Heather R. Mattila

Hornets (genus Vespa) are a conspicuous taxon of large eusocial wasps that are predators of other insects. Increasingly, hornets are gaining notoriety as damaging invaders after repeated introductions into novel habitats. Most hornets are highly effective predators, so they have the potential to greatly impact local entomofauna, including economically important pollinators. In 2016, Vespa tropica, a hornet with a broad natural range throughout subtropical and tropical Asia, was detected on Guam, although few details have been published since the initial alert. We provide the first comprehensive update on the status and impact of V. tropica hornets on Guam based on nine years of beekeeper and public reports, as well as field collections of nests, hornets, and videos of hunting behavior in managed apiaries. We show that the population of non-native V. tropica is established and thriving on Guam. Nests were found in a diversity of sites: below and above ground, sheltered and exposed, and in urban and greenspaces. V. tropica was a year-round predator in apiaries, with up to 12% of colony losses per year attributed to hornet attacks. Notably, hornets often attacked single honey bee (Apis mellifera) colonies in groups, similar to the hunting strategy of their close relatives, the giant hornets Vespa mandarinia and Vespa soror. Hornets killed defending workers, eventually weakening colonies and entering hives to consume bee brood. Bees mounted defenses that included alarm piping, bee ‘carpets’, and attempts to ball hornets. Hornets were active all year, but were significantly more active during the wet season (July‒December). Preliminary analysis of color forms suggested that the source of V. tropica on Guam is likely continental southeast Asia, although genetic analyses are required. Our study reveals that Guam is facing a fierce invader in V. tropica, which is placing strong predatory pressure on pre-established honey bees.

Giant hornets in the genusVespaare apex predators that are known throughout Asia for their exceptional size and devastating group attacks on social insect colonies. The giant hornets includeVespa mandarinia, a well-studied and widespread temperate species, andVespa soror, a poorly known sister species that is limited to subtropical and tropical regions of Southeast Asia. Both species have been recently documented on the west coast of North America, raising urgent questions about their potential impact in novel ecosystems. To better understand the biology ofV. soror, we describe the nest architecture, caste morphology, and genetic structure of colonies collected in Vietnam. Comparisons of colony metrics between the two giant hornet species suggest important differences that are likely a consequence of the relatively warmer climate in whichV. sororoccurs. LikeV. mandarinia,V. sororconstructs large, underground nests of partially enveloped horizontal combs. However, compared to temperateV. mandariniacolonies, the longer nesting period of subtropicalV. sororcolonies likely resulted in relatively larger colony sizes and nests by the end of their annual cycle.Vespa sororworkers and gynes were larger than males, distinguishable based on wing shape and body size (total length and measures of six body parts), and equivalent in size to female castes ofV. mandarinia. We genotyped colony members from three mature nests, which revealed that males and females were offspring of singly mated queens. Two colonies were monogynous, but one colony was comprised of two unrelated matrilines. Polygyny has not been observed forV. mandarinia, but is more common in tropical hornet species. Our study sheds light on essential details about the biology of an understudied species of giant hornet, whose populous colonies and long nesting period suggest the potential for substantial ecological impact wherever they occur.

Many social wasps in the speciose subfamilies Polistinae and Vespinae have two sternal glands—the van der Vecht gland and the Richards gland—that are not found in other insects. The presence of these glands has been confirmed in only 6 of 22 hornet species (genus Vespa) and images of their fine structure have not been produced. Here; we characterize the external morphology associated with both glands for workers of nine Vespa species using scanning electron microscopy. All hornets had similar gland configurations; although gland-associated external features differed among species. Scaled for size, glands were equivalently sized for the giant hornets (V. mandarinia and V. soror) and their closest phylogenetic relatives (V. tropica and V. ducalis). Relative size of gland-associated structures was reduced by half for V. simillima; V. velutina; and V. affinis workers. The remaining species (V. crabro and V. analis) had intermediately sized features. Differences among species in external gland structure were best explained by selective pressures related to predatory behavior, rather than defense of nests against ants. However, a lack of information about how Vespa workers use their van der Vecht and Richards glands limits a comparative interpretation of the function of their external gland morphology.

The activities of social insect colonies are supported by exocrine glands and the tremendous functional diversity of the compounds that they secrete. Many social wasps in the subfamilies Vespinae and Polistinae have two sternal glands—the van der Vecht and Richards’ glands—that vary in their features and function across the species in which they are found. Field observations suggest that giant hornets use secretions from the van der Vecht gland to chemically mark targeted nests when workers initiate group attacks on social insect prey. However, descriptions of giant hornets’ sternal glands and details about their recruitment behavior are lacking. We describe the morphology of the sternal glands of the giant hornet Vespa soror du Buysson and consider their potential to contribute to a marking pheromone. We also assess the gastral rubbing behavior of workers as they attacked Apis cerana F. (Hymenoptera: Apidae) colonies. V. soror workers have well-developed van der Vecht and Richards’ glands on their terminal gastral sternites, with morphologies that robustly support the synthesis, storage, and dissemination of their secretory products. Observations confirm that the van der Vecht gland is exposed during gastral rubbing, but that the Richards’ gland and glands associated with the sting apparatus may also contribute to a marking pheromone. Workers briefly but repeatedly rubbed their gasters around hive entrances and on overhead vegetation. Colonies were heavily marked over consecutive attacks. Our findings provide insight into the use of exocrine secretions by giant hornets as they recruit nestmates to prey colonies for group attacks.

Asian honeybees use an impressive array of strategies to protect nests from hornet attacks, although little is understood about how antipredator signals coordinate defences. We compared vibroacoustic signalling and defensive responses ofApis ceranacolonies that were attacked by either the group-hunting giant hornetVespa sororor the smaller, solitary-hunting hornetVespa velutina.Apis ceranacolonies produced hisses, brief stop signals and longer pipes under hornet-free conditions. However, hornet-attack stimuli—andV. sororworkers in particular—triggered dramatic increases in signalling rates within colonies. Soundscapes were cacophonous whenV. sororpredators were directly outside of nests, in part because of frenetic production of antipredator pipes, a previously undescribed signal. Antipredator pipes share acoustic traits with alarm shrieks, fear screams and panic calls of primates, birds and meerkats. Workers making antipredator pipes exposed their Nasonov gland, suggesting the potential for multimodal alarm signalling that warns nestmates about the presence of dangerous hornets and assembles workers for defence. Concurrent observations of nest entrances showed an increase in worker activities that support effective defences against giant hornets.Apis ceranaworkers flexibly employ a diverse alarm repertoire in response to attack attributes, mirroring features of sophisticated alarm calling in socially complex vertebrates.

Honey bees (genusApis)are well known for the impressive suite of nest defenses they have evolved to protect their abundant stockpiles of food and the large colonies they sustain. In Asia, honey bees have evolved under tremendous predatory pressure from social wasps in the genusVespa, the most formidable of which are the giant hornets that attack colonies in groups, kill adult defenders, and prey on brood. We document for the first time an extraordinary collective defense used byApis ceranaagainst the giant hornetVespa soror. In response to attack byV.soror,A.ceranaworkers foraged for and applied spots of animal feces around their nest entrances. Fecal spotting increased after colonies were exposed either to naturally occurring attacks or to chemicals that scout hornets use to target colonies for mass attack. Spotting continued for days after attacks ceased and occurred in response toV.soror, which frequently landed at and chewed on entrances to breach nests, but notVespa velutina, a smaller hornet that rarely landed at entrances. Moderate to heavy fecal spotting suppressed attempts byV.sororto penetrate nests by lowering the incidence of multiple-hornet attacks and substantially reducing the likelihood of them approaching and chewing on entrances. We argue thatA.ceranaforages for animal feces because it has properties that repel this deadly predator from nest entrances, providing the first report of tool use by honey bees and the first evidence that they forage for solids that are not derived from plants. Our study describes a remarkable weapon in the already sophisticated portfolio of defenses that honey bees have evolved in response to the predatory threats they face. It also highlights the strong selective pressure honey bees will encounter if giant hornets, recently detected in western North America, become established.

The negative effects on adult behavior of juvenile undernourishment are well documented in vertebrates, but relatively poorly understood in invertebrates. We examined the effects of larval nutritional stress on the foraging and recruitment behavior of an economically important model invertebrate, the honey bee (Apis mellifera). Pollen, which supplies essential nutrients to developing workers, can become limited in colonies because of seasonal dearths, loss of foraging habitat, or intensive management. However, the functional consequences of being reared by pollen-stressed nestmates remain unclear, despite growing concern that poor nutrition interacts with other stressors to exacerbate colony decline. We manipulated nurse bees’ access to pollen and then assessed differences in weight, longevity, foraging activity, and waggle-dance behavior of the workers that they reared (who were co-fostered as adults). Pollen stress during larval development had far-reaching physical and behavioral effects on adult workers. Workers reared in pollen-stressed colonies were lighter and shorter lived than nestmates reared with adequate access to pollen. Proportionally fewer stressed workers were observed foraging and those who did forage started foraging sooner, foraged for fewer days, and were more likely to die after only a single day of foraging. Pollen-stressed workers were also less likely to waggle dance than their unstressed counterparts and, if they danced, the information they conveyed about the location of food was less precise. These performance deficits may escalate if long-term pollen limitation prevents stressed foragers from providing sufficiently for developing workers. Furthermore, the effects of brief pollen shortages reported here mirror the effects of other environmental stressors that limit worker access to nutrients, suggesting the likelihood of their synergistic interaction. Honey bees often experience the level of stress that we created, thus our findings underscore the importance of adequate nutrition for supporting worker performance and their potential contribution to colony productivity and quality pollination services.