Evaluation of Pest Risks Associated with 

Importation of Honey Bees (Apis mellifera

L.) from Australia 

T.W. Culliney 

United States Department of Agriculture 

Animal and Plant Health Inspection Service 

Plant Protection and Quarantine 

Center for Plant Health Science and Technology 

Plant Epidemiology and Risk Analysis Laboratory 

1730 Varsity Drive, Suite 300 

Raleigh, North Carolina 27606 

November 12, 2009
Introduction

In March 2002, the United States Department of Agriculture’s Animal and Plant Health 

Inspection Service issued a report assessing the risks of pest introduction into the United States 

in imports of honey bees (Apis mellifera L.) from Australia (Wehling, 2002). These 

consignments were to comprise drone semen, adult queens, and package bees, which are boxes 

of bees, typically consisting of 8000-12,000 workers, a few drones, and a young, mated queen 

(Morse, 1975). The evaluation of imports from Australia identified 15 pathogens and pests of 

bees in that country, all of which also occur in the United States. The risk assessment concluded 

that there were no quarantine-significant honey bee pathogens or pests occurring in Australia. 

In the seven years since completion of the risk assessment for Australian bees, new threats to the 

U.S. honey bee population have emerged. One of the most prominent of these is the so-called 

colony collapse disorder, a mysterious syndrome characterized by the abrupt disappearance of a 

colony’s adult worker bee population, leaving a substantial population of healthy brood; an 

absence of dead bees both within and surrounding affected colonies; and the delayed invasion of 

hive pests (e.g., small hive beetle, wax moths) and robbing of hive stores by neighboring 

colonies (vanEngelsdorp et al., 2009). A link between the disorder, first reported in the United 

States in 2006, and honey bee imports from Australia (which began in 2005) has been suggested 

(Cox-Foster et al., 2007). The May 2007 discovery of colonies of the Asiatic honey bee, Apis 

cerana F., near Cairns, Victoria (R. Williams, Australian Embassy, Washington, D.C., in litt., 

February 13, 2009), has raised concerns that exotic honey bee pathogens or parasites may have 

been introduced into Australia with the arrival of this foreign bee. Concerns also have been 

raised about the potential for exotic bee pests to be introduced into the United States from 

Canada, which has imported queens and package bees from Australia since 1973 (Wehling, 

2002). These developments suggest a need to re-evaluate the risks involved in importation of 

bees from Australia, as well as other foreign countries. This document re-examines potential pest 

risks involved in the importation of honey bees from Australia. 

Hazard Identification

Hazard identification is an essential step, necessarily preceding risk assessment (OIE, 2009). It 

involves the identification of the pestiferous agents (e.g., parasites, pathogens), the introduction 

of which potentially could produce adverse consequences. The risk assessment is concluded if 

hazard identification fails to identify potential hazards. 

Pest Categorization—Identification of Quarantine Pests and Quarantine Pests Likely to 

Follow the Pathway

A search of the available literature and other sources of information identified 143 organisms 

associated with honey bees, and which also occur in Australia (Table 1). Based on the available 

evidence, nine of these species occur in Australia, but are not known to be established in the 

United States, and have the potential to be introduced into the United States in consignments of 

imported honey bees. Two organisms were not determined to species, and thus were not 

amenable to risk assessment (IPPC, 2004). 
2

Table 1. Organisms associated or potentially associated with honey bees (Apis mellifera L.) in 

Australia.

Species 

Common 

Name or 

Condition 

Geographic 

Distribution1 

Quarantine 

Pest2 

Likely to 

Follow 

Pathway3 References 

ARTHROPODS 

ACARI

Acaridae 

Acarus siro L. (= 

Tyroglyphus farinae [De 

Geer]) 

House dust 

mite, flour 

mite 

AU, US No No4 Baker et al. (1976); 

CABI (2007); 

Eickwort (1988); 

Shanahan & Shelton 

(1948) 

Forcellinia galleriella

Womersley 

House dust 

mite 

AU Yes No5

 Eickwort (1988); 

Womersley (1963) 

Tyrolichus casei

(Oudemans) 

Cheese mite AU, US No No4

 CSIRO (2005); 

Eickwort (1988); 

Krantz (1955) 

Tyrophagus communis

Fan & Zhang 

 AU, US No No6

 Fan & Zhang (2007) 

Tyrophagus curvipenis

Fain & Fauvel 

AU Yes Yes7, 8 Fan & Zhang (2007) 

Tyrophagus longior

(Gervais) 

Seed mite AU, US No No4

 Eickwort (1988); Fan 

& Zhang (2007) 

Tyrophagus putrescentiae

(Schrank) 

House dust 

mite, mold 

mite 

AU, US No No4

 Eickwort (1988); Fan 

& Zhang (2007) 

Tyrophagus vanheurni

Oudemans 

AU Yes Yes9 Fan & Zhang (2007) 

Ameroseiidae 

Afrocypholaelaps 

africana (Evans) 

AU, US10 Yes Yes11 Eickwort (1988); 

Halliday (1997) 

Hattena panopla

Domrow 

 AU Yes No12 Seeman (1996) 

Neocypholaelaps sp. AU Yes No13 Brimblecombe & 

Roff (1960) 

Ascidae 

Blattisocius dentriticus

(Berlese) 

House dust 

mite 

AU, US No No14 Eickwort (1988); 

Halliday et al.

(1998); Yoshikawa & 

Bennett (1979) 

Blattisocius tarsalis

(Berlese) 

House dust 

mite 

AU, US No No15 Eickwort (1988); 

Hagstrum & Sharp 

(1975); Halliday et 

al. (1998) 

Proctolaelaps pygmaeus

(Müller) 

 AU, US No No16 Eickwort (1988); 

Halliday et al.

(1998); Minor & 

Norton (2004) 
3

Species 

Common 

Name or 

Condition 

Geographic 

Distribution1 

Quarantine 

Pest2 

Likely to 

Follow 

Pathway3 References 

Cheyletidae 

Cheyletus eruditus

(Schrank) 

House dust 

mite 

AU, US No No17 AFD (2007); Custer 

& Pence (1979); 

Eickwort (1988) 

Eriophyidae 

Aceria litchii (Keifer) Lychee 

erinose mite 

AU Yes No18 Waite (1999) 

Glycyphagidae 

Glycyphagus domesticus

(De Geer) 

House dust 

mite, cheese 

mite 

AU, US No No4

 Dicke et al. (1953); 

Eickwort (1988); 

Shanahan & Shelton 

(1948) 

Laelapidae 

Melittiphis alvearius

(Berlese) 

Pollen mite AU, US No No19 Delfinado-Baker 

(1994); Knihinicki & 

Halliday (1995) 

Macrochelidae 

Macrocheles glaber

(Müller) 

 AU, US No No20 Eickwort (1988); 

Halliday (2000) 

Macrocheles 

muscaedomesticae

(Scopoli) 

 AU, US No No21 Eickwort (1988); 

Halliday (2000); 

Rueda & Axtell 

(1997) 

Pyemotidae 

Pyemotes ventricosus

(Newport) 

Grain itch 

mite 

AU, US No No22 Betz et al. (1982); 

Brimblecombe & 

Roff (1960); 

Eickwort (1988) 

Pyroglyphidae 

Dermatophagoides 

pteronyssinus

(Trouessart) 

House dust 

mite 

AU, US No No4

 Abramson et al.

(2006); AFD (2007); 

Eickwort (1988) 

Tarsonemidae 

Acarapis sp. AU Yes Yes Brimblecombe & 

Roff (1960) 

Acarapis dorsalis

Morgenthaler 

 AU, US No Yes AFD (2007); 

Shimanuki & Knox 

(2000) 

Acarapis externus

Morgenthaler in Morison 

 AU, US No Yes AFD (2007); 

Shimanuki & Knox 

(2000) 

COLEOPTERA 

Anobiidae 

Stegobium paniceum (L.) Drugstore 

beetle 

AU, US No No23 Caron (1997); 

Lawrence & Britton 

(1991); Philips 

(2002) 
4

Species 

Common 

Name or 

Condition 

Geographic 

Distribution1 

Quarantine 

Pest2 

Likely to 

Follow 

Pathway3 References 

Nitidulidae 

Aethina tumida Murray Small hive 

beetle 

AU, US No24 No25 Neumann & Elzen 

(2004) 

Ptinidae 

Ptinus exulans Erichson AU Yes No26 Caron (1997) 

Ptinus fur (L.) Whitemarked 

spider 

beetle 

AU, US No No27 Caron (1997); Rees 

(2004) 

Scarabaeidae 

Copris lunaris L. AU28 Yes No29 Caron (1997); Kirk & 

Feehan (1984) 

DIPTERA 

Braulidae 

Braula coeca Nitzsch Bee-louse AU,30 US No Yes Weems & Sanford 

(2000) 

Drosophilidae 

Drosophila busckii

Coquillett 

 AU, US No Yes Bailey & Ball (1991); 

Oakeshott et al.

(1989); Stone et al.

(1965) 

Sarcophagidae 

Senotainia tricuspis

(Meigen) 

AU Yes Yes Bailey & Ball (1991) 

Syrphidae 

Tenthredomyia australis

Shannon 

 AU Yes No31 Sammataro (1997) 

HYMENOPTERA 

Apidae 

Apis cerana F. Indian 

honey bee, 

Asiatic 

honey bee, 

eastern hive 

bee 

AU Yes No32 Anonymous (2009) 

Eulophidae 

Melittobia acasta

(Walker) 

 AU, US No No33 Fell (1997); González

et al. (2004) 

Formicidae 

Linepithema humile

(Mayr) 

Argentine 

ant 

AU, US No No34 Fell (1997) 

Monomorium destructor

(Jerdon) 

Singapore 

ant 

AU, US No No35 Eisner et al. (1996); 

Fell (1997); 

Hoffmann et al.

(1999) 
5

Species 

Common 

Name or 

Condition 

Geographic 

Distribution1 

Quarantine 

Pest2 

Likely to 

Follow 

Pathway3 References 

Monomorium pharaonis

(L.) 

Pharaoh ant AU, US No No35 Fell (1997); 

Hoffmann et al.

(1999) 

Pheidole megacephala

(F.) 

Bigheaded 

ant 

AU, US No No35 Fell (1997); 

Hoffmann et al.

(1999); Warner & 

Scheffrahn (2007) 

Solenopsis invicta Buren Red 

imported 

fire ant 

AU, US No No35 Dominiak et al.

(2005); Fell (1997) 

LEPIDOPTERA 

Pyralidae 

Achroia grisella (F.) Lesser wax 

moth 

AU, US No No36 Common (1990); 

Zhang (1994) 

Ephestia kuehniella

Zeller (= Anagasta

kuehniella [Zeller]) 

Mill moth AU, US No No36 CABI (2007); 

Shimanuki & Knox 

(2000); Steidle et al.

(2001) 

Galleria mellonella (L.) Greater wax 

moth 

AU, US No No36 Common (1990); 

Williams (1997) 

PSOCOPTERA 

Trogiidae 

Trogium pulsatorium (L.) Pollen louse AU, US No No37 Gillott (1995); Most 

(1989); Smithers 

(1965) 

VIRUSES 

Bee virus F AU Yes Yes Anderson (1993) 

Bee virus X AU Yes Yes Ellis & Munn (2005) 

Bee virus Y AU, US No Yes Allen & Ball (1996) 

Black queen cell virus 

(Dicistroviridae) 

 AU, US No Yes Allen & Ball (1996) 

Chronic bee-paralysis 

satellite virus (= chronic 

paralysis virus associate) 

AU Yes Yes Ellis & Munn (2005); 

Mayo et al. (2005) 

Chronic paralysis virus AU, US No Yes Allen & Ball (1996) 

Cloudy wing virus AU, US Yes38 Yes Allen & Ball (1996) 

Cricket paralysis virus 

(Dicistroviridae) 

 AU, US No Yes Anderson & Gibbs 

(1988); Moore (1991)

Filamentous virus AU, US No Yes Allen & Ball (1996) 

Israeli acute paralysis 

virus (Dicistroviridae) 

 AU, US No Yes Cox-Foster et al.

(2007) 

Kashmir bee virus 

(Dicistroviridae) 

 AU, US No Yes Allen & Ball (1996) 

Sacbrood virus 

(Iflaviridae) 

 AU, US No Yes Allen & Ball (1996) 

Slow paralysis virus AU Yes Yes DAFF (2002) 
6

Species 

Common 

Name or 

Condition 

Geographic 

Distribution1 

Quarantine 

Pest2 

Likely to 

Follow 

Pathway3 References 

BACTERIA 

Achromobacter eurydice

(White) (Burkholderiales) 

 AU, US No Yes Djordjevic et al.

(2000); Shimanuki & 

Knox (2000) 

Bacillus brevis Migula 

(Bacillales) 

 AU, US No Yes Gilliam & Valentine 

(1976); Kollmorgen 

& Jones (1975) 

Bacillus cereus

Frankland & Frankland 

(Bacillales) 

 AU, US No Yes Gilliam & Valentine 

(1976); Scurrah et al.

(2006) 

Bacillus circulans Jordan 

(Bacillales) 

 AU, US No Yes Gilliam & Valentine 

(1976); Scurrah et al.

(2006) 

Bacillus coagulans

Hammer (Bacillales) 

 AU, US No Yes Ohye & Murrell 

(1962); Vandenberg 

& Shimanuki (1990); 

Yan et al. (1985) 

Bacillus licheniformis

(Weigmann) Chester 

(Bacillales) 

 AU, US No Yes Gilliam & Valentine 

(1976); Scurrah et al.

(2006) 

Bacillus macerans

Schardinger (Bacillales) 

 AU, US No Yes Gilliam & Valentine 

(1976); Halsall & 

Gibson (1985) 

Bacillus megaterium de 

Bary (Bacillales) 

 AU, US No Yes Gilliam & Valentine 

(1976); Lacey et al.

(2007); Murrell & 

Rankine (1979) 

Bacillus polymyxa

(Prazmowski) Mace 

(Bacillales) 

 AU, US No Yes Gilliam & Valentine 

(1976); Oedjijono et 

al. (1993) 

Bacillus pumilus Meyer 

& Gottheil (Bacillales) 

 AU, US No Yes Gilliam & Valentine 

(1976); Scurrah et al.

(2006) 

Bacillus sphaericus

Meyer & Neide 

(Bacillales) 

 AU, US No Yes Gilliam & Morton 

(1978); Greaves 

(1973) 

Bacillus subtilis

(Ehrenberg) Cohn 

(Bacillales) 

 AU, US No Yes Gilliam & Valentine 

(1976); Oedjijono et 

al. (1993) 

Enterobacter aerogenes

Hormaeche & Edwards 

(Enterobacteriales) 

 AU, US No Yes Gilliam & Valentine 

(1974); Gordon & 

FitzGibbon (1999) 

Enterobacter cloacae

(Jordan) Hormaeche & 

Edwards 

(Enterobacteriales) 

 AU, US No Yes Gilliam & Valentine 

(1974); Gordon & 

FitzGibbon (1999) 
7

Species 

Common 

Name or 

Condition 

Geographic 

Distribution1 

Quarantine 

Pest2 

Likely to 

Follow 

Pathway3 References 

Enterococcus faecalis

(Andrewes & Horder) 

Schleifer & Kilpper-Bälz 

(Lactobacillales) 

 AU, US No Yes Djordjevic et al.

(2000); Shimanuki & 

Knox (2000) 

Enterococcus faecium

(Orla-Jensen) Schleifer & 

Kilpper-Bälz 

(Lactobacillales) 

 AU, US No Yes Christensen et al.

(2008); Djordjevic et 

al. (2000) 

Escherichia coli (Migula) 

Castellani & Chalmers 

(Enterobacteriales) 

 AU, US No Yes Gilliam & Valentine 

(1974); Gordon & 

FitzGibbon (1999) 

Hafnia alvei Moller (= 

Enterobacter hafniae

Ewing and Fife) 

(Enterobacteriales) 

Septicemia AU, US No Yes Bailey & Ball (1991); 

Euzéby (1997); 

Gilliam & Valentine 

(1974); Okada & 

Gordon (2003) 

Klebsiella oxytoca

(Flügge) Lautrop 

(Enterobacteriales) 

 AU, US No Yes Gilliam & Valentine 

(1974); Gordon & 

FitzGibbon (1999); 

Waites et al. (2006) 

Klebsiella pneumoniae

(Schroeter) Trevisan 

(Enterobacteriales) 

 AU, US No Yes Gilliam & Valentine 

(1974); Gordon & 

FitzGibbon (1999) 

Melissococcus plutonius

corrig. (ex White) Bailey 

& Collins (= M. pluton

[White] Bailey & 

Collins) (Lactobacillales) 

European 

foulbrood 

AU, US No Yes Euzéby (1997); 

Matheson (1993) 

Paenibacillus alvei

(Cheshire & Cheyne) Ash 

et al. (= Bacillus alvei

Cheshire & Cheyne) 

(Bacillales) 

 AU, US No Yes Djordjevic et al.

(2000); Gilliam & 

Valentine (1976); 

Shimanuki & Knox 

(2000) 

Paenibacillus larvae 

larvae (White) Ash et al. 

(Bacillales) 

American 

foulbrood 

AU, US No Yes Matheson (1993) 

Proteus vulgaris Hauser 

(Enterobacteriales) 

 AU, US No Yes Berdela et al. (1994); 

Gilliam & Valentine 

(1974); Whittington

et al. (1996) 

Providencia alcalifaciens

(de Salles Gomes) Ewing 

(Enterobacteriales) 

 AU, US No Yes Albert et al. (1992); 

Gilliam & Valentine 

(1974); Holmes et al.

(1988) 
8

Species 

Common 

Name or 

Condition 

Geographic 

Distribution1 

Quarantine 

Pest2 

Likely to 

Follow 

Pathway3 References 

Providencia stuartii

(Buttiaux et al.) Ewing 

(Enterobacteriales) 

 AU, US No Yes Gilliam & Valentine 

(1974); Kuzina et al.

(2001); Murray & 

Edwards (1987) 

Pseudomonas aeruginosa

(Schroeter) Migula (= P. 

apiseptica [Burnside] 

Landerkin & Katznelson) 

(Pseudomonadales) 

Septicemia AU, US No Yes Bailey & Ball (1991); 

Shimanuki & Knox 

(2000); Syrmis et al.

(2008) 

Pseudomonas fluorescens

(Trevisan) Migula 

(Pseudomonadales) 

 AU, US No Yes Bailey & Ball (1991); 

Flores-Vargas & 

O’Hara (2006); 

Raaijmakers et al.

(1999) 

Salmonella enteritidis

(Gaertner) Castellani & 

Chalmers 

(Enterobacteriales) 

 AU, US No Yes Altekruse et al.

(2006); Anonymous 

(2004); Gilliam & 

Valentine (1974) 

Serratia liquefaciens

(Grimes & Hennerty) 

Bascomb et al. 

(Enterobacteriales) 

 AU, US No Yes Cox & Mac Rae 

(1989); Gilliam & 

Morton (1974) 

Serratia marcescens

Bizio (Enterobacteriales) 

Septicemia AU, US No Yes Bailey & Ball (1991); 

Bradbury (1986); 

Sharma et al. (2007) 

Yersinia 

pseudotuberculosis

(Pfeiffer) Smith & Thal 

(Enterobacteriales) 

Septicemia AU, US No Yes Bailey & Ball (1991); 

Hubbert et al. (1971); 

Miao et al. (2001) 

FUNGI 

Alternaria tenuissima

(Nees & T. Nees:Fr.) 

Wiltshire (Ascomycetes: 

Pleosporales) 

 AU, US No Yes Gilliam & Prest 

(1977); Pethybridge

et al. (2004) 

Ascosphaera apis

(Maasen ex Claussen) 

Olive & Spiltoir 

(Ascomycetes) 

Chalkbrood AU, US No Yes Matheson (1993) 

Ascosphaera atra Skou & 

Hackett (Ascomycetes) 

 AU, US No No39 Anderson et al.

(1998) 

Ascosphaera duoformis

Anderson & Gibson 

(Ascomycetes) 

 AU Yes No39 Anderson et al.

(1998) 

Aspergillus flavus

Link:Fr. (Ascomycetes: 

Eurotiales) 

Stonebrood AU, US No Yes Farr et al. (2006); 

Shimanuki & Knox 

(2000) 
9

Species 

Common 

Name or 

Condition 

Geographic 

Distribution1 

Quarantine 

Pest2 

Likely to 

Follow 

Pathway3 References 

Aspergillus fumigatus

Fresen. (Ascomycetes: 

Eurotiales) 

Stonebrood AU, US No Yes Bhartiya et al.

(2007); Shimanuki & 

Knox (2000) 

Aspergillus nidulans 

(Eidam) Winter 

(Ascomycetes: 

Eurotiales) (teleomorph: 

Emericella nidulans

[Eidam] Vuill.) 

 AU, US No Yes Farr et al. (2006); 

Gilliam & 

Vandenberg (1997); 

Hollomon (1970) 

Aspergillus niger Tiegh. 

(Ascomycetes: 

Eurotiales) 

Stonebrood AU, US No Yes Farr et al. (2006); 

Shimanuki & Knox 

(2000) 

Aspergillus ochraceus

Wilh. (Ascomycetes: 

Eurotiales) 

 AU, US No Yes Bryant & Rogers 

(1991); Farr et al.

(2006); Gilliam & 

Vandenberg (1997) 

Aspergillus sydowii

(Bainier & Sartory) 

Thom & Church 

(Ascomycetes: 

Eurotiales) 

 AU, US No Yes Gilliam et al.

(1974a); Hill et al.

(1995) 

Aspergillus terreus Thom 

(Ascomycetes: 

Eurotiales) 

 AU, US No Yes Gilliam et al.

(1974a); Wakcup 

(1957) 

Aureobasidium pullulans

(de Bary) Arnaud 

(Ascomycetes: 

Dothideales) 

 AU, US No Yes Farr et al. (2006); 

Gilliam & 

Vandenberg (1997) 

Candida albicans

(Robin) Berkhout 

(Saccharomycetes: 

Saccharomycetales) 

 AU, US No Yes Chen et al. (2008); 

Farr et al. (2006); 

Gilliam et al. (1974b) 

Candida glabrata

(Anderson) Mey. & 

Yarrow 

(Saccharomycetes: 

Saccharomycetales) (= 

Torulopsis glabrata

[Anderson] Lodder & de 

Vries) 

 AU, US No Yes Gilliam et al.

(1974b); Kirk 

(2004b); Pirotta & 

Garland (2006) 

Candida guilliermondii

(Castell.) Langeron & 

Guerra 

(Saccharomycetes: 

Saccharomycetales) 

(teleomorph: Pichia 

guilliermondii Wick.) 

 AU, US No Yes Crockett et al.

(1992); Farr et al.

(2006); Gilliam et al.

(1974b) 
10

Species 

Common 

Name or 

Condition 

Geographic 

Distribution1 

Quarantine 

Pest2 

Likely to 

Follow 

Pathway3 References 

Candida krusei (Castell.) 

Berkhout 

(Saccharomycetes: 

Saccharomycetales) 

 AU, US No Yes Eisen et al. (2002); 

Farr et al. (2006); 

Gilliam et al. (1974b) 

Candida lipolytica

(Harrison) Diddens & 

Lodder 

(Saccharomycetes: 

Saccharomycetales) 

 AU, US No Yes Gilliam et al.

(1974b); Roostita & 

Fleet (1996) 

Candida parapsilosis

(Ashford) Langeron & 

Talice (Saccharomycetes: 

Saccharomycetales) 

 AU, US No Yes Chen et al. (2008); 

Cooke (1970); 

Gilliam et al. (1974b) 

Candida pelliculosa

Redaelli 

(Saccharomycetes: 

Saccharomycetales) 

 AU, US No Yes Ardhana & Fleet 

(1989); Cooke 

(1970); Gilliam et al.

(1974b) 

Candida pulcherrima

(Lindner) Windisch 

(Saccharomycetes: 

Saccharomycetales) (= 

Metschnikowia 

pulcherrima Pitt & Mill.) 

 AU, US No Yes Barker et al. (1984); 

Gilliam et al.

(1974b); Tournas et 

al. (2006) 

Candida rugosa

(Anderson) Diddens & 

Lodder 

(Saccharomycetes: 

Saccharomycetales) 

 AU, US No Yes Gilliam et al.

(1974b); Pfaller et al.

(2006) 

Candida scottii Diddens 

& Lodder 

(Saccharomycetes: 

Saccharomycetales) (= 

Leucosporidium scottii

Fell et al.) 

 AU, US Yes Cooke (1970); 

Gilliam et al.

(1974b); NITE 

(2004) 

Candida tenuis Diddens 

& Lodder 

(Saccharomycetes: 

Saccharomycetales) 

 AU, US No Yes Barker et al. (1984); 

Cooke (1970); 

Gilliam et al. (1974b) 

Candida tropicalis

(Castell.) Berkhout 

(Saccharomycetes: 

Saccharomycetales) 

 AU, US No Yes Chen et al. (2008); 

Gilliam et al.

(1974b); Vogel et al.

(2007) 

Chaetomium globosum

Kunze:Fr. (Ascomycetes: 

Sordariales) 

 AU, US No Yes Farr et al. (2006); 

Gilliam & Prest 

(1987); Greaves 

(1972) 
11

Species 

Common 

Name or 

Condition 

Geographic 

Distribution1 

Quarantine 

Pest2 

Likely to 

Follow 

Pathway3 References 

Cladosporium 

cladosporioides (Fresen.) 

De Vries (Ascomycetes: 

Mycosphaerellales) 

 AU, US No Yes Farr et al. (2006); 

Gilliam et al. (1974a) 

Cryptococcus albidus

(Saito) Skinner 

(Basidiomycetes: 

Filobasidiales) 

 AU, US No Yes Gilliam et al. (1977); 

Roostita & Fleet 

(1996) 

Curvularia brachyspora

Boedijn (Ascomycetes: 

Pleosporales) 

 AU, US No Yes Farr et al. (2006); 

Gilliam et al. (1974a) 

Debaryomyces hansenii

(Zopf) Lodder & Kreger 

(Saccharomycetes: 

Saccharomycetales) 

 AU, US No Yes Gilliam et al.

(1974b); Nout et al.

(1997); Roostita & 

Fleet (1996) 

Eurotium amstelodami

Mangin (= Aspergillus 

amstelodami Thom & 

Church) (Ascomycetes: 

Eurotiales) 

 AU, US No Yes Farr et al. (2006); 

Gilliam & Prest 

(1972); Hill et al.

(1995) 

Kloeckera apiculata

(Reess) Janke (= 

Saccharomyces 

apiculatus Reess) 

(Saccharomycetes: 

Saccharomycetales) 

 AU, US No Yes Drysdale & Fleet 

(1989); Gilliam et al.

(1974b); Kirk 

(2004d); Michailides

et al. (2004) 

Mucor hiemalis Wehmer 

(Zygomycetes: 

Mucorales) 

 AU, US No Yes Farr et al. (2006); 

Gilliam & 

Vandenberg (1997); 

Shipton et al. (1981) 

Nosema apis Zander 

(Microsporidia: 

Apansporoblastina)40 

Nosema 

disease 

AU, US No Yes Matheson (1993) 

Nosema ceranae Fries et

al. (Microsporidia: 

Apansporoblastina)40

 AU, US No Yes Cox-Foster et al.

(2007); Klee et al.

(2007) 

Paecilomyces lilacinus

(Thom) Samson 

(Ascomycetes: 

Eurotiales) 

 AU, US No Yes Gilliam et al. (1977); 

Park et al. (2004) 

Penicillium 

aurantiogriseum Dierckx 

(= P. cyclopium

Westling, P. 

lanosocoeruleum Thom) 

(Ascomycetes: 

Eurotiales) 

 AU, US No Yes Gilliam & Prest 

(1987); Gilliam et al.

(1977); Hill et al.

(1995); Kirk (2004e) 
12

Species 

Common 

Name or 

Condition 

Geographic 

Distribution1 

Quarantine 

Pest2 

Likely to 

Follow 

Pathway3 References 

Penicillium 

brevicompactum Dierckx 

(Ascomycetes: 

Eurotiales) 

 AU, US No Yes Andrews et al.

(1997); Gilliam et al.

(1977) 

Penicillium citrinum

Thom (Ascomycetes: 

Eurotiales) 

 AU, US No Yes Gilliam & Prest 

(1977); Phillott & 

Elsmore (2004) 

Penicillium corylophilum

Dierckx (Ascomycetes: 

Eurotiales) 

 AU, US No Yes Farr et al. (2006); 

Gilliam & Prest 

(1987) 

Penicillium funiculosum

Thom (Ascomycetes: 

Eurotiales) 

 AU, US No Yes Farr et al. (2006); 

Prest et al. (1974) 

Penicillium glabrum

(Wehmer) Westling (= P. 

frequentans Westling) 

(Ascomycetes: 

Eurotiales) 

 AU, US No Yes Farr et al. (2006); 

Gilliam & Prest 

(1972) 

Penicillium griseofulvum

Dierckx (= P. urticae

Bainier) (Ascomycetes: 

Eurotiales) 

 AU, US No Yes Farr et al. (2006); 

Gilliam & Prest 

(1987); Wakelin et 

al. (2004) 

Rhizopus arrhizus Fisch. 

(Zygomycetes: 

Mucorales) 

 AU, US No Yes Farr et al. (2006); 

Gilliam et al. (1974a) 

Rhizopus stolonifer

(Ehrenb.:Fr.) Vuill. 

(Zygomycetes: 

Mucorales) 

 AU, US No Yes Farr et al. (2006); 

Gilliam et al. (1977) 

Rhodotorula glutinis

(Fresen.) Harrison 

(Urediniomycetes: 

Sporidiales) 

 AU, US No Yes Farr et al. (2006); 

Gilliam et al. (1974b) 

Rhodotorula rubra 

(Demme) Lodder (= R.

mucilaginosa [Jörg.] 

Harrison) 

(Urediniomycetes: 

Sporidiales) 

 AU, US No Yes Farr et al. (2006); 

Gilliam et al.

(1974b); Schabrun et 

al. (2006) 

Saccharomyces 

cerevisiae Meyen ex 

Hansen 

(Saccharomycetes: 

Saccharomycetales) 

 AU, US No Yes Dupin et al. (2000); 

Farr et al. (2006); 

Gilliam et al. (1974b) 
13

Species 

Common 

Name or 

Condition 

Geographic 

Distribution1 

Quarantine 

Pest2 

Likely to 

Follow 

Pathway3 References 

Scopulariopsis 

brevicaulis (Sacc.) 

Bainier (Ascomycetes: 

Microascales) 

Yellow 

brood, 

black brood 

AU, US No Yes Farr et al. (2006); 

Gilliam & 

Vandenberg (1997); 

Rowbottom (1983) 

Trichoderma viride Pers. 

(= T. lignorum [Tode] 

Harz) (Ascomycetes: 

Hypocreales) 

 AU, US No Yes Farr et al. (2006); 

Gilliam & 

Vandenberg (1997) 

Yarrowia lipolytica

(Wick. et al.) Van der 

Walt & Arx (= 

Saccharomycopsis 

lipolytica [Wick. et al.] 

Yarrow) (Ascomycetes) 

 AU, US No Yes Bailey & Ball (1991); 

Ismail et al. (2000); 

Kirk (2004a); Ross et 

al. (2000) 

Zygosaccharomyces 

rouxii (Boutroux) Yarrow 

(= Saccharomyces rouxii

Boutroux) 

(Saccharomycetes: 

Saccharomycetales) 

 AU, US No Yes Gilliam et al.

(1974b); Kirk 

(2004c); Praphailong 

& Fleet (1997); Saha

et al. (2007) 

PROTOZOA 

Crithidia mellificae

Langridge & McGhee 

(Kinetoplastida) 

 AU, US41 No Yes Langridge & 

McGhee (1967) 

Malpighamoeba 

mellificae Prell 

(Amoebida) 

Amoeba 

disease 

AU, US No Yes Matheson (1993) 

1

Distribution: AU = Australia, US = United States 

2

Organisms listed at the level of genus, although regarded as quarantine pests because of their uncertain identity, are 

not considered for further analysis as their identity is not defined clearly enough to ensure that the risk assessment 

is performed on a distinct organism (IPPC, 2004). 3

The pathway comprises consignments of package bees and queens imported from Australia. 

4

Species is a scavenger, with only a facultative association with honey bee colonies (Eickwort, 1988). 5

Species is an obligate scavenger of hive detritus (Delfinado-Baker & Baker, 1987; Eickwort, 1988). 6

Species of Tyrophagus tend to be scavengers, with only a facultative association with honey bee colonies 

(Eickwort, 1988). Collection records for T. communis indicate no association with bees themselves (Fan & Zhang, 

2007). 7

Specimens were said to have been “washed off bee” (Fan & Zhang, 2007, p. 61). 8

Pest is non-actionable (AQAS, 2009). 

9

Specimens were collected from “washings off bees” (Fan & Zhang, 2007, p. 66). 10Occurs only in Hawaii (Daly & Coville, 1982). 

11Species is phoretic on adult honey bees (Eickwort, 1988, 1997), and thus has the potential to accompany 

commercial bee consignments. 12Association with honey bees apparently is rare. Seeman (1996) reported finding only one mite in a collection of 51 

bees foraging at flowers. The mite is not considered likely to be present in consignments of bees from Australia. 13Species of Neocypholaelaps are pollen feeders (De Jong et al., 1982; Eickwort, 1997), and exhibit only a 

facultative association with honey bee colonies (Eickwort, 1988). 14Species commonly is found associated with stored products (Halliday et al., 1998), and is incidental to honey bee 

colonies (Eickwort, 1988). 
14

15Species commonly is found associated with stored products (Halliday et al., 1998), where it may be predaceous on 

eggs and larvae of stored-products pests (Riudavets et al., 2002; Nielsen, 2003), and is incidental to honey bee 

colonies (Eickwort, 1988). 16Species commonly is found in association with soil, stored products, and decomposing organic matter (Halliday et 

al., 1998), and is incidental to honey bee colonies (Eickwort, 1988). 17Species is predaceous on other mites (Žďárková et al., 2003), and has only a facultative association with honey bee 

colonies (Eickwort, 1988). 18Association with honey bees is accidental, the mites becoming caught in the body hairs of bees as they forage at 

flowers (Waite, 1999). 19Species feeds on stored pollen (Barreto et al., 2004). 20Species is associated with decomposing organic matter (Błoszyk et al., 2005), and is only incidental to honey bee 

colonies (Eickwort, 1988). 21Species is associated with decomposing organic matter (Rueda & Axtell, 1997; Błoszyk et al., 2005), and is only 

incidental to honey bee colonies (Eickwort, 1988). 22Incidental to honey bee colonies (Eickwort, 1988). Species of Pyemotes feed on eggs, larvae, and pupae of insects 

(Van Laere & Van Daele, 1981), and are unlikely to occur in consignments of adult bees. 23Reported to infest chalkbrood mummies (Caron, 1997), but not associated with adult bees. 24Interstate movement of honey bees into Hawaii is prohibited to prevent introduction of this pest (7 CFR §322.2). 25Larvae tunnel through comb, and are not obligately associated with adult bees (Stedman, 2006). Adults and larvae 

occasionally have been intercepted in low numbers at U.S. ports in packages of bees from Australia (USDAAPHIS, PPQ records). 26Species is saprophagous (Šefrová & Laštůvka, 2005), probably feeding on stored hive products. 27Species attacks comb (Caron, 1997), and is not associated with adult bees. 28Species was introduced into Australia, but apparently failed to become established (Edwards, 2007). 29Reported to consume honey in hives (Caron, 1997). 

30Found only in Tasmania (Goodman & Kaczynski, 2008). 

31Larvae infest honeycomb (Sammataro, 1997). 

32Pest is under official control (R. Martin, Biosecurity Australia, in litt., November 28, 2008). 33Species is reported to parasitize honey bee brood or queen pupae (Fell, 1997), but is considered unlikely to be 

associated with adult bees. 34Species is a general predator, and only incidental to honey bee colonies (Fell, 1997). 35Species is reported to enter or nest in honey bee colonies (Fell, 1997), but is considered unlikely to accompany 

consignments of worker or queen bees. 36Larvae infest comb (Shimanuki & Knox, 2000). 

37Species feeds on fungi and dead organic matter (Hall, 1988), and is incidental to honey bee colonies. 38Record of occurrence in the United States is erroneous (J. Pettis, J. Evans, and Y. Chen, USDA-ARS Bee Research 

Laboratory, in litt., October 8, 2009). 39Fungus is apathogenic, saprophytic in stored pollen and honey (Anderson & Gibson, 1998). 

40Although traditionally classified as a protozoan, recent studies suggest that Nosema spp. and other Microsporidia 

should be placed in Fungi or in a closely related group (Hirt et al., 1999; Arisue et al., 2002). 41Species recently has been found to be established in the United States (J. Pettis, J. Evans, and Y. Chen, USDAARS Bee Research Laboratory, in litt., October 8, 2009).

Risk Assessment 

Release Assessment 

This step consists of describing the biological pathway or pathways necessary for an importation 

to “release” (i.e., introduce) pestiferous agents into the United States, and estimating the 

probability of that occurring (OIE, 2009). 
15

Tyrophagus spp. 

Species of Tyrophagus commonly are found infesting stored food products (Smiley, 1987). 

Many are associates of various insect species or inhabitants of the nests of vertebrates (Fan & 

Zhang, 2007). Some occur as scavengers in honey bee nests (Eickwort, 1988). Association with 

other animals appears largely to be casual, the mites living and feeding in detritis and dead 

organic matter. However, in preparing their treatise of the Tyrophagus species of Australasia, 

Fan & Zhang (2007) examined specimens of T. curvipenis Fain & Fauvel and T. vanheurni

Oudemans, which had been collected from the bodies of living adult honey bees in New Zealand. 

Some species of Tyrophagus (e.g., T. formicetorum Volgin, T. longior [Gervais]) are known to 

have phoretic relationships with insects (Binns, 1982; Houck & OConnor, 1991). The intimate 

association of T. curvipenis and T. vanheurni with bees suggests that the mites could have a high 

probability of accompanying bee consignments from Australia imported into the United States. 

Afrocypholaelaps africana

Several species of Ameroseiidae also are known to be phoretic on honey bee workers, thus 

aiding their efficient dispersal among flowers (Eickwort, 1997). Seeman & Walter (1995) 

reported that Afrocypholaelaps africana (Evans) was common on honey bees foraging at flowers 

in Australia. A majority of the mites remained with bees even after immersion in alcohol, 

indicating that they are not readily dislodged from their places of attachment. As this mite 

commonly attaches itself to adult bees, there is a significant chance that it will accompany 

consignments of bees imported from Australia. 

Senotainia tricuspis

Senotainia tricuspis (Meigen) is a common endoparasite of adult honey bees, particularly in 

warm regions, such as southern Europe (Hamida, 1999). It also has been reported from Australia 

(Bailey & Ball, 1991). Females larviposit on foraging workers and drones (Hamida, 1999). 

Larvae then penetrate the body through the membrane between head and thorax. Parasitization 

rates of up to 25-40% have been recorded (Mathis, 1975; Bailey & Ball, 1991). Because it 

parasitizes adult worker bees, and may be quite common where it occurs (e.g., Liakos et al., 

1994; Piazza & Marinelli, 2000), S. tricuspis has the potential to accompany bee consignments 

from Australia. 

Viruses 

Anderson (1993) detected bee virus F in adult drones collected from colonies in eastern 

Australia. Bee virus X, chronic bee-paralysis satellite virus, cloudy wing virus, and slow 

paralysis virus also are reported from Australia (DAFF, 2002; Ellis & Munn, 2005). As all of 

these viruses infect adult honey bees (Bailey & Ball, 1991), including, in the case of bee virus F, 

drones, which may be present in packages in significant proportions (Strange et al., 2008), they 

have the potential to be introduced into the United States in consignments of bees from Australia. 
16

Exposure Assessment

This step consists of describing the biological pathway or pathways necessary for an importation 

to expose susceptible populations in the importing country to the hazards (bee parasites and 

pathogens) released from a given risk source, and estimating the probability that exposure will 

occur (OIE, 2009). 

An intimate association with adult honey bees has been reported for all of the organisms. 

Tyrophagus curvipenis and T. vanheurni were collected in washings off bees (presumably 

workers) in the course of surveillance activities by government inspectors in New Zealand (Fan 

& Zhang, 2007). Afrocypholaelaps africana attaches itself externally to the bodies of bees 

(Seeman & Walter, 1995), and individual bees may host large numbers of the mite (Halliday, 

1997). Senotainia tricuspis and the viruses are internal parasites of bees (Bailey & Ball, 1991). 

Package bees, which are used by beekeepers as starter colonies (Morse, 1975), are introduced 

directly into empty hives in established apiaries (bee yards). As “drifting” of honey bee workers 

among different colonies is a common occurrence (Winston, 1987), neighboring colonies 

potentially are exposed immediately to the newcomers and any pathogens or parasites they may 

harbor. Migratory beekeeping could disperse these organisms over much broader geographic 

areas. There thus could be a high probability of their encountering and establishing themselves in 

honey bee colonies in the United States. 

Consequence Assessment

Consequence assessment consists of describing the relationship between specified exposures to a 

biological agent and the consequences of those exposures (OIE, 2009). A causal process must 

exist, by which exposures produce adverse health or environmental consequences, which may in 

turn lead to economic consequences. Consequence assessment involves describing the potential 

consequences of a given exposure, and estimating the probability of their occurring. 

Tyrophagus spp. 

The genus Tyrophagus comprises a group of primarily fungivorous mites, commonly found in 

stored food products and decaying organic matter; some are facultatively phytophagous (Fan & 

Zhang, 2007). They are the most economically important mites found in stored food products. 

Tyrophagus curvipenis was reported to feed on algae and pollen (Fain & Fauvel, 1993) and on a 

wide variety of other plant and animal materials (Fan & Zhang, 2007). Nothing is known of the 

species’ economic importance (Zhang, 2003). The habitats and hosts of T. vanheurni also 

comprise a variety of plant and animal materials, including stored products (Fan & Zhang, 2007). 

However, the available, published information gives no indication that these two species are of 

any economic or environmental significance, particularly in their potential impacts on honey bee 

populations. 

Afrocypholaelaps africana

Little is known about species of Afrocypholaelaps (Seeman & Walter, 1995). They are 

principally flower-feeding mites (Eickwort, 1994) and are considered non-parasitic (Sammataro
17

et al., 2000), although they may affect to some degree the normal pollen and nectar collecting 

capacity of bees (Putatunda & Abrol, 2003). There is no evidence that A. africana is of any 

economic or environmental significance. 

Senotainia tricuspis

There are conflicting reports regarding the damage to honey bee colonies caused by this parasite, 

some sources claiming high mortality in populations, others reporting no appreciable damage in 

colonies parasitized at similar rates (Bailey & Ball, 1991). Pinzauti & Santini (1995) reported 

widespread, heavy summer losses to colonies. In discussing control of the fly, Piazza & 

Marinelli (2000) indicated that infestations are of some economic significance. However, 

infestations tend to be episodic and at low levels (e.g., Orantes Bermejo et al., 1996). Even high 

rates of parasitization, in the absence of other parasitic or pathogenic agents, were not considered 

to be significant contributors to colony losses (Piazza et al., 2001). Under normal conditions, 

infestations are not considered to affect seriously the overall health of colonies (Liakos et al., 

1994). The weight of evidence suggests that, generally, S. tricuspis is of little economic 

significance. 

Viruses 

Bee virus X significantly shortens the lives of infected bees, and is most prevalent during winter, 

when increased mortality may cause colonies to dwindle and die (Allen & Ball, 1996; Ball & 

Bailey, 1997). Virulence of cloudy wing virus was deemed by Brown & Fries (2008) to be 

severe; bees infected with the virus die quickly (Bailey & Ball, 1991). The virus has been 

implicated as a contributor to colony death in New Zealand (Todd et al., 2007) and Britain 

(Allen & Ball, 1996). Slow paralysis virus causes mortality in adult bees and brood in colonies 

infested with varroa mite, Varroa destructor Anderson & Trueman (Allen & Ball, 1996). It was 

suggested as a possible cause of some of the many unexplained losses of bees (Bailey & Woods, 

1974). The combination of viral infection and mite infestation may result in colony death 

(Aubert, 2008b). No information is available concerning the pathogenicity of bee virus F. As 

many of the known bee viruses cause severe and often fatal diseases (Ball & Bailey, 1997), this 

virus is considered a potential threat to the U.S. honey bee population. Chronic bee-paralysis 

satellite virus depends on chronic paralysis virus for its replication (Allen & Ball, 1996). Since it 

interferes with the multiplication of chronic paralysis virus, it may help protect colonies from the 

effects of the latter virus. It therefore appears to have little, if any, negative impact on bees. 

Risk Estimation

Risk estimation consists of integrating the results from the release, exposure, and consequence 

assessments to produce an estimate of overall risk associated with the hazards identified at the 

outset (OIE, 2009) (Table 2). Thus, risk estimation takes into account the whole of the risk 

pathway from hazard identified to unwanted outcome. 
18

Table 2. Estimated overall pest risk associated with honey bee imports from Australia. 

Pest 

Release 

Assessment 

Exposure 

Assessment 

Consequence 

Assessment Risk Potential 

Tyrophagus curvipenis Fain & 

Fauvel 

High High Low Low

Tyrophagus vanheurni Oudemans High High Low Low

Afrocypholaelaps africana

(Evans) 

High High Low Low

Senotainia tricuspis (Meigen) High High Low Low

Bee virus F High High High High

Bee virus X High High High High

Chronic bee-paralysis satellite 

virus 

High High Low Low 

Cloudy wing virus High High High High 

Slow paralysis virus High High High High

Conclusions

Among the organisms identified in this document as close associates or pathogens of bees in 

Australia, and not known to occur in the United States, of greatest concern are the viruses. Ellis 

& Munn (2005) suggested that bee viruses may not be as widespread globally as other bee 

pathogens, pests, or parasites. Slow paralysis virus, in particular, appears to have a very limited 

distribution. Since viruses may persist in bees as inapparent infections, which are not readily 

detected, the movement of apparently healthy stocks of bees, as in trade, may introduce viruses 

into new areas (Allen & Ball, 1996). There, they may have a significant, negative impact, solely 

or in combination with other pathogens or parasites, on the resident bee population and on 

beekeeping. For example, viruses that were long considered harmless were found to be 

pathogenic in colonies when associated with infestations of V. destructor (Aubert, 2008a). That 

author concluded (p. 5) that “the increasing prevalence of bee diseases—with a significant role 

of bee viruses—contributes to the current decline in honey bee populations.” Recent work has 

suggested a link between colony collapse disorder and increased prevalence of viral infection in 

colonies (Johnson et al., 2009; vanEngelsdorp et al., 2009). Bee virus F, bee virus X, cloudy 

wing virus, and slow paralysis virus are considered to present a high risk to the U.S. honey bee 

population, such that zoosanitary measures may be required to minimize the probability of their 

introduction in commercial consignments of bees from Australia. 

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