Biol Invasions https://doi.org/10.1007/s10530-019-01917-x (0123456789().,-volV)( 0123456789().,-volV) PERSPECTIVES AND PARADIGMS How to slow the global spread of small hive beetles, Aethina tumida Marc Oliver Scha¨fer . Ilaria Cardaio . Giovanni Cilia . Bram Cornelissen . Karl Crailsheim . Giovanni Formato . Akinwande Kayode Lawrence . Yves Le Conte . Franco Mutinelli . Antonio Nanetti . Jorge Rivera-Gomis . Anneke Teepe . Peter Neumann Received: 21 September 2017 / Accepted: 14 January 2019 Ó The Author(s) 2019 Abstract Small hive beetles (SHBs) are parasites of propose to take advantage of SHB invasion history and social bee colonies endemic to sub-Saharan Africa and biology to enrol a feasible plan involving all stake- have become a widespread invasive species. In the holders. Raising awareness, education and motivation new ranges, SHBs can cause damage to apiculture and of stakeholders (incl. adequate and timely compensa- wild bees. Although the further spread seems inevi- tion of beekeepers) is essential for success. Moreover, table, eradication of new introductions and contain- sentinel apiaries are recommended in areas at risk, ment of established ones are nevertheless urgently because early detection is crucial for the success of required to slow down the invasion speed until better eradication efforts. Given that introductions are mitigation options are available. However, at present detected early, SHB eradication is recommended, there is no adequate action plan at hand. Here, we incl. destruction of all infested apiaries, installation of M. O. Scha¨fer (&) A. K. Lawrence National Reference Laboratory for Bee Diseases, Entomology Research Laboratory, Department of Friedrich-Loeffler-Institute (FLI), Federal Research Biology, Federal University of Technology, Akure, Institute for Animal Health, Greifswald Insel-Riems, Nigeria Germany e-mail: marc.schaefer@fli.de Y. Le Conte INRA Centre de Recherche Provence-Alpes-Coˆte d’Azur, I. Cardaio Á G. Cilia Á A. Nanetti Unite` Abeilles et Environnement, UMR PrADE, Domaine Council for Agricultural Research and Economics, Saint Paul, Site Agroparc, 84914 Avignon, France Agriculture and Environment Center (CREA-AA), Via di Saliceto 80, 40128 Bologna, Italy F. Mutinelli National Reference Laboratory for Beekeeping, Istituto B. Cornelissen Zooprofilattico Sperimentale delle Venezie, Legnaro, PD, Wageningen Plant Research, Wageningen University and Italy Research, Wageningen, The Netherlands A. Teepe K. Crailsheim Centre for Tropical Bee Research (CINAT), National Institute of Biology, University of Graz, Graz, Austria University of Costa Rica, Heredia, Costa Rica G. Formato Á J. Rivera-Gomis P. Neumann Istituto Zooprofilattico Sperimentale del Lazio e della Institute of Bee Health, Vetsuisse Faculty, University of Toscana ‘‘M. Aleandri’’, Rome, Italy Bern, Bern, Switzerland 123 M. O. Scha¨fer et al. sentinel colonies to lure escaped SHBs and a ban on Neumann 2006; Hoffmann et al. 2008; stingless bees: migratory beekeeping. If wild perennial social bee Halcroft et al. 2008, 2011; Mutsaers 2006; Pen˜a et al. colonies are infested, eradication programs are con- 2014; Greco et al. 2010; Wade 2012). Accordingly, a demned to fail and a strategic switch to a containment range of pest mitigation measures has been developed, strategy is recommended. Containment includes ade- but at present SHB diagnosis and control are not quate integrated pest management and a strict ban on sufficient (Neumann et al. 2016). In particular, control migratory beekeeping. Despite considerable gaps in outside of managed apiaries is not available yet, which our knowledge of SHBs, the proposed action plan will is urgently required to limit the impact of SHBs on help stakeholders to slow down the global spread of wild bees. Thus, there is an urgent and apparent need SHBs. to slow down the continuing global spread of SHBs until better mitigation methods are available. How- Keywords Apis mellifera Á Apiculture Á Bees Á ever, at present, there is no international strategy for Contingency plan Á Honeybee Á Parasite SHBs. Therefore, we here propose a best-practice action plan for A. tumida invasions (Fig. 1). Introduction Suggested contingency measures Biological invasions typically follow a jump-dispersal Stakeholder awareness and engagement pattern (Canning-Clode 2015) and eradication of recent introductions combined with containment of A science-based approach should be taken to raise established ones have been proven as a means to slow stakeholder awareness of all relevant impacts of SHBs down the global spread for a number of species (e.g. on managed and wild social bees (Table 1). All Campbell and Donlan 2005; Boser et al. 2017). stakeholders should be aware that anytime SHBs Efficient approaches for both eradication and contain- might arrive in their country or region. Therefore, it is ment require measures based on the biology of the important to take adequate actions (Table 1), before invasive species in question, the local situation as well new introductions occur. All stakeholders should be as adequate stakeholder involvement (Anonymous provided with information on how to access tools and Editorial 2017). Here, we focus on the small hive guidelines that enable recognition of new infestations. beetle (SHB), Aethina tumida (Coleoptera: Nitiduli- However, stakeholders may value the costs of invasive dae). This beetle has originally been described as a species differently according to their business (Sim- parasite and scavenger of honeybee colonies native to berloff 2003). Moreover, the degree of stakeholder sub-Saharan Africa (Lundie 1940). In 1996, it engagement varies between countries due to resource emerged as an invasive species, which has now constraints (finances, knowledge, etc.) possibly lead- reached all continents except Antarctica (Neumann ing to a weakest link scenario (Stokes et al. 2006). et al. 2016; DePaz 2017; Lee et al. 2017). The spread Nevertheless, success is only possible if stakeholders of SHBs is ongoing, as evidenced by a number of agree and share a common view on the planned recent introductions (2014: Italy, Brazil; 2015: Philip- measures and respective consequences on their busi- pines; 2017: Belize, Canada, South Korea; 2018: nesses and apiculture in general. Stakeholders, in Mauritius; cf. Neumann et al. 2016; Lee et al. 2017; particular beekeepers, should regard integrated pest DePaz 2017; Sturgeon 2017; Muli et al. 2018). management (IPM) of SHBs, incl. adjusted manage- Outside of its endemic range, SHBs can cause severe ment and adequate sanitation of apiaries and other damage to apiculture as well as wild honeybee apicultural facilities (Hood 2011; Neumann et al. colonies and may also endanger other social bees 2016). In particular, adequate and fast compensation serving as alternative hosts (bumblebees: Spiewok and for beekeepers appears to be central for success. P. Neumann Swiss Bee Research Centre, Agroscope, Bern, Switzerland 123 How to slow the global spread of small hive beetles, Aethina tumida Raising stakeholder Improve stakeholder Import control Sentinel apiaries awareness and motivation education Early detection Pest detected Yes No Counter measures First assessment of introduction stage Early Epidemiological assessment stage of introduction stage Eradication Containment Continuous monitoring Fig. 1 Flow diagram that demonstrates the proposed action zones have to be implemented and an assessment on the stage of plan to limit the global spread of small hive beetles. Import the introduction must be determined. Depending on the size and control is essential to limit intoductions. Raise awareness and the location of the infested area, it must be decided if eradication improve education among all stakeholders (especially beekeep- is possible or if the outbreak has to be limited through ers) to detect new infestations faster. Furthermore, the containment. For both scenarios, continuous monitoring, installation of regularly visited sentinel apiaries, in places including the immediate installation of sentinel colonies (trap chosen according to higher risks of importation, will enlarge the hives) at the actual outbreak sites is necessary to prevent the chances of early detection. Immediately after detection of further spread of adult small hive beetles that might escape the A. tumida counter measures like the establishment of protection control measures Early detection Border control and quarantine measures within a suitable legal framework are clearly the first line of Evidence strongly suggests that only if a new intro- defence against SHB invasion and should be imple- duction of SHBs is detected early, eradication can be mented by every country. Moreover, all stakeholders successful (Neumann et al. 2016; Mutinelli 2016). In should be able to recognize A. tumida infestations via the USA, the first unidentified SHB specimens were adult and larval morphology as well as clinical signs at collected in November 1996 (Neumann and Elzen the colony level (Neumann et al. 2016). In particular, 2004), but it took 2 years until A. tumida was beekeepers should be cognizant during their routine officially confirmed (Hood 2000). By then, SHBs practice and apiary inspections. Competent laborato- were already well established and widespread (Neu- ries are required to confirm or reject suspicion by mann and Elzen 2004), rendering an eradication beekeepers. This holds especially true for eggs and impossible. The same holds true for the introduction larvae, which cannot be assigned to A. tumida based