# Evaluation of Pest Risks Associated with Importation of Honey Bees ( Apis mellifera L.) from Australia

T.W. Culliney United States Departm ent of Agriculture Animal and Plant Health Inspection Service Plant Protection and Quarantine Center for Plant Health Science and Technology Plant Epidemiology an d Risk Analysis Laboratory 1730 Varsity Drive, Suite 300 Raleigh, North Carolina 27606

November 12, 2009Introduction

In March 2002, the United States Department of Agriculture’s Animal and Plant Health Inspection Service issued a report assessing the risks of pest intr oduction 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 work ers, 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 wh ich also occur in the United States. The risk assessment concluded that there were no quarantine-si gnificant honey bee pathogens or pests occurring in Australia.

In the seven years since completion of the risk a ssessment for Australian bees, new threats to the U.S. honey bee population have emerged. One of th e most prominent of these is the so-called colony collapse disorder, a mysterious syndrome characterized by the abr upt disappearance of a colony’s adult worker bee popula tion, leaving a substa ntial 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 moth s) and robbing of hive stores by neighboring colonies (vanEngelsdorp et al. , 2009). A link between the disord er, first reported in the United States in 2006, and honey bee imports from Austra lia (which began in 20 05) has been suggested (Cox-Foster et al. , 2007). The May 2007 discovery of co lonies of the Asiatic honey bee, Apis

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

., February 13, 2009), has raised concerns that e xotic 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 e xotic bee pests to be introduced into the United States from Canada, which has imported queens and packag e bees from Australia since 1973 (Wehling, 2002). These developments suggest a need to re-e valuate the risks involved in importation of bees from Australia, as well as other foreign countries. This doc ument re-examines potential pest risks involved in the importation of honey bees from Australia.

Hazard Identification

Hazard identification is an essent ial step, necessarily preceding risk assessment (OIE, 2009). It
involves the identification of th e pestiferous agents (e.g., paras ites, pathogens), the introduction of which potentially could produce adverse conseque nces. The risk assessment is concluded if
hazard identification fails to identify potential hazards.

Pest Categorization—Identificat ion 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 Austra lia, but are not known to be established in the United States, and have the potenti al to be introduced into the United States in consignments of imported honey bees. Two organisms were not de termined to species, and thus were not amenable to risk assessment (IPPC, 2004).2 Table 1. Organisms associated or poten tially associated with honey bees ( Apis mellifera L.) in
Australia.

Species Common
Name or
Condition Geographic
Distribution 1 Quarantine

Pest 2 Likely to
Follow Pathway 3 References
ARTHROPODS
ACARI
Acaridae

Acarus siro L. (= Tyroglyphus farinae [De Geer]) House dust mite, flour
mite AU, US No No 4 Baker et al. (1976); CABI (2007); Eickwort (1988);
Shanahan & Shelton (1948) Forcellinia galleriella Womersley House dust
mite AU Yes No 5 Eickwort (1988); Womersley (1963) Tyrolichus casei (Oudemans) Cheese mite AU, US No No 4 CSIRO (2005); Eickwort (1988); Krantz (1955) Tyrophagus communis Fan & Zhang AU, US No No 6 Fan & Zhang (2007)

Tyrophagus curvipenis
Fain & Fauvel AU Yes Yes 7, 8 Fan & Zhang (2007)

Tyrophagus longior (Gervais) Seed mite AU, US No No 4 Eickwort (1988); Fan & Zhang (2007) Tyrophagus putrescentiae (Schrank) House dust mite, mold
mite AU, US No No 4 Eickwort (1988); Fan & Zhang (2007)

Tyrophagus vanheurni
Oudemans AU Yes Yes 9 Fan & Zhang (2007)

Ameroseiidae Afrocypholaelaps africana (Evans) AU, US 10 Yes Yes 11 Eickwort (1988); Halliday (1997) Hattena panopla
Domrow AU Yes No 12 Seeman (1996)

Neocypholaelaps sp. AU Yes No 13 Brimblecombe & Roff (1960)
Ascidae

Blattisocius dentriticus (Berlese) House dust
mite AU, US No No 14 Eickwort (1988); Halliday et al. (1998); Yoshikawa & Bennett (1979)

Blattisocius tarsalis (Berlese) House dust
mite AU, US No No 15 Eickwort (1988); Hagstrum & Sharp (1975); Halliday et al. (1998) Proctolaelaps pygmaeus (Müller) AU, US No No 16 Eickwort (1988); Halliday et al. (1998); Minor & Norton (2004)3 Species Common
Name or
Condition Geographic
Distribution 1 Quarantine

Pest 2 Likely to
Follow Pathway 3 References Cheyletidae Cheyletus eruditus (Schrank) House dust
mite AU, US No No 17 AFD (2007); Custer & Pence (1979); Eickwort (1988) Eriophyidae
Aceria litchii (Keifer) Lychee
erinose mite AU Yes No 18 Waite (1999)

Glycyphagidae Glycyphagus domesticus (De Geer) House dust mite, cheese
mite AU, US No No 4 Dicke et al. (1953); Eickwort (1988);
Shanahan & Shelton (1948) Laelapidae Melittiphis alvearius (Berlese) Pollen mite AU, US No No 19 Delfinado-Baker (1994); Knihinicki & Halliday (1995)
Macrochelidae Macrocheles glaber (Müller) AU, US No No 20 Eickwort (1988); Halliday (2000)

Macrocheles
muscaedomesticae (Scopoli) AU, US No No 21 Eickwort (1988); Halliday (2000);
Rueda & Axtell (1997) Pyemotidae Pyemotes ventricosus (Newport) Grain itch
mite AU, US No No 22 Betz et al. (1982);
Brimblecombe & Roff (1960); Eickwort (1988) Pyroglyphidae Dermatophagoides pteronyssinus (Trouessart) House dust
mite AU, US No No 4 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 No 23 Caron (1997);
Lawrence & Britton (1991); Philips (2002)4 Species Common
Name or
Condition Geographic
Distribution 1 Quarantine

Pest 2 Likely to
Follow Pathway 3 References
Nitidulidae
Aethina tumida Murray Small hive
beetle AU, US No 24 No 25 Neumann & Elzen (2004)
Ptinidae
Ptinus exulans Erichson AU Yes No 26 Caron (1997) Ptinus fur(L.) Whitemarked spider
beetle AU, US No No 27 Caron (1997); Rees (2004)

Scarabaeidae Copris lunaris L. AU 28 Yes No 29 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 No 31 Sammataro (1997)

HYMENOPTERA Apidae Apis cerana F. Indian honey bee,
Asiatic honey bee,
eastern hive
bee AU Yes No 32 Anonymous (2009)

Eulophidae

Melittobia acasta (Walker) AU, US No No 33 Fell (1997); González
et al. (2004)
Formicidae Linepithema humile (Mayr) Argentine

ant AU, US No No 34 Fell (1997)

Monomorium destructor (Jerdon) Singapore

ant AU, US No No 35 Eisner et al. (1996); Fell (1997);
Hoffmann et al. (1999)5 Species Common
Name or
Condition Geographic
Distribution 1 Quarantine

Pest 2 Likely to
Follow Pathway 3 References Monomorium pharaonis (L.) Pharaoh ant AU, US No No 35 Fell (1997);
Hoffmann et al. (1999) Pheidole megacephala (F.) Bigheaded

ant AU, US No No 35 Fell (1997);
Hoffmann et al. (1999); Warner & Scheffrahn (2007) Solenopsis invicta Buren Red imported
fire ant AU, US No No 35 Dominiak et al. (2005); Fell (1997)

LEPIDOPTERA Pyralidae Achroia grisella (F.) Lesser wax
moth AU, US No No 36 Common (1990); Zhang (1994) Ephestia kuehniella Zeller (= Anagasta
kuehniella [Zeller]) Mill moth AU, US No No 36 CABI (2007);
Shimanuki & Knox (2000); Steidle et al. (2001)
Galleria mellonella (L.) Greater wax
moth AU, US No No 36 Common (1990); Williams (1997)
PSOCOPTERA Trogiidae Trogium pulsatorium (L.) Pollen louse AU, US No No 37 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 Yes 38 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
Distribution 1 Quarantine

Pest 2 Likely to
Follow Pathway 3 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
Distribution 1 Quarantine

Pest 2 Likely to
Follow Pathway 3 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
Distribution 1 Quarantine

Pest 2 Likely to
Follow Pathway 3 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 No 39 Anderson et al. (1998) Ascosphaera duoformis
Anderson & Gibson (Ascomycetes) AU Yes No 39 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
Distribution 1 Quarantine

Pest 2 Likely to
Follow Pathway 3 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
Distribution 1 Quarantine

Pest 2 Likely to
Follow Pathway 3 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
Distribution 1 Quarantine

Pest 2 Likely to
Follow Pathway 3 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
Distribution 1 Quarantine

Pest 2 Likely to
Follow Pathway 3 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
Distribution 1 Quarantine

Pest 2 Likely to
Follow Pathway 3 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, US 41 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 asso ciation with honey bee colo nies (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 be es themselves (Fan & Zhang, 2007).

7 Specimens were said to have been “washe d 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).

10 Occurs only in Hawaii (Daly & Coville, 1982).

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

commercial bee consignments.

12 Association with honey bees apparently is rare. Seeman (1 996) 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.

13 Species of Neocypholaelaps are pollen feeders (De Jong et al. , 1982; Eickwort, 1997), and exhibit only a

facultative association with honey bee colonies (Eickwort, 1988).

14 Species commonly is found associated with stored products (Halliday et al. , 1998), and is incidental to honey bee colonies (Eickwort, 1988).14 15 Species 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).

16 Species commonly is found in association with soil, stor ed products, and decomposing organic matter (Halliday et

al. , 1998), and is incidental to honey bee colonies (Eickwort, 1988).

17 Species is predaceous on other mites (Ž ď árková et al. , 2003), and has only a facultative association with honey bee

colonies (Eickwort, 1988).

18 Association with honey bees is accidental, the mites becomi ng caught in the body hairs of bees as they forage at

flowers (Waite, 1999).

19 Species feeds on stored pollen (Barreto et al. , 2004).

20 Species is associated with decomposing organic matter (B ł oszyk et al. , 2005), and is only incidental to honey bee colonies (Eickwort, 1988).

21 Species is associated with decomposing organic matter (Rueda & Axtell, 1997; B ł oszyk et al. , 2005), and is only incidental to honey bee colonies (Eickwort, 1988).

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

(Van Laere & Van Daele, 1981), and are unlikel y to occur in consignments of adult bees.

23 Reported to infest chalkbrood mummies (Caron, 1997), but not associat ed with adult bees.

24 Interstate movement of honey bees into Hawaii is prohibite d to prevent introduction of this pest (7 CFR §322.2).

25 Larvae tunnel through comb, and are no t obligately associated w ith adult bees (Stedman, 2006). Adults and larvae

occasionally have been intercepted in low numbers at U.S. ports in packages ofbees from Australia (USDAAPHIS, PPQ records).

26 Species is saprophagous (Šefrová & Lašt ů vka, 2005), probably feeding on stored hive products.

27 Species attacks comb (Caron, 1997), and is not associated with adult bees.

28 Species was introduced into Australia, but apparen tly failed to become established (Edwards, 2007).

29 Reported to consume honey in hives (Caron, 1997).

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

31 Larvae infest honeycomb (Sammataro, 1997).

32 Pest is under official control (R. Martin, Biosecurity Australia, in litt ., November 28, 2008).

33 Species is reported to parasitize honey bee brood or queen pupae (Fell, 1997), but is considered unlikely to be

associated with adult bees.

34 Species is a general predator, and only incide ntal to honey bee colonies (Fell, 1997).

35 Species is reported to enter or nest in honey bee coloni es (Fell, 1997), but is cons idered unlikely to accompany

consignments of worker or queen bees.

36 Larvae infest comb (Shimanuki & Knox, 2000).

37 Species feeds on fungi and dead organic matter (Hall, 1988), and is incidental to honey bee colonies.

38 Record 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).

39 Fungus is apathogenic, saprophytic in stored pollen and honey (Anderson & Gibson, 1998).

40 Although 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).

41 Species recently has been found to be established in th e 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 st ored 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, 1 988). Association with other animals appears largely to be casual, th e 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 (B inns, 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 Ameroseiid ae also are known to be phoretic on honey bee workers, thus aiding their efficient dispersa l among flowers (Eickwort, 1997). Seeman & Walter (1995) reported that Afrocypholaelaps africana (Evans) was common on honey b ees foraging at flowers in Australia. A majority of the mites remained with bees even after immersion in alcohol, indicating that they are not read ily 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 th e body through the membrane between head and thorax. Parasitization rates of up to 25-40% have been recorded (M athis, 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-paralysi s satellite virus, cloudy wing virus, and slow paralysis virus also are reported from Austra lia (DAFF, 2002; Ellis & Munn, 2005). As all of these viruses infect adult honey b ees (Bailey & Ball, 1991), including, in the case of bee virus F, drones, which may be present in packag es 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 impor ting country to the haza rds (bee parasites and pathogens) released from a given risk source, a nd estimating the probability that exposure will occur (OIE, 2009).

An intimate association with a dult 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 activitie s 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 para sites of bees (Bailey & Ball, 1991). Package bees, which are used by beekeepers as starter colonies (Morse, 1975), are introduced directly into empty hives in es tablished apiaries (bee yards). As “drifting” of honey bee workers among different colonies is a common occu rrence (Winston, 1987), ne ighboring colonies potentially are exposed immediatel y to the newcomers and any pat hogens or parasites they may harbor. Migratory beekeeping c ould disperse these organisms over much broader geographic areas. There thus could be a high probability of their encountering and esta blishing themselves in honey bee colonies in the United States.

Consequence Assessment

Consequence assessment consists of describing th e relationship between specified exposures to a biological agent and the consequences of thos e 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. Conseque nce assessment involves describing the potential consequences of a given exposure, and estim ating the probability of their occurring.

Tyrophagus spp.

The genus Tyrophagus comprises a group of primarily f ungivorous mites, commonly found in stored food products and decaying organic matter; some are facultatively phytophagous (Fan & Zhang, 2007). They are the most economically im portant 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 materi als (Fan & Zhang, 2007). No thing is known of the species’ economic importance (Zhan g, 2003). The habitats and hosts of T

. vanheurni also comprise a variety of plant and animal material s, including stored pr oducts (Fan & Zhang, 2007). However, the available, published information gi ves no indication that th ese two species are of any economic or environmental significance, partic ularly in their potent ial 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 consid ered non-parasitic (Sammataro17 et al. , 2000), although they may affect to some de gree the normal pollen and nectar collecting capacity of bees (Putatunda & Abro l, 2003). There is no evidence that A

. africana is of any economic or environmental significance.

Senotainia tricuspis

There are conflicting reports rega rding the damage to honey bee co lonies caused by this parasite, some sources claiming high mortality in populati ons, others reporting no a ppreciable damage in colonies parasitized at similar rates (Baile y & 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 pa thogenic agents, were not considered to be significant contribu tors to colony losses (Piazza et al. , 2001). Under normal conditions,
infestations are not considered to affect se riously 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 wa s deemed by Brown & Fries (2008) to be severe; bees infected with the virus die qui ckly (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 mo rtality 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 m ite infestation may re sult in colony death (Aubert, 2008b). No information is available con cerning the pathogenicity of bee virus F. As many of the known bee viruses cause severe and of ten fatal diseases (Ba ll & Bailey, 1997), this virus is considered a potential threat to the U.S. honey bee po pulation. Chronic bee-paralysis satellite virus depends on chroni c paralysis virus for its replica tion (Allen & Ball, 1996). Since it interferes with the multiplication of chronic paralysi s 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 inte grating the results fr om 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 estima tion takes into account th e whole of the risk pathway from hazard identified to unwanted outcome.18 Table 2. Estimated overall pest risk associat ed 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 Stat es, 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 viru s, 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 appare ntly 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 pa rasites, on the resident bee population and on beekeeping. For example, viruses that were long considered harmless were found to be pathogenic in colonies when asso ciated with infestations of V

. destructor (Aubert, 2008a). That author concluded (p. 5) that “the increasing pr evalence of bee diseases—with a significant role
of bee viruses—contributes to the current d ecline in honey bee populations.” Recent work has suggested a link between colony coll apse disorder and increased pr evalence 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 vi rus 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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