Distribution,spread, and impact of the invasive hornet Vespa velutina in South Korea

Hornets (Vespa spp) are top insect predators that can control pests, but their venomous stings and defensive behavior cause numerous human deaths throughout Asia. Hornets usually inhabit rural areas which reduces potential conflict with humans. In 2003, the invasive hornet, Vespa velutina, arrived in southern Korea (Yeongdo region) and became established. It is currently spreading northwards at a rate of 10–20 km per year. Despite originating in tropical/subtropical areas of Indo-China, its nesting biology and life cycle in South Korea are similar to those found throughout its native range, with mature colonies containing 1000–1200 adults. In 7 years, V. velutina has become the most abundant hornet species in Southern Korea by displacing native Vespa species such as V. simillima, which has a similar nesting biology. We also found a significant positive correlation between the abundance of V. velutina and the degree of urbanization, indicating that this invasive species was well adapted to urban environments. This was supported by our finding that 41% of emergency call-outs (119 Rescue Services) to deal with social wasps/hornet problems were due to V. velutina, which was twice as high as the number of calls about the next most abundant species. The rapid spread of V. velutina across southern Korea indicates that this species will continue to spread north-westward in the Korean peninsula and will become a major problem as more people and beekeepers come into contact with this aggressive invasive hornet.     

First detection of <Emphasis Type="Italic">Vespa velutina nigrithorax</Emphasis> (Hymenoptera: Vespidae) in the Balearic Islands (Western Mediterranean): a challenging study case

The yellow-legged hornet, Vespa velutina nigrithorax is an Invasive Alien Species introduced into Europe in 2004, and is currently present in France, Italy, Spain, Portugal, Germany, and Belgium. It was also recently introduced in the United Kingdom and Switzerland. Here we present the first detection of V. velutina in the westernmost Mediterranean islands (Majorca, Balearic archipelago). In October 2015, a specimen of hornet, which was later identified as V. velutina, was sent to the laboratory of Zoology at the University of the Balearic Islands by a beekeeper from the locality of Sóller (northwest of Majorca). After the identification, and in coordination with the local authorities, an intensive survey was implemented in the area of first detection using sticky traps baited with protein and nest detection by directly observing the flight route of adult hornets from two or three feeding points. The first nest was detected on 30th October 2015 and was entirely removed. The next year, nine other nests were located from August to November 2016 in the same area and again, all of them were removed entirely. It is the first report on an island of destroying nests as a means of controlling the spread, a scenario very different to mainland Europe. All nests were detected in evergreen tree species (pines, holm oaks, and common cypress) in the “Serra de Tramuntana”, a mountain range located in the north-west of the island of Majorca (3667 km²), which is situated 176 km off the mainland. Considering the presumably early stage of the invasion of V. velutina in Majorca, the size of the island, and the confinement of the detection area, we consider that this species could be eradicated if resources and a specific program for eradication in Majorca are implemented in coordination with all involved partners.     

Complete Mitochondrial Genome of Echinostoma hortense (Digenea: Echinostomatidae)

Echinostoma hortense (Digenea: Echinostomatidae) is one of the intestinal flukes with medical importance in humans. However, the mitochondrial (mt) genome of this fluke has not been known yet. The present study has determined the complete mt genome sequences of E. hortense and assessed the phylogenetic relationships with other digenean species for which the complete mt genome sequences are available in GenBank using concatenated amino acid sequences inferred from 12 protein-coding genes. The mt genome of E. hortense contained 12 protein-coding genes, 22 transfer RNA genes, 2 ribosomal RNA genes, and 1 non-coding region. The length of the mt genome of E. hortense was 14,994 bp, which was somewhat smaller than those of other trematode species. Phylogenetic analyses based on concatenated nucleotide sequence datasets for all 12 protein-coding genes using maximum parsimony (MP) method showed that E. hortense and Hypoderaeum conoideum gathered together, and they were closer to each other than to Fasciolidae and other echinostomatid trematodes. The availability of the complete mt genome sequences of E. hortense provides important genetic markers for diagnostics, population genetics, and evolutionary studies of digeneans.     

Relationship between the age of Vespa velutina workers and their defensive behaviour established from colonies maintained in the laboratory

As the structural bases of insect societies are essential to colony survival, nests must be protected from predation. Nest defence behaviours are among the most important roles assigned to worker members. However, in hornet societies, temporal polyethism (age-dependent division of labour among workers) is assumed to be weak. Few studies have investigated this phenomenon, probably because hornet nests are aggressively defended and dangerous to approach. In the present study, we propose a method for rearing nests of Vespa velutina, a species newly introduced into Europe. This method enables the handling of hornets, and thus the design of experiments. By marking all newly emerged hornets, we recorded aggressiveness in workers of different ages from three captive colonies. We observed that nest defence behaviour in V. velutina depends on the age of the workers. Nest defence appears to be mediated by the queen, probably through pheromones that promote nest organization. We also identified a previously unreported but important behaviour in V. velutina that workers are aggressive towards male hornets. This behaviour might be a strategy to avoid inbreeding. Collectively, our results provide new research perspectives for the management of social hymenopteran predators.     

Population genetic characterization of the endangered silver skipper,Leptalina unicolor (Lepidoptera: Hesperiidae), using novel microsatellite markers and mitochondrial DNA gene sequences

The silver stripped skipper, Leptalina unicolor, is listed as an endangered species with a paucity of leftover populations in Korea. Prior population genetic analysis is essential for the establishment of effective conservation strategies. In the present study, we investigated the genetic diversity and the relationships of L. unicolor populations in Korea using 12 newly developed L. unicolor-specific microsatellite markers and two mitochondrial DNA (mtDNA) sequences (a total of 1283 bp from COI and CytB). Due to the endangered status and rarity, a total of 33 individuals from two localities in Gangwon-do Province (Seohwa and Girin) and one in Gyeongsangnam-do Province (Danjang) were sampled. The concatenated mtDNA sequences revealed very low genetic diversity in each population, with only one to three independent haplotypes per population. F_ST, principal coordinate analysis, and independent structural analysis of the concatenated mtDNA sequences and the 12 microsatellite loci developed in this study showed that each L. unicolor population in Korea is nearly completely isolated, although inbreeding has not yet occurred. Long-term conservation habitat recovery that increases the available population appears to be important in the prevention of genetic drift and inbreeding, which occur in small isolated populations and reduce the viability of populations under fluctuating environmental conditions.     

Competition between the native and the introduced hornets Vespa crabro and Vespa velutina: a comparison of potentially relevant life‐history traits

1. Invasive alien species are a major threat to biodiversity. In addition to predation and parasitism, native species might suffer from competition when invasive alien species occupy a similar ecological niche. 2. This study focused on the potential interspecific interaction between two hornets: the Asian yellow‐legged hornet, Vespa velutina, a high‐concern invasive alien species recently arrived in Europe; and the native European hornet, Vespa crabro. The two species share a similar ecological niche and V. velutina is rapidly expanding across Europe, which suggests that V. crabro might suffer from competition. 3. Under laboratory‐controlled conditions, two life‐history traits that might cause the two species to compete were investigated: (i) the ability of workers to find food sources and their flexibility in exploiting them (through individual food item choice tests and exploration assays); and (ii) the worker resistance to pathogens (through immune challenge tests). 4. The results show that trophic preference of both species highly overlaps, with a marked dietary preference for honeybees compared with other insect prey and non‐prey protein items. No differences were observed in the exploratory behaviour of both species. Finally, constitutive antibacterial activity was greater in workers of the native species than in workers of the invasive hornet. 5. This laboratory study provides a first assessment under controlled conditions of the factors affecting competition between workers of two hornet species and proposes a framework to assess, in wild contexts, the magnitude of the competition and the impact of the introduced V. velutina on the native V. crabro.     

Rearing techniques for hornets with emphasis on Vespa velutina (Hymenoptera: Vespidae): A review

Of the 34 vespid species recorded worldwide as invasive aliens, particular attention is currently being given to the yellow-legged hornet Vespa velutina that has invaded Europe, Japan, and Korea. The hornet is a voracious predator of bees and a serious threat to bee colonies and bee pollination. Control measures are needed, but their development has been challenging as biological and ecological studies are limited by the short field season and the cryptic nesting behavior of these hornets. A Vespa rearing process can generate the large numbers of workers, gynes, and males that are essential for studying chemical ecology and life history and for experimental testing of various hypotheses. We present a synthesis of suitable methods and techniques for year-round Vespa hornet rearing. Particular reference is given to Chinese know-how and experience with Vespa rearing for medicinal and culinary motivations. We also draw on observations with reared insects that have a similar life history as Vespa hornets, namely Bombus bumblebees and Vespula yellowjackets. Key challenges to optimizing Vespa hornet rearing are identified and discussed.     

Invasion dynamics of Asian hornet, <Emphasis Type="Italic">Vespa velutina</Emphasis> (Hymenoptera: Vespidae): a case study of a commune in south-west France

Asian hornet, Vespa velutina Lepeletier nests were discovered in 2007 in Andernos-les-Bains on the south-west coast of France, 3 years after the first reported sightings in France. The number of nests increased in the commune over the following 7 years, despite local authorities enacting a destruction policy. The nests existed in close proximity to one another leading to a high density of over 10 nests per square kilometre in urban areas. New information on the chosen habitat for nests is presented, and the differences between primary and secondary locations are evident, with primary nests mostly occupying buildings and man-made structures, while secondary nests were found on trees. Using Bayesian inference methods, we fit a basic model to the observational data, which allows us to estimate key demographic parameters. This model fit is highly informative for predicting V. velutina spread and colonisation of other at-risk regions, and suggests that local control has a limited impact on the spread of V. velutina once established within a region.     

Olfactory Attraction of the Hornet Vespa velutina to Honeybee Colony Odors and Pheromones

Since the beginning of the last century, the number of biological invasions has continuously increased worldwide. Due to their environmental and economical consequences, invasive species are now a major concern. Social wasps are particularly efficient invaders because of their distinctive biology and behavior. Among them, the yellow-legged hornet, Vespa velutina, is a keen hunter of domestic honeybees. Its recent introduction to Europe may induce important beekeeping, pollination, and biodiversity problems. Hornets use olfactory cues for the long-range detection of food sources, in this case the location of honeybee colonies, but the exact nature of these cues remains unknown. Here, we studied the orientation behavior of V. velutina workers towards a range of hive products and protein sources, as well as towards prominent chemical substances emitted by these food sources. In a multiple choice test performed under controlled laboratory conditions, we found that hornets are strongly attracted to the odor of some hive products, especially pollen and honey. When testing specific compounds, the honeybee aggregation pheromone, geraniol, proved highly attractive. Pheromones produced by honeybee larvae or by the queen were also of interest to hornet workers, albeit to a lesser extent. Our results indicate that V. velutina workers are selectively attracted towards olfactory cues from hives (stored food, brood, and queen), which may signal a high prey density. This study opens new perspectives for understanding hornets’ hunting behavior and paves the way for developing efficient trapping strategies against this invasive species.     

Testing muzzle and ploy devices to reduce predation of bees by Asian hornets

Since its accidental introduction in 2004, the Asian yellow-legged hornet (Vespa velutina) has quickly spread in France. V. velutina specializes in the emblematic honeybee, Apis mellifera which are unable to protect their colonies efficiently against this fierce new predator. Here, we investigated whether two defence devices, a ploy and a muzzle, can protect bee colonies. Our results showed that neither device was able to reduce the number of hornets present in front of the hive or their predation efficiency (i.e. the number of captured bees). However, we found more flying bees and a smaller bee carpet in the presence of a muzzle, evidence that this very cheap method of protection can reduce the hornets’ impact on the activity of the bee colony and thus probably enabling its survival. We also showed that the number of agonistic interactions among V. velutina individuals increased with the number of hornets but without influencing the predation rate in our experimental conditions. The threat to honey bees is now well described, but the Asian yellow-legged hornet very likely has an impact on another insect species that has been the subject of far fewer studies: The native European hornet (Vespa cabro). Monitoring of several apiaries suggests that high densities of both V. velutina and V. crabro are exclusive and that the two species are engaged in an exploitative competition interaction. We are thus already in a position to underline the need for combined protection, as well as for further studies to better understand the ecology of V. velutina, to reduce the damage they cause.     

Quantitative analysis of research topics and public concern on V. velutina as invasive species in Asian and European countries

We analyzed the research topics and public concern on Vespa velutina as an invasive species in Asian and European countries quantitatively though digitized texts such as scientometrics and conservation culturomics. We collected 126 scientific publications of V. velutina published during the last three decades, and 423 news articles on V. velutina in South Korea. In total, 22 countries have contributed to scientific research on V. velutina. Research topics were clearly classified to studies on taxonomy and invasion of V. velutina. In South Korea, people have recognized the ecological and health impact of V. velutina. Although scientific and public interest in V. velutina has increased since 2000, research topics may be narrow and information of news articles may be simple. To achieve the sustainable management of V. velutina, multilateral studies including environmental, social, and economic research on V. velutina are necessary.     

How <Emphasis Type="Italic">Apis mellifera</Emphasis> Behaves with its Invasive Hornet Predator <Emphasis Type="Italic">Vespa velutina</Emphasis>?

Invasive species are now recognized as a major cause of native biodiversity loss worldwide. In the current deleterious context for pollinators, the invasive yellow-legged hornet, Vespa velutina, represents an additional threat to the domestic honeybee, Apis mellifera, in Europe. Therefore, understanding the impact of this predator on honeybee colonies is of major importance. In the present study, we tried to assess the impact of V. velutina on the honeybee foraging and defence behaviour based on the video monitoring of two hives. Balling behaviour is reported here for the first time under natural conditions in A. mellifera against V. velutina in Europe. Although these results are preliminary and should be carefully considered, we found that the number of hornets impacted honeybee foraging and defence behaviours. More defensive behaviours were notified in the hive, which survives slightly longer. This may suggest that selecting for more defensive colonies may provide an interesting perspective.     

Behavioral syndrome in a native and an invasive hymenoptera species

Recent studies have focused on the role of behavior in biological invasions. Individuals may differ consistently in time for several behavioral traits (personality) which covary (behavioral syndrome) resulting in different behavioral types, some of them favoring invasion. Social hymenopterans have a strong potential to be invaders and their success depends primarily on the foundresses’ ability to found viable colonies. They are expected to be active, explorative and bold for optimally establishing their nest. In Europe, 2 hornet species coexist: the native Vespa crabro and the invasive Vespa velutina. These 2 species may compete for nesting sites and we suggest that the initial success of V. velutina has been favored by its behavior in outperforming V. crabro for the traits involved in nest initiation. Here, we (i) defined the personality of V. crabro and V. velutina, (ii) tested for the existence of behavioral syndrome in these species, and (iii) compared their performances using an open‐field test. Our results show that V. crabro foundresses behave consistently but not V. velutina; this lack of consistency being mainly due to reduced variance among individuals. This result questions the possibility of detecting consistent behavioral differences in species having recently undergone a strong bottleneck. Both species exhibit the same correlations between activity, boldness and exploration and V. velutina clearly outperforms V. crabro for all traits. Our results suggest that activity, boldness, and exploration are implicated in both hornet nest initiation and invasion process which contributed to explain why social hymenopterans are so successful at colonization.     

Options for the biological and physical control of Vespa velutina nigrithorax (Hym.: Vespidae) in Europe: A review

Recently, the environmental economist J.M. Salles (Salles, 2016 ) declared that “the Asian hornet was likely to be the most threatening invader insect in France.” Thirteen years after the accidental introduction in France, the Asian hornet (Vespa velutina nigrithorax) has invaded most west European countries. Little has been done to date to limit its progression and its economic, ecological and social impact. Although it is illusory to try to eradicate this species, it is known that a targeted control would limit its threatening trend. Current V. velutina control in France is mainly based on (i) high scale volunteer trapping by citizens and (ii) volunteer spotting of the nest. Evaluation of trapping strategies developed so far to control V. velutina expansion has highlighted their failure and has demonstrated the need to optimize nest detection techniques and to investigate on new control strategies. This review describes most of the means aimed to control predation and expansion of V. velutina, whether they have been scientifically assessed or only tested on field with decent success. Published prospective control methods and biological control techniques are also presented.     

Involvement of two differenturf-s related mitochondrial sequences in the molecular evolution of the CMS-specificS-Pcf locus in petunia

In petunia, a mitochondrial (mt) locus,S-Pcf, has been found to be strongly associated with cytoplasmic male sterility (CMS). TheS-Pcf locus consists of three open reading frames (ORF) that are co-transcribed. The first ORF,Pcf, contains parts of theatp9 andcoxII genes and an unidentified reading frame,urf-s. The second and third ORFs contain NADH dehydrogenase subunit 3 (nad3) and ribosomal protein S12 (rps12) sequences, respectively. Thenad3 andrps12 sequences included in theS-Pcf locus are identical to the corresponding sequences on the mt genome of fertile petunia. In both CMS and fertile petunia, only a single copy ofnad3 andrps12 has been detected on the physical map of the main mt genome. The origin of theurf-s sequence and the molecular events leading to the formation of the chimericS-Pcf locus are not known. This paper presents evidence indicating that two different mt sequences, related tourf-s and found in fertile petunia lines (orf-h and Rf-1), might have been involved in the molecular evolution of theS-Pcf locus. Southern analysis of mtDNA derived from both fertile and sterile petunia plants suggests that one of theseurf-s related sequences (showing 100% homology tourf-s and termedorf-h) is located on a sublimon. An additional, low-homologyurf-s related sequence (Rf-1) is shown to be located on the main mt genome 5′ to thenad3 gene. It is, thus, suggested that the sequence of events leading to the generation of theS-Pcf locus might have involved introduction of theorf-h sequence, via homologous recombination, into the main mt genome 5′ tonad3 at the region where the Rf-1 sequence is located.     

Honey Bees Modulate Their Olfactory Learning in the Presence of Hornet Predators and Alarm Component

In Southeast Asia the native honey bee species Apis cerana is often attacked by hornets (Vespa velutina), mainly in the period from April to November. During the co-evolution of these two species honey bees have developed several strategies to defend themselves such as learning the odors of hornets and releasing alarm components to inform other mates. However, so far little is known about whether and how honey bees modulate their olfactory learning in the presence of the hornet predator and alarm components of honey bee itself. In the present study, we test for associative olfactory learning of A. cerana in the presence of predator odors, the alarm pheromone component isopentyl acetate (IPA), or a floral odor (hexanal) as a control. The results show that bees can detect live hornet odors, that there is almost no association between the innately aversive hornet odor and the appetitive stimulus sucrose, and that IPA is less well associated with an appetitive stimulus when compared with a floral odor. In order to imitate natural conditions, e.g. when bees are foraging on flowers and a predator shows up, or alarm pheromone is released by a captured mate, we tested combinations of the hornet odor and floral odor, or IPA and floral odor. Both of these combinations led to reduced learning scores. This study aims to contribute to a better understanding of the prey-predator system between A. cerana and V. velutina.     

Both olfactory and visual cues promote the hornet Vespa velutina to locate its honeybee prey Apis cerana

Predators use olfactory, visual and sometimes acoustic cues from the preys to assess food information. However, it is not known if the aggressive hornets (Vespa spp.) use olfactory, visual, or both types of information to find and recognize prey. In the present study, we trained hornet workers (Vespa velutina) to a feeding area. Once the hornets began consistently foraging at this feeding area, we determined whether they located prey (bees, Apis cerana) via olfactory or visual cues. We did this by testing whether hornets were attracted to a dummy bait (bee dummy bait or non-bee dummy bait) treated with extracts of honeybee cuticular hydrocarbons. We then tested whether hornets could distinguish between bee dummy bait and cotton ball dummy bait, both treated with bee odors. Hornets preferred the dummy treated with bee odors, and bee dummies (with bee images) were more attractive to the hornet than the cotton ball dummies with only bee odors. These results clearly indicate that a combination of olfactory and visual cues helps the hornet to locate its prey.     

Native Prey and Invasive Predator Patterns of Foraging Activity: The Case of the Yellow-Legged Hornet Predation at European Honeybee Hives

Contrary to native predators, which have co-evolved with their prey, alien predators often benefit from native prey naïveté. Vespa velutina, a honeybee predator originating from Eastern China, was introduced into France just before 2004. The present study, based on video recordings of two beehives at an early stage of the invasion process, intends to analyse the alien hornet hunting behaviour on the native prey, Apis mellifera, and to understand the interaction between the activity of the predator and the prey during the day and the season. Chasing hornets spent most of their time hovering facing the hive, to catch flying honeybees returning to the hive. The predation pressure increased during the season confirming previous study based on predator trapping. The number of honeybee captures showed a maximum peak for an intermediate number of V. velutina, unrelated to honeybee activity, suggesting the occurrence of competition between hornets. The number of honeybees caught increased during midday hours while the number of hornets did not vary, suggesting an increase in their efficacy. These results suggest that the impact of V. velutina on honeybees is limited by its own biology and behaviour and did not match the pattern of activity of its prey. Also, it could have been advantageous during the invasion, limiting resource depletion and thus favouring colonisation. This lack of synchronization may also be beneficial for honeybee colonies by giving them an opportunity to increase their activity when the hornets are less effective.     

Vespa velutina nest distribution at a local scale: An 8‐year survey of the invasive honeybee predator

Vespa velutina is an invasive species that was observed for the first time in France and Europe in 2004, which rapidly threatened domestic honeybees with active predation. For the first time in this study, we analyzed the distribution of V. velutina nests at a local scale to understand the pattern of nesting, and in 8 years of monitoring, a total of 528 nests were surveyed. With the exception of 2 years, the nests of V. velutina were randomly distributed within the monitored area, which suggested that intraspecific competition for nesting sites and/or food was unlikely. When the data for all years were combined, an aggregated distribution of nests at the seafront in the vicinity of the oyster farm and sportfishing activities was observed. This distribution suggested that seafood, attractive to vespids, might provide a valuable alternative food source that favored colony development. We also tested the effect of spring queen trapping of V. velutina on the distribution of nests in 2014, which was the year with the greatest number of colonies within the area; the position of the traps did not influence the distribution of the nests. For the first time, this study showed that (i) intraspecific competition was unlikely to be a mechanism for population regulation, (ii) some areas were more likely favored for hornet nests, and (iii) spring queen wasp trapping was inefficient as a method to limit the distribution of the V. velutina population.     

DNA data and morphology suggest an occurrence of Dendrolimus sibiricus Tschetverikov, 1908 (Lepidoptera: Lasiocampidae) instead of D. superans Butler, 1877, in South Korea

In the present study, specimens of Dendrolimus superans collected from South Korea suggest the presence of D. sibiricus, instead of D. superans. Comparisons of the wing morphology, female and male genitalia, 3′‐end region of the cytochrome c oxidase I (COI) gene sequence, and internal transcribed spacer (ITS) 2 sequence of the Korean specimens with those of the D. superans specimens from Japan consistently supported the presence of D. sibiricus in South Korea. Phylogenetic analyses of the concatenated sequences of COI and ITS2 from the available sequence types of D. sibiricus and D. superans, along with South Korean specimens, were conducted using the Bayesian inference (BI) and maximum likelihood (ML) methods. These phylogenetic analyses placed the South Korean specimens with the Russian D. sibiricus as an inclusive group, excluding the Japanese D. superans, indicating the distribution of D. sibiricus in South Korea. Nevertheless, D. superans formed a distinct group only by BI analysis (Bayesian posterior probabilities = 0.89), whereas D. sibiricus, including the South Korean samples, formed a distinct group only by the ML analysis (99%), suggesting a low genetic divergence between the two species.