Resident Hymenopteran Parasitoids with Potential Drosophilid Associations in Andean North Patagonia: Implications for the Biological Control of the Spotted Wing Drosophila.

The spotted wing drosophila, Drosophila suzukii Matsumura, is native to Southeast Asia and has become a serious pest of soft-skinned fruits worldwide. Several control methods are being tested worldwide as part of an integrated pest management approach. Biological control is a promising alternative tactic that can be used to manage D. suzukii populations, especially in unmanaged areas. This study aimed at exploring the diversity of resident hymenopteran parasitoids of drosophilids in northwestern Patagonia, where D. suzukii is considered an important pest. The survey also aimed to investigate possible associations between parasitoids and D. suzukii in several crops and non-crop fruits, and to determine D. suzukii fruits infestation levels. Fourteen sites with mainly berry crops were sampled biweekly using cider vinegar traps and collecting fresh fruits from a variety of crop and non-crop fruit plants. We identified five species of hymenopteran parasitoids, obtained from the baited traps, that have the potential to associate with D. suzukii: Leptopilina heterotoma Thomson, Ganaspis brasiliensis Ihering, Hexacola hexatoma Hartig (Figitidae), Pachycrepoideus vindemmiae Rondani (Pteromalidae), and Spalangia endius Walker (Spalangiidae). Leptopilina heterotoma is reported for the first time in Argentina. High numbers of D. suzukii adults were recovered from baited traps and field-collected fruits. However, no parasitoid emerged from D. suzukii pupae recovered from fruits, nor were any dead parasitoids recorded inside D. suzukii pupae. Overall infestation levels of D. suzukii on field-collected fruits did not differ significantly between species/varieties. The results are discussed with emphasis on the possible functionality and perspectives of using these species as biological control agents.

Gustatory responsiveness in Vespula germanica workers: exploring the interplay between sensory perception and task specialization.

Workers' task specialization and division of labor are critical features of social insects' ecological success. It has been proposed that the division of labor relies on response threshold models: individuals varying their sensitivity (and responsiveness) to biologically relevant stimuli and performing a specific task when a stimulus exceeds an internal threshold. In this work, we study carbohydrate and protein responsiveness and their relation to worker task specialization in Vespula germanica, an invasive social wasp. The sucrose and peptone responsiveness of two different subcastes, preforagers and foragers, was determined by stimulating the antenna of the wasps with increasing concentrations of the solution and quantifying whether each concentration elicited a licking response. We studied responsiveness in five different ways: (1) response threshold, (2) concentration 50 (concentration to which at least 50% of wasps responded), (3) maximum response, (4) mean scores and (5) median scores. Our results suggest that V. germanica foragers are more sensitive to sucrose (lower thresholds) than preforager workers. However, we found no differences for peptone thresholds (i.e., a protein resource). Nonetheless, this is the first study to investigate response thresholds for protein resources. The intercaste variation in sucrose responsiveness shown in our work contributes to the existing knowledge about response threshold theory as a mechanism for task specialization observed in V. germanica.

Sugar responsiveness could determine foraging patterns in yellowjackets.

Sympatric-related species often exhibit resource partitioning. This can occur through different mechanisms, such as behavioral, morphological, and sensory variations, leading to qualitative, temporal, or spatial differences in resource exploitation, such as consuming different types of food. Sensory-based niche partitioning could be the underlying mechanism through which closely related species effectively reduce niche overlap. Here we ask whether variations in sensory responses to carbohydrates could reflect differences in the foraging patterns of two Vespula species present in Patagonia. For this, we established (i) the response thresholds toward carbohydrate solutions of foraging V. germanica and V. vulgaris in the laboratory, (ii) the sugar concentration of foraged carbohydrates in the field, and (iii) possible effects of incoming sugar concentration and performance at individual and colony levels. Results indicate a higher sucrose response threshold in V. germanica than V. vulgaris. Field results indicate that higher carbohydrate concentrations foraged by V. germanica, with 57% of V. germanica foragers returning with concentrations above 50% w/w, while only 23% of V. vulgaris foragers did so. These differences in sucrose sensitivity and foraging patterns positively correlate with colony size, irrespective of the species. Our results suggest that competition could be reduced in these closely related invasive social wasp species through sensory differences in their sugar perception levels, which would lead to them foraging different carbohydrate sources. This study suggests that sensory niche partitioning could promote species coexistence in these social wasps.

Allee effects in an invasive social wasp: an experimental study in colonies of Vespula germanica.

Allee effects rely on the existence of mutually beneficial intraspecific interactions that increase individual fitness and per capita growth rate, as the number of individuals in a population or group increases. When the number of individuals falls below a given number, the success of a group or population drops. Social insects heavily rely on cooperation between individuals for various tasks such as foraging and breeding. In this study, we experimentally explored component Allee effects and the underlying mechanisms in colonies of the social wasp Vespula germanica. After the removal of workers, we counted the number of gynes produced, estimated the body mass index as a proxy of their quality, and registered the protein-food collected by foragers in colonies. Our research revealed a correlation between the decrease in worker population and a subsequent decrease in the production of gynes. However, the removal of workers did not impact the quality of the produced gynes or the quantity of protein-food collected by the colonies. These findings highlight the crucial role of the worker caste in the success of eusocial species and suggested an ability of workers to perform multiple tasks that enable colonies to respond to disturbances. Additionally, our study provides the first evidence of Allee effects at the colony level of V. germanica, with potential practical implications for managing this invasive species.

Honeydew production by the giant willow aphid (Tuberolachnus salignus, Hemiptera: Aphididae) and its effect on foraging yellowjackets (Hymenoptera: Vespidae).

BACKGROUND: Understanding the factors that promote the success of invasive species is important for managing biological invasions. Interactions between invasives and other species (e.g. competitors, pathogens, or predators), could favor or limit their success. In recent decades, yellowjacket wasps, including Vespula germanica and Vespula vulgaris, have successfully established in Patagonia. Additionally, the invasive willow Salix fragilis has invaded areas next to watercourses, which in turn are typically colonized by the giant willow aphid (GWA, Tuberolagnus salignus), an additional species characterized as a successful invader in many regions worldwide. Aphid exudate (honeydew) has been reported to be used as a carbohydrate source by social wasps. The aim of our study was to gain a better understanding of the infestation pattern of the GWA in north-western Patagonia, its effect on exudate availability and its relationship with yellowjacket foraging patterns. The study was conducted under the working hypothesis that the increase in the size of GWA colonies and resulting honeydew production, will fuel an increase in local Vespula spp. RESULTS: We found that the aphid honeydew is produced in relatively high amounts in the region (estimated at 1517 ± 139 kg/ha/season), with strong indications that it is used by yellowjackets because of the significantly higher abundance levels of yellowjackets foraging on honeydew compared to nearby areas. CONCLUSION: Given its effect on yellowjacket foraging behavior, the interaction of these three invasive species, willows, GWA and yellowjackets, needs to receive special attention to develop future environmentally-sound mitigation tools of these nuisance pest. © 2023 Society of Chemical Industry.

Long-term coexistence of two invasive vespid wasps in NW Patagonia (Argentina).

In Patagonia (Argentina) two non-native vespid wasps became established in the last decades. Vespula germanica was first detected in 1980, while V. vulgaris arrived some 30 years later. Both species can have a strong negative impact on agro-industrial economic activities, the natural environment, and outdoor human activities. Biological invasions may be influenced negatively by the degree of interaction with the resident native community and alien species already present. The sequential arrival and coexistence of Vespula wasps in Argentina for several years allows us to understand key questions of invasion ecology. Additionally, recognizing the outcome of the invasion by vespids in Patagonia, a region lacking native social wasps, may help plan species-focused mitigation and control strategies. We explored the role of competition in terms of invasion success, and the strategies that promote coexistence. Two possible scenarios, using niche overlap indices and isocline equations, were proposed to determine competition coefficients. Using a simple mathematical modeling framework, based on field collected data, we show that food resources do not play a central role in competitive interaction. The competition coefficients obtained from the equations were different from those inferred from the overlap indices (0.53 and 0.54-0.076 and 0.197, respectively). Together, these findings suggest that no matter the arrival order, V. vulgaris, always reaches higher densities than V. germanica when both species invade new regions. Our work contributes to further our understanding on the worldwide invasion processes deployed by these two eusocial insects.

Flexible foraging decisions made by workers of the social wasp Vespula germanica (Hymenoptera: Vespidae) in response to different resources: influence of ontogenetic shifts and colony feedback.

Decisions made by foraging animals conform a complex process based on the integration of information from multiple external environmental stimuli and internal physiological signals, which in turn are modulated by individual experience and a detection threshold of each individual. For social insects in which foraging is limited to given age subcastes, individual foraging decisions may also be affected by ontogenetic shifts and colony requirements. We studied the short-term changes in foraging preferences of the generalist wasp Vespula germanica, focusing on whether the individual response to different resources could be influenced by the ontogenetic shifts and/or by social interaction with nestmates. We carried both laboratory and field experiments to confront worker wasps to a short-term resource switch between either protein or carbohydrate-based foods. We tested the response of (1) Preforager workers (no foraging experience nor interaction with other wasps), (2) Forager workers (experience in foraging and no colony feedback), and (3) Wild forager workers (foraging naturally and exposed to free interactions with nestmates). We evaluated the maxilla-labium extension response (MaLER) for laboratory assays or the landing response for field assays. We observed that for wasps deprived of colony feedback (either preforagers or foragers), the protein-rich foods acceptance threshold increased (and thus a lower level of foraging on that item was observed) if they had foraged on carbohydrates previously, whereas carbohydrates were accepted in all assays. However, wasps immersed in a natural foraging context did accept protein foods regardless of their first foraging experience and reduced the carbohydrates collected when trained on protein foods. We provide evidence that short-term changes in foraging preferences depend on the type of resource foraged and on the social interactions, but not on ontogenetic shifts.

Nest-departure behaviour of gynes and drones in the invasive yellowjacket Vespula germanica (Hymenoptera: Vespidae).

Inbreeding costs can be high in haplodiploid hymenopterans due to their particular mechanism of sex determination (i.e., single-locus complementary sex-determination system, sl-CSD), as it can lead to the production of sterile males. Therefore, mechanisms contributing to reduced inbred matings can be beneficial. In this sense, asynchronous nest departure of sibling drones and gynes could reduce kin encounters in social hymenopterans. Using six observation colonies, we determined under field conditions the nest departure behaviour of sibling reproductives of the social wasp Vespula germanica (Hymenoptera: Vespidae). We determined that sexuals leave the nests definitively and detected asynchronous departure not fixed to a particular caste at a seasonal scale in some colonies, as gynes or drones delayed their departure as a function of the departure of the opposite sex, depending on the colony. At a higher temporal resolution (i.e., within a day), we discovered that drones consistently began to leave nests 1 h before gynes and this difference was driven by those individuals that left on the same day as did the opposite-sex kin. Even though other mechanisms such as polyandry and differential dispersal could also be important at reducing inbred matings in the species, the observed departure patterns (i.e., in some colonies actually leave together with the opposite caste, while in others temporal segregation seems to occur) from nests could be complementary to the former and be important at reducing the negative effects of inbreeding in this invasive species.

Drone aggregation behavior in the social wasp Vespula germanica (Hymenoptera: Vespidae): Effect of kinship and density.

Inbreeding can have negative consequences on population viability because of the reduced fitness of the progeny. In general, most species have developed mechanisms to minimize inbreeding such as dispersal and kin avoidance behavior. In the eusocial Hymenoptera, related individuals typically share a common nest and have relatively short mating periods, this could lead to inbreeding, and because of their single-locus complementary sex determination system, it may generate diploid males that could result in infertile triploid progeny representing a cost for the colony. Vespula germanica, is an eusocial wasp that has invaded many parts of the world, despite likely facing a reduced genetic pool during the arrival phases. We ask whether male wasp display specific aggregation behavior that favors genetic diversity, key to reduce inbreeding. Through a set of laboratory experiments, we investigated the effects of drone nestmateship and density on the aggregation behavior of V. germanica drones. We show that drones avoid aggregating with their nestmates at all densities while non-nestmates are avoided only at high densities. This suggests that lek genetic diversity and density could be regulated through drone behavior and in the long run minimize inbreeding favoring invasion success.

First detection of the cosmopolitan invader Leptoglossus occidentalis Heidemann (Heteroptera: Coreidae) in Argentina.

Leptoglossus occidentalis Heidemann is a conifer seed bug, native to North America. This species is considered invasive and has reached several countries in the Northern Hemisphere and most recently Chile in South America. This work reports the first detection of this species in Argentina, with specimens from the Rio Negro province, in 2017. Ecological traits and its potential rapid spread were also discussed.

Dispersal behavior of yellowjacket (Vespula germanica) queens.

Understanding the factors that affect animal dispersal behavior is important from both fundamental and applied perspectives. Dispersal can have clear evolutionary and ecological consequences, but for nonnative insect pests, dispersal capacity can also help to explain invasion success. Vespula germanica is a social wasp that, in the last century, has successfully invaded several regions of the world, showing one of the highest spread rates reported for a nonnative insect. In contrast with nonsocial wasps, in social species, queens are responsible for population redistribution and spread, as workers are sterile. For V. germanica, it has been observed that queen flight is limited to 2 distinct periods: early autumn, when new queens leave the nest to mate and find sheltered places in which to hibernate, and spring when new colonies are founded. Our aim was to study the flight behavior of V. germanica queens by focusing on the different periods in which dispersal occurs, characterizing as well the potential contribution of queen flight (i.e., distance) to the observed geographical spread. Our results suggest that the distances flown by nonoverwintered queens is greater than that flown by overwintered individuals, suggesting that the main queen dispersal events would occur before queens enter hibernation. This could relate to a behavioral trait of the queens to avoid the inbreeding with related drones. Additionally, given the short distances flown and remarkable geographical spread observed, we provide evidence showing that queen dispersal by flight is likely to contribute proportionately less to population spread than human-aided factors.

Brewer's Yeast, Saccharomyces cerevisiae, Enhances Attraction of Two Invasive Yellowjackets (Hymenoptera: Vespidae) to Dried Fruit and Fruit Powder.

The German yellowjacket, Vespula germanica F., and common yellowjacket, Vespula vulgaris L. (Hymenoptera: Vespidae), are pests of significant economic, environmental, and medical importance in many countries. There is a need for the development and improvement of attractive baits that can be deployed in traps to capture and kill these wasps in areas where they are a problem. Yellowjackets are known to feed on fermenting fruit, but this resource is seldom considered as a bait due to its ephemeral nature and its potential attractiveness to nontarget species. We analyzed the headspace volatiles of dried fruit and fruit powder baits with and without Brewer's yeast, Saccharomyces cerevisiae, using gas chromatography-mass spectrometry, and we field tested these baits for their attractiveness to yellowjackets in Argentina. The addition of yeast to dried fruit and fruit powder changed the volatile compositions, increasing the number of alcohols and acids and decreasing the number of aldehydes. Dried fruit and fruit powder baits on their own were hardly attractive to yellowjackets, but the addition of yeast improved their attractiveness by 9- to 50-fold and surpassed the attractiveness of a commercial heptyl butyrate-based wasp lure. We suggest that further research be done to test additional varieties and species of yeasts. A dried fruit or fruit powder bait in combination with yeast could become a useful tool in the management of yellowjackets.

No evidence of enemy release in pathogen and microbial communities of common wasps (Vespula vulgaris) in their native and introduced range.

When invasive species move to new environments they typically experience population bottlenecks that limit the probability that pathogens and parasites are also moved. The invasive species may thus be released from biotic interactions that can be a major source of density-dependent mortality, referred to as enemy release. We examined for evidence of enemy release in populations of the common wasp (Vespula vulgaris), which attains high densities and represents a major threat to biodiversity in its invaded range. Mass spectrometry proteomic methods were used to compare the microbial communities in wasp populations in the native (Belgium and England) and invaded range (Argentina and New Zealand). We found no evidence of enemy release, as the number of microbial taxa was similar in both the introduced and native range. However, some evidence of distinctiveness in the microbial communities was observed between countries. The pathogens observed were similar to a variety of taxa observed in honey bees. These taxa included Nosema, Paenibacillus, and Yersina spp. Genomic methods confirmed a diversity of Nosema spp., Actinobacteria, and the Deformed wing and Kashmir bee viruses. We also analysed published records of bacteria, viruses, nematodes and fungi from both V. vulgaris and the related invader V. germanica. Thirty-three different microorganism taxa have been associated with wasps including Kashmir bee virus and entomophagous fungi such as Aspergillus flavus. There was no evidence that the presence or absence of these microorganisms was dependent on region of wasp samples (i.e. their native or invaded range). Given the similarity of the wasp pathogen fauna to that from honey bees, the lack of enemy release in wasp populations is probably related to spill-over or spill-back from bees and other social insects. Social insects appear to form a reservoir of generalist parasites and pathogens, which makes the management of wasp and bee disease difficult.