The Asian yellow-legged hornet (Vespa velutina) has been invading Italy since 2013, and it was subjected to management programs to counter its spread and raise awareness about its impacts. We administered a questionnaire to a sample of 358 beekeepers in Italy, asking them about their sources of information on V. velutina and their perception of its potential impacts and severity, compared to other threats to beekeeping. We also explored Internet searching volumes on Google and Wikipedia about V. velutina, to identify seasonal and long-term trends in public awareness. Workshops, journals or bulletins, the Internet and word-of-mouth with colleagues were the primary sources of information about V. velutina. Internet searches peaked during the activity period of the species and increased over time, with thousands of visits to Wikipedia each month. Beekeepers believed V. velutina to affect beekeeping by predating on honey bees (Apis mellifera), paralyzing foraging, reducing honey availability and depleting the winter cluster. Moreover, V. velutina has been deemed a severe threat to beekeeping, similar to other threats like pesticides and the varroa mite (Varroa destructor). Our findings indicate that beekeepers seem to be aware of the potential impacts of V. velutina in Italy, both within and outside of its invaded area, considering it a major threat to beekeeping. Moreover, citizens seem to have become progressively curious about the species. Information campaigns on the Internet and specialized magazines might be helpful to communicate about the impacts of the species, and the need to develop diffused surveillance networks.

Beekeeping, biological invasions, Google, Google Trends, species management, Wikipedia

Biological invasions are a major driver of change globally, with environmental and socio-economic impacts, whose frequency and magnitude are increasing in synergy with international trade and climate change (Hulme 2009; Robinson et al. 2020). Therefore, many countries have developed public policies aimed at preventing, counteracting, or mitigating biological invasions (Turbelin et al. 2017), including both dedicated legal frameworks and also financial support for specific conservation projects targeting invasive alien species (e.g. the LIFE programme in the European Union, European Commission Directorate-General for Environment 2015).

Most conservation projects include outreach activities to raise the awareness of specific stakeholders, and/or the general public about biological invasions and invasive alien species (Lioy et al. 2019a). Awareness raising is a prerequisite for attitudinal and behavioral change, which could in turn foster compliance with regulations about biological invasions or the long-term endorsement of dedicated policies (Heberlein 2012). Surveys based on questionnaires are a common approach to measure awareness about biological invasions. Before-and-after designs (Novoa et al. 2017) and repeated cross-sectional designs (Russell 2014) are commonly adopted to test for temporal changes in public awareness. However, while these studies might be effective for specific stakeholders or over small spatial scales, they might fail to consider broader changes in public awareness that occur at larger spatial and temporal levels of detail. For example, while a before-and-after survey could measure changes in public awareness following a project about a particular invasive alien species, the same species might be targeted by multiple projects over a time span of several years. Designing a specific survey for this scope might be unfeasible and expensive.

On the other hand, at a time where the Internet is becoming a primary source of information worldwide, many studies showed that a growing number of people search on the Internet for those topics they are curious about, or have heard about, from various sources of information. Therefore, the analysis of online searching volumes on search engines and Wikipedia could become a valuable tool to measure public interest towards political (Mellon 2013, 2014) as well as environmental issues (Nghiem et al. 2016; Burivalova et al. 2018), including biological invasions (Cerri et al. 2020; Cerri et al. 2022). In this study, we aimed to show that it is possible to combine questionnaire-based surveys with the analysis of Internet searching volumes to draw conclusions about the awareness of stakeholders and the general public on invasive alien species by considering the case of the invasive Asian yellow-legged hornet (Vespa velutina Lepeletier, 1836) in Italy.

V. velutina has become invasive in Europe, where it was first reported in 2004 in France, and is increasing its distribution across Central and Mediterranean countries and in the UK (Laurino et al. 2020). From 2013 onwards, several nests of the species have been reported in Italy, where it colonized the westernmost portion of the Liguria region, close to the French border, from which it then expanded to some areas of the Piedmont and Tuscany regions (Bertolino et al. 2016; Lioy et al. 2019b).

Apart from its impact on native insects and wild pollinators, its intensive predation upon the western honey bee (Apis mellifera), its reproductive potential and the lack of specialized predators, V. velutina can have severe impacts on beekeeping in Europe (Laurino et al. 2020). The predation of honey bees could decrease the pollination services they provide, undermine honey production and reduce the availability of individuals for the winter cluster, with consequences for the overwinter survival of the colonies (Monceau et al. 2013). The predator activity of V. velutina also limits the foraging activity of honey bees by promoting homing failure and determining a “foraging paralysis”, where honey bees do not leave the colony fearing its predation (Requier et al. 2019), which could further reduce pollination services and honey production. V. velutina could also damage fruit production, as adult individuals need sweet carbohydrates to sustain their metabolism. Finally, V. velutina, by building nests mainly on artificial structures or trees in or near urban areas, can also be problematic due to the risk of stings to people (de Haro et al. 2010) that in some cases could lead to fatalities caused by anaphylactic reactions to stings (Feás Sánchez and Charles 2019).

The management of invasive V. velutina is becoming an important issue for some European countries, with France documenting an expenditure of about €23 million for nest removal in the 2006–2015 period (Barbet-Massin et al. 2020), while Spanish beekeepers from la Coruña province reported an expenditure of about €67,000 just for 2016 (Ferreira Golpe et al. 2016). The hypothetical cost for managing the species if it were to colonize all the climatically suitable areas in France, Italy, and the UK is estimated to reach about €29.5 million per year (Barbet-Massin et al. 2020).

Due to its potential impacts on beekeeping, and its associated costs, the invasion of V. velutina has been targeted by various conservation projects in Italy. These include the LIFE STOPVESPA (https://www.vespavelutina.eu) and the LIFE ASAP (https://www.lifeasap.eu) projects, the Aliem Interreg Med project (http://interreg-maritime.eu/web/aliem), all three projects co-founded by the European Union, and the projects VELUTINA and STOPVELUTINA (https://www.stopvelutina.it/il-progetto). While these initiatives differed in their spatial scale and specific goals, all of them included many outreach initiatives about V. velutina, such as press campaigns, meetings with stakeholders and workshops at beekeeping events, with the main intention of raising the awareness of both beekeepers and laypeople.

The aim of the present study was to investigate public awareness about the invasive hornet V. velutina in Italy by implementing two different approaches for analyzing i) how beekeepers perceived the impact of the species, and ii) how online searches on V. velutina varied over time. Therefore, we first administered a questionnaire to a sample of beekeepers in Italy to ask them about their perception of V. velutina and its impact (also in relation to the other threats affecting honey bees) and their primary sources of information about the species. Then, we conducted a time-series analysis to identify long-term trends in on-line searches on Google and Wikipedia about V. velutina in Italy to capture temporal trends in public awareness about the species.

Datasets and reproducible software code are available at https://osf.io/efs7k/.

To the best of our knowledge, this study constituted a first attempt to draw conclusions about the awareness of beekeepers and citizens towards V. velutina in an invaded area of Europe. While another study (Requier et al. 2020) explored the behavior of beekeepers in response to V. velutina, no study formally asked beekeepers about their beliefs on the potential impacts of V. velutina, or about its potential magnitude with respect to other threats that could affect honey bees and beekeeping activity. Taken together, findings from the questionnaire for the beekeepers and the analysis of Internet searching volumes, indicate that public awareness increased over the years after the detection of the species in Italy, and that stakeholders are aware about the invasion of V. velutina and its social and ecological impacts. The different conservation projects developed in Italy over the years may have contributed to achieving these results, together with dissemination activities by beekeeper associations and by the media in general.

Beekeepers in Central and Northern Italy seem to have received considerable exposure to news concerning V. velutina and its potential environmental and socio-economic impacts. Such exposure, in turn, affected their concerns about the species. The vast majority of our sample believed that V. velutina could have detrimental impacts on the conservation of honey bees and beekeeping, in line with the available scientific evidence (Requier et al. 2019; Laurino et al. 2020). Respondents from invaded areas seemed to be even more concerned about this. They believed V. velutina to have greater impacts than the native V. crabro, another species that could prey on honey bees. Moreover, these impacts were also considered relevant for beekeeping and the conservation of honey bees. V. velutina severity was considered comparable to that of other major causes of honey bee decline, such as pesticides (Sánchez-Bayo et al. 2016; Tsvetkov et al. 2017) or Varroa destructor (Thoms et al. 2019), and even more severe than other stressors, such as the predation from other native Hymenoptera, or viral, fungal and bacterial diseases. While our findings came from a convenient sample of beekeepers, which may have been more in contact with beekeeping organizations and more aware than the “average” beekeeper, we believe our findings to be strong enough that it is unlikely that the scenario from the overall beekeeping community is very much different. V. velutina seems to be considered a species with systematic and not-negligible impacts on honey bees and beekeeping.

Moreover, we found that beekeepers apprised themselves about V. velutina from a wide range of different channels, encompassing both the Internet and specialized magazines, and also activities with other members of their community, like other beekeepers and professionals holding workshops. On the other hand, conventional media and mailing lists seemed to be minor information sources on V. velutina.

These findings might help to design communication campaigns about V. velutina among beekeepers. The fact that beekeepers seem to be at least familiar with the species and its impacts indicate that they might have stable attitudes about this topic (Heberlein 2012). Their involvement in ongoing management initiatives confirms this. Both LIFE STOPVESPA and STOPVELUTINA projects have seen the participation of many beekeepers in the monitoring of V. velutina distribution (see projects website). The awareness of the impact caused by V. velutina and the willingness to collaborate in its management is fundamental for the extension at the national scale of an Early Warning and Rapid Response system already developed in the invaded area (Porporato 2016). Considering the sources of information that are adopted the most by beekeepers, conservationists should further promote participation in management activities through peer-to-peer communication within the beekeeping community, by publishing papers on specialized magazines and advertising on Internet sites about beekeeping, decreasing their expenditures for communication campaigns on traditional media. Italy hosts approximately 40,000 amateur and 18,000 professional beekeepers, and their engagement in rapid detection and early warning activities could be fundamental to monitor the species at the national scale.

The seasonality of Internet searches about V. velutina seems to be correlated with the phenology of the species, since online searching volumes increased when people can observe the species in the environment (Mittermeier et al. 2019). Searches on Google increased during the activity season of the species, between April and October, with two peaks in May-June and August-September, corresponding to the first phase of nest construction and to the time of the year when colonies reach considerable size, becoming a concern for people. However, the observed seasonality could also be affected by the news published by the media or by ongoing conservation projects, which seems to have a higher frequency during the months of activity of the species (Lioy et al. 2019c).

Consultation to the Wikipedia page about the species was in the order of thousands of visits per month, with peaks of more than 10,000 visits. We believe that such a high number of visits is unlikely to have been generated by stakeholders or researchers alone, and that it probably involved laypeople as well. The overall volume of Internet searches about V. velutina and their long-term trend indicated a progressive awareness of laypeople about its progressive establishment into new areas and related consequences. This aspect was confirmed by the long term-trends of the Google Trends index for the two Italian words for the species, which increased between 2013 and 2020, reflecting the progressive spread of the species in Italy and the emergence of relevant impacts on beekeeping (Bertolino et al. 2016). The Google Trends index is discounted for the overall number of searches on Google, which strongly increased between 2013 and 2020 (Bologna et al. 2018): the fact that such index grew steadily during this period indicates that a growing proportion of people were interested in V. velutina and searched for it on the Internet.

The analysis of Internet searching volumes might be a promising complementary tool for monitoring the presence of V. velutina in Italy and Europe. As Google Trends can be downloaded at the regional level, peaks in searches about V. velutina could signal the species’ colonization of a certain area. This approach is already adopted in epidemiology to trace the circulation of viral disease (Carneiro and Mylonakis 2009), and other studies considered it for the monitoring of common invasive alien species, such as the tiger mosquito (Aedes albopictus, Cerri and Bertolino 2020). As V. velutina actively exploits human buildings for constructing its nests, becoming visible and concerning to residents, this approach should work well in its invaded range due to the high proportion of urban and rural landscapes. Nevertheless, due to the high misidentification rate of the species with native insects, peaks in searches should be followed by insights or direct monitoring with traps (Demichelis et al. 2014; Lioy et al. 2020) for assessing with certainty the presence of V. velutina. Moreover, the analysis of seasonal patterns in relation to searches on Google and Wikipedia might also highlight spatial patterns in the phenology of the species in its invaded range, contributing to improve our understanding of how the phenological plasticity of invasive alien species affects their invasion success at a time of climate change (Manfredini et al. 2019).

The authors are grateful to all the beekeepers who participated in the survey of the perceived impacts posed by the presence of V. velutina in Italy. Special thanks are also directed to the following beekeeper associations, that promoted the distribution of the survey to the beekeepers: Aspromiele, AgriPiemonte Miele, Consociazione Apicoltori della Provincia di Torino, AlpaMiele, Apiliguria, Toscana Miele, Consorzio Apicoltori della Provincia di Udine. We also thank a reviewer for his effort in improving the manuscript.

This research was funded by the LIFE project ASAP (LIFE15 GIE/IT/001039 ASAP Project).