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. 2023 Nov 1;10(1):e1310. doi: 10.1002/vms3.1310

The oriental hornet (Vespa orientalis) as a potential vector of honey bee's pathogens and a threat for public health in North‐East Italy

Paolo Zucca 1, Anna Granato 2,✉, Franco Mutinelli 2, Eliana Schiavon 3, Fulvio Bordin 2, Marco Dimech 4, Roberto Andrea Balbo 4, David Mifsud 5, Maurizio Dondi 6, Claudio Cipolat‐Gotet 6, Marie Christin Rossmann 7, Metka Pislak Ocepek 8, Dino Scaravelli 9, Manlio Palei 1, Luca Zinzula 10, Kimberly Spanjol 11
PMCID: PMC10766061  PMID: 37909468

Abstract

Background

Oriental hornets are large predatory hymenoptera that occur in the southern part of Asia and the southeastern Mediterranean. Among many pests of bee colonies, Vespa orientalis was recorded to be one of the most destructive.

Objectives

The aim of this study was to: (1) monitor the presence of pathogens carried by V. orientalis that could potentially threaten honey bees and public health; (2) describe the hornet's predatory behavior on honey bee colonies and (3) collect the medical history of a V. orientalis sting suffered by a 36‐year‐old woman.

Methods

Observations of V. orientalis predatory behavior and the catches of hornets for parasitological and microbiological examination, using molecular and bacteriological analyses, were carried out in three experimental apiaries, both in spring in order to capture the foundress queens and during the summer to capture the workers. Furthermore, the medical history and photographic documentation of a V. orientalis sting suffered by a 36‐year‐old woman have been collected.

Results

The results obtained highlight that V. orientalis is capable of causing serious damage to beekeeping by killing bees, putting under stress the honey bee colonies and by potentially spreading honey bee pathogens among apiaries. These hornets may also become a public health concern, since they are capable of inflicting multiple, painful stings on humans.

Conclusions

Only the development of an Integrated Management Control Program will be able to contain the negative effects of anomalous population growth and the potentially negative impact on honey bees and public health of V. orientalis.

Keywords: Apis mellifera, honey bee health, oriental hornet, public health, vector, Vespa orientalis

Over the past years, the oriental hornet has colonized several European countries and among many pests of bee colonies, V. orientalis was recorded to be one of the most destructive. This study shows that the oriental hornet is capable of causing serious damage to beekeeping by killing bees, putting under stress the bee colonies and by potentially spreading honey bee pathogens among apiaries. These hornets may also become a public health concern, since they are capable of inflicting multiple, painful stings on humans.

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1. INTRODUCTION

Oriental hornets (Vespa orientalis Linnaeus, 1771) are large eusocial predatory hymenoptera of the family Vespidae. Global warming and the globalized movement of people and goods are the main factors that are facilitating the expansion of historical distribution and the colonization of new territories by V. orientalis (Archer, 1998; Graziani and Cianferoni, 2021; Mahfouz et al., 2022). They originally appeared in the southern part of southwest Asia (Khoobdel et al., 2014), India, the Middle East, North‐eastern/Eastern Africa (Fouad et al., 2021) and the South‐eastern Mediterranean Area (Ćetković, 2003; Temreshev, 2018). Over the past few years, partly thanks to anthropogenic introductions, V. orientalis has also colonized several European countries, recorded since 2012 in Spain (Hernández et al., 2013), 2019 in Romania (Zachi and Ruicanescu, 2021) and 2021 in France (Brunet et al., 2022; Gereys et al., 2021) and the Greek islands (Ceccolini, 2022) (Figure 1). The distribution of V. orientalis in Italy was historically mostly confined to Sicily, Calabria, Campania and Lazio, but has greatly extended its range, and the hornet is now also present in Tuscany, Sardinia, Liguria and Friuli Venezia Giulia (Bressi et al., 2019; Graziani and Cianferoni, 2021) with different population densities. In Malta the species has been reported as indigenous since it has been recorded in literature for almost a century (Valletta, 1983). However, in recent years, the V. orientalis population growth curve has exponentially increased all around the island (Arena, 2022). This hornet has also been introduced by humans to Chile, Mexico and China (Dvořák, 2006; Ríos et al., 2020).

FIGURE 1.

FIGURE 1

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Current distribution map of V. orientalis based on 1627 geo‐referenced records (iNaturalist, 2023).

The length of V. orientalis is 25–35 mm, with queens larger than the drones (males) and workers. The body is reddish‐brown, with sulphur‐yellow bands on the abdomen and yellow patches between the eyes (Figure 2). Males have longer antennal segments than females. They are sometimes confused with the European hornet (Vespa crabro) or with the Asian hornet (Vespa velutina) because all three species show predatory behaviour toward honey bees (Apis mellifera). The activity pattern of V. orientalis is different from that of all the other hornets since this species is the only one able to use solar radiation to produce energy. Their cuticular pigments are able to absorb part of the solar radiation, and some form of solar energy harvesting is performed in the cuticle (Ishay et al., 2004; Plotkin et al., 2010). Thanks to this unique physiological peculiarity, while most hornet's species exhibit a peak of activity in the early morning and evening, V. orientalis shows a peak of activity in the middle of the day (Ishay, 1976). The stronger the insolation, the more intense the flight activity and vice versa (Plotkin et al., 2009). The particular physiological and sensory endowments of these hornets are not limited to the ability for using solar energy. In fact, they are also characterized in the abdominal cuticle by a dense distribution of peripheral electromagnetic receptors that might be the sensory organs of a complex gravity detection system (Ishay et al., 2004; Jongebloed et al., 1999).

FIGURE 2 .

FIGURE 2 

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Vespa orientalis worker feeding on flowers, lateral, frontal and posterior view, Trieste harbuor 2022.

In temperate zones, the biological cycle of V. orientalis colonies is annual (Archer, 1998). After winter hibernation, the foundress queens seek out a suitable site for nesting in spring for building the so‐called primary nest, which consists of about 20–30 cells. After about a month, towards mid‐June, the first workers relieve the queen from the ordinary management of the nest and from the procurement of food for the developing brood, allowing her to devote herself only to oviposition. At this point, the queen no longer needs to leave the nest, and thanks to the activity of the workers the colony grows until it reaches a considerable size and number with peaks of up to 400 individuals. The colony, with seasonal variations linked to latitude, reaches its maximum development during the summer months. The new foundress queens born from each nest mate with the drones at the end of the summer and beginning of the autumn, will be mated before hibernating in cavities and ravines to start a new cycle the following year.

Despite the fact that a number of pests attack A. mellifera colonies, V. orientalis was recorded to be one of the most destructive because it causes heavy losses and the spread of bee pathogens among apiaries (Arena, 2022; Nowar, 2016; Sweelam et al., 2019). Adults are fed carbohydrates and sugary substances such as nectar, honeydew and ripe fruits (Archer, 1998; Smith‐Pardo et al., 2020), while oriental hornet's larvae need a great amount of proteins in order to develop properly. Therefore, V. orientalis feeds their brood mainly with animal proteins represented by large‐bodied insects like grasshoppers, flies and especially honey bees. Active hunting behaviour is always associated with scavenger activities because the protein sources are also represented by fresh or spoiled meat and fish. The greatest impact of predation on A. mellifera hives occurs usually from July to November, coinciding with the exponential growth in protein demand by V. orientalis larvae. The hives are a favourite source of food since they make available to this predator both the proteins of animal origin destined to feed the larvae, and the sugary substances preferred by adults to this predator (Archer, 1998; Baracchi et al., 2010; Castro and del Pico, 2021; Villemant et al., 2010). The negative impact of the oriental hornet on the bee's health and consequently on the honey production is not limited to the damage caused by the direct predation of bees but must also take into consideration the capacity of this species to act as a potential vector and spreader for pathogens of honey bees. A biomolecular investigation carried out in Italy has isolated the presence of six honey bee viruses in V. orientalis as follows: Acute Bee Paralysis Virus (ABPV), Black Queen Cell Virus (BQCV), Chronic Bee Paralysis Virus (CBPV), Deformed Wing Virus (DWV), Kashmir Bee Virus (KBV) and Sacbrood Virus (SBV). In two‐thirds of the cohort examined (20 on 30 samples processed), several co‐infections were also identified (Power et al., 2022). Oriental hornets can also be a public health concern, since these large, aggressive insects are capable of inflicting multiple, painful bites and stings (Nejabat et al., 2022; USAPHC, 2022). They are not more aggressive than the other hornet species like V. crabro, but considering that these insects prefer to establish colonies and forage for food and water in densely populated urban areas, the probability of contact, even involuntary, between oriental hornets and humans is much higher than for other hornet species that instead nest in wooded environments far from the cities (Dehghani et al., 2019).

The aim of this study is to monitor the presence of pathogens carried by Vespa orientalis that could potentially threaten honey bees and public health. The decision to carry out a field experiment in the Province of Trieste, North East Italy, is motivated by the fact that this city has only recently been colonized by the oriental hornet, which has presumably arrived with the goods unloaded from ships in the local commercial port. The first sightings of an anomalous hornet by local beekeepers date back to 2016, while a validation of this observation by entomologists took place a few years later (Bressi et al., 2019). Currently, V. orientalis has colonized the urban centre of the city and is expanding year after year towards the suburbs. Furthermore, during the summer of 2022 we had the opportunity to collect the medical history and produce photographic documentation of a V. orientalis sting suffered by a 36‐year‐old woman.

2. MATERIALS AND METHODS

2.1. Observations of predatory behaviour

Since February 2022, three experimental apiaries have been set up, each consisting of three Dadant‐Blatt hives with three bee colonies (hybrids of Apis mellifera ligustica × A. m. carnica) in different positions and altitudes. The first apiary was installed in an urban park located in the centre of the city and was identified as ‘apiary 1– urban’; the second apiary was installed in an inhabited but peripheral area of the city at a higher altitude than the first, about 200 m above sea level (a.s.l.) and was identified as ‘apiary 2 – suburb hill’; while the third apiary was installed in the thick of the woods in an uninhabited area 4 km away, far from the city center, at an altitude even higher than the previous locations, equal to about 300 m a.s.l. and it has been identified as ‘apiary 3– karst wood.’ Behavioural observations relating to the presence and predatory behaviour of V. orientalis on honey bee colonies were carried out systematically in the three experimental apiaries, with 3 weekly hours of observation divided into 20‐min‐period randomized within the days of the week. The aim of the behavioural observations was to describe the ethogram of the predatory behaviour of V. orientalis towards honey bees and to collect qualitative data about the stressful effect of this predatory behaviour on the beehives. The peculiar predation behaviours were photographed and videotaped with a Canon EOS 6D Mark II camera and a Canon EF 70‐300 mm 70‐300 f/4.0–5.6 L IS USM lens with image stabilizer and tripod.

2.2. Sampling

The catches aimed at carrying out the molecular and microbiological tests were carried out both in the spring (May) in order to capture the foundress queens (n = 10), and during the summer (July) to capture the workers (n = 5) in two of the three experimental apiaries (apiary 1–urban center; apiary 2– outskirts of the hills). No V. orientalis has ever been seen or captured at apiary 3– Karst wood. A purpose‐built trap cage measuring 40 × 30 × 35 h cm was used. The four sides of the trap are covered with metal mosquito net while the roof was built with a queen excluder in such a way as to allow the honey bees to get out of the trap without letting the Oriental hornets escape. The bottom is made of wood with a wire mesh cone in the center that fit inside the cage towards the roof. The cone of net allows the hornets to enter but makes it impossible to get out in analogy to what happens for fishes in pots. Salmon cat food bait was placed under the trap and replaced daily. The trapping mechanism of hornets is based on the predatory behavioural pattern of V. orientalis which, when catching a prey, tends to fly upwards rather than move sideways. Therefore, the oriental hornet alights alongside the trap, walks under the bottom to the bait, takes a piece of bait and then flying upwards with the bait in its jaws and enters the trap.

The low number of foundress queens’ samples examined was conditioned by the greater difficulty in capturing them with traps, since in addition to being fewer than the worker population, they are much more attracted to hives and slightly less to the baits used to get them into the traps. Ten foundress queens were captured, and all hornets were subjected to gross examination to identify the presence of lesions. Only four were considered suitable for carrying out the examinations, as they were in perfect storage condition and not contaminated or ruined by ants or other insects. The number of workers was calibrated accordingly. The subjects were frozen and immediately sent to the Italian National Reference Laboratory for honey bee health at the Istituto Zooprofilattico Sperimentale delle Venezie, Legnaro (Padua), Italy, without being washed or treated in any other way. Although ethical review and approval are not required for studies on insects, the sampling procedures of this study were carried out in such a way as to cause the least possible harm to the hornets.

2.3. Laboratory investigations

Before laboratory investigations, V. orientalis samples were macroscopically examined to evaluate the possible presence of morphological alterations or parasites.

The investigated pathogens and the methods used for their detection are given in Table 1.

TABLE 1.

Investigated pathogens and methods used.

Pathogens Laboratory techniques
Nosema spp. Microscopic analysis
Acute Bee Paralysis Virus (ABPV) One step real time RT‐PCR
Chronic Bee Paralysis Virus (CBPV) One step real‐time RT‐PCR
Deformed Wing Virus (DWV) One step real time RT‐PCR
Black Queen Cell Virus (BQCV) One step real time RT‐PCR
Sacbrood Bee Virus (SBV) One step real time RT‐PCR
Israeli acute paralysis Virus (IAPV) RT‐PCR
Kashmir bee virus (KBV) RT‐PCR
Lotmaria passim PCR
Crithidia mellificae PCR
Salmonella spp. Microbiology examination
Listeria spp. Microbiology examination
Bacteriology panel Maldi‐TOF
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For parasitological and viral examination, each sample was analysed individually, while bacteriological tests were performed on a pool of individuals, divided into the sub‐groups of ‘foundress queens’ and ‘workers’. To detect the presence of Nosema spp. spores, honey bee viruses and trypanosomatids (Lotmaria passim and Crithidia mellificae), each individual was homogenized by Tissue Lyser II (Qiagen) (2 cycles, 1 min each, at 30 Hz) in the presence of a 5 mm stainless steel bead and 1 mL of PBS. The presence of Nosema spp. spores was evaluated examining about 30 μL of homogenate on a slide by light microscopy at 400×. For honey bee viruses and trypanosomatids detection, RNA and DNA extraction were performed starting from 200 μL of homogenate using the High Pure Viral Nucleic Acid Kit (Roche Diagnostics) and QIAamp® DNA Mini Kit (Qiagen), respectively, according to manufacturer's instructions. Molecular diagnosis was then carried out as previously described by Bordin et al. (2022). Bacterial isolation was performed according to standard laboratory culture techniques. Briefly, the pool of all the subjects was diluted in 1 mL of nutritive broth (Heart Infusion Broth, HIB); 10 and 100 μL from this suspension were respectively inoculated into different solid media such as Nutrient blood agar and MacConkey agar to search for aerobic microorganisms. Nutrient blood agar (Blood Agar Base n° 2, BA, Biolife), with 5% sterile de‐fibrinated sheeps blood (Allevamento Blood, Teramo) and MacConkey agar (home produced) were inoculated and incubated at 22 ± 1°C for 24 h under aerobic conditions. The culture media were evaluated at 24 h and in case of absence of bacterial growth on the agar culture media, but turbidity of the nutrient broths, the plates were re‐incubated for a further 24 h, and broth seeding was performed as previously described. Species identification was performed by MALDI‐TOF MS Microflex LT instrument (MALDI Biotyper, Bruker Daltonics) equipped with FlexControl software (version 3.3, Bruker Daltonics). The result of the analysis is expressed with the full name of the microorganism being tested, accompanied by the identification reliability score provided by the instrument. The score value will be between 0 and 3 and the reliability of the identification must be interpreted according to the following legend: score < 1.699: unreliable identification; score between 1.700 and 1.999: identification of probable genus; score between 2.000 and 2.299: safe genus identification and probable species identification; score > 2.300: high probability of genus and species identification.

2.4. Clinical case

An Italian 36‐year‐old woman with no previous pathology and no history of allergy to hymenoptera venoms was stung by a V. orientalis aboard a touristic boat in the port of Valletta, Malta, in the summer of 2022, when she was on vacation. The hornet was lured onto the boat, as fruits were available in a basket. The Oriental hornet landed on the left arm of the woman, who remained still. The hymenoptera was identified without any doubt as V. orientalis by both the woman and the crew of the tourist boat. The boat crews also suggested the woman not to move, however, after 1 min, the hornet stung the woman. The woman returned to Trieste, Italy, 2 days after the puncture, and we collected a detailed report of the symptoms, signs, treatment and follow‐up until the complete remission of the symptoms through face‐to‐face direct interviews.

3. RESULTS

3.1. Observations of predatory behaviour

The predation of honey bees in the urban apiary (apiary 1) has also been documented since the first days of May 2022 by the foundress queens of V. orientalis, a behaviour that has never been reported in the literature to date. The negative impact of this phase of the biological cycle induced by the foundress queens on the honey bee colonies seems to be very low from the point of view of the number of bees’ catches, but high if considering the stress on the colony. In particular, the first contact with V. orientalis is extremely stressful for the colony, which tends to reduce foraging behaviour and increase defence behavioural patterns at the entrance to the hive, especially during the afternoon hours. The predatory behavioural patterns of the foundress queens are the same as those of the workers: the hornet approaches and in a slow and insistent patrolling flight, then searches the entrance, the sides and the grid of the bottom of the hive in order to be able to capture the bees that have carelessly found themselves separated from the group. If the colony is too alarmed or there are no bees on the bottom grid, V. orientalis lands on the left or right corner of the flight board of the hive, catching the foraging bees returning or leaving the hive. Once the bee has been captured, the oriental hornet takes off and settles high on the walls or nearby trees or under the hive, flexes its abdomen, curving on itself to better tear the prey to pieces, eliminating the head, wings and abdomen. It keeps only the thorax, which contains the flight muscles and the most valuable protein nutrients. The anti‐predatory behaviour most frequently implemented by the colony was to increase the number of guardian bees defending the entrance to the hive, in such a large number as to generate a ‘bee beard’ in front of the entrance. The defensive bee ball formation behaviour has never been observed although, in some cases, the bees actively attacked and fought tenaciously, trying in vain to pierce the cuticle of the oriental hornet with their stinger, but without succeeding. The bee's sting only partially sticks into the hornet's body, and the bee cannot inject its venom (Figure 3).

FIGURE 3.

FIGURE 3

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A V. orientalis worker is dissecting a honey bee under the hive. The flexed abdomen helps the hornet to fix and cut the prey in smaller parts, keeping the thorax only.

3.2. Pathogens detection

Foundress queens and workers underwent macroscopical, parasitological, viral and bacteriological examination. All the samples investigated did not reveal the presence of morphological alterations or parasites. In addition, they were negative for Nosema spp. spores, L. passim, Chritidia mellificae, IAPV and KBV. Five different bee viruses have been identified both in hornet's foundress queens and in workers, as reported in Figure 4. The most detected honey bee viruses were BQCV (9/9 samples) and SBV (8/9 samples), followed in terms of prevalence by DWV (6/9 samples), CBPV (2/9 samples) and ABPV (1/9 samples), and the last two were detected only in workers. The rate of co‐infections with more than one of the honey bee viruses was high, and the association of BQCV and SBV was the most frequent (8/9 samples). As shown in Table 2, five (ABPV, CBPV, DWV, BQCV and SBV) and four (CBPV, DWV, BQCV and SBV) of the seven viruses investigated were identified, respectively, in worker 5 (1/9; W5) and in worker 2 (1/9; W2). Three samples (3/9; Q3, W3 and W4) tested positive for three viruses (DWV, BQCV and SBV), while in four samples (4/9; Q1, Q2, Q4 and W1) 2 viruses were detected (BQCV, SBV in Q1, Q4 and W1; DWV, BQCV in Q2).

FIGURE 4.

FIGURE 4

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Prevalence of different bee's viruses in foundress queens and workers of V. orientalis trapped in Trieste during spring (foundress queens) and summer (workers) 2022.

TABLE 2.

Honey bee virus co‐infections in V. orientalis foundress queens (Q) and workers (W).

BEE VIRUSES Q1 Q2 Q3 Q4 W1 W2 W3 W4 W5
Acute Bee Paralysis Virus (ABPV) − − − − − − − − +
Chronic Bee Paralysis Virus (CBPV) − − − − − + − − +
Deformed Wing Virus (DWV) − + + − − + + + +
Black Queen Cell Virus (BQCV) + + + + + + + + +
Sacbrood Virus (SBV) + − + + + + + + +
Israeli Acute Paralysis Virus (IAPV) − − − − − − − − −
Kashmir Bee Virus (KBV) − − − − − − − − −
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Positive (+); negative (‐).

Furthermore, three bacteria have been isolated both in foundress queens and workers, as reported in Table 3.

TABLE 3.

Positivity to different bacteria in foundress queens (pool) and workers (pool) of V. orientalis trapped in Trieste during the spring (foundress queens) and summer (workers) 2022.

BACTERIOLOGICAL EXAMINATION Queens (Spring) Workers (Summer)
Salmonella spp. negative negative
Listeria spp. negative negative
Enterococcus fecalis positive score 2.24 positive score 1.82
Lactococcus garvieae positive score 1.87 negative
Serratia marcescens negative positive score 2.02
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3.3. Clinical case of a sting victim

An Italian 36‐year‐old woman with no previous pathology and no history of allergy to hymenoptera venoms was stung by a V. orientalis. After the stung, she reported feeling severe pain with an intensity perceived as 10 on a scale of 1 to 10, described as having flames on her arm. After a few minutes, sweating began, and she suffered blood pressure lowering with chills, tachycardia and dizziness. Corticosteroids were injected at a local clinic after about 30 min. The painful symptoms and hypotension were reduced within a few hours, but the pain and inflammation at the site of inoculation of the poison extended to the entire arm. A spill with a diameter of about 10 cm formed at the injection site. The next day, the systemic symptoms disappeared but the pain, inflammation and effusion all over the arm persisted. On clinical examination 4 days after the sting, the halo of the effusion with a diameter of about 4 cm was still evident. On palpation, the area was edematous and hot. The woman complained about symptomatology related to sun exposure on the affected arm. If the area of the effusion was exposed to solar radiation, within a few minutes she suffered a strong neuralgia all over the arm up to the fingertips of the hands. This sun‐exposure‐related pain persisted for about 10 days after the sting, while the complete remission of symptoms took 2 weeks (Figure 5).

FIGURE 5.

FIGURE 5

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Blood effusion on the left arm of a woman 4 days after being stung by V. orientalis.

4. DISCUSSION

The behavioural observations made it possible to highlight that the impact of V. orientalis on the experimental honey bee apiaries was quite negative. The mere presence of a few hornets, as in the case of the few foundress queens that visit the hives in spring, is sufficient to stress the honey bee colony, which then reduces its foraging activity and remains in a constant state of alarm. After a short break in May–June, when the first contingent of workers of the oriental hornet was developing, visits and attacks on the honey bee colonies become more and more frequent, with the collapse of the weak colonies. The anti‐predatory behaviours recorded in the hybrids of A. m. ligustica × A. m. carnica are sporadic and ineffective. This observation confirms what is already described in the available literature, namely that the different subspecies of A. mellifera show different anti‐predatory responses towards attacks by hornets (Vespa spp.), with particular reference to V. crabro and V. orientalis. The Italian bee (A. m. ligustica) seems to be the most defenceless compared to the eastern subspecies (A. m. syriaca) or the Cyprus subspecies (A. m. cypria) (Glaiim, 2009; Papachristorofou et al., 2007). Moreover, the strategy of overheating the hornet with the bee ball anti‐predatory defence strategy, which in any case is very rarely implemented by the Italian subspecies, has no effect on the oriental hornet since this species is able to withstand temperatures much higher (up to 50°C) than the European hornet (V. crabro) (Castro and del Pico, 2021). Only the subspecies A. m. cypria, which has been interacting with this predator for a long evolutionary time, has modified the strategy of the anti‐predatory defence bee ball by directing it to block the hornet inside the bee ball in order to prevent it from breathing and thus causing death by asphyxiation (Papachristorofou et al., 2007).

The role of V. orientalis as a potential vector for honey bee viruses has been confirmed. However, the low number of V. orientalis samples analysed represents an objective limit of the laboratory part of this study and is linked above all to the considerable difficulty in trapping and sampling the founder queens in spring. Anyway, the detection of honey bee viruses in hornets’ foundress queens in spring supports the hypothesis that the contamination occurred the previous year, and that the pathogens persist on this species for long periods, overwintering in the new foundress queens. The high co‐infection rate with multiple viruses connotes V. orientalis as a possible bee's infection “super‐spreader,” confirming the results obtained by other authors (Power et al., 2022). Oriental hornet's damage to beekeeping is caused by concomitant predation to honey bees, colony stress and infectious agents’ transmission. These three factors prevent the collection of honey and pollen, thus, reducing winter reserves and jeopardizing the survival of the colonies during the winter. Furthermore, V. orientalis is not attacking only domestic bees, but also kills wild pollinator populations, being a generalist predator (Castro and del Pico, 2021). Therefore, the loss of so many bees has far‐reaching implications for the honey industry as well as the agricultural sector at large. Apart from the loss of honey, the important role of bees as pollinators will have an impact on local fruit trees and other indigenous flora for which the bees are essential as a pollinators.

The aspect related to the prevention of unwanted effects on human health should not be neglected, since the negative impacts of V. orientalis will be increasingly felt in situations where human–hornet co‐existence will be closer such as in cities, favourite nesting and feeding areas. The increasing contacts between oriental hornets and humans is not a problem confined only to the Middle East, the western Palearctic and the countries of the Mediterranean basin. In fact, this species has already colonized some countries of South America and based on the modelling of possible expansion in the Americas, four main regions have been identified as moderately or highly suitable for the oriental hornet: the Gulf of Mexico and some areas in western California in the USA, central west Chile and the north‐western region of Argentina (Werenkraut et al., 2022). Individuals stung by hymenoptera can have different clinical outcomes, from common local reactions to severe systemic reactions, without important differences in clinical symptoms and development of the allergic reaction depending on the different species of hornets and wasps as well as other hymenoptera (Perkins & Yates, 2018). However, it seems that immunotherapy with commercial venoms is efficacious for anaphylactic reactions to V. orientalis stings (Goldberg et al., 2013). Following the interaction between hornets and humans through the sting event, the detection of three bacteria in hornet's queens and workers (Table 3) should be taken into consideration since they can act as opportunistic pathogens in humans. Thus, they need attention and appropriate therapeutic options. Among them, Enterococcus faecalis can also act as secondary pathogen in European foulbrood of honey bees. The possible microbial hazard for humans posed by accidental contact through stinging with honey bees, wasps and hornets has been recently experimentally investigated by Gkitsaki et al. (2023). They revealed that most of the suspect colonies isolated from wasps and hornets belonged to important opportunistic bacteria known as hygienic indicators. An additional reason of concern could be the isolation of some other important opportunistic pathogens known for multidrug resistance.

The understanding of a complex and multifactorial phenomenon, such as the impact of the oriental hornets on honey bee health, human health and on the ecosystem, cannot focus only on the analysis of the proximate explanations, but must also take into consideration the evolutionary aspects—that is, why we have come to this point? Certainly, the fault is not on the oriental hornet, since among the ultimate evolutionary explanations, the main cause of the territorial and numerical expansion of this species, now considered by many to be invasive, are anthropic activities. In particular, global warming, human activities and the availability of food/garbage sources in urban areas represent some of the evolutionary explanations for why we have reached this potentially critical situation in such a short time. A multifactorial problem never has a single solution, and only the development of an Integrated Management Control Program (IMCP) will be able to contain the negative effects of anomalous population growth and the potentially negative impact on honey bee health of this hymenoptera species. The key points of the IMCP are given by: (1) correct information to the citizens; (2) implementation of an early warning and monitoring system including citizen science initiative; (3) reduction in the number of oriental hornet queens in the spring through the use of hive traps; (4) active search and removing of nests in urban areas and near apiaries during the summer months with the help of innovative technologies (Mahfouz et al., 2022; Maggiora et al., 2019; Neal et al., 2004).

AUTHOR CONTRIBUTIONS

Paolo Zucca: conceptualization, investigation, methodology, writing—original draft, writing—review & editing. Anna Granato: data curation, formal analysis, investigation, methodology, writing—original draft, writing—review & editing. Franco Mutinelli: data curation, formal analysis, investigation, methodology, writing—review & editing. Eliana Schiavon: data curation, formal analysis, investigation, methodology, writing—review & editing. Fulvio Bordin: data curation, formal analysis, investigation, methodology, writing—review & editing. Marco Dimech: writing—review & editing, Roberto Andrea Balbo: writing—review & editing. David Mifsud: writing—review & editing. Maurizio Dondi: writing—review & editing. Claudio Cipolat‐Gotet: writing—review & editing. Marie Christin Rossmann: writing—review & editing. Metka Pislak Ocepek: writing—review & editing. Dino Scaravelli: writing—review & editing. Manlio Palei: writing—review & editing. Luca Zinzula: writing—review & editing. Kimberly Spanjol: writing—review & editing.

CONFLICT OF INTEREST STATEMENT

The authors declare no conflict of interest.

FUNDING INFORMATION

The authors received no financial support for the research, authorship or publication of this article.

ETHICS APPROVAL STATEMENT AND PATIENT CONSENT STATEMENT

The present study was performed on samples either collected from live insects by Public Health Authorities for official sanitary surveillance. All samples were collected and submitted to the Italian Reference Laboratory for honey bee health. In Italy, such procedures do not require any specific ethical approval and the sampling procedures were performed in compliance with the country's own legislation and the recommendations of international institutions. According to the national legislation regulating animal experimentation, no ethical approval or permit was required for collecting and processing the type of insect's samples examined for this study. Regarding the case report of the 36‐year‐old woman stung by the Oriental hornet, the personal data collection procedure has been approved by the Data Protection Officer (DPO) of the Friuli Venezia Giulia Region (Italy) as follows: informed consent relating to the processing of personal data and of the images pursuant to Regulation 2016/679 of the European Parliament and of the Council of 27 April 2016, as well as the Italian Legislative Decree 196/03 (‘Code regarding the protection of personal data’) was obtained from the patient and the data presented in this paper have been anonymised in such a way as to not be able to trace the identity of the patient.

PEER REVIEW

The peer review history for this article is available at https://publons.com/publon/10.1002/vms3.1310

ACKNOWLEDGEMENTS

Comune di Trieste, Michela Nola, Virgilio Carboni and Piero Marcelli for their useful advices and support to the study and Dr. Adrian Ruicănescu, Institute of Biological Research Cluj‐Napoca branch of National Institute of Research and Development for Biological Sciences, Romania for the information and references provided.

Open access funding provided by BIBLIOSAN.

Zucca, P. , Granato, A. , Mutinelli, F. , Schiavon, E. , Bordin, F. , Dimech, M. , Balbo, R. A. , Mifsud, D. , Dondi, M. , Cipolat‐Gotet, C. , Rossmann, M. C. , Ocepek, M. P. , Scaravelli, D. , Palei, M. , Zinzula, L. , & Spanjol, K. (2024). The oriental hornet (Vespa orientalis) as a potential vector of honey bee's pathogens and a threat for public health in North‐East Italy. Veterinary Medicine and Science, 10, e1310. 10.1002/vms3.1310

DATA AVAILABILITY STATEMENT

The data that support the findings of this study are available from the corresponding author upon reasonable request.

REFERENCES

  1. Archer, M. E. (1998). Taxonomy, distribution and nesting biology of Vespa orientalis L. Entomologist's Monthly Magazine, 134, 45–51. [Google Scholar]
  2. Arena, J. (2022). 70 per cent of local beehives destroyed by oriental hornets. Very little honey will be produced by apiarists next year. Times of Malta . Retrieved from https://timesofmalta.com/articles/view/70‐per‐cent‐local‐beehives‐destroyed‐oriental‐hornets.988298
  3. Baracchi, D. , Cusseau, G. , Pradella, D. , & Turillazzi, S. (2010). Defence reactions of Apis mellifera ligustica against attacks from the European hornet Vespa crabro . Ethology Ecology & Evolution, 22, 281–294. 10.1080/03949370.2010.502323 [DOI] [Google Scholar]
  4. Bordin, F. , Zulian, L. , Granato, A. , Caldon, M. , Colamonico, R. , Toson, M. , Trevisan, L. , Biasion, L. , & Mutinelli, F. (2022). Presence of known and emerging honey bee pathogens in apiaries of Veneto region (Northeast of Italy) during spring 2020 and 2021. Applied Sciences, 12, 2134. 10.3390/app12042134 [DOI] [Google Scholar]
  5. Bressi, N. , Colla, A. , & Tomasin, G. (2019). Orientali Verso Nord: Insediamento di una popolazione urbana di calabrone orientale (Vespa orientalis Linnaeus 1771) a Trieste, NE Italy (hymenoptera, Vespidae). Atti Museo Civico di Storia Naturale di Trieste, 60, 273–275. [Google Scholar]
  6. Brunet, J. L. , Girodet, B. , & Pham‐Thi, N. (2022). Le frelon oriental (Vespa orientalis) arrive en France. Revue Française d'Allergologie, 62, 91–92. 10.1016/j.reval.2021.12.006 [DOI] [Google Scholar]
  7. Castro, L. , & del Pico, C. (2021). Sobre el problema de Vespa orientalis Linnaeus 1771 (hymenoptera: Vespidae) en el sur de España. Revista Gaditana De Entomología, 12, 183–206. [Google Scholar]
  8. Ceccolini, F. (2022). New records and review of the occurrence of the oriental hornet Vespa orientalis Linnaeus, 1771 in the islands of Greece (hymenoptera: Vespidae: Vespinae). Entomologia Hellenica, 31, 41–49. 10.12681/eh.28762 [DOI] [Google Scholar]
  9. Ćetković, A. (2003). Review of the European distribution of the oriental hornet (Hymenoptera, Vespidae: Vespa orientalis L.). Ekologija, 37, 1–22. [Google Scholar]
  10. Dehghani, R. , Kassiri, H. , Mazaheri‐Tehrani, A. , Hesam, M. , Valazadi, N. , & Mohammadzadeh, M. (2019). A study on habitats and behavioral characteristics of hornet wasp (Hymenoptera: Vespidae: Vespa orientalis), an important medical‐health pest. Biomedical Research, 30, 61–66. 10.35841/biomedicalresearch.30-18-1187 [DOI] [Google Scholar]
  11. Dvořák, L. (2006). Oriental hornet Vespa orientalis Linnaeus, 1771 found in Mexico (Hymenoptera, Vespidae, Vespinae). Entomololgical Problems, 36, 80. [Google Scholar]
  12. Fouad, M. , Darwish, M. , & Roby, A. E. L. (2021). Behavioral study of the dangerous insect predator (Vespa orientalis) on the honeybee colonies in Minia Region. Egyptian Journal of Plant Protection & Pathology, 12, 713–715. 10.21608/jppp.2021.205739 [DOI] [Google Scholar]
  13. Gereys, B. , Coache, A. , & Filippi, G. (2021). Présence en France métropolitaine d'un frelonallochtone: Vespa orientalis Linnaeus, 1771 (Le Frelon oriental) (hymenoptera, Vespidae, Vespinae). Faunitaxys, 9, 1–5. 10.57800/faunitaxys-9(32) [DOI] [Google Scholar]
  14. Gkitsaki, I. , Papachristoforou, A. , Michailidou, S. , Karamvalis, N. , Iliadis, I. , Graikini, D. , Sakarikou, C. , Tsoukis, E. , Argyriou, A. , & Giaouris, E. (2023). The transmittable through stinging microbiota differs between honeybees and wasps: A potentially greater microbial risk of the wasp sting for humans. International Microbiology, 26(3), 663–674. 10.1007/s10123-023-00332-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Glaiim, M. K. (2009). Hunting behaviour of the Oriental Hornet, Vespa orientalis, and defense behaviour of the honey bee, Apis Mellifera . IBulletien of Iraq Natural History Museum, 10, 17–30. [Google Scholar]
  16. Goldberg, A. , Shefler, I. , Panasoff, J. , Paitan, Y. , & Confino‐Cohen, R. (2013). Immunotherapy with commercial venoms is efficacious for anaphylactic reactions to Vespa orientalis stings. International Archives of Allergy and Immunology, 161, 174–180. 10.1159/000345139 [DOI] [PubMed] [Google Scholar]
  17. Graziani, F. , & Cianferoni, F. (2021). The northernmost record of Vespa orientalis Linnaeus, 1771 (hymenoptera: Vespidae) in peninsular Italy. Revista Gaditiana de Entomologia, 12, 173–178. [Google Scholar]
  18. Hernández, R. , García‐Gans, F. J. , Selfa, J. , & Rueda, J. (2013). Primera cita de la avispa oriental invasora Vespa orientalis Linnaeus 1771 (hymenoptera: Vespidae) en la Península Ibérica. Boletín de la SEA, 52, 299–300. [Google Scholar]
  19. iNaturalist . (2023). Oriental hornet, observations, map. Retrieved from https://www.inaturalist.org/taxa/83801‐Vespa‐orientalis
  20. Ishay, J. (1976). Comb bulding by the oriental hornet (Vespa orientalis). Animal Behaviour, 24, 72–83. 10.1016/S0003-3472(76)80101-7 [DOI] [Google Scholar]
  21. Ishay, J. S. , Pertsis, V. , Skutelsky, E. , Kalicharan, D. , & van der Want, H. (2004). Ontogenesis of peripheral electromagnetic receptors in hornets. Journal of Electronic Microscopy, 53, 281–291. 10.1093/jmicro/53.3.281 [DOI] [PubMed] [Google Scholar]
  22. Jongebloed, W. L. , Rosenzweig, E. , Kalicharan, D. , van der Want, J. J. L. , & Ishay, J. S. (1999). Ciliary hair cells and cuticular photoreceptor of the hornet Vespa orientalis as components of a gravity detecting system: an SEM/TEM investigation. Journal of Electronic Microscopy, 48, 63–75. 10.1093/oxfordjournals.jmicro.a023652 [DOI] [Google Scholar]
  23. Khoobdel, M. , Tavassoli, M. , Salari, M. , & Firozi, F. (2014). The stinging Apidae and Vespidae (Hymenoptera: Apocrita) in Iranian islands, Qeshm, Abu–Musa, Great Tunb and Lesser Tunb on the Persian Gulf. Asian Pacific Journal of Tropical Biomedicine, 4, S258–S262. 10.12980/APJTB.4.2014C1153 [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mahfouz, H. M. , & Al‐Fattah, M. A. A. (2022). Climatic changes expose honey bee colonies to eradication due to increasing ferocity of attacking predator Oriental Hornet Vespa orientalis L, in North Sinai Region. Menoufia Journal of Plant Protection, 7, 71–87. 10.21608/mjapam.2022.228663 [DOI] [Google Scholar]
  25. Maggiora, R. , Saccani, M. , Milanesio, D. , & Porporato, M. (2019). An innovative harmonic radar to track flying insects: the case of Vespa velutina . Scientific Reports, 9, 11964. 10.1038/s41598-019-48511-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Neal, M. E. O. , Landis, D. A. , Rothwell, E. , Kempel, L. , & Reinhard, D. (2004). Tracking insects with harmonic radar: A case study. American Entomology, 50, 212–218. 10.1093/ae/50.4.212 [DOI] [Google Scholar]
  27. Nejabat, S. , Haghshenas, M. R. , & Farjadian, S. (2022). Allergenome profiling of Vespa orientalis venom by serum IgE in patients with anaphylactic reaction to this hornet sting. Toxicon, 214, 130–135. 10.1016/j.toxicon.2022.05.039 [DOI] [PubMed] [Google Scholar]
  28. Nowar, E. E. (2016). Oriental hornet (Vespa orientalis) as AFB disease vector to honeybee (Apis mellifera L.) colonies. Middle East Journal of Applied Sciences, 06, 934–940. [Google Scholar]
  29. Papachristoforou, A. , Rortais, A. , Zafeiridou, G. , Theophilidis, G. , Garnery, L. , Thrasyvoulou, A. , & Arnold, G. (2007). Smothered to death: hornets asphyxiated by honeybees. Current Biology, 17, R795–R796. 10.1016/j.cub.2007.07.033 [DOI] [PubMed] [Google Scholar]
  30. Perkins, J. B. , & Yates, A. B. (2018). Allergy to stinging insects: diagnosis and management. European Medical Journal Allergy and Immunology, 3(1), 99–105. 10.33590/emjallergyimmunol/10314229 [DOI] [Google Scholar]
  31. Power, K. , Altamura, G. , Martano, M. , & Maiolino, P. (2022). Detection of honeybee viruses in Vespa orientalis . Frontiers Cellular Infectious Microbiology, 12, 896932. 10.3389/fcimb.2022.896932 [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Plotkin, M. , Volynchik, S. , Itzhaky, D. , Lis, M. , Bergman, D. J. , & Ishay, J. S. (2009). Some liver functions in the oriental hornet (Vespa orientalis) are performed in its cuticle: exposure to UV light influences these activities. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 153, 131–135. 10.1016/j.cbpa.2009.01.016 [DOI] [PubMed] [Google Scholar]
  33. Plotkin, M. , Hod, I. , Zaban, A. , Boden, S. A. , Bagnall, D. M. , Galushko, D. , & Bergman, D. J. (2010). Solar energy harvesting in the epicuticle of the oriental hornet (Vespa orientalis). Naturwissenschaften, 97, 1067–1076. 10.1007/s00114-010-0728-1 [DOI] [PubMed] [Google Scholar]
  34. Ríos, M. , Barrera‐Medina, R. , & Contreras, J. M. (2020). Primer reporte del género Vespa Linnaeus (Hymenoptera: Vespidae: Vespinae) en Chile. Revista Chilena de Entomologia, 46, 237–242. 10.35249/rche.46.2.20.14 [DOI] [Google Scholar]
  35. Smith‐Pardo, A. H. , Carpenter, J. M. , & Kimsey, L. (2020). The diversity of hornets in the genus Vespa (hymenoptera: Vespidae Vespinae), their importance and interceptions in the United States. Insect Systematics and Diversity, 4, 1–27. 10.1093/isd/ixaa006 [DOI] [Google Scholar]
  36. Sweelam, M. E. , Abdelaal, A. A. , Khattaby, A. M. , & Mettwaly, Y. A. (2019). Integrated management of Vespa orientalis in honeybee colonies at Elsharkia governorate. Menoufia Journal of Plant Protection, 4, 163–172. [Google Scholar]
  37. Temreshev, I. I. (2018). On the expansion of the areas of Vespa orientalis and Polistes wattii (Hymenoptera: Vespidae) on the territory of the Republic of Kazakhstan. Acta Biologica Sibirica, 4, 38–45. 10.14258/ABS.V4I1.3915 [DOI] [Google Scholar]
  38. USAPHC . (2022). Oriental Hornets, FACT SHEET 18‐074‐0616, U.S. Army Public Health Center. Retrieved from https://usaphc.amedd.army.mil/PHC%20Resource%20Library/OrientalHornets_FS_18‐074‐0616.pdf
  39. Valletta, A. (1983). Mit‐Tfulija man‐Natura, Interprint Malta.
  40. Villemant, C. , Rome, Q. , & Muller, F. (2010). Vespa velutina, un nouvel envahisseur prédateur d'abeilles. La lettre de la SECAS, 62, 14–18. [Google Scholar]
  41. Werenkraut, V. , Arbetman, M. P. , & Fergnani, P. N. (2022). The oriental hornet (Vespa orientalis L.): a threat to the Americas? Neotropical Entomology, 51, 330–338. 10.1007/s13744-021-00929-4 [DOI] [PubMed] [Google Scholar]
  42. Zachi, M. , & Ruicanescu, A. (2021). Vespa orientalis, a new alien species in Romania. Travaux du Muséum National d'Histoire Naturelle, 64, 67–72. 10.3897/travaux.64.e61954 [DOI] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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