7 CrossRefGoogle Scholar
  25. Monceau K, Arca M, Leprêtre L, Mougel F, Bonnard O, Silvain JF et al (2013b) Native prey and invasive predator patterns of foraging activity: the case of the yellow-legged hornet predation at European honeybee hives. PLoS ONE 8(6):e66492.  https://doi.org/10.1371/journal.pone.0066492 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Monceau K, Bonnard O, Thiéry D (2014a) Vespa velutina: a new invasive predator of honeybees in Europe. J Pest Sci 87(1):1–16.  https://doi.org/10.1007/s10340-013-0537-3 CrossRefGoogle Scholar
  27. Monceau K, Bonnard O, Moreau J, Thiéry D (2014b) Spatial distribution of Vespa velutina individuals hunting at domestic honeybee hives: heterogeneity at a local scale. Insect Sci 21(6):765–774.  https://doi.org/10.1111/1744-7917.12090 CrossRefPubMedGoogle Scholar
  28. Monceau K, Maher N, Bonnard O, Thiéry D (2015a) Evaluation of competition between a native and an invasive hornet species: Do seasonal phenologies overlap? Bull Entomol Res 105(4):462–469.  https://doi.org/10.1017/S0007485315000280 CrossRefPubMedGoogle Scholar
  29. Monceau K, Moreau J, Poidatz J, Bonnard O, Thiéry D (2015b) Behavioral syndrome in a native and an invasive hymenoptera species. Insect Sci 22(4):541–548.  https://doi.org/10.1111/1744-7917.12140 CrossRefPubMedGoogle Scholar
  30. National Weather Service (2017) Meteogalicia-Xunta de Galicia http://www.meteogalicia.es/. Accessed 26 Jan 2018
  31. Neiker-Tecnalia (2010) Avispa “Vespa velutinahttp://www.avisosneikercom/c/plagas/avispa-vespa-velutina/. Accessed 26 Jan 2018
  32. Porporato M, Manino A, Laurino D, Demichelis S (2014) Vespa velutina Lepeletier (Hymenoptera Vespidae): a first assessment 2 years after its arrival in Italy. Redia 97:189–194Google Scholar
  33. Robinet C, Suppo C, Darrouzet E (2017) Rapid spread of the invasive yellow-legged hornet in France: the role of human-mediated dispersal and the effects of control measures. J Appl Ecol 54(1):205–215.  https://doi.org/10.1111/1365-2664.12724 CrossRefGoogle Scholar
  34. Rome Q, Perrard A, Muller F, Villemant C (2011) Monitoring and control modalities of a honeybee predator, the yellow-legged hornet Vespa velutina nigrithorax (Hymenoptera: Vespidae). Aliens 31:7–15Google Scholar
  35. Rome Q, Muller FJ, Touret-Alby A, Darrouzet E, Perrard A, Villemant C (2015) Caste differentiation and seasonal changes in Vespa velutina (Hym.: Vespidae) colonies in its introduced range. J Appl Entomol 139(10):771–782.  https://doi.org/10.1111/jen.12210 CrossRefGoogle Scholar
  36. Souto MJ, Balseiro CF, Pérez-Muñuzuri V, Xue M, Brewster K (2003) Impact of cloud analysis on numerical weather prediction in the Galician region of Spain. J Appl Meteorol 42(1):129–140.  https://doi.org/10.1175/1520-0450(2003)042%3c0129:IOCAON%3e2.0.CO;2 CrossRefGoogle Scholar
  37. Villemant C, Barbet-Massin M, Perrard A, Muller F, Gargominy O, Jiguet F, Rome Q (2011) Predicting the invasion risk by the alien bee-hawking Yellow-legged hornet Vespa velutina nigrithorax across Europe and other continents with niche models. Biol Conserv 144(9):2142–2150.  https://doi.org/10.1016/j.biocon.2011.04.009 CrossRefGoogle Scholar
  38. Wen P, Cheng YN, Dong SH, Wang ZW, Tan K, Nieh JC (2017) The sex pheromone of a globally invasive honey bee predator, the Asian eusocial hornet, Vespa velutina. Sci Rep 7(1):12956.  https://doi.org/10.1038/s41598-017-13509-7 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Vegetal Biology and Soil Sciences, Faculty of SciencesUniversity of VigoOurenseSpain

Personalised recommendations