Honey Bee Bugs

1For a review of chalkbrood and its control see Hornitzky, M (2014). Literature review of chalkbrood: a fungal disease of honeybees NSW Agriculture RIRDC Publication No 01/150 https://www.hgsc.bcm.edu/sites/default/files/images/review_Chalkb.pdf Asc0ophaera apis is also affects bumblebees and at least one species of carpenter bee. The genus including Ascosphaera callicarpa affect a range of bee species.

2Nosema bombi is a parasite of bumblebees.

3Reported to cause colony losses possibly in association with Nosema. The Australasian Beekeeper (2017) 119(5):8-9.

4Affects some species of Bombus and has been occasionally detected in A. mellifera.

5Crithidia bombi is a bumblebee parasite.

6Secondary invaders, putrifying bacteria, have been listed as Achromobacter euridice , Brevibacillus laterosporus, Enterococcus faecalis and Paenibacillus alvei but are not the cause of the disease.

7Burritt N.L., Foss, N.J., Neeno-Eckwall, E.C., Church, J.O., Hilger, A.M., Hildebrand, J.A., Warshauer, D.M., Perna, N.T. and Burritt, J.B. (2016). Sepsis and hemocyte loss in honey bees (Apis mellifera) infected with Serratia marcescens strain sicaria. PLoS ONE 11(12): e0167752. doi:10.1371/journal.pone.0167752 This bacterium is probably transmitted by Varroa destructor.

8An Australian beetle that has not been reported to affect stored beekeeping material in Australia but is causing serious damage in California (Editorial Notes (2017). Australasian Beekeeper 118(8): 341.

9Other known species of Braula not found in Australia and are not considered to be bee parasites are: B. kohli, B. orientalis, B. pretoriensis and B. shmitzi.

10The aphids produce melezitose trisaccharide honeydew sugars from willows and poplars that form a hard candy and that bees cannot metabolise. More a pest than of serious concern though the product uses hive storage space and may be a contributing factor in bees starving.

11Apis andreniformis is mainly sympatric with Apis florea but probably developed allopatrically and their ranges then converged. Together they may harbour a range of bee diseases but do not harbour arachnid mites of concern to A. mellifera. The giant honey bees Apis dorsata and Apis laboriosa, the sources of Tropilaelaps spp., are so closely related that have been recently re-designated as four Apis dorsata subspecies: Apis d. dorsata, Apis d. binghami (Indonesian Honey Bee), A. d. breviligula (Giant Philippine Honey Bee) and A. d. laboriosa (Himalayan Honey Bee). Their biogeographic origins may be important for understanding the importance of Tropilaelaps as a honey bee disease. Relatives of Apis cerana, A. koschevnikovi (Koschevnikov’s Honey Bee of Kalimantan-Sumateran-Peninsular Malaysia) is sympatric with, and closely related to A. cerana while the Philippine honey bees, Apis nuluensis and Apis nigrocincta are all of interest as the Apis cerana group are the original vectors of Varroa. A. koschevnikovi is the vector of Varroa rindereri.

12Some authors are now giving A. cerana indica separate species status. Charles D. Michener (2007) Bees of the World recognises three large groups of related extant species: 1. Small species with single exposed combs; dances on expanded horizontal base of comb: Apis florea Fabricius, Apis andreniformis Smith. 2. Large species with single exposed combs; dance on vertical curtains of bees or on comb: Apis dorsata Fabricius, Apis laboriosa Smith, Apis binghami Cockerell, Apis breviligula Maa. The last two are probably allopatric segregates of A. dorsata and may not represent distinct species. 3. Middle-sized species with multiple combs in cavities; dance on vertical surfaces of combs in the dark: Apis mellifera Linnaeus, Apis cerana Fabricius, Apis koschevnikovi Buttel-Reepen, Apis nigrocincta Smith, Apis nuluensis Tinget, Koeniger and Koeniger. The last two are only recently recognised as specifically distinct from Apis cerana. Damus, M.S and Otis,G.W. A morphometric analysis of Apis cerana F and Apis nigrocincta Smith populations from Southeast Asia. Apidologie 28:309-323. http://www.apidologie.org/articles/apido/abs/1997/04/Apidologie_0044-8435_1997_28_5_ART0007/Apidologie_0044-8435_1997_28_5_ART0007.html and Arias, Mc,, S Tingek, Kelitu, A. and Sheppard, Ws. (1996). Apis nuluensis Tingek, Koeniger and Koeniger, 1996 and its genetic relationship with sympatric species inferred from DNA sequences. https://hal.archives-ouvertes.fr/hal-00891385/document

13Recognised subspecies of Apis dorsata (variously classified as separate species) are A. d. dorsata, A. breviligula, A. d. binghami and A. d. laboriosa.

14Small Hive Beetle may be controlled by Kodamea ohmeri, a fungus symbiotic with SHB, is also a likely pathogen for immunocompromised individuals. Other fungi, Metarhizium anisopliae and Beauveria bassiana show potential for control of larvae of SHB. Leemon, D. (2012). In-hive fungal biocontrol of small hive beetle. RIRDC Publication No. 12/012 https://rirdc.infoservices.com.au/downloads/12-012
SHB is now widespread in Australia but not in Western Australia where it is presently confined to the Kimberley.

15Kwadha, C.A., Ong’amo, G.O., Ndegwa, P.N., Raina, S.K. and Fombong, A.T. (2017). The biology and control of the Greater Wax Moth, Galleria mellonella. Insects, 8, 61, 17pp. doi:10.3390/insects8020061

16Jean-Danie, C. and Imdorf, A. (1999). Protection of honey combs from wax moth damage. American Bee Journal 139:627-630. https://www.researchgate.net/publication/294472170_Protection_of_honey_combs_from_wax_moth_damage?enrichId=rgreq-fcbe3cc54eb76184c7779897abf0a10f-XXX&enrichSource=Y292ZXJQYWdlOzI5NDQ3MjE3MDtBUzozNDA2MTAxODQ2OTU4MjBAMTQ1ODIxOTIwNDk2MA%3D%3D&el=1_x_3&_esc=publicationCoverPdf

17Euvarroa wongsirii and E. sinhai are both parasites of Apis andreniformis. Euvarroa sinhai, but not E. wongsirii, is also a parasitise Apis florea. Euvarroa sinhai is known to have reproduced on Apis mellifera.

18Original Tropilaelaps hosts are the Asian bees Apis dorsata, specifically its subspecies A. d. breviligula and A. d. laboriosa. Tropilaelaps clareae (Philippines and Sulawesi (except Palawan Island), Luzon Island is a parasite of A. cerana, A. dorsata, A. florea , A. d. laboriosa and A. mellifera); Tropilaelaps koenigerum (Asia including Indonesia except Sulawesi) is a parasite of A. d. breviligula. It is now also a parasite of A. dorsata,, A. d. laboriosa, A. mellifera]; Tropilaelaps mercedesae; (Asia except Sulawesi incl. PNG) is a parasite of A. ceranae, A. dorsata, A. d. laboriosa(?), A. mellifera); Tropilaelaps thaii (Vietnam) is a parasite of A. d. laboriosa.

19Varroa species are natural parasites of the Asian honey bee, Apis cerana and its close relatives A. nululensis (or Apis cerana nuluensis), A. nigrocincta and A. koschevnikovi: Varroa destructor (from Apis cerana) appears to have taken 50-100 years to host shift to A. mellifera and has done so at least twice. Varroa jacobsoni (also a parasite of Apis cerana) is widespread but appears to have crossed over to A. mellifera in PNG although this assessment has now been revised [Anderson, D.L. and Trueman, J.W.H. (2000) Varroa jacobsoni (Acari: Varroidae) is more than one species. Experimental and Applied Acarology 24: 165–189.] since V. jacobsoni now represents more than one species and may include a A. mellifera pathogenic halotype of V. destructor. Two of eighteen Varroa destructor halotypes, the common Korean halotype and the less common Japan-Thailand halotype found in this region and in the Americas: Varroa rindereri (host is Apis koschevnikovi) is not known to cross over to other species and was, for a long time, thought to be identical to V. jacobsoni. Varroa underwoodi (host is A. cerana but is also found on Apis nuluensis and Apis nigrocincta) has been found on, but has not reproduced on, A. mellifera in PNG.
Euvarroa species are carried by the dwarf honey bees, Apis florea and A. andreniformis, E. sinhai (host is A. florea) – has been reared on A. mellifera and on A cerana. Euvarroa wongsirii has only been found on Apis andreniformis.

20The key viruses associated with Varroa destructor are DWV, KBV, ABPV, SBPV and IAPV. Martin, S.J. (2001). The role of Varroa and viral pathogens in the collapse of honeybee colonies: a modelling approach. Journal of Applied Ecology 38: 1082-1093. http://onlinelibrary.wiley.com/doi/10.1046/j.1365-2664.2001.00662.x/full. The paralysis viruses are more virulent than more common DWV some forms of which appear to be avirulent.

21Fourteen RNA bee viruses are recorded by Bailey, L. and Ball, B.V. (1991) Honey Bee Pathology 2^nd edn. Academic Press, London, UK. [cited in Martin, S.J. (2001) although another assessment suggests 24 spp http://www.coloss.org/beebook/II/virus/1/1]

22Sometimes associated with chronic paralysis satellite virus (CBPSV) of unknown symptomology.

23Deformed Wing Virus has very closely related viruses: Kakugo Virus, Varroa destructor Virus, and asymptomatic Egypt Bee Virus variously affecting bee temperament and variously associated with and without Varroa destructor. See also https://www.ncbi.nlm.nih.gov/pubmed/21652054 PHA will monitor for two strains of DWV from 2018.

24DWV type A pathogenic and B non pathogenic variants. Mordecai, G.J., Wilfert, L., Martin, S.J. Jones, I.M. and Schroeder, D.C. (2015). Diversity in a honey bee pathogen: first report of a third master variant of the Deformed Wing Virus quasispecies. The ISME Journal 1–10.

25Turns haemolymph milky white but otherwise symptomless.

26Sac Brood Virus is closely related to Thai SacBbrood Virus that adversely affects Apis cerana.

27There are two distinct strains of SBPV. de Miranda, J.R., Dainat, B., Locke, B., Cordoni, G., Berthoud, H., Gauthier, L., Neumann, P., Budge, G.E., Ball, B.V. and Don B. Stoltz, D.B. (2010). Genetic characterization of slow bee paralysis virus of the honeybee (Apis mellifera L.). Journal of General Virology 91:2524–2530. www.nationalbeeunit.com/downloadDocument.cfm?id=954
Slow Bee Paralysis Virus is closely related to Moku Virus. http://www.nature.com/articles/srep34983 PHA is monitoring for two strains of SBPV from 2018.

28ALPV is a virus of pest aphid species that appears to be transmitted to bees through honeydew. ALPV has some affinities with BSRV and BBV and, while numbers in bees build up with honeydew, their impact on bees has not been ascertained though they impact on aphid populations.

29BBV and ABPV occur together and are symptomless.

30BV-X and BV-Y are serologically related viruses that are symptomless in adult bees and do not multiply in honey bee larvae and pupae: BV-X is associated with the winter diarrhorea-inducing protozoan Malpighamoeba mellificae [see protozoan diseases] while BV-Y is associated with Nosema apis.

31Closely related species that are in turn related to CBPV. They are seemingly symptomless and likely related to BV-X and BV-Y. Two other strains of Lake Sinhai Virus have also been isolated.

32Symptoms of AIV are similar to those of CBPV affecting flight in adults.

33Remnant, E.J. (2017). A diverse range of novel RNA viruses in geographically distinct honey bee populations. Journal of Virology 91(16):e00158-17. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5533899/

34Vectored by Varroa.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5732965/