Individual variability of Nosema ceranae infections in Apis mellifera colonies

Insects

Volumn 3, Issue 4, 2012, Pages 1143-1155

  Mulholland, Grace E ^a   Traver, Brenna E ^a   Johnson, Nels G ^a   Fell, Richard D F ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

Apis mellifera; Nosema apis; Nosema ceranae; Real time PCR; Spore count; Variability

Indexed keywords

APIS; APIS MELLIFERA; APOIDEA; BACTERIA (MICROORGANISMS); MICROSPORIDIA; NOSEMA; NOSEMA APIS; NOSEMA CERANAE;

EID: 84878755961     PISSN: None     EISSN: 20754450     Source Type: Journal    
DOI: 10.3390/insects3041143     Document Type: Article

References (64)

1. Fries, I. Protozoa. Honey Bee Pests, Predators, & Diseases; 3rd ed.; Morse, R.A., Flottum, K., Eds.; A.I. Root Company: Medina, Saudi Arabia, 1997; pp. 59-76.
2. Bailey, L. The measurement and interrelationships of infections with Nosema apis and Malpighamoeba mellificae of honey-bee populations. J. Invertebr. Pathol. 1968, 12, 175-179.
3. Bailey, L. Infectious Diseases of the Honey Bee, 1st ed.; Land Books: London, UK, 1963.
4. Fries, I.; Feng, F.; da Silva, A.; Slemenda, S.B.; Pieniazek, N.J. Nosema ceranae n. sp. (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). Eur. J. Protistol. 1996, 32, 356-365.
5. Fries, I.; Martín, R.; Meana, A.; García-Palencia, P.; Higes, M. Natural infections of Nosema ceranae in European honey bees. J. Apic. Res. 2006, 45, 230-233.
6. Higes, M.; Martín, R.; Meana, A. Nosema ceranae, a new microsporidian parasite in honeybees in Europe. J. Invertebr. Pathol. 2006, 92, 93-95.
7. Huang, W.-F.; Jiang, J.-H.; Chen, Y.-W.; Wang, C.-H. A Nosema ceranae isolate from the honeybee Apis mellifera. Apidologie 2007, 38, 30-37.
8. Dyess, E. A study of the seasonal variations of Nosema apis Zander of honey bees in Mississippi. Am. Bee J. 1978, 118, 33-35.
9. Fries, I. Nosema apis- A parasite in the honey bee colony. Bee World 1993, 74, 5-19.
10. Farrar, C.L. Nosema disease contributes to winter losses and queen supersedure. Gleanings Bee Culture 1942, 70, 660-661, 701.
11. Moeller, F.E. Nosema disease- its control in honey bee colonies. In Technical Bulletin No. 1569; USDA, Ed.; Science and Education Administration: Washington, DC, USA, 1978.
12. Jeffree, E.P.; Allen, M.D. The influence of colony size and of nosema disease on the rate of population loss in honey bee colonies in winter. J. Econ. Entomol. 1956, 49, 831-834.
13. Higes, M.; Martín-Hernández, R.; Botías, C; Bailón, E.G.; González-Porto, A.V.; Barrios, L.; Nozal, M.J.d.; Bernal, J.L.; Jiménez, J.J.; Palencia, P.G.; Meana, A. How natural infection by Nosema ceranae causes honeybee colony collapse. Environ. Microbiol. 2008, 10, 2659-2669.
14. Higes, M.; Martín-Hernández, R.; Garrido-Bailón, E.; González-Porto, A.; García-Palencia, P.; Meana, A.; María; Mayo, R.; Bernal, J. Honeybee colony collapse due to Nosema ceranae in professional apiaries. Environ. Microbiol. Reports 2009, 1, 110-113.
15. Traver, B.E.; Fell, R.D. Prevalence and infection intensity of Nosema in honey bee (Apis mellifera L.) colonies in Virginia. J. Invertebr. Pathol. 2011, 107, 43-49.
16. Mussen, E.C.; Furgala, B.; Hyser, R.A. Enzootic levels of Nosema disease in the continental United States (1074). Am. Bee J. 1975, 115, 48-50, 58.
17. Fries, I. Nosema ceranae in European honey bees (Apis mellifera). J. Invertebr. Pathol. 2010, 103, S73-S79.
18. Jaycox, E.R. Surveys for Nosema disease in honey bees in California. J. Econ. Entomol. 1960, 53, 95-98.
19. Doull, K.M.; Eckert, J.E. A survey of the incidence of Nosema disease in California. J. Econ. Entomol. 1962, 55, 313-317.
20. Doull, K.M.; Cellier, K.M. A survey of the incidence of nosema disease (Nosema apis Zander) of the honey bee in South Australia. J. Insect Pathol. 1961, 3, 280-288.
21. Pickard, R.S.; El-Shemy, A.A.M. Seasonal variation in the infection of honeybee colonies with Nosema apis Zander. J. Apic. Res. 1989, 28, 93-100.
22. Martin-Hernandez, R.; Meana, A.; Prieto, L.; Salvador, A.M.; Garrido-Bailon, E.; Higes, M. Outcome of the colonization of Apis mellifera by Nosema ceranae. Appl. Environ. Microbiol. 2007, 73,6331-6338.
23. Traver, B.E.; Williams, M.R.; Fell, R.D. Comparison of within hive sampling and seasonal activity of Nosema ceranae in honey bee colonies. J. Invertebr. Pathol. 2012, 109, 187-193.
24. Bailey, L. The natural mechanism of suppression of Nosema apis Zander in enzootically infected colonies of the honey bee, Apis mellifera Linnaeus J. Insect Pathol. 1959, 1, 347-350.
25. Higes, M.; Martín-Hernández, R.; Meana, A. Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie 2010, 41, 375-392.
26. Gisder, S.; Hedtke, K.; Mockel, N.; Frielitz, M.C.; Linde, A.; Genersch, E. Five-Year Cohort Study of Nosema spp. in Germany: Does Climate Shape Virulence and Assertiveness of Nosema ceranae? Appl. Environ. Microbiol. 2010, 76, 3032-3038.
27. Copley, T.R.; Jabaji, S.H. Honeybee glands as possible infection reservoirs of Nosema ceranae and Nosema apis in naturally infected forager bees. J. Appl. Microbiol. 2012, 112, 15-24.
28. Martin-Hernandez, R.; Meana, A.; Garcia-Palencia, P.; Marin, P.; Botias, C; Garrido-Bailon, E.; Barrios, L.; Higes, M. Effect of temperature on the biotic potential of honeybee microsporidia. Appl. Environ. Microbiol. 2009, 75, 2554-2557.
29. Meana, A.; Martín-Hernández, R.; Higes, M. The reliability of spore counts to diagnose Nosema ceranae infections in honey bees. J. Apic. Res. 2010, 49, 212-214.
30. Cantwell, G.E. Standard methods for counting Nosema spores. Am. Bee J. 1970, 110, 22-223.
31. OIE Chapter 2.2.4 Nosemosis of honey bees. Available online: http://www.oie.int/fileadmin/ Home/eng/Health_standards/tahm/2.02.04_NOSEMOSIS.pdf (acessed on 14 October 2012).
32. LArrivee, J.C.M. The effects of sampling sites on Nosema determination J. Insect Pathol. 1963, 5, 349-355.
33. Seeley, T.D. The Wisdom of the Hive: The Social Physiology of Honey Bee colonies; Harvard University Press: Cambridge, Massachusetts, UK, 1995; p. 295.
34. Fries, I.; Ekbohm, G.; Villumstad, E. Nosema apis, sampling techniques and honey yield. J. Apic. Res. 1984, 23, 102-105.
35. Paxton, R.J.; Klee, J.; Korpela, S.; Fries, I. Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie 2007, 38, 558-565.
36. Wu, J.Y.; Smart, M.D.; Anelli, CM.; Sheppard, W.S. Honey bees (Apis mellifera) reared in brood combs containing high levels of pesticide residues exhibit increased susceptibility to Nosema (Microsporidia) infection. J. Invertebr. Pathol. 2012, 109, 326-329.
37. Muz, M.N.; Girisgin, A.O.; Muz, D.; Aydin, L. Molecular detection of Nosema ceranae and Nosema apis infections in Turkish apiaries with collapsed colonies. J. Apic. Res. 2010, 49, 342.
38. Suwannapong, G.; Yemor, T.; Boonpakdee, C; Benbow, M.E. Nosema ceranae, a new parasite in Thai honeybees. J. Invertebr. Pathol. 2011, 106, 236-241.
39. Chaimanee, V.; Warrit, N.; Chantawannakul, P. Infections of Nosema ceranae in four different honeybee species. J. Invertebr. Pathol. 2010, 105, 207-210.
40. Yoshiyama, M.; Kimura, K. Distribution of Nosema ceranae in the European honeybee, Apis mellifera in Japan. J. Invertebr. Pathol. 2011, 106, 263-267.
41. Giersch, T.; Berg, T.; Galea, F.; Hornitzky, M. Nosema ceranae infects honey bees (Apis mellifera) and contaminates honey in Australia. Apidologie 2009, 40, 117-123.
42. Higes, M.; Martín-Hernández, R.; Garrido-Bailón, E.; Botías, C; Meana, A. The presence of Nosema ceranae (Microsporidia) in North African honey bees (Apis mellifera intermissa). J. Apic. Res. 2009, 48, 217-219.
43. Invernizzi, C; Abud, C; Tomasco, I.H.; Harriet, J.; Ramallo, G.; Campá, J.; Katz, H.; Gardiol, G.; Mendoza, Y. Presence of Nosema ceranae in honeybees (Apis mellifera) in Uruguay. J. Invertebr. Pathol. 2009, 101, 150-153.
44. Calderón, R.A.; Sanchez, L.A.; Yañez, O.; Fallas, N. Presence of Nosema ceranae in africanized honey bee colonies in Costa Rica. J. Apic. Res. 2008, 47, 328-329.
45. Williams, G.R.; Shafer, A.B.A.; Rogers, R.E.L.; Shutler, D.; Stewart, D.T. First detection of Nosema ceranae, a microsporidian parasite of European honey bees (Apis mellifera), in Canada and central USA. J. Invertebr. Pathol. 2008, 97, 189-192.
46. Chen, Y.; Evans, J.D.; Smith, I.B.; Pettis, J.S. Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States. J. Invertebr. Pathol. 2008, 97, 186-188.
47. Topolska, G.; Kasprzak, S. First cases of Nosema ceranae infection in bees in Poland. Medycyna Weterynaryjna 2007, 63, 1504-1506.
48. Klee, J.; Besana, A.M.; Genersch, E.; Gisder, S.; Nanetti, A.; Tam, D.Q.; Chinh, T.X.; Puerta, F.; Ruz, J.M.; Kryger, P.; Message, D.; Hatjina, F.; Korpela, S.; Fries, I.; Paxton, R.J. Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J. Invertebr. Pathol. 2007, 96, 1-10.
49. Paxton, R.J.; Klee, J.; Korpela, S.; Fries, I. Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie 2007, 38, 558-565.
50. Chauzat, M.P.; Higes, M.; Martin-Hernandez, R.; Meana, A.; Cougoule, N.; Faucon, J.P. Presence of Nosema ceranae in French honey bee colonies. J. Apic. Res. 2007, 46, 127-128.
51. Farrar, C.L. Fumagillin for nosema control in package bees. Am. Bee J. 1954, 94, 52-53, 60.
52. Gochnauer, T.A. Fumidil B and Nosema control in wintering colonies. Glean. Bee Cult. 1957, 85, 528-529.
53. Doull, K.M. The effects of time of day and method of sampling on the determination of nosema disease in beehives. J. Invertebr. Pathol. 1965, 7, 1-4.
54. LArrivee, J.C.M. Comparison of composite versus individual bee sampling for Nosema apis Zander. Journal of Insect Pathology 1963, 5, 434-439.
55. Bailey, L. The transmission of nosema disease. Bee World 1953, 34, 171-172.
56. Bailey, L. The control of nosema disease. Bee World 1954, 35, 111-113.
57. Bailey, L. The epidemiology and control of nosema disease of the honey bee. Ann. Appl. Biol. 1955, 43, 379-389.
58. Langridge, D.F. Nosema disease of the honeybee and some investigations into its control in Victoria, Australia. Bee World 1961, 42, 36-40.
59. Fingler, B.D.; Nash, W.T.; Szabo, T.I. A comparison of two techniques for the measurement of Nosema disease in honey bee colonies wintered in Alberta, Canade. Am. Bee J. 1982, 122, 369-371.
60. Smart, M.D.; Sheppard, W.S. Nosema ceranae in age cohorts of the western honey bee (Apis mellifera). J. Invertebr. Pathol. 2012, 109, 148-151.
61. El-Shemy, A.A.M.; Pickard, R.S. Nosema apis Zander infection levels in honeybees of known age. J. Apic. Res. 1989, 28, 101-106.
62. Morse, R.A.; Flottum, K. Honey Bee Pests, Predators, & Diseases, 3rd Ed.; A.I. Root Company: Medina, Saudi Arabia, 1997; p. 718.
63. Cantwell, G.E. Standard methods for counting Nosema spores. Am. Bee J. 1970, 110, 222-223.
64. Traver, B.E.; Fell, R.D. Prevalence and infection intensity of Nosema in honey bee (Apis mellifera L.) colonies in Virginia. J. Invertebr. Pathol. 2011, 107, 43-49.