Stakeholder awareness and engagement
A science-based approach should be taken to raise stakeholder awareness of all relevant impacts of SHBs on managed and wild social bees (Table 1). All stakeholders should be aware that anytime SHBs might arrive in their country or region. Therefore, it is important to take adequate actions (Table 1), before new introductions occur. All stakeholders should be provided with information on how to access tools and guidelines that enable recognition of new infestations. However, stakeholders may value the costs of invasive species differently according to their business (Simberloff 2003). Moreover, the degree of stakeholder engagement varies between countries due to resource constraints (finances, knowledge, etc.) possibly leading to a weakest link scenario (Stokes et al. 2006). Nevertheless, success is only possible if stakeholders agree and share a common view on the planned measures and respective consequences on their businesses and apiculture in general. Stakeholders, in particular beekeepers, should regard integrated pest management (IPM) of SHBs, incl. adjusted management and adequate sanitation of apiaries and other apicultural facilities (Hood 2011; Neumann et al. 2016). In particular, adequate and fast compensation for beekeepers appears to be central for success.
Evidence strongly suggests that only if a new introduction of SHBs is detected early, eradication can be successful (Neumann et al. 2016; Mutinelli 2016). In the USA, the first unidentified SHB specimens were collected in November 1996 (Neumann and Elzen 2004), but it took 2 years until A. tumida was officially confirmed (Hood 2000). By then, SHBs were already well established and widespread (Neumann and Elzen 2004), rendering an eradication impossible. The same holds true for the introduction of SHBs into Australia (Neumann and Elzen 2004).
Border control and quarantine measures within a suitable legal framework are clearly the first line of defence against SHB invasion and should be implemented by every country. Moreover, all stakeholders should be able to recognize A. tumida infestations via adult and larval morphology as well as clinical signs at the colony level (Neumann et al. 2016). In particular, beekeepers should be cognizant during their routine practice and apiary inspections. Competent laboratories are required to confirm or reject suspicion by beekeepers. This holds especially true for eggs and larvae, which cannot be assigned to A. tumida based on morphometrics alone (Neumann et al. 2016). Any apiary under suspicion should be taken under strict and immediate sanitary restrictions and all movements of bees (colonies and queens), bee products and used bee equipment, into and out of such apiaries must be banned until the competent authority has investigated the case.
At present, neither pheromones nor host kairomones have been identified for host finding SHBs yet. Therefore, the only known efficient attractants for adult SHBs are functional honeybee colonies. To be able to identify the pest early and to investigate a new outbreak in detail, it is therefore recommended to install sentinel apiaries, which consist of fully functional queenright honeybee colonies, to attract and trap SHBs in zones at risk for new introductions (Chauzat et al. 2016; Mutinelli 2016; Keeling et al. 2017). Such sentinel apiaries enable a cheaper and more efficient monitoring compared to active surveillance of hobby or commercial apiaries (Rivera-Gomis et al. 2017). Respective sentinel hives should be composed of one hive-box only with fewer frames than actually fit, to foster efficient and quick diagnosis. The hives should also be equipped with SHB traps that can be quickly checked (reviewed by Neumann et al. 2016). Inspectors are advised to regularly scale down these colonies by replacing brood frames with empty ones and to visit the hives at least every two weeks when local weather conditions foster SHB pupation (reviewed by Neumann et al. 2016). Surveillance in temperate and subtropical zones should therefore be reinforced from spring to autumn and all year long in tropical zones. During winter in temperate climates those traps should be preferentially used that allow monitoring but limit disturbance of the colonies (Neumann et al. 2016).
Official confirmation of infestation with A. tumida should be given, if the competent authority identifies SHB eggs, larvae, pupae or adults. Then, a protection zone should be installed immediately to limit further spread, including a strict ban on movements of bees and beekeeping equipment, because migratory beekeeping poses the highest risk of spreading A. tumida (Neumann and Elzen 2004). The ban on movement requires an appropriate and permanent official control system to ensure application and compliance as well as traceability. The protection zone should be large enough to detect all possible natural spread, but small enough to be manageable with the local human resources available. As the maximum flight range of adult SHBs is still unknown, it is obviously impossible to define a safe distance. However, since all apiaries and beekeeping facilities (including abandoned ones) in the protection zone have to be investigated as quickly as possible and will potentially be placed under permanent restrictions, the size of the protection zone should initially be rather small (~ 10 km radius). It can subsequently be enlarged if required by the population status (e.g. when infested colonies are confirmed outside of the initial zone). In order to enhance chances of detecting new infestations, visual diagnosis should only be performed by trained staff (Spiewok et al. 2007; Neumann et al. 2013; OIE 2017b), effective traps should be installed (cf. Neumann et al. 2016), and hive debris samples, workers or other hive matrices should be investigated with specific DNA diagnostics (Ward et al. 2007; Ouessou Idrissou et al. 2018). To ensure that the locations of all beekeeping facilities inside the protection zone are known, every local beekeeper should be obliged to register and to update the competent authority about apiaries (in operation or not), honey houses, storage rooms and beeswax rendering or royal jelly plants. It is apparent that registration and control of movements might at present be unmanageable in some countries. Respective legislation and law enforcement is therefore recommended.
It is further recommended to establish a surveillance zone surrounding the protection zone, in which sentinel apiaries should be implemented (see above), movements of hives be registered and all apiaries sampled to detect any further spread as soon as possible (Chauzat et al. 2016; Granato et al. 2017).
In conclusion, a combination of sentinel sites as well as highly motivated (adequately compensated) and well-educated beekeepers appears to be the optimal approach fostering early SHB detection.
The population status of every new SHB case should be investigated as soon as possible and the potential economic and environmental consequences should be evaluated, before starting an eradication process. These investigations are indispensable, as it seems to be possible to eradicate SHBs only if a new introduction is recognized early and the spread is still limited to a manageable area. Apicultural trade and migratory beekeeping activities, abandoned or not registered apiaries, commercial bumblebee hives as well as possible infestations of wild host populations must be considered (e.g. in Australia, feral honeybee nests in trees were inspected, cf. Neumann et al. 2016). As soon as wild social bees with perennial colonies (i.e. Apis spp.) are infested, eradication seems impossible, as such colonies might host SHBs over several years and cannot be entirely discovered. Likewise, unsuccessful eradication measures of managed apiaries over two seasons strongly suggest reservoirs outside of the reach of control. Then, it appears prudent to switch from eradication to containment.
Given that the introduction of SHBs appears to be early and infestations are still localized in a few managed apiaries, then it appears worthwhile starting eradication. Examples for successful eradications have been Perth, Australia and Sicily, Italy (cf. Neumann et al. 2016; Mutinelli 2016). Most important is that eradication must begin as soon as the population status is sufficiently clear. Every day counts as adult SHBs may disperse into the wild bee populations, thereby escaping eradication. It is mandatory to stamp out all colonies of the SHB-infested apiaries as soon as possible, because false negative diagnostics are especially likely in case of low infestation levels. For eradication, the entrances of all colonies should be sealed in the early afternoon (before the peak flight activity of adult SHBs, Neumann et al. 2016). Then, the bees should be killed (e.g. with sulphur dioxide) and all the material destroyed (e.g. burning) without any delay under the supervision of the competent authorities (Mutinelli et al. 2014; Mutinelli 2016). The soil surrounding SHB-infested colonies poses the risk of reinfection due to SHB-pupation and should be treated adequately (Hood 2000, 2011; Mutinelli et al. 2014; Neumann et al. 2016). Continuous monitoring has to be considered and sentinel colonies must be installed before all colonies of an infested apiary are destroyed, as a considerable number of adult SHBs may stay outside of hives (Annand 2011). These sentinel colonies in situ will attract free-flying SHBs that may have survived the local eradication effort.
Even though SHBs are able to reproduce on fruits and other food in the laboratory and in semi-field assays (Buchholz et al. 2008), field surveys so far were not able to confirm any association of SHBs with alternative food sources outside of social bee colonies (Mutinelli et al. 2015; Mutinelli and Maroni Ponti 2017; Willcox et al. 2017). It appears most effective to focus on control measures for well-known major routes for SHB transmission and reproduction (cf. Neumann et al. 2016). In the case of eradication, any movement of managed bees into and out of the protection zone must be prohibited at all costs. Costs for stakeholders due to inadequate pollination should be covered by the competent authority. If one makes the decision to eradicate, one must be very strict to be successful. If one weakens the restrictions, the potential for further spread of SHB rises in the area, which increases the possibility for SHB to establish outside of managed beekeeping, making eradication impossible.
For the 5 years following the last report of the presence of A. tumida an annual survey, supervised by a competent authority, should be carried out on a representative sample of apiaries in the concerned country or zone, and no signs of the presence of A. tumida should be detected. Only if this condition is met, the free status as a result of an eradication program can be recognized (OIE 2017a).
To enhance chances of eradication success, substantial efforts should be made to ensure that all stakeholders work closely together and communicate necessary measures clearly and on a fair base. In particular, adequate and timely compensation of beekeepers is highly recommended. It must be prevented that beekeepers feel forced to handle the problem by themselves, in view of substantial financial losses.
If eradication is not an option anymore, SHB containment must be applied to limit further spread. Protection zones have to be established (see above) and inside these zones, measures have to be applied to limit SHB reproduction, especially destructive mass reproduction (Neumann et al. 2016). The measures should include the use of in-hive traps (Neumann and Hoffmann 2008; Bernier et al. 2015; Levot et al. 2015), a beekeeping management that is adapted to the presence of SHB, incl. adequate sanitation of apiaries and other apicultural facilities (Hood 2011; Neumann et al. 2016) and the treatment of the surrounding soil, if damage by SHB larvae or other clear signs (i.e. slime traces of wandering larvae) have been observed inside the colonies (Neumann et al. 2016).
However, it is indispensable that stakeholders have legitimate access to products for SHB pest treatment (e.g. medication in hives and/or adequate soil drenching products; reviewed by Neumann et al. 2016). Most unfortunately, no such products are currently available in the EU. Furthermore, implications for declaring SHBs established in a region/country should be considered, particularly the possible impact on international commercial movement (i.e. restrictions, ban, etc.) of honeybees, bee equipment and bee products.