Differential susceptibility across honey bee colonies in larval chalkbrood resistance

Apidologie

Volumn 40, Issue 5, 2009, Pages 524-534

  Jensen, Annette Bruun ^a   Pedersen, Bo Vest ^a   Eilenberg, Jørgen ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Ascosphaera apis; Bioassay; Brood disease; In vitro rearing; Insect pathogen

Indexed keywords

BIOASSAY; BROOD REARING; COLONY; DISEASE RESISTANCE; DOSE-RESPONSE RELATIONSHIP; FUNGAL DISEASE; HONEYBEE; SPORE; SUBSPECIES;

APIS; APIS MELLIFERA; APIS MELLIFERA CARNICA; ASCOSPHAERA APIS; BACTERIA (MICROORGANISMS); FUNGI; HEXAPODA;

EID: 70349637257     PISSN: 00448435     EISSN: 12979678     Source Type: Journal    
DOI: 10.1051/apido/2009029     Document Type: Article

References (45)

1. Alonso J.M., Rey J., Puerta F., Hermoso de Mendosa J., Hermoso de Mendosa M., Flores J.M. (1993) Enzymatic equipment of Ascosphaera apis and the development of infection by this fungus in Apis mellifera, Apidologie 24, 383-390.
2. Aronstein K.A., Murray K.D., De Leon J.H., Qin X., Weinstock G.M. (2007) High mobility group (HMG-box) genes in the honey bee fungal pathogen Ascosphaera apis, Mycologia 99, 553-561.
3. Aupinel P., Fortini D., Dufouri H., Taséi J.-N., Michaud B., Odoux F., Pham-Delègue M.-H. (2005) Improvement of artificial feeding in a standard in vitro method for rearing Apis mellifera larvae, Bull. Insectol. 58, 107-111.
4. Bailey L. (1967) The effect of temperature on the pathogenecity of the fungus Ascosphaera apis for the larvae of the honeybee, Apis mellifera, in: Van der Laan PA (Ed.), Insect Pathology and Microbial Control, North Holland Publishing Co, Amsterdam, The Netherlands, pp. 162-167.
5. Beauvais A., Latgè J.P. (1988) A simple medium for growing entomophthoralean protoplasts, J. Invertebr. Pathol. 51, 175-178.
6. Behrens D., Forsgren E., Fries I., Moritz R.F.A. (2007) Infection of drone larvae (Apis mellifera) with American foulbrood, Apidologie 38, 281-288.
7. Brødsgaard C.F., Ritter W., Hansen H. (1998) Response of in vitro reared honey bee larvae to various doses of Paenibacillus larvae larvae spores, Apidologie 29, 569-578.
8. Chorbiński P. (2004) The development of the infection of Apis mellifera larvae by Ascosphaera apis, Electronic J. Polish Agric. Univ., Vet. Med., 7, #03 [online]. http://www.ejpau.media.pl/volume7/issue2/veterinary/art- 03.html.
9. Cremer S., Armitage S., Schmid-Hempel P. (2007) Social Immunity, Curr. Biol. 17, 693-702.
10. Decanini L.I., Collins A.M., Evans J.D. (2007) Variation and heritability in immune gene expression by diseased honeybees, J. Hered. 98, 195-201.
11. Evans J.D. (2006) Beepath: An ordered quantitative- PCR array for exploring honey bee immunity and diseases, J. Invertebr. Pathol. 93, 135-139.
12. Evans J.D., Pettis J.S. (2005) Colony-level impacts of immune responsiveness in honey bees, Apis mellifera, Evolution 59, 2270-2274.
13. Flores J.M., Ruiz ?.A., Ruz J.M., Puerta F., Bustos M., Padilla F., Campano F. (1996) effect of temperature and humidity of sealed brood on chalkbrood development under controlled conditions, Apidologie 27, 185-192.
14. Franck P., Garnery L., Loiseau A., Oldroyd B.P., Hepburn H.R., Solignac M., Cornuet J.-M. (2001) Genetic diversity of the honeybee in Africa: microsatellite and mitochondrial data, Heredity 86, 420-430.
15. Garnery L., Solignac M., Celebrano G., Cornuet J.- M. (1993) A simple test using restricted PCRamplified mitochondrial DNA to study the genetic structure of Apis mellifera L., Experientia 49, 1016-1021.
16. Gilliam M., Vandenberg J. (1997) Fungi, in: Morse R.A., Flottum K. (Eds), Honey Bee Pests, Predators and Diseases, 3rd ed., The A.I. Root Company,Ohio), pp. 79-112.
17. Gilliam M., Taber S., Lorenz B.J., Prest D.B. (1988) Factors affecting development of chalkbrood disease in colonies of honey bees, Apis mellifera, fed pollen contaminated with Ascosphaera apis, J. lnvertebr. Pathol. 52, 314-325.
18. Genersch E., Ashiralieva A., Fries I. (2005) Strain and genotype-specific differences in virulence of Paenibacillus larvae subsp. larvae, a bacterial pathogen causing American foulbrood disease in honeybees, Appl. Environ. Microbiol. 71, 7551-7555.
19. Glinski Z. (1981) Studies on the effect of the fungus Ascosphaera apis on the larvae of the honey bee, Apis mellifera L., Pol. Archiw. Wet. 23, 9-15.
20. Glinski Z., Buczek K. (2003) Response of Apoidea to fungal infections, Apiacta 38, 183-189.
21. Heath L.A.F., Gaze B.M. (1987) Carbon dioxide activation of spores of the chalkbrood fungus Ascosphaera apis, J. Apic. Res. 26, 243-246.
22. Hughes W.O.H., Boomsma J.J. (2004) Genetic diversity and disease resistance in leaf-cutting ant societies, Evolution 58, 1251-1260.
23. James R.R., Buckner J.S. (2004) Lipids stimulate spore germination in the entomopathogenic ascomycete Ascosphaera aggregata, Mycopathology 158, 293-302.
24. Jensen A.B., Thomsen L., Eilenberg J. (2001) Intraspecific variation and host specificity of Entomophthora muscae s.str. isolates revealed by random amplified polymorphic DNA, universal primed PCR, PCR-restriction fragment length polymorphism, and conidial morphology, J. Invertebr. Pathol. 78, 251-259.
25. Jensen A.B., Palmer K.A., Boomsma J.J., Pedersen B.V. (2005) Varying degrees of Apis mellifera ligustica introgression in protected populations of the black honeybee, Apis mellifera mellifera, in northwest Europe, Mol. Ecol. 14, 93-106.
26. Lunder R. (1972) Undersøkelse av kalkyngel i 1971 [Investigation on chalkbrood in 1971], Birøkteren 88, 55-60.
27. Malone L.A., Stefanovic S. (1999) Comparison of the responses of two races of honeybees to infection with Nosema apis Zander, Apidologie 30, 375-382.
28. McKee B., Goodman R.D., Hornitzky M.A. (2004) The transmission of European foulbrood (Melissococcus plutonius) to artificially reared honey bee larvae (Apis mellifera), J. Apic. Res. 43, 93-100.
29. Naug D., Camazine S. (2002) The role of colony organization on pathogen transmission in social insects, J. Theor. Biol. 215, 427-439.
30. Palmer A.K., Oldroyd B.P (2003) Evidence for intra-colonial genetic variance in resistance to American foulbrood of honey bees (Apis mellifera): Further support for the parasite/pathogen hypothesis for the evolution of polyandry, Naturwissenschaften 90, 265-268.
31. Payton M.E., Greenstone M.H., Schenker N. (2003) Overlapping confidence intervals or standard error intervals: What do they mean in terms of statistical significance? J. Insect Sci. 3, 34.
32. Puerta F., Flores J.M., Bustos M., Pad?lla F., Campano F. (1994) Chalkbrood development in honey brood under controlled conditions, Apidologie 25, 1-7.
33. Robertson J.L., Preisler H.K. (1992) Pesticide Bioassays with Arthropods, CRC Press, Boca Raton.
34. Ruttner F. (1988) Biogeography and taxonomy of honey bees, Springer Verlag, Berlin.
35. Sahinler N., Kurt S. (2004) A study on antifungal activity of formic acid and propolis extract against Chalkbrood disease pathogen Ascosphera apis, J. Anim. Vet. Adv. 3, 554-556.
36. Schmid-Hempel P. (2005) Evolutionary ecology of insect immune defenses, Annu. Rev. Entomol. 50, 529-551.
37. Solorzano C.D., Szalanski A.L., Kence M., McKern J.A., Austin J.W., Kence A. (2009) Phylogeography and population genetics of honey bees (Apis mellifera) from Turkey based on COI-COII sequence data, Sociobiology 53, 1-10.
38. Spiltoir C.F., Olive L.S. (1955) A reclassification of the genus Pericystis Betts, Mycologia 47, 238-244.
39. Starks P.T., Blackie C.A., Seeley T.D. (2000) Fever in honeybee colonies, Naturwissenschaften 87, 229-231.
40. St. Leger R.J., Staples R.C., Roberts D.W. (1993) Entomopathogenic isolates of Metarhizium anisopliae, Beauveria bassiana, and Aspergillus flavus produce multiple extracellular chitinase isozymes, J. Invertebr. Pathol. 61, 81-84.
41. Sučnik S., Kozmus P., Poklukar J., Megliic V. (2004) Molecular characterisation of indigenous Apis mellifera carnica in Slovenia, Apidologie 35, 623-636.
42. Tarpy D.R. (2003) Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth, Proc. R. Soc. Lond. B Biol. Sci. 270, 99-103.
43. Tarpy D.R., Seeley T.D. (2006) Lower disease infections in honeybee (Apis mellifera) colonies headed by polyandrous vs monandrous queens, Naturwissenschaften 93, 195-199.
44. Theantana T., Chantawannakul P. (2008) Protease and beta-N- acetylglucosaminidase of honey bee chalkbrood pathogen Ascosphaera apis, J. Apic. Res. 47, 68-76.
45. Whitfield C.W., Behura S.K., Berlocher S.H., Clark A.G., Johnston J.S., Sheppard W.S., Smith D.R., Suarez A.V., Weaver D., Tsutsui N.D. (2006) Thrice out of Africa: Ancient and recent expansions of the honey bee, Apis mellifera, Science 314, 642-645.