small hive beetle infestation

Pictures

Picture	Title	Caption	Copyright
Title Adult Caption Small hive beetle (Aethina tumida); dorsal view of adult, museum set specimen. Florida, USA. Copyright ©Jeffrey W. Lotz/Florida Dept. of Agriculture & Consumer Services/Bugwood.org - CC BY 3.0 US	Adult	Small hive beetle (Aethina tumida); dorsal view of adult, museum set specimen. Florida, USA.	©Jeffrey W. Lotz/Florida Dept. of Agriculture & Consumer Services/Bugwood.org - CC BY 3.0 US
Title Adults on comb Caption Small hive beetle (Aethina tumida); adults on comb. USA. Copyright ©Jessica Lawrence/Eurofins Agroscience Services/Bugwood.org - CC BY 3.0 US	Adults on comb	Small hive beetle (Aethina tumida); adults on comb. USA.	©Jessica Lawrence/Eurofins Agroscience Services/Bugwood.org - CC BY 3.0 US
Title Larvae on comb Caption Small hive beetle, (Aethina tumida) larvae on a comb of honey; Moultrie, Georgia, United State. 01 September, 2004 Copyright ©James D. Ellis/University of Florida/Bugwood.org - CC BY 3.0 US	Larvae on comb	Small hive beetle, (Aethina tumida) larvae on a comb of honey; Moultrie, Georgia, United State. 01 September, 2004	©James D. Ellis/University of Florida/Bugwood.org - CC BY 3.0 US

Identity

Preferred Scientific Name

• small hive beetle infestation

Other Scientific Names

• Aethina tumida infestation

Pathogen/s

Overview

This datasheet is about small hive beetle infestation as defined by the World Organisation for Animal Health, or OIE (OIE, 2012), i.e. an infestation of bee colonies by the beetle Aethina tumida, which is a free-living predator and scavenger affecting populations of the honey bee, Apis mellifera. Bumble bee, Bombus terrestris, colonies can also be parasitized under experimental conditions, and infestation has also been reported in commercial B. impatiens colonies. Although infestation has not been observed in wild Bombus spp. populations they should be considered susceptible.

The beetles are native to Africa, but have been introduced to the USA, Canada, Mexico, Jamaica, Australia and Italy, and reported but not substantiated in Egypt (Thomas, 1998; OIE, 2013; FERA, 2010; Cuthbertson et al., 2013b; Mutinelli et al., 2014). They are considered to be a minor pest in Africa, but a major problem in areas where they have been introduced; heavy infestations may result in desertion of the hive. The fact that the adult beetles are able to fly several kilometres has resulted in the rapid spread of infestation (OIE, 2012).

A. tumida infestation is on the list of diseases notifiable to the OIE.

Host Animals

Hosts/Species Affected

A. tumida is considered to have secondary pest status in its native area of southern Africa, where it is a scavenger of weakened bee colonies. However, in areas where it has been introduced the reports are very different, and it causes significant damage to colonies (Delaplane, 1998), although weak colonies, along with those with a surplus of combs stored in them, are more attractive to bees. It is these factors that will encourage their rapid growth (Calderón et al., 2006).

As well as honey bees, bumble bee (Bombus terrestris) colonies can also be parasitized under experimental conditions; commercial B. impatiens colonies in North America have also been found to be infested (FERA, 2010). Although infestation has not been observed in wild Bombus spp. populations they should be considered susceptible (OIE, 2012).

Distribution

A. tumida is native to sub-Saharan Africa; it has been introduced to the USA, Canada, Mexico, Jamaica, Australia and Italy, and reported but not substantiated in Egypt (Thomas, 1998; OIE, 2013; FERA, 2010; Delaplane, 1998; Cuthbertson et al., 2013b; Mutinelli et al., 2014). The Distribution table contains records for all countries where it has been introduced, but in the native range only for those countries where records are readily available.

Distribution Table

The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Diagnosis

In sub-Saharan Africa, where A. tumida is native, it acts as a scavenger of weakened colonies. The beetles damage weak or stressed colonies, abandoned honeybee nests and stored bee products of the African subspecies of honey bees (Kokkinis, 2005). Much more severe signs of infestation have been observed in areas where the parasite has been introduced. For example, in Florida, considerable damage and colony loss has been reported and beetle larvae tunnel though combs, kill bee brood and ruin combs. Bees have been reported to abandon combs and entire colonies that have become infested in Florida (Delaplane, 1998).

Fermenting honey, causing a frothy mess in supers and honey houses, is a sign that beetles have been defecating in the honey. In Florida, it was reported that the fermenting honey smelt like rotting oranges (Delaplane, 1998).

Schafer et al. (2008) investigated a method for diagnosing A. tumida in field colonies of bees using corrugated plastic strips, designed to house the beetles while preventing access to bees. They reported an overall strip efficacy of 35.4±20.6 % and that numbers of A. tumida in the traps correlated with total numbers in the hives.

Bottom boards, such as those reported by Torto et al. (2010) in Kenya, can be used to monitor the occurrence and seasonal abundance of the beetle in honey bee colonies. Baited Langstroth hive bottom board trap captures indicated that the beetles were present throughout the year in small numbers, but were most abundant in the rainy season.

Ward et al. (2007) reported a DNA method for screening hive debris for A. tumida. The method uses real-time PCR alongside automated DNA extraction and was able to detect DNA from eggs, larvae and adult beetles from Africa, Australia and North America. The method was found to be reliable because extraction efficiency was consistent between hive debris samples.

Stedman (2006) provides further information on how to detect and identify A. tumida and distinguish them from similar-looking insects.

Disease Course

The growth of the beetle population is rapid, so while early signs of infestation may go unnoticed, the hive can suffer from high bee mortality (OIE, 2012). The symptoms in bee colonies infested with A. tumida include tunneling in combs and fermenting honey. In Florida, fermenting honey was reported to smell like rotting oranges (Delaplane, 1998) and fermentation is probably due to yeasts associated with the beetle such as Kodamaea ohmeri, which is predominant (Schafer et al., 2009).

Epidemiology

A. tumida is native to southern Africa, and has been introduced to the USA, Egypt (unconfirmed), Canada, Australia, Mexico, Jamaica and Italy (Thomas, 1998; OIE, 2013; FERA, 2010; Cuthbertson et al., 2013; Mutinelli et al., 2014). It is able to survive in cold climates anywhere that bees exist (FERA, 2010). The beetles are scavengers and parasites of honeybee colonies. The adult and larval beetles feed on honeybee larvae, pollen, honey and brood (OIE, 2013).

Under its native conditions of southern Africa, A. tumida requires 38-81 days to develop from egg to adult, and can produce 5 generations per year under suitable conditions (Delaplane, 1998; Cuthbertson et al., 2008).  The adults lay eggs in infested hives, usually in irregular masses in crevices or brood combs. The eggs hatch after 2-6 days and the larvae feed voraciously on brood comb, bee eggs, pollen and honey in the hive. Each female can produce about 1000 eggs in 4-6 months of life. The larvae take about 10-29 days to reach maturity, at which point they exit the hive and burrow in the soil around the hive entrance (OIE, 2013; Delaplane, 1998). Different soil conditions, such as moisture levels and temperature, will determine how successful completion of development is (Delaplane, 1998) and pupation may take 2-12 weeks (OIE, 2013).

Environmental conditions determine the life span of the adults, but on average they can live for at least 6 months, and when conditions are favourable, the female can lay new egg batches every 5-12 weeks (OIE, 2012). The adult beetles are able to fly up to 6-13 km from the nest site, aiding the rapid spread of infestation (OIE, 2012). The beetles may also be spread during the routine tasks carried out by apiarists (Delaplane, 1998). The beetles are able to survive for at least 2 weeks without food and 50 days on brood combs (OIE, 2012). Wandering larvae can survive fopr 48 days without food (Cuthbertson et al., 2008).

There is experimental evidence to suggest that A. tumida is a vector of the cause of American foul brood (AFB), Paenibacillus larvae. Larvae and adults of A. tumida were shown to become contaminated with spores of P. larvae when exposed to honeybee brood combs with clinical AFB symptoms, under laboratory conditions. Contamination persisted on pupae and newly-emerged adults. It was stated that the low number of P. larvae spores on adult beetles suggested that clinical AFB outbreaks are unlikely, but that even small spore numbers can be enough to spread P. larvae. It was concluded that any control measures should account for this risk (Schäfer et al., 2010).

In another study, A. tumida fed with dead worker bees with deformed wings, fed with brood testing positive for deformed wing virus (DWV), or associated with DWV-contaminated wax, were shown to test positive for DWV (Eyer et al., 2009). Further evidence suggested virus replication within the beetles. It was concluded that the beetle can be contaminated with the virus and therefore has the potential of being a vector for it.

Impact

Economic Impact

Infestations of A. tumida can cause considerable financial loss to beekeepers (Delaplane, 1998). Time and labour to detect and control the beetles, and losses in honey production and pollination, are the main economic losses suffered by the beekeeping industry (Calderón et al., 2006).

Adult A. tumida eat bee eggs and the larvae consume brood, pollen and honey and heavily damage wax comb (Calderón et al., 2006). Beekeepers in Florida have suffered considerable damage and colony loss, where beetle larvae have tunnelled through combs, killed bee brood and ruined combs; abandoning of combs and entire colonies by bees once they have become infested has been reported in Florida (Delaplane, 1998).

The beetles defecate in the honey and cause it to ferment; this produces a frothy mess in supers and honey houses. Honey that is contaminated is no longer saleable and is also unpalatable to bees so it cannot be used as bee feed (Delaplane, 1998).

Within two years of the discovery of A. tumida in the USA, at least 20,000 bee colonies had been destroyed by it, costing many millions of dollars. It has had a serious detrimental effect on the beekeeping industry in Australia as well (FERA, 2010).

Environmental Impact

Impact on habitats

A decline in bee numbers has been attributed to various bee pests and diseases, such as A. tumida. Bee decline will have a significantly negative affect on pollination in habitats where plants rely on bees. The value of pollination is estimated to exceed the value of products from beehives many-fold (Delaplane and Mayer, 2000).

Impact on biodiversity

A decline in native bees, such as A. mellifera, due to infestation by small hive beetles will have a negative impact on bee biodiversity (Cuthbertson and Brown, 2009).

Disease Treatment

See 'Prevention and Control' section.

Prevention and Control

Prevention

OIE (2012) makes recommendations for minimizing the risk of introducing A. tumida with bees or apiculture equipment or products. These include inspection of consignments, transporting live bees only from areas known to be free of A. tumida, covering bee consignments with fine mesh to keep beetles out, cleaning of equipment and freezing of honey.

Control

As A. tumida is not restricted to beehives but can survive and reproduce in other natural environments, feeding on other resources such as fruit, it is very difficult to eradicate from an area (OIE, 2012).

Cultural control

Simple measures to help prevent infestation by A. tumida include good husbandry practices, such as ensuring the area of the honey house is clean and reducing the amount of time that filled supers are left standing and cappings are exposed. Beekeepers should be aware that supering colonies, making splits, exchanging combs, or the use of Porter bee escapes can aid the spread of beetles or provide more room for beetles to become established away from the cluster of protective bees (Delaplane, 1998).

Host resistance

Bee hygienic behaviour refers to cell uncapping and the removal of diseased or parasitized larvae, as well as other nest-cleaning and defensive traits; African bees keep the beetle population at low levels in this way (FERA, 2010). Bee resistance to brood infectious diseases can be increased by selecting for hygienic bees. In a factsheet about the small hive beetle, Delaplane (1998) suggests that colonies should be monitored for hygienic behaviour and queen lines found to be beetle-resistant should be propagated. Even though bees will not normally clean supers, or equipment that is contaminated with beetle-fermented honey, they may finish the job if a beekeeper washes out as much honey as possible first.

Chemical control

A. tumida larvae migrate to the soil surrounding colonies in order to pupate, so a soil insecticide is recommended for their control (Delaplane, 1998); Annand (2008) suggests using permethrin. Colonies themselves can be treated with coumaphos-impregnated beehive pest control strips. Neumann and Hoffman (2008) investigated the efficacy of bottom boards and coumaphos strips for the control and diagnosis of small hive beetles in Australia. As with other studies (e.g. Buchholz et al., 2009), they reported that coumaphos traps were efficient, but mortality assessment showed that only a limited proportion of beetles were affected at the colony level. It was concluded that bottom boards provide a first estimate of infestation levels.

Coumaphos is actually an acaracide, but has been shown to be effective against A. tumida. Ellis and Delaplane (2007) investigated the efficacy of acaracides in 3 chemical classes, including organophosphates (coumaphos), pyrethroids (fluvalinate) and botanical extracts (thymol, camphor, menthol and eucalyptol). The acaricides varied in their toxicity to A. tumida, but it was concluded that there was potential to develop chemical controls based on these data.

Schafer et al. (2009) investigated the effects of organic acid treatments on A. tumida and the associated yeast, Kodamaea ohmeri. Organic acids are used to control other bee pests and were applied using the standard concentrations. Lactic, formic and acetic acids were shown to inhibit the growth of K. ohmeri under laboratory conditions. Acetic acid was found to be effective against the adult beetles and formic acid significantly reduced larval infestation.

Stored equipment can be fumigated with aluminium phosphide (phosphine); care is needed as this is very toxic (Annand, 2008).

Pesticide treatment carries a risk of residues in honey (OIE, undated).

Biological control

Other control measures that have been suggested as part of integrated control management programmes include entomopathogenic nematodes (e.g. Cabanillas and Elzen, 2006; Muerrle et al., 2006; Ellis et al., 2010; Cuthbertson et al., 2012). Ellis et al. (2010) evaluated the potential of 7 nematode species. The results of generational persistence and field bioassays suggested that Steinernema riobrave and Heterorhabditis indica displayed potential to control the beetles at tolerable levels as part of IPM schemes in bee colonies.

Other

Other investigations have looked at the use of lime, diatomaceous earth, or organic acids as alternative control measures for small hive beetles. Buchholz et al. (2009) investigated the use of slaked lime, powdered limestone and diatomaceous earth; they concluded that the best-performing formulation of diatomaceous earth showed potential as an in-hive treatment and suggested that further research was required for slaked lime.

References

Akinwande KL, Badejo MA, Ogbogu SS, 2013. Challenges associated with the honey bee (Apis mellifera adansonii) colonies establishment in south western Nigeria. African Journal of Food, Agriculture, Nutrition and Development, 13(2):7467-7484. http://www.ajfand.net/Volume13/No2/Akinwande12175.pdf

Annand N, 2008. Small hive beetle management options. Orange, New South Wales, Australia: New South Wales Department of Primary Industries, 7 pp. http://www.dpi.nsw.gov.au/__data/assets/pdf_file/0010/220240/small-hive-beetle-management-options.pdf

Buchholz S, Merkel K, Spiewok S, Pettis JS, Duncan M, Spooner-Hart R, Ulrichs C, Ritter W, Neumann P, 2009. Alternative control of Aethina tumida Murray (Coleoptera: Nitidulidae) with lime and diatomaceous earth. Apidologie, 40(5):535-548. http://www.edpsciences.org/journal/index.cfm?edpsname=apido

Cabanillas HE, Elzen PJ, 2006. Infectivity of entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) against the small hive beetle Aethina tumida (Coleoptera: Nitidulidae). Journal of Apicultural Research, 45(1):49-50

Calderón RA, Arce H, Ramírez JF, 2006. The small hive beetle Aethina tumida Murray, an important problem affecting honey bees. (El pequeño escarabajo de la colmena Aethina tumida Murray, un problema importante que afecta las abejas melíferas.) Ciencias Veterinarias (Heredia), 24(1):49-55

Cuthbertson AGS, Brown MA, 2009. Issues affecting British honey bee biodiversity and the need for conservation of this important ecological component. International Journal of Environmental Science and Technology, 6(4):695-699. http://www.ceers.org/ijest

Cuthbertson AGS, Mathers JJ, Blackburn LF, Marris G, 2013. Lifecycle of the Small hive beetle, Aethina tumida. Bee Craft, 95(5):32-33

Cuthbertson AGS, Mathers JJ, Blackburn LF, Powell ME, Marris G, Pietravalle S, Brown MA, Budge GE, 2012. Screening commercially available entomopathogenic biocontrol agents for the control of Aethina tumida (Coleoptera: Nitidulidae) in the UK. Insects, 3(3):719-726. http://www.mdpi.com/2075-4450/3/3/719

Cuthbertson AGS, Mathers JJ, Blackburn LF, Wakefield ME, Collins LE, Luo WeiQi, Brown MA, 2008. Maintaining Aethina tumida (Coleoptera: Nitidulidae) under quarantine laboratory conditions in the UK and preliminary observations on its behaviour. Journal of Apicultural Research, 47(3):192-193. http://www.ibra.org.uk

Cuthbertson AGS, Wakefield ME, Powell ME, Marris G, Anderson H, Budge GE, Mathers JJ, Blackburn LF, Brown MA, 2013. The small hive beetle Aethina tumida: a review of its biology and control measures. Current Zoology, 59(5):644-653. http://www.actazool.org/temp/%7B02A6F36B-3FC8-4D97-AFFA-33FBBA383F27%7D.pdf

Delaplane KS, 1998. The small hive beetle, Aethina tumida. A new beekeeping pest. Tifton, Georgia, USA: University of Georgia, 2 pp. http://www.bugwood.org/factsheets/small_hive_beetle.html

Delaplane KS, Mayer DF, 2000. Crop pollination by bees. Wallingford, UK: CABI Publishing, xv + 344 pp. http://www.cabi.org/CABeBooks/default.aspx?site=107&page=45&LoadModule=PDFHier&BookID=26

Donovan BJ, Paul F, 2005. Pseudoscorpions: the forgotten beneficials inside beehives and their potential for management for control of varroa and other arthropod pests. Bee World, 86(4):83-87

Ellis JD, Delaplane KS, 2007. The effects of three acaricides on the developmental biology of small hive beetles (Aethina tumida). Journal of Apicultural Research, 46(4):256-259

Ellis JD, Spiewok S, Delaplane KS, Buchholz S, Neumann P, Tedders WL, 2010. Susceptibility of Aethina tumida (Coleoptera: Nitidulidae) larvae and pupae to entomopathogenic nematodes. Journal of Economic Entomology, 103(1):1-9. http://esa.publisher.ingentaconnect.com/content/esa/jee/2010/00000103/00000001/art00001

El-Niweiri MAA, El-Sarrag MS, Neumann P, 2008. Filling the Sudan gap: the northernmost natural distribution limit of small hive beetles. Journal of Apicultural Research, 47(3):184-185. http://www.ibra.org.uk

Eyer M, Chen YP, Schäfer MO, Pettis J, Neumann P, 2009. Small hive beetle, Aethina tumida, as a potential biological vector of honeybee viruses. Apidologie, 40(4):419-428. http://www.edpsciences.org/journal/index.cfm?edpsname=apido

FERA (Food and Environment Research Agency), 2010. The Small Hive Beetle: a serious threat to European apiculture. Sand Hutton, UK: Food and Environment Research Agency, 23 pp. https://secure.fera.defra.gov.uk/beebase/downloadDocument.cfm?id=17

Kokkinis MI, 2005. Small hive beetle [SHB], Aethina tumida. Deltion tes Ellenikes Kteniatrikes Etaireias = Journal of the Hellenic Veterinary Medical Society, 56(3):228-238

Kozak P, 2010. Small Hive Beetle. Guelph, Ontario, Canada: Ontario Ministry of Agriculture, Food and Rural Affairs, 4 pp. http://www.omafra.gov.on.ca/english/food/inspection/bees/info-shb.pdf

Kozak P, 2012. Biosecurity practices for preventing the spread of Small Hive Beetle. Guelph, Ontario, Canada: Ontario Ministry of Agriculture, Food and Rural Affairs, 4 pp. http://www.omafra.gov.on.ca/english/food/inspection/bees/biosecurity.pdf

Muerrle TM, Neumann P, Dames JF, Hepburn HR, Hill MP, 2006. Susceptibility of adult Aethina tumida (Coleoptera: Nitidulidae) to entomopathogenic fungi. Journal of Economic Entomology, 99(1):1-6. http://miranda.esa.catchword.org/vl=5478027/cl=18/nw=1/rpsv/cw/esa/00220493/v99n1/s1/p1

Murilhas AM, 2005. Aethina tumida arrives in Portugal. Will it be eradicated? EurBee Newsletter, 2:7-9

Mutinelli F, Montarsi F, Federico G, Granato A, Ponti MA, Grandinetti G, Ferrè N, Franco S, Duquesne V, Rivière MP, Thiéry R, Henrkix P, Ribière-Chabert M, Chauzat MP, 2014. Detection of Aethina tumida Murray (Coleoptera: Nitidulidae.) in Italy: outbreaks and early reaction measures. Journal of Apicultural Research, 53(5):569-575. http://dx.doi.org/10.3896/IBRA.1.53.5.13

Neumann P, Hoffmann D, 2008. Small hive beetle diagnosis and control in naturally infested honeybee colonies using bottom board traps and CheckMite+strips. Journal of Pest Science, 81(1):43-48. http://www.springerlink.com/content/4830215644411151/fulltext.pdf

OIE (Office International des Epizooties), undated. Diseases of bees. Paris, France: Office International des Epizooties, 6 pp. http://www.oie.int/fileadmin/Home/eng/Media_Center/docs/pdf/Disease_cards/BEES-EN.pdf

OIE (World Organisation for Animal Health), 2012. Terrestrial Animal Health Code, edition 21. Paris, France: Office International des Epizooties. http://www.oie.int/international-standard-setting/terrestrial-code/access-online/

OIE (World Organisation for Animal Health), 2013. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals. Paris, France: World Organisation for Animal Health. http://www.oie.int/en/international-standard-setting/terrestrial-manual/access-online/

OIE, 2009. World Animal Health Information Database - Version: 1.4. World Animal Health Information Database. Paris, France: World Organisation for Animal Health. http://www.oie.int

Papadopoulo P, 1964. Enemies of bees (1). Rhodesia Agricultural Journal, 61(6):114-115 pp

Roberts E, 1971. A survey of beekeeping in Uganda. Bee World, 52(2):57-67

Schäfer MO, Pettis JS, Ritter W, Neumann P, 2008. A scientific note on quantitative diagnosis of small hive beetles, Aethina tumida, in the field. Apidologie, 39(5):564-565. http://www.edpsciences.org/journal/index.cfm?edpsname=apido

Schäfer MO, Ritter W, Pettis J, Neumann P, 2010. Small hive beetles, Aethina tumida, are vectors of Paenibacillus larvae. Apidologie, 41(1):14-20. http://www.edpsciences.org/journal/index.cfm?edpsname=apido

Schäfer MO, Ritter W, Pettis JS, Teal PEA, Neumann P, 2009. Effects of organic acid treatments on small hive beetles, Aethina tumida, and the associated yeast Kodamaea ohmeri. Journal of Pest Science, 82(3):283-287. http://www.springerlink.com/content/b757803l567h7618/?p=44ff5f5bd86346bf8086df5eb7625e26&pi=10

Spiewok S, Duncan M, Spooner-Hart R, Pettis JS, Neumann P, 2008. Small hive beetle, Aethina tumida, populations II: dispersal of small hive beetles. Apidologie, 39(6):683-693. http://www.edpsciences.org/journal/index.cfm?edpsname=apido

Spiewok S, Pettis JS, Duncan M, Spooner-Hart R, Westervelt D, Neumann P, 2007. Small hive beetle, Aethina tumida, populations I: Infestation levels of honeybee colonies, apiaries and regions. Apidologie, 38(6):595-605. http://www.edpsciences.org/journal/index.cfm?edpsname=apido

Stedman M, 2006. Small Hive Beetle (SHB): Aethina tumida Murray (Coleoptera: Nititulidae). Glenside, South Australia, Australia: Primary Industries and Resources South Australia, 15 pp. http://www.pir.sa.gov.au/__data/assets/pdf_file/0015/41262/apiary_shb_fact_sheet_2006.pdf

Thomas MC, 1998. Florida pest alert - the small hive beetle. American Bee Journal, 138(8):565

Torto B, Fombong AT, Arbogast RT, Teal PEA, 2010. Monitoring Aethina tumida (Coleoptera: Nitidulidae) with baited bottom board traps: occurrence and seasonal abundance in honey bee colonies in Kenya. Environmental Entomology, 39(6):1731-1736. http://esa.publisher.ingentaconnect.com/content/esa/envent/2010/00000039/00000006/art00005

Ward L, Brown M, Neumann P, Wilkins S, Pettis J, Boonham N, 2007. A DNA method for screening hive debris for the presence of small hive beetle (Aethina tumida). Apidologie, 38(3):272-280. http://www.edpsciences.org/journal/index.cfm?edpsname=apido

Distribution References

Akinwande K L, Badejo M A, Ogbogu S S, 2013. Challenges associated with the honey bee (Apis mellifera adansonii) colonies establishment in south western Nigeria. African Journal of Food, Agriculture, Nutrition and Development. 13 (2), 7467-7484. http://www.ajfand.net/Volume13/No2/Akinwande12175.pdf

Annand N, 2008. Small hive beetle management options., Orange, New South Wales, Australia: New South Wales Department of Primary Industries. 7 pp. http://www.dpi.nsw.gov.au/__data/assets/pdf_file/0010/220240/small-hive-beetle-management-options.pdf

CABI, Undated. CABI Compendium: Status as determined by CABI editor. Wallingford, UK: CABI

El-Niweiri M A A, El-Sarrag M S, Neumann P, 2008. Filling the Sudan gap: the northernmost natural distribution limit of small hive beetles. Journal of Apicultural Research. 47 (3), 184-185. http://www.ibra.org.uk

FERA (Food and Environment Research Agency), 2010. The Small Hive Beetle: a serious threat to European apiculture., Sand Hutton, UK: Food and Environment Research Agency. 23 pp. https://secure.fera.defra.gov.uk/beebase/downloadDocument.cfm?id=17

Kozak P, 2010. Small Hive Beetle., Guelph, Ontario, Canada: Ontario Ministry of Agriculture, Food and Rural Affairs. 4 pp. http://www.omafra.gov.on.ca/english/food/inspection/bees/info-shb.pdf

Kozak P, 2012. Biosecurity practices for preventing the spread of Small Hive Beetle., Guelph, Ontario, Canada: Ontario Ministry of Agriculture, Food and Rural Affairs. 4 pp. http://www.omafra.gov.on.ca/english/food/inspection/bees/biosecurity.pdf

Murilhas AM, 2005. Aethina tumida arrives in Portugal. Will it be eradicated? In: EurBee Newsletter, 2 7-9.

Mutinelli F, Montarsi F, Federico G, Granato A, Ponti A M, Grandinetti G, Ferrè N, Franco S, Duquesne V, Rivière M P, Thiéry R, Henrikx P, Ribière-Chabert M, Chauzat M P, 2014. Detection of Aethina tumida Murray (Coleoptera: Nitidulidae.) in Italy: outbreaks and early reaction measures. Journal of Apicultural Research. 53 (5), 569-575. http://www.ibra.org.uk/categories/JAR-Archive-tables-of-contents DOI:10.3896/IBRA.1.53.5.13

OIE, 2009. World Animal Health Information Database - Version: 1.4., Paris, France: World Organisation for Animal Health. https://www.oie.int/

Papadopoulo P, 1964. Enemies of bees (1). Rhodesia Agricultural Journal. 61 (6), 114-115 pp.

Roberts E, 1971. A survey of beekeeping in Uganda. Bee World. 52 (2), 57-67.

Spiewok S, Pettis J S, Duncan M, Spooner-Hart R, Westervelt D, Neumann P, 2007. Small hive beetle, Aethina tumida, populations I: Infestation levels of honeybee colonies, apiaries and regions. Apidologie. 38 (6), 595-605. http://www.edpsciences.org/journal/index.cfm?edpsname=apido DOI:10.1051/apido:2007042

Torto B, Fombong A T, Arbogast R T, Teal P E A, 2010. Monitoring Aethina tumida (Coleoptera: Nitidulidae) with baited bottom board traps: occurrence and seasonal abundance in honey bee colonies in Kenya. Environmental Entomology. 39 (6), 1731-1736. http://esa.publisher.ingentaconnect.com/content/esa/envent/2010/00000039/00000006/art00005 DOI:10.1603/EN10013

Organizations

World: IBRA, International Bee Research Association, Unit 6, Centre Court, Main Avenue, Treforest, RCT, CF37 5YR, UK, www.ibra.org.uk

World: OIE (World Organisation for Animal Health), 12, rue de Prony, 75017 Paris, France, http://www.oie.int/

UK: British Beekeepers’ Association, National Beekeeping Centre, Stoneleigh Park, Stoneleigh, Warwickshire, CV8 2LG, UK, www.britishbeekeepers.com

Contributors

23/03/2012: Original text by:

Dr Claire Beverley, CABI, Nosworthy Way, Wallingford. OX10 8DE.

Distribution Maps