This risk assessment is based on the Great Britain Non-Native Species Risk Assessment Template V1.3 (09/11/2011)

Transcription

1 This risk assessment is based on the Great Britain Non-Native Species Risk Assessment Template V1.3 (09/11/2011) GB NON-NATIVE ORGANISM RISK ASSESSMENT SCHEME Name of organism: Tropilaelaps spp.: Tropilaelaps clareae and Tropilaelaps mercedesae Authors: Helen Anderson and Gay Marris Date: 31/3/2012 Draft:2 Risk Assessment Area: Great Britain (i.e. England, Scotland and Wales) 1

2 SECTION A Organism Information and Screening Stage 1. Organism Information 1. Identify the organism. Is it clearly a single taxonomic entity and can it be adequately distinguished from other entities of the same rank? 2. If not a single taxonomic entity, can it be redefined? (if necessary use the response box to redefine the organism and carry on) 3. Does a relevant earlier risk assessment exist? (give details of any previous risk assessment) RESPONSE Genus Tropilaelaps (Acari: Laelapidae) Specific species: Tropilaelaps clareae and Tropilaelaps mercedesae N/A Yes - several COMMENT Although Tropilaelaps clareae and Tropilaelaps mercedesae are separate species, there are enough similarities for them to be considered together in this PRA. They have only recently been identified as separate organisms (Anderson & Morgan, 2007) previously both being assumed to be T. clareae. Molecular and morphological studies (Anderson & Morgan, 2007) differentiated four distinct Tropilaelaps species, but only T. clareae and T. mercedesae use Western honey bees as hosts and are thus of relevance to this risk assessment (see Stage 1., Comment 8, and Stage 2. Comment 10, be). Earlier risk assessments for another exotic bee pest, Aethina tumida (the Small hive beetle) exist for the UK, the latest being from 2010 (Anderson et al., 2010). Additionally a non native species risk assessment was recently completed for the Asian hornet (Vespa velutina) (Marris et al., 2011). Aspects of both these have relevance to the assessment of risk for Tropilaelaps spp. In addition three import risk analyses have been carried out by Biosecurity New Zealand, the Biosecurity Authority of the Ministry of Agriculture and Forestry, and a USDA APHIS (Animal and Plant Health Inspection Service) pest risk assessment has been carried out on bees imported from Australia to the USA. Each of these look at the potential association of Tropilaelaps spp. with trade (APHIS, 2002; MAF Biosecurity, 2002; MAF Biosecurity, 2003; MAF Biosecurity, 2004). 2

3 4. If there is an earlier risk assessment is it still entirely valid, or only partly valid? 5. Where is the organism native? Partially valid in each case. SE Asia The earlier risk assessments are only partially valid as the focus of the earlier UK risk assessments is on other exotic pests and the focus of the import risk analyses on Tropilaelaps spp. is on potential pathways only. 6. What is the global distribution of the organism (excluding Great Britain)? 7. What is the distribution of the organism in Great Britain? See Appendix 1: Tables A-C Not present Figure 1. Map (courtesy of Dominic Eyre, Fera) shows distribution records (as of 2010) of T. clareae sensu stricto and T. mercedesae. Table A shows the recorded distribution of T. clareae prior to the work which demonstrated that there are actually two species which parasitise A. mellifera: T. clareae and T. mercedesae. Tables B and C show the known distribution of T. clareae and T. mercedesae foling the work of Anderson and Morgan (2007). Specimens from some regions where T. clareae has been reported (Table A) have not yet been tested and it is therefore unclear which species is present, although T. mercedesae does seem to be the more widespread of the two. 8. Is the organism Yes. Tropilaelaps mites are ectoparasites of honey bee brood. Molecular research and morphology have 3

4 known to be invasive (i.e. to threaten organisms, habitats or ecosystems) anywhere in the world? Stage 2. Screening Questions 9. Who requested this risk assessment? 10. What is the reason for performing the risk assessment? To examine the relative threats of Tropilaelaps species to the Western honey bee - Apis mellifera L. For this reason the risk assessment will focus on species known to parasitise A. mellifera. i.e. T. clarae and T. mercedeseae. revealed four species: T. clareae, T. koenigerum, T. mercedesae and T. thaii (Anderson & Morgan, 2007). Primary hosts are Apis dorsata and / or Apis laboriosa, the giant honey bees of Asia (Anderson & Morgan, 2007). However, T. clareae and T. mercedeseae are known to have expanded their host range and also parasitise Apis mellifera, the Western honey bee, which has been introduced in Asia. The work by Anderson and Morgan (2007) in identifying the different Tropilaelaps species suggests that, in many areas of mainland Asia, mite populations that were believed to be T. clareae are actually T. mercedesae. Prior to the splitting of the species, T. clareae had been reported to have spread beyond the geographical range of its primary host to Iran, Afghanistan, Kenya, South Korea and the Western Pacific island of New Guinea, and in many cases caused persistent damage to Apis mellifera (Anderson & Morgan, 2007). Without further molecular work it is unclear at present whether these reports are actually of T. clareae, or the apparently more widespread T. mercedesae (see Appendix 1). This risk assessment forms part of the Fera led bee health project PH0506: Control and risk management of honey bee pests and diseases. Table 1. Honey bee hosts utilised by different Tropilaelaps species Key + - known host; - not used as a host species Species A. dorsata A. laboriosa A. mellifera A. cerana A. florea T. clareae host host host host host T. koenigerum host host host host T. thaii host T. mercedesae host host host 4

5 11. Does the organism have intrinsic attributes that indicate that it could be invasive, i.e. threaten species, habitats or ecosystems? 12. Does the organism occur outside effective containment in GB? 13. Is the organism widely distributed in GB? 14. Does at least one species (for herbivores, predators and parasites) or suitable habitat vital for the survival, development and multiplication of the organism occur in GB, in the open, in protected conditions or both? 15. Does the organism require another species for critical Yes see section 8. No No Yes No evidence for such but some uncertainty Apis mellifera, the Western honey bee. This is the only managed honey bee in GB. There are, however, several hundred bee species in GB. Association of Tropilaelaps is not known with any of these other species, but feral colonies of A. mellifera are known to be present in a variety of areas, as well as the managed colonies (Thompson et al., 2010). Tropilaelaps would be a potential threat both to beekeeping and feral honey bees in Great Britain. Some Tropilaelaps population distributions are difficult to explain purely from the distribution and movement of known bee hosts and there has been some speculation regarding Tropilaelaps using an intermediate host species to enable their spread. There is a much quoted record from 1961 (Delfinado & 5

6 stages in its life cycle such as growth (e.g. root symbionts), reproduction (e.g. pollinators; egg incubators), spread (e.g. seed dispersers) and transmission, (e.g. vectors)? Baker) of Tropilaelaps mites being taken from field rats nesting near beehives in the Philippines. There is no further detail available on this record and, given that Tropilaelaps is believed to be unable to survive on adult bees, the mites are very un to have been feeding on the rats, but may have been present as hitchhikers on rats that had come into close contact with the honey bee colonies. As with their presence on adult honey bees, mites hitchhiking on rats, or any other organism, are un to survive for long periods. 16. Is the other critical species identified in question 15 (or a similar species that may provide a similar function) present in GB or to be introduced? If in doubt, then a separate assessment of the probability of introduction of this species may be needed. 17. Does the known geographical distribution of the organism include ecoclimatic zones comparable with N/A Yes / possible Although primarily known from tropical and sub-tropical locations, Tropilaelaps has been found in more temperate areas in Afghanistan, Nepal and China (See Annex 1). Figure 2 maps comparative climate classifications across the world, including GB and those parts of Asia where relevant Tropilaelaps species are present. Figure 3 is a CLIMEX map, constructed to illustrate all areas that are climatically suitable for Tropilaelaps based on known geographical distribution. 6

7 those of GB or sufficiently similar for the organism to survive and thrive? Although these illustrate that the geographical distribution of the organism includes ecoclimatic zones comparable with some areas of GB, it is important to note that climatic conditions may not in fact exert a direct influence on Tropilaelaps mites: Mites are almost exclusively confined to infested colonies (only spreading naturally during brief transport on adult bees), the temperature of which is maintained by the bees themselves (Simpson, 1961). Even when ambient temperatures are be freezing, honey bees maintain the broodnest at a steady temperature between C, as long as it contains brood (Southwick, 1982; 1991). However, the limiting factor to Tropilaelaps survival (presence of year round honey bee brood) is completely dependent on the breeding biology of the bees which is, in turn, affected by climate - so the influence of climate of honey bee hosts breeding behaviour will exert an indirect influence on the ability of Tropilaelaps to survive and thrive. What is important, therefore, is that conditions in GB are such that this can occur and Tropilaelaps is then able to survive and thrive on its honey bee host. 7

8 Figure 2. World map of Köppen-Geiger climate classification Figure 3. CLIMEX map (courtesy of Dominic Eyre, Fera) ecoclimatic indices for Tropilaelaps world wide (i.e. all areas that are climatically suitable for honey bee infestation with Tropilaelaps) 18. Could the organism establish under protected conditions (e.g. glasshouses, aquaculture facilities, terraria, zoological gardens) in GB? Probably In South Korea T. clareae sensu lato is reported to overwinter in honey bee colonies in greenhouses (Woo et al., 1995). This suggests that Tropilaelaps mites could establish under protected conditions, however, protected conditions are not relevant to beekeeping practices in GB, which are outdoor based. 8

9 19. Has the organism entered and established viable (reproducing) populations in new areas outside its original range, either as a direct or indirect result of man s activities? Yes Molecular work by Anderson and Morgan (2007) confirmed a report that T. clareae (now identified as T. mercedesae) was introduced to New Guinea by humans importing A. mellifera from Java, as the haplotype of T. mercedesae found in New Guinea matched that present in Java. Spread of Tropilaelaps spp. to other areas beyond the range of their primary host (see section 8) is also believed to be due to human movement of A. mellifera. 20. Can the organism spread rapidly by natural means or by human assistance? 21. Could the organism as such, or acting as a vector, cause economic, environmental or social harm in GB? Yes Yes Tropilaelaps mites are mobile and can readily move between bees and within the hive. However, movement between colonies depends on transport on adult bees through the natural processes of drifting, robbing, and swarming - Spread by natural means is therefore to be s, possibly over years. Spread by human means could be rapid, through the distribution of infested combs and bees through beekeeping management and movement of colonies (e.g. for pollination services). The National Bee Unit s (NBU) annual Husbandry Survey suggest that of the registered beekeepers surveyed in England and Wales, 7% move their colonies for e.g. honey production (Ben Jones, NBU, pers. comm.). Observations in Afghanistan in the early 1980 s suggest that 90% of the colonies of A. mellifera were lost to ectoparasites and that Tropilaelaps spp. played a significant part in this loss (Wokye, 1984a). Although its presence was limited to areas warm enough for brood to be reared all year round, this suggests that damage could occur in Great Britain in areas where brood is continuously present. In Asia, Tropilaelaps mites have been documented causing serious economic losses, with the loss of 30-70% of A. mellifera colonies in some parts of Korea being attributed to Tropilaelaps clareae (Woo & Lee, 1997). Recently T. mercedesae from China was shown to be associated with deformed wing virus (DWV) (Forsgren et al., 2009; Dainat et al., 2009). Previously known to be associated with Varroa destructor, DWV infection on its own rarely causes visible symptoms, or any apparent negative impact on host fitness, however transmission by V. destructor to developing pupae seems to select a more pathogenic strain and can cause pupal death and adult bees emerging with deformed wings, a bloated shortened abdomen and discolouration. These bees are not viable and die soon after emergence, thus contributing to the collapse of the honey bee colony (Miranda and Genersch, 2010; Martin et al., 2012). This link with Tropilaelaps is therefore an additional concern. 9

10 SECTION B Detailed assessment PROBABILITY OF ENTRY Important instructions: Entry is the introduction of an organism into GB. Not to be confused with spread, the movement of an organism within GB. For organisms which are already present in GB, only complete the entry section for current active pathways of entry or if relevant potential future pathways. The entry section need not be completed for organisms which have entered in the past and have no current pathways of entry. Note rating response and confidence is lighted in bold, the alternative responses being left in the text to put this in context. QUESTION RESPONSE CONFIDENCE COMMENT 1.1. How many active pathways are relevant to the potential entry of this organism? (If there are no active pathways or potential future pathways respond N/A and move to the Establishment section) 1.2. List relevant pathways through which the organism could enter. Where possible give detail about the specific origins and end points very few few moderate number many very many 1. Importation of colonies (i.e. adult bees with associated brood combs). very Five Pathways. Listed in order of level of estimated risk: 1. Importation of Apis mellifera (A. m.) colonies; 2. Importation live adult A. m. bees; 3. Movement on beekeeping equipment; 4. Movement with honey bee swarms (A. m. & other species) or other organisms; 5. Trade in hive products. For the purposes of this assessment potential pathways from both third countries and the EU will be considered. 10

11 of the pathways. For each pathway answer questions 1.3 to 1.10 (copy and paste additional rows at the end of this section as necessary). 2. Importation of packaged bees, queens and attendant workers (i.e. live, adult, queen honey bees, worker bees and drones without associated brood combs). For the purposes of this assessment potential pathways from both third countries and the EU will be considered. 3. Movement on beekeeping clothing / equipment. 4. Movement with honey bee swarms or othe organisms - either spreading naturally or i association with freight containers an transport vehicles. 5. Trade in hive products specifically beeswax in form of honeycomb and any other wax products and comb honey. For the purposes of this assessment potential pathways from both third countries and the EU will be considered. For the purposes of this assessment potential pathways from both third countries and the EU will be considered. For the purposes of this assessment potential pathways from both third countries and the EU will be considered. Pathway name: 1. Importation with honey bee colonies. QUESTION RESPONSE CONFIDENCE COMMENT 1.3. Is entry along this pathway intentional (e.g. the organism is imported for trade) or accidental (the organism is a contaminant of imported goods)? intentional accidental very It is legal to import bees in the foling live groups, although additional constraints on origin are imposed in some cases: (i) As colonies these consignments contain all life stages of a hive, i.e. a queen, adult workers, drones and brood; (ii) As packaged adults these consignments contain adults only; 11

12 (If intentional, only answer questions 4, 9, 10, 11) 1.4. How is it that large numbers of the organism will travel along this pathway from the point(s) of origin over the course of one year? Subnote: In your comment discuss how the organism is to get onto the pathway in the first place. very un un very very (iii) As queens and attendant workers these consignments each contain a queen and approx. 5-6 attendant workers. For the purposes of this risk assessment, Pathway 1. considers risks associated with importation of nucleus colonies i.e. adult bees and honey bee brood Group (i) above. Tropilaelaps entry would be accidental, through association with trade in live bees. Legal trade from third countries is limited to bees themselves and not associated brood. Volume of illegal trade from third countries unknown Note: there is anecdotal evidence that brood combs may be imported into UK for human consumption (in British Asian communities) drone brood for food can be traded for sums of money (Mike Brown NBU, pers.comm.). Legal trade in honey bee colonies from the EU is permitted, but with restrictions (see 1.7). Generally colonies are traded as small nucleus colonies, but larger colonies may be traded e.g. for pollination purposes (NBU, pers.comm.). The level of trade in nucleus colonies is not (Table 2.) and trade in larger colonies (not presented) is even er (NBU, pers. comm.). Should Tropilaelaps be present in the EU, large numbers of mites on the pathway are un as these would be noticed in consignments. However, it is important to note that the level of illicit trade entering the UK is unknown and by its nature not monitored (NBU, pers. comm.). Table 2: Volume of trade in nucleus honey bee colonies from the EU - imported into England/Wales in 2011 (Information from BeeBase, N.B. BeeBase is the NBU s online database. Country of Batched no. of nucleus colonies origin Czech Republic 40 Ireland 15 Italy 300 Poland 50 Total

13 1.5. How is the organism to survive during passage along the pathway (excluding management practices that would kill the organism)? Subnote: In your comment consider whether the organism could multiply along the pathway How is the organism to survive existing management practices during passage along the pathway? 1.7. How is the organism to enter GB undetected? very un un very very un un very very un un very very very very Providing that brood is present the survival of Tropilaelaps is if conditions and duration of transit al honey bee brood to survive then mites will also survive. A total transit time from point of origin to introduction into a U.K. colony of <5 days would not be unusual (Mike Brown NBU, pers. comm.). Reproduction and multiplication would not be impossible, but are considered very un during short transit required for sake of colony health. There are no treatments made to the commodity that are to affect the ability of Tropilaelaps to survive. Trade from third countries: Legal trade is limited to bees themselves and not associated brood. However it is important to note that the level of illicit trade entering the UK is unknown and by its nature not monitored (NBU, pers. comm.). Imports from the EU: Legal consignments of honey bees from other EU member states must be accompanied by an original health certificate (Annex E part 2, Council Directive 92/65/EEC) the electronic paperwork of which is held on the TRACE system. Importers must also give 24 hours written notice to the Animal Health Office responsible for the region where their consignment is destined to arrive. This letter, copied to the NBU gives details of the planned date and arrival time and details of the final destination. NBU inspectors have the power to check the paperwork and have a requirement to look at the paperwork of 50% of consignments. 30% of these must be subject to physical checks this is an increase in the level of vigilance (from 10% physical checks (see BH2 of Fera Plant & Bee Health Business Plan 2012/13)). However there is no border inspection 13

14 point (BIP) for the checks of EU honey bee imports i.e. BIPs only check paperwork and lack facilities/expertise to maintain and screen live bees. The checks may not be at the point of entry at all, but at the final destination, when imported bees have already been introduced into an apiary. The physical checks may therefore involve checking an imported nucleus or full sized colony for pests and diseases and possibly checking the colonies into which imported queens have been introduced (Brown, M., 2006a; Bee Health Policy, 2009; NBU, 2010). There is additional uncertainty over the detection of Tropilaelaps due to the possibility of illicit trade entering the UK without any documentation and no notification of the authorities. Volume of this trade is unknown, but is to be larger from the EU than third countries due to the ease of transport. Note: Should Tropilaelaps spp. be confirmed as present in an EU Member State, EC legislation doesn t permit the UK to ban imports. However, imported honey bees must come from an area of at least 100km radius which is not subject to any restrictions associated with suspicion or confirmed occurrence of Tropilaelaps and they and the packaging must have undergone a detailed examination to ensure no life stage of the pest is present (Bee Health Policy, 2009; NBU, 2010) How is the organism to arrive during the months of the year most appropriate for very un un In summary: (i) likelihood of detection on legal EU imports is only moderate, as not everything is physically checked; (ii) likelihood of detection on illegal EU imports zero; (iii) likelihood of detection in illegal third country imports = zero. Current legislation limits the chance of the pest entering undetected, but does not rule it out. The main areas of concern are that not all consignments are physically checked in the UK and that those checks which are made may be done at the final destination of the consignment (i.e. when bees have already been introduced into a hive, and not the point of entry. Honey bee imports typically occur between April and September, regardless of whether the imports are of EU or third country origin (NBU, pers. comm.). These six months cover the key beekeeping months of the year in 14

15 establishment? 1.9. How is the organism to be able to transfer from the pathway to a suitable habitat or host? Estimate the overall likelihood of entry into GB based on this pathway? very very un un very very un un very very very very the UK. These dates are based on imports that are notified to the NBU directly or through TRACES, but even unofficial imports are un during the UK winter season as spring / summer would be when conditions are appropriate for bee establishment. If bees can establish successfully, then Tropilaelaps will also be able to. Being transported with honey bees and associated brood, Tropilaelaps would enter the PRA area already associated with suitable hosts. Honey bees and colonies imported from the EU may be introduced to new colonies or established in their final homes before checks are made on the health of the bees and not all imports are officially checked (see 1.7). Tropilalelaps mites could enter the risk assessment area if brought in accidentally with infested brood from EU origin. However, levels of imports from this source are very and Tropilaelaps is currently believed to be absent from the EU. They may also enter via illicit trade from third countries. Levels of this trade are unknown. Pathway name - 2. Importation of packaged bees, queens and attendant workers QUESTION RESPONSE CONFIDENCE COMMENT 1.3. Is entry along this pathway intentional (e.g. the organism is imported for trade) or accidental (the organism is a contaminant of imported goods)? (If intentional, only answer questions 4, 9, 10, 11) intentional accidental very It is legal to import bees in the foling live groups although additional constraints on origin are imposed in some cases: (i) As colonies these consignments contain all life stages of a hive, i.e. a queen, adult workers, drones and brood; (ii) As packaged adults these consignments contain adults only; (iii) As queens and attendant workers these consignments each contain a queen and approx. 5-6 attendant workers. For the purposes of this risk assessment, Pathway 2. considers risks of importation of adult bees (workers, queens and drones) only Groups (ii) 15

16 and (iii) above How is it that large numbers of the organism will travel along this pathway from the point(s) of origin over the course of one year? Subnote: In your comment discuss how the organism is to get onto the pathway in the first place. very un un very very Tropilaelaps entry would be accidental, through association with trade in live bees. Large numbers of mites are un as these would be noticed in consignments. However, less heavy infestations are much more to go un-noticed. Note: it only takes a very few gravid female mites to ultimate cause an incursion. Legal trade volumes from both third countries and the EU are documented, but it is important to note that the level of illicit trade entering the UK is unknown and by its nature not monitored (NBU, pers. comm.). Volume of trade from third countries: In 2011, a total of 1762 honey bee queens were legally imported into England and Wales from third countries: New Zealand 1242; Australia 420; Argentina (Information from BeeBase, 2012). Tropilaelaps mites are not known to be present in any of these countries. Volume of trade from the EU: The volume of legal trade of honey bee consignments of any type that contains adult bees is. Annual figures for England and Wales in 2011 are provided in Table 3. Table 3. Volume of trade in honey bees: Queens imported from the EU into England/Wales in 2011 (Information from BeeBase, 2010)). Country of origin Batched no. of queens Cyprus 363 Czech Republic 165 Denmark 185 France 100 Germany 139 Greece 2800 Italy 50 Slovenia 262 Total How is the organism to very un The likelihood of survival of Tropilaelaps during transport of adult bees 16

17 survive during passage along the pathway (excluding management practices that would kill the organism)? Subnote: In your comment consider whether the organism could multiply along the pathway. un very very would be dependent on the length of time taken to transport the bees and length of time before they were introduced to a colony where bee brood is present. Survival on adults hosts: Tropilaelaps mites do not survive for long periods of time away from the food source i.e. bee brood. They are unable to feed on adult bees as their mouthparts are unable to pierce the body wall membrane of the bees. This ers the risk of this pest being associated with the importation of live bees, compared to the risk of Varroa destructor. The exact length of time Tropilaelaps mites can survive without the presence of brood is not entirely clear. Woyke (1984) stated that without food adult T. clareae could survive for two days, but no mites were found surviving more than 60 hours. Wilde (2000) quoted in the OIE Terrestrial Manual (2008) states that survival could be as much as 5-10 days. (These intervals contrast markedly to those for V. destructor, which is able to survive for several months on adult bees (Woyke, 1987a; Woyke et al., 2004). If Tropilaelaps mites really cannot survive more than 60 hours without brood it is un that they will survive passage on adult bees, but if mites can actually survive longer (as emerging research may confirm) this may be possible. Timing introduction to destination colony: Given the biology of Tropilaelaps, for quarantine purposes Article of the OIE Terrestrial Animal health Code (2011) recommends bees to be held in isolation from brood and bees for at least 7 days. However, the OIE have recently suggested increasing this isolation period to 21 days (OIE, 2012). The work (data) on which this is based is not currently available, but demonstrate survival on adult bees for more than 9 days. Survival at er temperatures has not been tested and therefore the even longer suggested period of isolation is to al a safety margin (Jeff Pettis, pers. comm.). While it is in the interests of the OIE to quarantine imported adults for an extended period of time, it is in the (conflicting) interests of the beekeeper to introduce imported bees into his/her apiary as soon as possible after receipt to maximise survival chances (Mike Brown NBU, pers. comm.) for any quarantine procedure to be effective it requires rigorous implementation by importers. Reproduction is dependent on the presence of brood and therefore impossible 17

18 1.6. How is the organism to survive existing management practices during passage along the pathway? 1.7. How is the organism to enter GB undetected? very un un very very un un from third countries from the EU very very very with this pathway. There are no treatments made to the commodity that are to affect the ability of Tropilaelaps to survive. Note that the authoritative legal position for the importation of bees into the UK can be found in the appropriate national legislation which is available at: and the European Commission legislation may be found at: It is also summarised in the NBU Standard Operating Procedure (SOP NBU/084) (Brown, 2006b). Third country imports: Honey bees may be imported into the EU from third countries provided that the three notifiable pests of bees in the EU, including Tropilaelaps spp., are confirmed as notifiable throughout the exporting country. Only Argentina, Australia, New Zealand and the US State of Hawaii currently meet these requirements and none of them are known to have Tropilaelaps mites present. (NB. But Hawaii s special derogation has recently been suspended since confirmation of SHB). Imports of honey bees from third countries are further restricted to consignments of queens and no more than 20 attendant workers, the exception to this being for New Zealand. Packaged honey bees (only not colonies) may be imported from New Zealand under a derogation of the Commission Decision 2006/855/EC. To import honey bees from other third countries, checks have to be made that they are able to comply with the requirements of the EC health certificate. Eligible third countries include the foling which are known to have Tropilaelaps spp.: China, India, Kenya and Thailand (Bee Health Policy, 2009; see Part I Annex II Regulation EU no. 206/210)). Imports from these countries are equally restricted to queen bees and no more than 20 attendant workers. All honey bees imported directly into England from a third country must enter through one of three designated Border Inspection 18

19 Posts (BIPs) Heathrow, Gatwick or Manchester airports where they are inspected by Veterinary Officers. As well as being accompanied by an appropriate health certificate the import should be notified in advance via the TRACES (Trade Control and Expert System) (See Brown, 2006b for more information on TRACES) and the NBU should also be notified of the import. All third country imports should be examined (Bee Health Policy, 2009; NBU, 2010). Upon receipt of queen honey bees from a third country the queens must be transferred to a new queen cage before they are introduced to any local colonies. The queen cages, attendant worker bees and other material accompanying queen bees from a third country should be sent to the NBU within 5 days for examination for exotic pests. According to legislation, queen honey bees from third countries must come from a breeding apiary which is supervised and controlled by the competent authority and the hives must have been inspected immediately prior to dispatch and show no clinical signs or suspicions of pests affecting bees. In addition if Tropilaelaps mites are known to be present in the exporting country imported honey bees must come from an area of at least 100km radius where this pest is absent. They and the packaging must have undergone a detailed examination to ensure that no life stage of the pest is present. The packaging material and cages and all accompanying products should be new and all precautions should be taken that they have not been in contact with infested bees (Bee Health Policy, 2009). NB. Although certification of health status and national pest surveillance are required, this requirement is not fully policed at country of origin (Mike Brown NBU, pers.comm.). The legislative framework for the control of honey bees imported to the EU from third countries is comprehensive. However, it is not always foled to the letter its effectiveness requires rigorous implementation by all stakeholders (exporters, importers, BIPs, beekeepers). The NBU has of occasions when the legal requirements have not been adhered to; for example queen bees imported from Australia without the packaging being sent to the NBU for examination; at least twice 19

20 A. mellifera imports from USA Georgia have been intercepted (Mike Brown NBU, pers. comm.). This is a concern, for the control of all bee pests, for example, the interception of the exotic pest Small hive beetle in Portugal was made in the packaging accompanying a third country import. There is also a concern that the queen honey bees themselves are not physically examined in the UK before being introduced to local colonies. This is because targeted methods of pest and disease screening in the laboratory are, necessarily, destructive. However the likelihood of Tropilaelaps spp. being associated with queen bees is. Imports from the EU: Consignments of honey bees from other EU member states must be accompanied by an original health certificate (Annex E part 2, Council Directive 92/65/EEC) the electronic paperwork of which is held on the TRACE system. Importers must also give 24 hours written notice to the Animal Health Office responsible for the region where their consignment is destined to arrive. This letter, copied to the NBU gives details of the planned date and arrival time and details of the final destination. NBU inspectors have the power to check the paperwork and have a requirement to look at the paperwork of 50% of consignments. 30% of these must be subject to physical checks this is an increase in the level of vigilance (from 10% physical checks (see BH2 of Fera Plant & Bee Health Business Plan 2012/13)). However there is no border inspection point (BIP) for the checks of EU honey bee imports i.e. BIPs only check paperwork and lack facilities/expertise to maintain and screen live bees. The checks may not be at the point of entry at all, but at the final destination, when imported bees have already been introduced into an apiary. The physical checks may therefore involve checking an imported nucleus or full sized colony for pests and diseases and possibly checking the colonies into which imported queens have been introduced (Brown, M., 2006a; Bee Health Policy, 2009; NBU, 2010). Should Tropilaelaps spp. be confirmed as present in an EU Member State, EC legislation doesn t permit the UK to ban imports. However, imported 20

21 honey bees must come from an area of at least 100km radius which is not subject to any restrictions associated with suspicion or confirmed occurrence of Tropilaelaps and they and the packaging must have undergone a detailed examination to ensure no life stage of the pest is present (Bee Health Policy, 2009; NBU, 2010) How is the organism to arrive during the months of the year most appropriate for establishment? 1.9. How is the organism to be able to transfer from the pathway to a suitable habitat or host? very un un very un from third countries very from the EU very very Current legislation limits the chance of the pest entering undetected, but does not rule it out. The main areas of concern are that not all consignments are physically checked in the UK and that those checks which are made may be done at the final destination of the consignment, after bees have been introduced into a hive, and not the point of entry. There is additional uncertainty over the detection of Tropilaelaps due to the possibility of illicit trade entering the UK without any documentation and no notification of the authorities. Volume of this trade is unknown, but is to be larger from the EU than third countries due to the ease of transport. It is believed that a proportion of EU imports may in fact originate from outside the EU. i.e. from third countries which enter the UK illegally via the EU. Honey bee imports typically occur between April and September, regardless of whether the imports are of EU or third country origin (NBU, pers. comm.). These six months cover the key beekeeping months of the year in the UK. These dates are based on imports that are notified to the NBU directly or through TRACES, but even unofficial imports are un during the UK winter season as spring / summer would be when conditions are appropriate for bee establishment. If bees can establish successfully, then Tropilaelaps will also be able to. Tropilaelaps would enter the PRA area associated with adult hosts however until these are transferred to a colony with bee brood already present the mite cannot feed or breed. The success of this transfer would be dependant on the length of time from the removal of the bees and mites from the colony of origin to a colony in the PRA area. If the survival of the mites is at the er end of the range reported this transfer would be un. The likelihood increases with the length of survival of the Tropilaelaps mites and 21

22 1.10. Estimate the overall likelihood of entry into GB based on this pathway? very un un very very the length of time that imports are kept isolated from destination colony (see 1.5 above: Survival on adults hosts and Timing introduction to destination colony). Honey bees imported from the EU may be introduced to new colonies or established in their final homes before checks are made on the health of the bees and not all imports are officially checked (see 1.7), whereas legal imports from third countries should not be directly introduced to new colonies (see 1.7). NB. The likelihood that an imported queen bee is directly introduced into a colony without inspection/isolation relates to the behaviours and degree of legal responsibility shown by the beekeeper for example, the NBU knows of the illegal introduction of several 100 queens imported from Argentina (Mike Brown, pers. comm.). The likelihood of survival of Tropilaelaps on adult bees imported legally or illegally from third countries is. Survival may be more if the mites establish in the EU and the trade originates here, but the overall risk is still quite. However, likelihood of entry via this pathway is ly dependent on level and consequences of illegal import. Hence overall moderate risk. Pathway name - 3. Movement on beekeeping clothing / equipment - such as PPE (Personal Protective Equipment) e.g. veils and suits, footwear, gloves; wooden hives, plastic hives, hive tools, smoker etc. Also included may be vehicles / machinery used by beekeepers and then brought into the UK. Any of these may be potentially contaminated. QUESTION RESPONSE CONFIDENCE COMMENT 1.3. Is entry along this pathway intentional (e.g. the organism is imported for trade) or accidental (the organism is a contaminant of imported goods)? intentional accidental very The pathway in this case involves the accidental movement of Tropilaelaps in association with beekeeping clothing or equipment, including used frames, which has come into contact with the pest and not been checked or cleaned adequately. (If intentional, only answer questions 4, 9, 10, 11) 22

23 1.4. How is it that large numbers of the organism will travel along this pathway from the point(s) of origin over the course of one year? Subnote: In your comment discuss how the organism is to get onto the pathway in the first place How is the organism to survive during passage along the pathway (excluding management practices that would kill the organism)? Subnote: In your comment consider whether the organism could multiply along the pathway. very un un very very un un very very very Numbers are to be very as large numbers would be detected. Any beekeeping equipment used in an area where Tropilaelaps spp. are known to be present could potentially be contaminated with the pest. The greatest risk of association is with hives themselves, which if not cleaned properly could harbour bee brood and enable the survival of the mites for longer periods than without food available. It is thought very un that wooden hives would be entering the UK from third countries which have Tropilaelaps (NBU, pers. comm.) due to the practicalities of transporting such large items by air. However, if shipped by sea in containers and any live brood debris remains, then risks of transporting () numbers of mites increases. For clothing the greatest risk of association is probably that of an adult mite, or infested debris from cleaning hives, trapped within the folds of the clothing (NBU, pers comm.). Overall, the likelihood of association between mites and equipment is believed to be, but er if the pest is present in the EU and equipment enters GB from here rather than a third country. Tropilaelaps mites are exclusively parasitic of honey bee larvae. However, there is much uncertainty regarding how long they are able to survive away from their larval hosts (see Pathway 2., Comment 1.5). If this survival is only a few days it would be impossible for them to survive long during passage along this pathway. However, if, as suggested by OIE recommendations this is longer survival would be more How is the organism to survive existing management practices during passage along the pathway? very un un very very There are no existing management practices on this pathway. The OIE recommends that used beekeeping equipment should either come from a country or zone free from Tropilaelaps infestation or contain no live honey bees or brood and have been held away from contact with live honey bees for at least seven days prior to shipment or have been treated to ensure the destruction of 23

24 1.7. How is the organism to enter GB undetected? 1.8. How is the organism to arrive during the months of the year most appropriate for establishment? 1.9. How is the organism to be able to transfer from the pathway to a suitable habitat or host? Estimate the overall likelihood of entry into GB based on this pathway? very un un very very un un very very un un very very un un very very very very very Tropilaelaps spp. UK beekeepers should maintain clean equipment, fol recommended hive sterilisation procedures and regularly wash their bee suits. However, the implementation of these recommendations are not policed. There is no regulation on the movement of hive equipment or personal protective clothing into the UK, from third countries or the EU. No checks on such commodities are therefore made. Imports / movements could potentially occur at any time of year. Un The likelihood of live Tropilaelaps being imported on this pathway is and the possibility of transfer to a colony with bee brood remote, though not impossible. Un Overall, the likelihoods of live Tropilaelaps being associated with this pathway, or surviving import on this pathway, in or on any abiotic substrate (beekeeping equipment of any kind) listed, are. Pathway name - 4. Movement with honey bee swarms or other organisms - either spreading naturally or in association with freigh containers and transport vehicles. 24

25 QUESTION RESPONSE CONFIDENCE COMMENT 1.3. Is entry along this pathway intentional (e.g. the organism is imported for trade) or accidental (the organism is a contaminant of imported goods)? intentional accidental very Entry on this pathway would involve the accidental introduction of Tropilaelaps in association with a swarm of adult honey bees or being carried as a hitchhiker by another organism. (If intentional, only answer questions 4, 9, 10, 11) 1.4. How is it that large numbers of the organism will travel along this pathway from the point(s) of origin over the course of one year? Subnote: In your comment discuss how the organism is to get onto the pathway in the first place. very un un very very It is considered un that large numbers of the organism will travel along this pathway, but there is no information on this. The pathway is dependant Tropilaelaps spp. being carried as hitchhikers from source to the PRA area. A factsheet produced by the North Carolina State University (Tarpy, 2007) states that there have been records of African honey bees hitchhiking as swarms on ships; Apis florae (a known host for Tropilaelaps) has been found in South Africa on machinery imported from Korea (Mike Allsopp Plant Protection Research Institute, ARC South Africa., pers. comm.); bee swarms have also occasionally been picked up on ships arriving in the UK (NBU, pers. comm.). It is possible, therefore, that Tropilaelaps could be associated with bee hosts (various species, see Stage 1., Table 1., above) transported by freight, but it s survival would be entirely dependent on the length of time taken from source to brood in the PRA area. It has been observed in Thailand that newly founded colonies (up to 14 days old) of Apis dorsata (a natural host of at least 3 Tropilaelaps spp.) do not contain any infestation by Tropilaelaps. This is believed to be due to the broodlessness period during swarming events that interrupt the mites lifecycle. This period can be lengthy as migratory swarms can rest between stages of flight, 25

26 sometimes for one to three days without building any comb and can spend more than one month on their migration. In Asia it is therefore believed that infestation of newly settled colonies comes from infested colonies nearby not due to mites travelling with migratory swarms (Kavinseksan et al., 2003). Association with a swarm may therefore only be feasible if its origin was very close to GB (i.e. in mainland Europe close to the coast), and if this swarm very quickly came into contact with bees from a colony where brood was already present. However, the situation re. survival in swarms remains quite unclear. NB. Even if association with a swarm may be un, volume in global trade (any commodity) is huge; billions of standard containers are transported around world each year (e.g. ships from China have capacity to carry up to 9000 standard containers/ship/trip) this affects overall probability of pathway How is the organism to survive during passage along the pathway (excluding management practices that would kill the organism)? Subnote: In your comment consider whether the organism could multiply along the pathway. very un un very very There is a much quoted record from 1961 (Delfinado & Baker) of Tropilaelaps mites being taken from field rats nesting near beehives in the Philippines. There is no further detail available on this record and given that Tropilaelaps is unable to feed on adult bees the mites are very un to have been feeding on the rats, but have been present as hitchhikers on rats that had come into close contact with the honey bee colonies. As with their presence on adult honey bees, mites hitchhiking on rats, or any other organism, are un to survive for long periods. Due to the survival time of Tropilaelaps away from its food source, i.e. honey bee brood, the chances of survival if associated with a honey bee swarm or other organism on shipping freight would be very un. If associated with some other transport, for example road vehicle it is possible that the length of time for transport from source to the PRA area would be enough for Tropilaelaps survival, but again very un and un bees, 26

27 1.6. How is the organism to survive existing management practices during passage along the pathway? 1.7. How is the organism to enter GB undetected? 1.8. How is the organism to arrive during the months of the year most appropriate for establishment? 1.9. How is the organism to be able to transfer from the pathway to a suitable habitat or host? very un un very very un un very very un un very very un un very very very or other organisms, would stay associated with a road vehicle for a prolonged period of time. It is also very un that an infested migratory swarm would naturally enter GB from mainland Europe. - Multiplication on this pathway would be impossible. There are no existing management practices on this pathway. Freight containers and the vehicles transporting them are not checked for hitchhiking invertebrates as discrete as Tropilaelaps mites. Swarms of bees stowing away may be more easily detectable and have been destroyed in the past (Tarpy, 2007), but it would be impossible to detect and control the movement of organisms like rats. It would be impossible to detect Tropilaelaps in naturally migrating swarms or on road transport vehicles. NB. Even if association with a transported swarm may be un, volume in global trade (any commodity) is huge; billions of standard containers are transported around world each year (e.g. ships from China have capacity to carry up to 9000 standard containers/ship/trip) this affects overall probability of pathway. When bees are swarming in other areas of the EU (especially the most risky area of north western EU) it will also be the bee season in GB. Entry of a honey bee swarm (e.g. on freight) originating from a third country, could occur at any time of year (NB. Likelihood of Tropilaelaps surviving for a long period of time in freight is extremely ). Entry on another organism could also, potentially, be at any time of year. If Tropilaelaps were able to survive within the honey bee swarm, then in theory, if a swarm reaches GB within a time period that is short enough for mites to survive, then the organism could transfer 27

28 1.10. Estimate the overall likelihood of entry into GB based on this pathway? very very un un very very very from the pathway into a suitable habitat. The length of time for which Tropilaelaps mites are able to survive away from their larval hosts is not clear, but is thought to be between two and nine days (see Pathway 2., Comment 1.5). Transfer to a suitable host would depend on the honey bee hosts entering an alternative colony that contains brood within the same timeframe. This is considered un. Transfer from another host, such as a rat, would be even more un, as they are much less to come into contact with a colony containing brood within a short time period after entering GB. Un Overall, the likelihood of live Tropilaelaps being associated with this pathway, or surviving import on this pathway, are. Likelihood of entry into an alternative host colony containing suitable brood is also very. Pathway name - 5. Trade in hive products specifically beeswax in form of honeycomb and any other wax products and comb honey. Honey bee semen, honey bee venom, honey packaged in jars, refined beeswax, propolis, royal jelly and pollen are excluded from this risk assessment due to the process of extraction and preparation and, in some cases, the end use of human consumption eliminating the risk of association with these commodities. QUESTION RESPONSE CONFIDENCE COMMENT 1.3. Is entry along this pathway intentional (e.g. the organism is imported for trade) or accidental (the organism is a contaminant of imported goods)? (If intentional, only answer questions 4, 9, 10, 11) intentional accidental very The Terrestrial Animal Health Code (OIE, 2011) contains recommendations for the importation of pollen, beeswax in the form of honeycomb, comb honey and propolis. Propolis and pollen are excluded from this risk assessment as it is believed that processes of extraction and preparation eliminate the risk with these commodities. The New Zealand Import Risk Analysis on honey bee hive products and used equipment (MAF Biosecurity, 28

29 1.4. How is it that large numbers of the organism will travel along this pathway from the point(s) of origin over the course of one year? Subnote: In your comment discuss how the organism is to get onto the pathway in the first place. very un un very very 2002) concluded that Tropilaelaps was very un to be introduced on honey bee hive products due to the lack of food source for the mites. In this risk assessment we will discuss the possibility of association with those products with the closest association to the honey bee brood, the food source for Tropilaelaps. - Entry along this pathway would be accidental association with these products. Unlike other exotic pests of the Western honey bee, Tropilaelaps mites (which are exclusively parasitic of honey bee larvae) are not attracted to or associated with hive products such as honey or beeswax etc. They are very un to get onto this pathway and very un to be associated with it in large numbers How is the organism to survive during passage along the pathway (excluding management practices that would kill the organism)? Subnote: In your comment consider whether the organism could multiply along the pathway. very un un very very Unlike other exotic pests of the Western honey bee, Tropilaelaps mites (which are exclusively parasitic of honey bee larvae) are not associated with hive products such as honey or beeswax etc, and are believed to be unable to survive on them for more than 2-4 days (Jeff Pettis, pers. comm.). It would be impossible for them to multiply along this pathway How is the organism to survive existing management practices during passage along the pathway? very un un very very The importation of unprocessed beeswax in the form of honeycomb (a product which contains both honey and beeswax) is completely banned from third countries (DEFRA, 2007). Illegal imports of honeycomb are not considered due to the difficulties with importing this product (NBU, pers. comm.). The import of this product is not banned from the EU but given the extremely likelihood of association with this product, it is not considered a risk from the EU. 29

30 1.7. How is the organism to enter GB undetected? very un un very very Beeswax for technical use must be refined or rendered before import from third countries and be accompanied by a commercial document. There is no definition of rendering for beeswax but OVS note 07/98 states that beeswax that has been melted and set in blocks would meet the requirements of Commission Regulation 829/2007 (2007) (DEFRA, 2007). Rendered beeswax has not been filtered for contaminants. Refined beeswax is filtered. Rendered beeswax is the crudest state of beeswax which may be legally imported into the UK from outside the EU. Large consignments of rendered beeswax are imported into the UK from China and Africa (Mike Brown NBU, pers. comm.). There are no restrictions on the UK import of wax products from within the EU and whether these would always have been rendered is unclear. However, there are no documented associations between Tropilaelaps mites and rendering plants. Third country imports: Council Directive 97/78/EC requires that all consignments of animal products from third countries imported into the European Community receive a documentary, identity and physical check under the responsibility of the Official Veterinary Surgeon (OVS) before being cleared for free circulation in the Community. The list of products that require veterinary checks is laid down in Commission Decision 2007/275 (DEFRA, 2009). Honey is classed as a Category II commodity which means that 100% of consignments have documentary and identity checks and physical checks are carried out on not less than 50% of consignments. Propolis is also checked as honey (DEFRA, 2009). Other apiculture products are classed as Category III, which means that 100% of consignments have documentary and identity checks. Physical checks are made on not less than 1% and not more than 10% of consignments (DEFRA, 2009). Apiculture products includes pollen. Commission regulation 829/2007 amended the by-products legislation to also require beeswax for technical use to 30

31 be checked on entry (DEFRA, 2009). Beeswax for technical use must be refined or rendered prior to importation. The importation of unprocessed beeswax in the form of honeycomb is completely banned by Commission regulation 829/2007 (DEFRA, 2007). EU imports: Products from other EU countries do not require checks (DEFRA, 2009) How is the organism to arrive during the months of the year most appropriate for establishment? 1.9. How is the organism to be able to transfer from the pathway to a suitable habitat or host? Estimate the overall likelihood of entry into GB based on this pathway? Estimate the overall likelihood of entry into GB based on all pathways (comment on the key issues that lead to very un un very very un un very very un un very very un un very very very Additional uncertainty lies in the unknown factor of illicit trade in regulated products and if such a trade exists. It is also unclear how thoroughly existing checks on legal imports are policed (Mike Brown NBU, pers. comm.). Potentially there is year round trade in honey and beeswax into the UK from countries where Tropilaelaps is known to be present (Eurostat, 2012: data on the imports of natural honey and rendered beeswax from third countries see Appendix 2, Table D). There is little information on what happens to the honey and beeswax commodities once they enter the UK. However, likelihood of transfer to a suitable host even in the un event that live mites were imported on the pathway is extremely. Very un Overall, the likelihood of live Tropilaelaps being associated with this pathway, or surviving import on this pathway, in or on any of the commodities listed, is extremely. Tropilaelaps mites are dependant on the availability of honey bee brood as a food source. Recent work does suggest the possibility of survival of mites on adult bees for longer than initially thought 31

32 this conclusion). very very (OIE, 2012). However, this survival has only been linked with the bees themselves and still for a limited time. For this reason pathways 3, 4 and 5 are considered least to facilitate entry as each involves a separation from this food source for a prolonged period of time. The likelihood of survival of Tropilaelaps on adult bees imported legally or illegally from third countries is small. Survival may be more if the mites establish in the EU and the trade originates here, but the overall risk is still un. Of most risk is the entry of Tropilaelaps mites brought in accidentally with infested brood from EU origin. However, levels of imports from this source are very and Tropilaelaps are currently believed to be absent from the EU. They may also enter via illicit trade from both the EU and third countries. Levels of this trade are unknown. Based on available information this pathway is considered. It is on this pathway of most risk that the overall likelihood of entry is based. 32

33 PROBABILITY OF ESTABLISHMENT Important instructions: For organisms which are already well established in GB, only complete questions 1.15 and 1.21 then move onto the spread section. QUESTION RESPONSE CONFIDENCE COMMENT How is it that the organism will be able to establish in GB based on the very similarity between climatic conditions in GB and the organism s current distribution? very un un very A recent study in China (Luo et al. 2011a) sampling Tropilaelaps mites from 72 locations in 25 provinces found all samples to be T. mercedesae. A fol up study on the prevalence of Tropilaelaps in China in colonies of A. mellifera found a infestation intensity in central, east, south and southwest China (Luo et al., 2011b). This confirms previous research showing prevalence of Tropilaelaps species in tropical and subtropical regions of Asia (Anderson & Morgan, 2007). However the study does indicate that Tropilaelaps spp. can survive further north in China than reported in a recent study on the suitability of the climate in Great Britain for the survival of Tropilaelaps (Eyre et al., unpublished), which used data from Yunnan province in south east China as being one of the coldest places where Tropilaelaps mercedesae had been reported. The mite was also found infesting A. mellifera in the colder areas of China (Xinjiang, Ningxia, Gansu, Hebei, Shanxi, Inner Mongolia and northeast China). Overwintered honey bee colonies in these areas have a period without brood in early spring and late winter (November February). There could be an explanation for the mites presence in that a proportion of beekeepers in China move colonies from south to north to exploit nectar fs after May fering and the intensity of infestation found was er in the southern regions than the temperate zone (Luo et al., 2011b). Further study on the distribution of Tropilaelaps is needed, but the ability of honey bees to overwinter with brood seems to be the major factor for establishment, rather than the effect of external temperature on the mite itself. There is data confirming that the climate within the hive itself is regulated by honey bee colonies. Where brood is present temperatures of C in the summer and 25 33

34 - 30 C in the winter are maintained in the middle of the brood area, regardless of outside temperature (-40 to +40 C). Without brood, temperatures are generally er, but temperatures in the centre of bee clusters are usually maintained at around 20 C, with the est recorded being 15 C (Simpson, 1961). This also suggests that the outside climate may not be the deciding factor for establishment of Tropilaelaps as they are insulated from the outside environment How is it that the organism will be able to establish in GB based on the similarity between other abiotic conditions in GB and the organism s current distribution? very un un very very Fig. 4: Map showing locations of the provinces in China. There is little information available on other abiotic factors which might affect the establishment of Tropilaelaps spp. in the UK. However, any abiotic factor that could affect the presence and amount of brood within the colonies is important to the establishment of a mite population. In the past this has been noted to be affected by a range of factors including colony size (Free & Percy, 1968), photoperiod (Kefuss, 1978), and food availability (Mattila & Otis, 2007) How is it that the organism will very un un In South Korea T. clareae sensu lato is reported to overwinter in honey bee colonies in greenhouses (Woo et al., 1995). This suggests that Tropilaelaps mites could 34

35 become established in protected conditions (in which the environment is artificially maintained, such as wildlife parks, glasshouses, aquaculture facilities, terraria, zoological gardens) in GB? very very establish under protected conditions, however, protected conditions are not relevant to beekeeping practices in GB, which are out-door based. Subnote: gardens are not considered protected conditions How widespread are habitats or species necessary for the survival, development and multiplication of the organism in GB? If the organism requires another species for critical stages in its life cycle then how is the organism to become associated with such species in GB? very isolated isolated widespread widespread ubiquitous NA very un un very very very In England and Wales there are in excess of 28,000 registered beekeepers who together manage around 130,000 colonies of A. mellifera (NBU, 2012), 80% of which are found in England, and it is estimated there may be many more (~ 40%) who are not registered on BeeBase, the National Bee Unit s online database (NBU, pers. comm.). Thousands more managed colonies are found in Scotland (est. 20,000; NBU, pers. comm.) and colonies of feral A. mellifera are also known to be present across GB (Thompson et al., 2010) How is it very un No known competitors. The parasitic mite V. destructor is present in most honey bee 35

36 that establishment will occur despite competition from existing species in GB? un very very colonies in the UK (NBU, pers comm.), but observations from China where both Varroa and T. mercedesae are present suggest that competition between the species is un to affect establishment. Luo et al. (2011a) report that of the apiaries they tested in China, 82.9% had both T. mecedesae and Varroa and that the infestation intensity of Tropilaelaps was significantly associated with the intensity of Varroa. They hypothesized that the effect on the colony of one mite infestation (and its potential associated viruses) ered the bees immune system and meant they were more susceptible to attack by other mites and diseases. Earlier work also suggests that a competitive situation does not occur as long as a colony is not severely affected by extremely mite populations and sufficient amounts of brood are available for both mite species (Rath et al., 1995). Tropilaelaps has a er reproductive rate than Varroa as it has a shorter life cycle. This is because they have a faster development time and a shorter phoretic phase (non-reproductive transport phase, time spent on the adult bees) between reproductive cycles. Consequently when both types of mite are present in the same colony Tropilaelaps populations build up far more rapidly than Varroa, by a factor of 25:1 in favour of Tropilaelaps (Burgett et al., 1983; CSL, 2005). Therefore if there are limited amounts of brood it may be more that Tropilaelaps could outcompete Varroa How is it that establishment will occur despite predators, parasites or pathogens already present in GB? very un un very very None known How is the organism to establish despite existing management practices in GB? very un un very Existing Surveillance for Tropilaelaps in the UK: The current Apiary Inspection Programme undertaken by the NBU for England and Wales includes an element of Exotic Pest Surveillance (EPS), specifically designed to monitor for the arrival of exotic threats including Tropilaelaps mites and the Small Hive Beetle. EPS focuses on at risk apiaries (ARAs), which are located at sites considered to be particularly 36

37 very vulnerable to exotic pest incursion. Search patterns and prioritisation for routine surveillance of ARAs for Tropilaelaps are coordinated by the Regional Bee Inspectors, each of whom has overall responsibility for one of the eight areas located across England and Wales. ARAs are identified by BeeBase and the GIS system, and include apiaries that satisfy one or more of the foling criteria: Apiaries within 5km of seaports Apiaries within 5km of airports, including military airfields Apiaries within 5km of freight depots Apiaries within 5km of container and cargo yards Apiaries owned by queen importers Fig. 5: Distribution of ARAs in England and Wales Beekeepers are strongly encouraged to monitor their hives for Tropilaelaps as part of their routine hive management. Throughout England and Wales debris samples or hive inserts can be collected and sent to the Bee Unit by either appointed Bee 37