**5. Control**

Control invasive alien species is difficult and expensive in the long term; therefore, every effort should be undertaken to prevent their establishment and diffusion in new areas. The many methods developed to control *V. v. nigrithorax* in Europe and in Asia outside of its native range have been previously reviewed [9,33,35,40,47].

Until now, no single control method has proved to be fully effective, but the coordinated use of several methods under an integrated pest managemen<sup>t</sup> approach should greatly reduce the impact of *V. v. nigrithorax* on honey bees and on the environment (Figure 7).

**Figure 7.** Integrated pest managemen<sup>t</sup> pyramid showing available or possible methods to control *V. v. nigrithorax*, from the low intervention and not toxic preventive methods to the high impact chemical methods that implies the use of toxic insecticides.

Control efforts may implemented against adult hornets or nests. In the first case, the baited traps used for monitoring purposes can be used either for controlling purposes, but traps are at the moment not selective enough to prevent extensive captures of non-target insects, with possible extensive impacts to native species [57,63]. Other types of control techniques are used or tested in Europe: Bucket poisoned baits, passive traps, electric traps, electric harps, badminton rackets, beehive muzzles, nest gunshot, or the use of the hornet workers as poison carriers [40].

The detection and destruction of the nests of *V. v. nigrithorax* is currently the most effective control method, especially when the nests themselves are destroyed before the reproductive phase of the colony which normally occurs in early September. In any case, it is important to search for and destroy active nests in all stages from foundation to winter [53]. Once a nest has been located, it must be destroyed in a complete way, paying special attention to killing the queen, the majority of the workers, and all the brood present in the combs.

The discovered nests should be immediately destroyed by people with specific training and equipped with suitable personal protective clothes and the necessary tools. The methods of intervention are various in relation to the place where the nests are built and the size of the colonies.

Nests are generally treated with insecticides for hornets and wasps, using also special extendable rods capable of reaching nests that are in high positions (Figure 8).

The control of the populations of *V. v. nigrithorax* is hindered by the difficulty of finding all nests. Embryo nests are small and difficult to observe; later the nests, although very voluminous, are often difficult to be located since covered by tree canopy. In fact, *V. v. nigrithorax* can build nests in several environments, such as natural, rural, and urban areas, and on different substrates [18]. They can be found on trees, shrubs, roofs or balconies of houses, inside gaps, but also in soil cavities or on rocky substrates (Figure 9).

**Figure 8.** Different methods to destroy the nests depending on their position.

**Figure 9.** Primary nest built under a roof canopy (left) and secondary nest (right) built on *Acacia dealbata* tree in Liguria Region (Italy).

## *5.1. Nest Detection*

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Several techniques are currently available to locate hornet nests, but they are all tedious, extremely labor consuming, and/or expensive [40].

The triangulation involves capturing at least three specimens and their subsequent release from various locations, in order to recording the direction of their flight; if the hornets tend to return in a straight direction, there is a good chance that the three directions they took would intersect at a point that will correspond to nest position [20,64]. The on-view tracking of tagged hornets, which are made more evident with a feather or a cotton, has been suggested [65]. The drone-assisted nest tracking, a theoretical study that uses several drones equipped with cameras capable of analysis an image of a hornet marked with a thread carrying a fluorescent Styrofoam ball, has recently been published [66].

Alternatively to these observational methods, it is possible locate the nests by using equipment developed in recent years.

The infrared thermal imaging camera has been tested in Portugal, in UK [67,68], and in Italy [69]. Radio-telemetry has been implemented in UK as a tool for tracking hornets back to their nests andefficientof [68].

environments

providingfindingcomplexA European LIFE project (LIFE STOPVESPA) has just been completed to contain the spread of *V. v. nigrithorax* in Italy by implementing an EWRRS (https://www.vespavelutina.eu/en-us/). For this reason, two prototypes of harmonic entomological radars able to track the flight of hornets in real time and quickly locate the position of nests were developed by the Polytechnic University of Turin (Italy). The radars are capable to follow the flight of hornets equipped with a passive transponder (tag). The radar emits a series of short pulses at a given frequency (9.41 GHz), which are then retransmitted at a double frequency (for this reason, it is called 'harmonic') by the tag fixed on the thorax of the hornets (Figure 10) [70,71]. The tracks obtained allow to follow the path of the hornets and locate the nests. Thanks to the high transmission power, a wide maximum operating distance of 490 m was obtained [72].

**Figure 10.** Harmonic radar able to follow the flight of hornets equipped with a passive transponder (left). On the map, the tracks obtained allowed to follow the path of the hornets and locate the nests (right).

## *5.2. Biological Control*

Identifying organisms capable of parasitizing hornets could allow the selection of potential control agents, always remembering that they could also be transmitted to native species. At the moment, there are no known effective enemies or adversities in Europe that could be used for the biological

control of *V. v. nigrithorax*. The main limitation for a biological control program is the lack of knowledge of the biology and ecology of *V. v. nigrithorax* in both the native and invaded territory.

In Asia *V. v. nigrithorax* is parasitized by *Bareogonalos jezoensis* (Yamane, 1973) (Hymenoptera Trigonalidae), but its use in biological control cannot be considered as a fighting agen<sup>t</sup> in Europe since it would also parasitize other species of wasps or other insects. Before any use of parasites or other exotic biological agents, preventive and rigorous verifications are always necessary to rule out any effects on other native species [73].

In France, larval forms of the *Conops vesicularis* (Diptera Conopidae) were found, inside the abdomen of some individuals of *V. v. nigrithorax*, which resulted in their death [57,74]. Spradbery [75] reports that adults of *C. vesicularis* can wait at the entrance of the nest for homing workers, attack them and oviposit their eggs. So individuals of *V. v. nigrithorax* may be parasitized by this species in the environment, during foraging activity, or near the nest. However, the effectiveness of *C. vesicularis* as a biological agen<sup>t</sup> for controlling *V. v. nigrithorax* populations appears limited.

Another potential parasite of *V. v. nigrithorax* has been confirmed by Villemant et al. [76], with the discovery of *Pheromermis vesparum* (Nematoda Mermithidae). This parasite was found in adult specimens of *V. v. nigrithorax* in France on two occasions, in November 2012 at Dompierre-sur-Besbre, and in January 2013 in Issigeac. However, even in this case, its effectiveness as biological control agen<sup>t</sup> appears limited, as they are the only two cases of nematodes found on *V. v. nigrithorax* specimens throughout Europe.

In France, an entomopathogenic fungus (*Beauveria bassiana*) has been described to infect the common wasp *Vespula vulgaris* [77]. French researchers are studying if it is therefore likely to infect other hornets such *V. v. nigrithorax*. Poidatz et al. [78] describe *Metarhizium robertsii* as potential biological control agents against the invasive hornet *V. v. nigrithorax*.

Some species of mammals (as *Meles meles*) and birds (as *Garrulus glandarius*, *Merops apiaster*, *Parus major, Pica pica, Sitta europaea,* and *Gallus gallus domesticus*) can prey upon *V. v. nigrithorax*, but the predatory activity carried out by these animals is essentially sporadic and not enough to limit the population of the hornet; *Pernis apivorus* was also reported to exploit active *V. v. nigrithorax* nests [38,79].
