Corrigendum to: “The Diversity of Hornets in the Genus Vespa (Hymenoptera: Vespidae; Vespinae), Their Importance and Interceptions in the United States”


 Hornets in the genus Vespa (Vespidae, Vespinae) are social wasps. They are primarily predators of other insects, and some species are known to attack and feed on honeybees (Apis mellifera L.), which makes them a serious threat to apiculture. Hornet species identification can be sometimes difficult because of the amount of intraspecific color and size variation. This has resulted in many species-level synonyms, scattered literature, and taxonomic keys only useful for local populations. We present a key to the world species, information on each species, as well as those intercepted at United States Ports of Entry during the last decade. Images of all the species and some of the subspecies previously described are also included.

Hornets in the genus Vespa are large, predatory, eusocial wasps native to Europe and Asia. They prey on a wide diversity of insects, but several species are predatory on honeybees. Vespa nests can be physically large, with over 1,000 workers, but usually with hundreds of workers (Archer 2008). Nests can be aerial, attached to tree branches or in shrubs, in crevices, under eaves or underground depending on the species. Depending on the latitude, nests can be either annual, started by a new queen every spring, or perennial, where young queens take over from old ones (Matsuura and Yamane 1990). Colonies in warm tropical climates tend to be perennial.
These wasps exhibit a range of color patterns that vary geographically. Previous authors have named numerous subspecies based solely on color patterns, but Vespa color patterns tend to grade from one region to the next Nguyen et al. (2006), Perrard et al. (2014. These subspecies were all synonymized by Carpenter and Kojima (1997). Beggs et al. (2011) assessed the distribution, abundance, impact, and management of invasive species of Vespidae worldwide. In the case of the hornets, several Vespa species have been introduced outside their native ranges, including V. crabro Linnaeus, 1758 (Hymenoptera: Vespidae) from Europe into the United States (Bequaert 1932, Shaw andWeidhaas 1956); V. velutina Lepeletier, 1836 (Hymenoptera: Vespidae) from Asia into Europe (Monceau et al. 2014); and V. tropica Linnaeus, 1758 (Hymenoptera: Vespidae) from continental Asia into the island of Guam (Anonymous 2016). There are also records of other species collected outside their ranges without becoming established (see Kimsey and Carpenter 2012 for North America).
Some of the introduced Vespa species have shown to be environmental stressors as predators of already declining populations of native insects, spiders, and honeybees (Shah and Shah 1991, Abrol 1994, Choi et al. 2011. They can also be competitors for food and nesting sites of native wasps (Cini et al. 2018), vectors of parasites or diseases that can affect honey bees and native wasps (Choi et al. 2011), and impact human safety because of their aggressiveness and fatal reactions to their venom (Nguyen et al. 2010, Kularatne et al. 2014. The invasion of V. velutina into Europe typifies these problems. These hornets prey on the domestic honey bee [Apis mellifera (Linnaeus) (Hymenoptera: Apidae)], disrupt the ecological role of honeybees as pollinators (Villemant et al. 2006a, b;Monceau et al. 2014), have potentially altered local biodiversity (Fedele et al. 2019), and are potentially deadly to people allergic to their stings.
In Europe, the native hornet, V. crabro, is protected in some regions, such as in Germany (Federal Species Protection Ordinance-BArtSchV/Federal Nature Conservation Act-BNatSchG). The introduced V. velutina may compete for food resources with V. crabro, which is a more generalist predator (Shaw andWeidhaas 1956, Baracchi et al. 2010). According to Monceau et al. (2014), some beekeepers have reported increased V. crabro predation on honeybees since the introduction of V. velutina in Europe.
This species was introduced into New York State in the mid-1800s (de Saussure 1898). Since then, it has since spread throughout eastern North America (Kimsey & Carpenter 2012). Vespa tropica was first found on Guam in 2016 (Anonymous 2016). Since then, it has become so widespread on the island it is no longer under quarantine, even though problems have arisen because it is aggressive and may nest close to human settlements.
Studies by Blanchard et al. (2008) and Yañez et al. (2012) had shown the potential transmission of the Israeli Acute Paralysis Virus (IAPV), one of the causes of Colony Collapse Disorder in honeybees (Cox-Foster et al. 2007) between honeybees and their non-Apis predators, such as hornets. The possibility of transmission from hornets to honeybees or other native species has yet to be determined.
The introduction of alien hornet species into the United States is a real risk and having a practical synthesis of the current knowledge on the basic biology and identification of the world's hornets would greatly increase our capacity to identify and enhance the detection of potentially invasive species of hornets or to monitor their dispersion if they are introduced.
In this study, we provide information on the species diversity of hornets, taxonomic keys and visual aids for the identification of the different species.

Materials and Methods
We performed an Ad hoc/ unlimited search for interceptions of species of Vespinae (Vespa and Vespula Thomson) at Ports of Entry (PE) to the United States using the USDA-APHIS, Plant Protection and Quarantine (PPQ) databases AQAS (Agricultural Quarantine Activity Systems) and ARM (Agricultural Risk Management System) going back to 2010. After the search, the data were processed, filtered and the total of interceptions for hornets (genus Vespa) was determined for the years 2010 to 2018. In addition, some information from interception records, such as origin and means of transportation, is given in the results and the discussion.
Taxonomic keys provided below were constructed in part based on previous keys by Archer (1989Archer ( , 2012. A revised, fully illustrated key was needed to clarify and simplify diagnostic characters used in previous keys. In addition to the keys, we provide, for the first time, high-resolution images of these features. Specimens used for the images were from the American Museum of Natural History (AMNH), New York, NY (C. Lebeau) and from the Bohart Museum of Entomology (BME), University of California, Davis (S. Heydon). Images were captured and edited using a Nikon SMZ18 System with a Nikon DS-fi2 camera, the stacking software, Helicon Focus 6.0, and Photoshop Elements 12.
Type repositories are given in parentheses at the end of species entries in synonym lists. These include BASEL = Naturhistorisches Museum, Basel, Switzerland; BERLIN = Museum für Naturkunde, Berlin, Germany; BUDAPEST = Zoological Department, Hungarian Natural History Museum, Budapest, Hungary; CALCUTTA = Zoological Survey of India, Calcutta; CAMBRIDGE = Museum of Comparative Zoology, (Fig. 2a), head vertex with the distance from the posterior ocellus to the posterior margin of vertex more than twice the distance between the posterior ocelli and the compound eye (Fig. 2b), the basal metasomal segment is anteriorly rounded (Fig. 1f), and the length of the forewing prestigma is three times or more the length of the pterostigma (Fig. 1b).

Keys to the Queens and Workers of the Species of Vespa of the World
1 Posterior ocelli about as close to compound eye as to each other (Fig. 2c)  Insect Systematics and Diversity, 2020, Vol. 4, No. 3 Downloaded from https://academic.oup.com/isd/article-abstract/4/3/2/5834678 by University of Cambridge user on 13 May 2020 2 Apical margin of clypeus with medial tooth between laterally produced margins (Fig. 2e) (Fig. 7f), or metasomal tergum 2 orange-yellow (Fig. 7e), or tergum 2 black with narrow, distal orange-yellow band that extends much less than one-third of tergal width (Fig. 7b).………..........………tropica (Linnaeus) 11 Metasomal terga 2, 5 and 6 reddish brown or dark brown; tergum 3 and usually tergum 4 mostly yellow, with basal reddish brown band extending medially and two small, lateral reddish brown spots ( Fig. 9a and b) (Fig. 10b); metasomal tergum 2 usually reddish brown (Fig. 10d), or if metasomal tergum is mostly black then the vertex is also black ..... affinis (Linnaeus) 14 Clypeus strongly bulging medially, strongly convex in side view (Fig. 11a) (Fig. 12a), or if without markings then metanotum entirely yellow (as in Fig. 12c  Discussion. This is one of the smaller bodied hornets, and is common in subtropical and tropical Asia. They are generalist scavengers, Insect Systematics and Diversity, 2020, Vol. 4, No. 3 Downloaded from https://academic.oup.com/isd/article-abstract/4/3/2/5834678 by University of Cambridge user on 13 May 2020 feeding on nectar, fruit, tree sap, carrion, and insects, including honeybees. Vespa affinis nests are usually built high in trees, but can also be found in shrubs, and on and in buildings (Archer 1997   Discussion. This is one of the most widely distributed species of Vespa. Its native range includes tropical Asia and extends north into Japan, Russia, and Korea. Nests are typically built in trees 2-3 m above the ground (Archer 1998b  Insect Systematics and Diversity, 2020, Vol. 4, No. 3 Downloaded from https://academic.oup.com/isd/article-abstract/4/3/2/5834678 by University of Cambridge user on 13 May 2020 Discussion. Vespa basalis occurs in forested regions between 500 m and 1,500 m (Archer 1999). Nests are built on tree branches, in shrubs, on buildings, in rock crevices, and even in the ground. The mostly dark brown to black metasoma is one of the more distinctive features of V. basalis. Distribution. Indonesia: Sumatra, Borneo (Kalimantan, Sarawak).

Vespa bellicosa de Saussure
Discussion. This species appears to be associated with lowland tropical forests in Borneo and Sumatra (Archer 1999  Insect Systematics and Diversity, 2020, Vol. 4, No. 3 Downloaded from https://academic.oup.com/isd/article-abstract/4/3/2/5834678 by University of Cambridge user on 13 May 2020 Discussion. This species of Vespa has a very distinctively marked black and yellow thorax, with a largely yellow metasoma. It preys on honeybees, and one species of Dendrobium orchid exploits this behavior. These orchids produce chemicals that mimic alarm pheromones of Asian (Apis cerana) and European (Apis mellifera) honeybees to attract the hornets to pollinate their flowers (Brodman et al. 2009).

Figs. 2c and 21
Vespa binghami du Buysson, 1905Buysson, (1904   Distribution. Eurasia, Algeria. Introduced into eastern North America, and Guatemala. Discussion. Vespa crabro usually nests in sheltered aboveground sites, such as tree hollows, wall voids, beehives, and outhouses (Archer 1993). However, nests have been found in subterranean  Discussion. This species of Vespa is quite different from the others. It preys on nests of other paper wasps, feeding the paper wasp pupae and larvae to their larvae. Their colonies are small with an average of 50 individuals, and nests are built underground, in tree hollows, and even in attics (Archer 1991  Insect Systematics and Diversity, 2020, Vol. 4, No Archer (1999).

Distribution. Philippines.
Discussion. This species has been found nesting in forested regions between 200 and 1,500 m elevation. The nests are built on tree branches, sometimes as high as 20 m above the ground (Archer 1999  Insect Systematics and Diversity, 2020, Vol. 4, No. 3 Downloaded from https://academic.oup.com/isd/article-abstract/4/3/2/5834678 by University of Cambridge user on 13 May 2020 Discussion. This species occurs in hilly regions. It nests in the ground, starting with mammal burrows or decayed root cavities, enlarging them as the colony develops (Archer 1995(Archer , 2008. This is another species of Vespa that preys on honeybees. Zhang (1989) reported the presence of Vespa magnifica in Miocene deposits in Shandong, China. This identification needs to be verified. This species has also been introduced into the Pacific Northwest, where nests have been found recently (Anonymous 2020 Discussion. Vespa multimaculata is found in lowland and montane forests in Southeast Asia (Archer 1999(Archer , 2011, and is unlikely to disperse to temperate regions. Martin (1995) found nests in the ground beneath the roots of a tree.  Insect Systematics and Diversity, 2020, Vol. 4, No Discussion. This is a distinctively marked reddish orange and yellow wasp. The nests are built in the ground in rodent burrows or rock crevices (Archer 1998a). Around human habitation, nests have also been found in empty beehives, under eaves or floorboards, and even in abandoned outhouses. It has been recorded from Mexico but is evidently not established (Dvořák 2006). Vespa orientalis are scavengers, feeding on nectar and fruit as well as insects and carrion. They also prey on honeybees and other pollinators. A study by Plotkin et al. (2010) found that this species has a novel form of photosynthesis using yellow pigments in the cuticle.

Discussion.
Little is known about the biology of this endemic species. A nest described by Starr (1987) from the island of Leyte was found in a cavity in the ground (Archer 1991 Discussion. Nests of this species have been found in the ground, and in sheltered above ground sites, such as hollow trees, wall voids, and attics. A queen of V. simillima was found in the village of Tsaochan in Taiwan in 2003, but it is unclear whether the species has established on the island (Sung et al. 2006). It is apparently not established in British Colombia (Kimsey and Carpenter 2012 Discussion. Little biology is known for this species. It has been found in hilly and montane sites up to 1,500 m in continental southeastern Insect Systematics and Diversity, 2020, Vol. 4, No. 3 Downloaded from https://academic.oup.com/isd/article-abstract/4/3/2/5834678 by University of Cambridge user on 13 May 2020 Asia (Archer 2008). The nests are typically underground. These wasps are predators of other insects and even small vertebrates, like geckos. They will also attack nests of honeybees and other social vespids, including hornets (Lee 2009 Discussion. Vespa velutina has distinctive yellow tarsi and velvety appearing dark brown to black thorax and metasoma. It is native across Asia. However, V. velutina was introduced into Europe apparently with Chinese pottery in the past couple of decades (Keeling et al. 2017). Although this species preys on a variety of insects, including flies, dragonflies, and Orthoptera, it is a notorious predator of pollinators, particularly honeybees (Apis mellifera and A. cerana). Apis cerana have adapted to this hornet using avoidance behaviors and balling behaviors where they heat the hornet to death (Abrol 2006 Distribution. India, Nepal, Myanmar, Thailand, China (Sichuan, Yunnan, Tibet), Taiwan.

Discussion.
Little is known about this south Asian Vespa species. In Taiwan, nests have been found in montane regions at elevations between 1,500 and 2,500 m (Archer 1994).

Conclusion
From 2010 to 2018, there have been close to 50 interceptions of Vespa (hornets) and Vespula (yellow jackets (Vespula) at US ports of entry. Little less than half of those interceptions were hornets. The Vespa species intercepted include V. bellicosa, V. crabro, V. orientalis, V. mandarinia, and V. tropica. One of the interceptions of significance was an entire nest of V. mandarinia containing live brood and pupae that was sent via express courier from Asia. All species of Vespa, except V. crabro, which is already introduced into the eastern United States, are considered of quarantine importance by the USDA-APHIS. As part of the work of monitoring for possible introductions of hornets in the United States, one of us (AHSP) created a website, Invasive Hornets (https://www. ipmimages.org/browse/projectthumb.cfm?proj=1159), which is part of a cooperation between the USDA, Animal Plant Health Inspection Service (APHIS), Plant Protection and Quarantine (PPQ) and the University of Georgia. This website contains more than 1,000 Insect Systematics and Diversity, 2020, Vol. 4, No. 3 Downloaded from https://academic.oup.com/isd/article-abstract/4/3/2/5834678 by University of Cambridge user on 13 May 2020 stacked, high-quality images of all the species and most of the races of the genus Vespa.
It is important to have the resources for the identification and prevention of introduction of non-native species and to understand the potential effects of invasive hornets in our ecosystems. Hornets are dangerous for the beekeeping industry because they can alter pollination in agriculture and disrupt the beekeeping industry, as well as create public health and safety problems.