Nosema ceranae
{{short description|Species of microsporidian}}
{{Speciesbox
| taxon = Nosema ceranae
| authority = (Fries et al., 1996)
}}
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.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/srep00326Doublet 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 In addition, the interaction between fipronil and N. ceranae induces changes in male physiology leading to sterility.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.
Range
Nosema ceranae was first described in 1996 and was identified as a disease of Apis mellifera in 2004 in Taiwan.(Wei-Fone Huang, Jing-Hao Jiang, Yue-Wen Chen and Chung-Hsiung Wang. A Nosema ceranae isolate from the honeybee Apis mellifera. Apidologie. Volume 38, Number 1, 2007. 30 – 37 DOI 10.1051/apido:2006054
; submitted in 2005 but published in 2007). Since its emergence in honeybees, N. ceranae has been identified in bumblebee species in South America,{{cite journal|last=Pilschuk|first=S.|title=South American native bumblebees (Hymenoptera: Apidae) infected by Nosema ceranae (Microsporidia), an emerging pathogen of honeybees (Apis mellifera)|journal=Environmental Microbiology Reports|date=2009|volume=135|issue=2|pages=131–135|url=http://www.bioapi.it/images/pdf/nosema_en_bombus.pdf| doi=10.1111/j.1758-2229.2009.00018.x|pmid=23765744|bibcode=2009EnvMR...1..131P |display-authors=etal}} China,{{cite journal|last=Li|first=J.|title=Diversity of Nosema associated with bumblebees (Bombus spp.) from China|journal=International Journal for Parasitology|date=2012|volume=42|issue=1|pages=49–61| doi=10.1016/j.ijpara.2011.10.005|pmid=22138016|display-authors=etal}} and England where infection studies indicate N. ceranae has a higher virulence in bumblebees than honeybees.{{cite journal|last=Graystock|first=P.|title=Emerging dangers: Deadly effects of an emergent parasite in a new pollinator host|journal=Journal of Invertebrate Pathology|date=2013|volume=114|issue=2|pages=114–119| doi=10.1016/j.jip.2013.06.005|pmid=23816821|bibcode=2013JInvP.114..114G |display-authors=etal}}
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.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.[http://comp.uark.edu/~aszalan/Site/Apis/Nosema_ceranae.html Population genetics and distribution of N. ceranae in the United States, University of Arkansas Social Insect Genetics Lab]{{dead link|date=March 2014}} 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.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
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.{{Cite journal |last1=Martín-Hernández |first1=Raquel |last2=Bartolomé |first2=Carolina |last3=Chejanovsky |first3=Nor |last4=Le Conte |first4=Yves |last5=Dalmon |first5=Anne |last6=Dussaubat |first6=Claudia |last7=García-Palencia |first7=Pilar |last8=Meana |first8=Aranzazu |last9=Pinto |first9=M. Alice |last10=Soroker |first10=Victoria |last11=Higes |first11=Mariano |date=2018-03-24 |title=Nosema ceranae in Apis mellifera : a 12 years postdetection perspective: Nosema ceranae in Apis mellifera |url=https://onlinelibrary.wiley.com/doi/10.1111/1462-2920.14103 |journal=Environmental Microbiology |language=en |volume=20 |issue=4 |pages=1302–1329 |doi=10.1111/1462-2920.14103|pmid=29575513 |hdl=10198/18545 |hdl-access=free }}{{Cite journal |last1=Schüler |first1=Vivian |last2=Liu |first2=Yuk-Chien |last3=Gisder |first3=Sebastian |last4=Horchler |first4=Lennart |last5=Groth |first5=Detlef |last6=Genersch |first6=Elke |date=2023-03-01 |title=Significant, but not biologically relevant: Nosema ceranae infections and winter losses of honey bee colonies |journal=Communications Biology |language=en |volume=6 |issue=1 |page=229 |doi=10.1038/s42003-023-04587-7 |issn=2399-3642 |pmc=9977864 |pmid=36859713}}{{Cite journal |last1=Higes |first1=Mariano |last2=Martín-Hernández |first2=Raquel |last3=Botías |first3=Cristina |last4=Bailón |first4=Encarna Garrido |last5=González-Porto |first5=Amelia V. |last6=Barrios |first6=Laura |last7=del Nozal |first7=M. Jesús |last8=Bernal |first8=José L. |last9=Jiménez |first9=Juan J. |last10=Palencia |first10=Pilar García |last11=Meana |first11=Aránzazu |date=2008-10-09 |title=How natural infection by Nosema ceranae causes honeybee colony collapse: Natural Nosema ceranae infection |url=https://onlinelibrary.wiley.com/doi/10.1111/j.1462-2920.2008.01687.x |journal=Environmental Microbiology |language=en |volume=10 |issue=10 |pages=2659–2669 |doi=10.1111/j.1462-2920.2008.01687.x|pmid=18647336 }}{{Cite journal |last1=Blot |first1=Nicolas |last2=Clémencet |first2=Johanna |last3=Jourda |first3=Cyril |last4=Lefeuvre |first4=Pierre |last5=Warrit |first5=Natapot |last6=Esnault |first6=Olivier |last7=Delatte |first7=Hélène |date=2023-07-26 |title=Geographic population structure of the honeybee microsporidian parasite Vairimorpha (Nosema) ceranae in the South West Indian Ocean |journal=Scientific Reports |language=en |volume=13 |issue=1 |pages=12122 |doi=10.1038/s41598-023-38905-0 |issn=2045-2322 |pmc=10372035 |pmid=37495608|bibcode=2023NatSR..1312122B }} 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."
{{cite news
|url=http://www.sfgate.com/cgi-bin/article.cgi?file=/c/a/2007/04/26/MNGK7PFOMS1.DTL
|title=UCSF scientist tracks down suspect in honeybee deaths
|author=Sabin Russell
|date=2007-04-26
|publisher=San Francisco Chronicle
|url=http://www.ecbc.army.mil/pr/download/042507_honey_bee_pathogens.pdf
|title=Scientists Identify Pathogens That May Be Causing Global Honeybee Deaths
|date=2007-04-25
|publisher=Edgewood Chemical and Biological Center
|access-date=2009-12-30
|archive-url=https://web.archive.org/web/20110722175623/http://www.ecbc.army.mil/pr/download/042507_honey_bee_pathogens.pdf
|archive-date=2011-07-22
|url-status=dead
}}{{check|date=December 2009}} 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."
{{cite news
|url=http://www.latimes.com/news/science/la-sci-bees26apr26,0,896792.story?coll=la-home-headlines
|title=Experts may have found what's bugging the bees
|author=Jia-Rui Chong and Thomas H. Maugh II
|date=2007-04-26
|work=Los Angeles Times
}} 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."
{{cite news
|url=https://news.yahoo.com/s/ap/20070502/ap_on_sc/honeybee_die_off
|title=Honeybee Die-Off Threatens Food Supply, The Associated Press (5/2/2007)
|author=Seth Borenstein
|access-date=2007-05-07
|date=2007-05-02
|agency=Associated Press
|archive-url=https://web.archive.org/web/20070505110220/http://news.yahoo.com/s/ap/20070502/ap_on_sc/honeybee_die_off
|archive-date=2007-05-05
|url-status=dead
}} Likewise, a Washington State beekeeper familiar with N. ceranae in his own hives discounts it as being the cause of CCD.
{{cite news
|url = http://www.whidbeynewstimes.com/portals-code/list.cgi?paper=84&cat=23&id=970700&more=
|title = Whidbey hives collapse
|author = Paul Boring
|date = 2007-04-25
|publisher = Whidbey News-Times
|url-status = dead
|archive-url = https://web.archive.org/web/20070927102246/http://www.whidbeynewstimes.com/portals-code/list.cgi?paper=84&cat=23&id=970700&more=
|archive-date = 2007-09-27
}} 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.{{cite journal | doi = 10.1111/j.1758-2229.2009.00014.x | pmid=23765741 | volume=1 | issue=2 | title=Honeybee colony collapse due to Nosema ceranae in professional apiaries | journal=Environmental Microbiology Reports | pages=110–113| year=2009 | last1=Higes | first1=Mariano | last2=Martín-Hernández | first2=Raquel | last3=Garrido-Bailón | first3=Encarna | last4=González-Porto | first4=Amelia V. | last5=García-Palencia | first5=Pilar | last6=Meana | first6=Aranzazu | last7=Del Nozal | first7=María J. | last8=Mayo | first8=R. | last9=Bernal | first9=José L. | bibcode=2009EnvMR...1..110H }}
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.
{{cite news
|url = http://www.businessweek.com/news/2010-10-07/bee-killing-disease-may-be-combination-attack-researchers-say.html
|title = Bee-Killing Disease May Be Combination Attack, Researchers Say, Bloomberg (10/7/2010)
|author = Drew Armstrong
|access-date = 2010-10-06
|date = 2010-10-07
|publisher = Bloomberg
|url-status = dead
|archive-url = https://web.archive.org/web/20101009213659/http://www.businessweek.com/news/2010-10-07/bee-killing-disease-may-be-combination-attack-researchers-say.html
|archive-date = 2010-10-09
}}
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,(Higes et al. 2006) 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.{{cite journal | last1 = Higes |display-authors=etal | year = 2009 | title = Honey bee colony collapse due to Nosema ceranae in professional apiaries | journal = Environmental Microbiology Reports | volume = 1 | issue = 2| pages = 110–113 |doi=10.1111/j.1758-2229.2009.00014.x |pmid=23765741 |bibcode=2009EnvMR...1..110H }}
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.{{cite journal | last1 = Cornman |display-authors=etal | year = 2009 | title = Genomic analyses of the microsporidian Nosema ceranae, an emergent pathogen of honey bees | journal = PLOS Pathogens | volume = 5 | issue = 6| page = e1000466 | doi = 10.1371/journal.ppat.1000466 |pmid=19503607 | pmc = 2685015 |doi-access=free }}{{cite journal|url=https://www.sciencedaily.com/releases/2009/06/090604222430.htm |title=Bee-killing Parasite Genome Sequenced ScienceDaily June 5, 2009 |journal=PLOS Pathogens |volume=5 |issue=6 |pages=e1000466 |doi=10.1371/journal.ppat.1000466 |pmid=19503607 |pmc=2685015 |publisher=Sciencedaily.com |access-date=2014-03-05|year=2009 |last1=Cornman |first1=R. S. |last2=Chen |first2=Y. P. |last3=Schatz |first3=M. C. |last4=Street |first4=C. |last5=Zhao |first5=Y. |last6=Desany |first6=B. |last7=Egholm |first7=M. |last8=Hutchison |first8=S. |last9=Pettis |first9=J. S. |last10=Lipkin |first10=W. I. |last11=Evans |first11=J. D. |doi-access=free }}
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.{{cite journal |title=Nosema ceranae escapes Fumagillin control in honey bees |journal=PLOS Pathogens |volume=9 |issue=3 |pages=e1003185 |date=2013-03-07 |doi=10.1371/journal.ppat.1003185 |pmid=23505365 |pmc=3591333 |last1=Huang |first1=Wei-Fone |last2=Solter |first2=Leellen F. |last3=Yau |first3=Peter M. |last4=Imai |first4=Brian S. |doi-access=free }}