Nosema ceranae

Nosema ceranae is a microsporidian, a small, unicellular parasite that mainly affects Apis cerana, the Asiatic honey bee. Along with Nosema apis, it causes the disease nosemosis, the most widespread of the diseases of adult honey bees. N. ceranae can remain dormant as a long-lived spore which is resistant to temperature extremes and dehydration. This fungus has been shown to act in a synergistic fashion with diverse insecticides such as fipronil or neonicotinoids, by increasing the toxicity of pesticides for bees, leading to higher bee mortality. It may thus play an indirect role in colony collapse disorder.[1][2] In addition, the interaction between fipronil and N. ceranae induces changes in male physiology leading to sterility.[3]

Nosema ceranae
Scientific classification
Kingdom:
Fungi
Division:
Microsporidia
Class:
Dihaplophasea
Order:
Dissociodihaplophasida
Family:
Nosematidae
Genus:
Nosema
Species:
N. ceranae
Binomial name
Nosema ceranae
(Fries et al., 1996)

Range

Nosema ceranae was first described in 1996 and was identified as a disease of Apis mellifera in 2004 in Taiwan.[4] Since its emergence in honeybees, N. ceranae has been identified in bumblebee species in South America,[5] China,[6] and England where infection studies indicate N. ceranae has a higher virulence in bumblebees than honeybees.[7]

Researchers in Spain have analysed samples of Apis mellifera, the European honey bee, mostly sent from colonies suffering unexpected decreases in bee population per hive or lower honey production, as reported by the beekeepers during the last two to three years. In 2004, 90% of some 3,000 samples had positive results for N. ceranae. In 2005, of 800 samples, 97% had positive results. During 2006, both France and Germany have detected the disease and recognized the genetic sequence of N. ceranae in their respective territories. In the United States, N. ceranae has been detected in honey bees from Nebraska, Wisconsin, Arkansas, New York, and South Dakota using PCR of the 16S gene.[8][9] In New York, N. ceranae was detected in 49 counties, and of the 1200 honey bee samples collected, 528 (44%) were positive for Nosema, from which, PCR analysis of 371 spore positive samples revealed that 96% were N. ceranae, 3% had both N. ceranae and N. apis, and 1% had N. apis only.[10]

Effects on bees

This pathogen has been tentatively linked to colony collapse disorder, a phenomenon reported primarily from the United States, since fall of 2006. Highly preliminary evidence of N. ceranae was reported in a few hives in the Central Valley area of California. "Tests of genetic material taken from a "collapsed colony" in Merced County point to a once-rare microbe that previously affected only Asian bees but might have evolved into a strain lethal to those in Europe and the United States."[11][12] The researcher did not, however, believe this was conclusive evidence of a link to CCD; "We don't want to give anybody the impression that this thing has been solved."[13] A USDA bee scientist has similarly stated, "while the parasite nosema ceranae may be a factor, it cannot be the sole cause. The fungus has been seen before, sometimes in colonies that were healthy."[14] Likewise, a Washington State beekeeper familiar with N. ceranae in his own hives discounts it as being the cause of CCD.[15] In early 2009, Higes et al. reported an association between CCD and N. ceranae was established free of confounding factors, and that weakened colonies treated with fumagillin recovered.[16]

News articles published in October 2010 quoted researchers who had discovered that Nosema fungus had joined with a previously unsuspected virus, invertebrate iridescent virus, or IIV6, dealing test bee colonies a lethal blow. Neither the fungus nor the virus alone kills all the test group, but the two combined do. Both the fungus and the virus are found with high frequency in hives that have suffered CCD. Final testing is in progress with field tests on colonies.[17]

N. ceranae and N. apis have similar lifecycles, but they differ in spore morphology. Spores of N. ceranae seem to be slightly smaller under the light microscope and the number of polar filament coils is between 20 and 23, rather than the more than 30 often seen in N. apis.

The disease afflicts adult bees and depopulation occurs with consequent losses in honey production. One does not detect symptoms of diarrhea as in N. apis.

The most significant difference between the two types is how quickly N. ceranae can cause a colony to die. Bees can die within 8 days after exposure to N. ceranae,[18] a finding not yet confirmed by other researchers. The forager caste seems the most affected, leaving the colony presumably to forage, but never returning. This results in a reduced colony consisting mostly of nurse bees with their queen, a state very similar to that seen in CCD. Little advice on treatment is available, but it has been suggested that the most effective control of N. ceranae is the antibiotic fumagillin as recommended for N. apis.[19] The genome of N. ceranae was sequenced in 2009. This should help scientists trace its migration patterns, establish how it became dominant, and help measure the spread of infection by enabling diagnostic tests and treatments to be developed.[20][21]

Treatment

N. ceranae is apparently released from the suppressive effects of fumagillin at higher concentrations than that of N. apis. At fumagillin concentrations that continue to impact honey bee physiology, N. ceranae thrives and doubles its spore production. The current application protocol for fumagillin may exacerbate N. ceranae infection rather than suppress it. Fumagillin application should be a major cause of N. ceranae dominance in this time.[22]

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References
  1. Aufauvre J., Biron D. G., Vidau C., Fontbonne R., Roudel M., Diogon M., Viguès B., Belzunces L. P., Delbac F., Blot N. (2012) Parasite - insecticide interactions: a case study of Nosema ceranae and fipronil synergy on honeybee. Scientific Reports 2:326 – DOI: 10.1038/srep00326
  2. Doublet V, Labarussias M, de Miranda JR, Moritz RFA, Paxton RJ (2015) Bees under stress: sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle. Environmental Microbiology 17(4): 969-983. https://doi.org/10.1111/1462-2920.12426
  3. Kairo G, Biron D.G, Ben A.F, Bonnet M, Tchamitchian S, Cousin M, ... & Brunet J.L (2017) Nosema ceranae, Fipronil and their combination compromise honey bee reproduction via changes in male physiology. Scientific reports, 7(1), 8556.
  4. (Huang et al., 2007; submitted in 2005 but published in 2007).
  5. Pilschuk, S.; et al. (2009). "South American native bumblebees (Hymenoptera: Apidae) infected by Nosema ceranae (Microsporidia), an emerging pathogen of honeybees (Apis mellifera)" (PDF). Environmental Microbiology Reports. 135 (2): 131–135. doi:10.1111/j.1758-2229.2009.00018.x. PMID 23765744.
  6. Li, J.; et al. (2012). "Diversity of Nosema associated with bumblebees (Bombus spp.) from China". International Journal for Parasitology. 42 (1): 49–61. doi:10.1016/j.ijpara.2011.10.005. PMID 22138016.
  7. Graystock, P.; et al. (2013). "Emerging dangers: Deadly effects of an emergent parasite in a new pollinator host". Journal of Invertebrate Pathology. 114 (2): 114–119. doi:10.1016/j.jip.2013.06.005. PMID 23816821.
  8. Chapon, L., M.D. Ellis, and A.L. Szalanski. 2009. Nosema and tracheal mites in the north central region – 2008 survey. Proceedings of the American Bee Research Conference. American Bee Journal 149: 585-586.
  9. Population genetics and distribution of N. ceranae in the United States, University of Arkansas Social Insect Genetics Lab
  10. Szalanski, A.L., J. Whitaker, and P. Cappy. 2010. Molecular diagnostics of Nosema ceranae and N. apis from honey bees in New York. Proceedings of the American Bee Research Conference. American Bee Journal 150: 508
  11. Sabin Russell (2007-04-26). "UCSF scientist tracks down suspect in honeybee deaths". San Francisco Chronicle.
  12. "Scientists Identify Pathogens That May Be Causing Global Honeybee Deaths" (PDF) (Press release). Edgewood Chemical and Biological Center. 2007-04-25. Archived from the original (PDF) on 2011-07-22. Retrieved 2009-12-30.
  13. Jia-Rui Chong and Thomas H. Maugh II (2007-04-26). "Experts may have found what's bugging the bees". Los Angeles Times.
  14. Seth Borenstein (2007-05-02). "Honeybee Die-Off Threatens Food Supply, The Associated Press (5/2/2007)". Associated Press. Archived from the original on 2007-05-05. Retrieved 2007-05-07.
  15. Paul Boring (2007-04-25). "Whidbey hives collapse". Whidbey News-Times. Archived from the original on 2007-09-27.
  16. Higes, Mariano; Martín-Hernández, Raquel; Garrido-Bailón, Encarna; González-Porto, Amelia V.; García-Palencia, Pilar; Meana, Aranzazu; Del Nozal, María J.; Mayo, R.; Bernal, José L. (2009). "Honeybee colony collapse due to Nosema ceranae in professional apiaries". Environmental Microbiology Reports. 1 (2): 110–113. doi:10.1111/j.1758-2229.2009.00014.x. PMID 23765741.
  17. Drew Armstrong (2010-10-07). "Bee-Killing Disease May Be Combination Attack, Researchers Say, Bloomberg (10/7/2010)". Bloomberg. Archived from the original on 2010-10-09. Retrieved 2010-10-06.
  18. (Higes et al. 2006)
  19. Higes; et al. (2009). "Honey bee colony collapse due to Nosema ceranae in professional apiaries". Environmental Microbiology Reports. 1 (2): 110–113. doi:10.1111/j.1758-2229.2009.00014.x. PMID 23765741.
  20. Cornman; et al. (2009). "Genomic analyses of the microsporidian Nosema ceranae, an emergent pathogen of honey bees". PLOS Pathogens. 5 (6): e1000466. doi:10.1371/journal.ppat.1000466. PMC 2685015. PMID 19503607.
  21. Cornman, R. S.; Chen, Y. P.; Schatz, M. C.; Street, C.; Zhao, Y.; Desany, B.; Egholm, M.; Hutchison, S.; Pettis, J. S.; Lipkin, W. I.; Evans, J. D. (2009). "Bee-killing Parasite Genome Sequenced ScienceDaily June 5, 2009". PLOS Pathogens. Sciencedaily.com. 5 (6): e1000466. doi:10.1371/journal.ppat.1000466. PMC 2685015. PMID 19503607. Retrieved 2014-03-05.
  22. Huang, Wei-Fone; Solter, Leellen F.; Yau, Peter M.; Imai, Brian S. (2013-03-07). "Nosema ceranae escapes Fumagillin control in honey bees". PLOS Pathogens. 9 (3): e1003185. doi:10.1371/journal.ppat.1003185. PMC 3591333. PMID 23505365.
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