Nosema ceranae

Last updated

Nosema ceranae
Scientific classification
Kingdom:
Division:
Class:
Order:
Family:
Genus:
Species:
N. ceranae
Binomial name
Nosema ceranae
(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. [1] [2] In addition, the interaction between fipronil and N. ceranae induces changes in male physiology leading to sterility. [3]

Contents

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. [11] [12] [13] [14] 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." [15] [16] 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." [17] 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." [18] Likewise, a Washington State beekeeper familiar with N. ceranae in his own hives discounts it as being the cause of CCD. [19] 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. [20]

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. [21]

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, [22] 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. [23] 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. [24] [25]

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. [26]

Related Research Articles

<span class="mw-page-title-main">Honey bee</span> Colonial flying insect of genus Apis

A honey bee is a eusocial flying insect within the genus Apis of the bee clade, all native to mainland Afro-Eurasia. After bees spread naturally throughout Africa and Eurasia, humans became responsible for the current cosmopolitan distribution of honey bees, introducing multiple subspecies into South America, North America, and Australia.

Nosema apis is a microsporidian, a small, unicellular parasite recently reclassified as a fungus that mainly affects honey bees. It causes nosemosis, also called nosema, which is the most common and widespread of adult honey bee diseases. The dormant stage of N. apis is a long-lived spore which is resistant to temperature extremes and dehydration, and cannot be killed by freezing the contaminated comb. Nosemosis is a listed disease with the Office International des Epizooties (OIE).

<i>Varroa destructor</i> Species of mite

Varroa destructor, the Varroa mite, is an external parasitic mite that attacks and feeds on honey bees and is one of the most damaging honey bee pests in the world. A significant mite infestation leads to the death of a honey bee colony, usually in the late autumn through early spring. Without management for Varroa mite, honey bee colonies typically collapse within 2 to 3 years in temperate climates. These mites can infest Apis mellifera, the western honey bee, and Apis cerana, the Asian honey bee. Due to very similar physical characteristics, this species was thought to be the closely related Varroa jacobsoni prior to 2000, but they were found to be two separate species after DNA analysis.

<span class="mw-page-title-main">Fumagillin</span> Chemical compound

Fumagillin is a complex biomolecule and used as an antimicrobial agent. It was isolated in 1949 from the microbial organism Aspergillus fumigatus.

<span class="mw-page-title-main">Small hive beetle</span> Species of beetle

Aethina tumida,commonly known as small hive beetle (SHB), is a beekeeping pest. It is native to sub-Saharan Africa, but has spread to many other regions, including North America, Australia, and the Philippines.

<i>Deformed wing virus</i> Species of virus

Deformed wing virus (DWV) is an RNA virus, one of 22 known viruses affecting honey bees. While most commonly infecting the honey bee, Apis mellifera, it has also been documented in other bee species, like Bombus terrestris, thus, indicating it may have a wider host specificity than previously anticipated. The virus was first isolated from a sample of symptomatic honeybees from Japan in the early 1980s and is currently distributed worldwide. It is found also in pollen baskets and commercially reared bumblebees. Its main vector in A. mellifera is the Varroa mite. It is named after what is usually the most obvious deformity it induces in the development of a honeybee pupa, which is shrunken and deformed wings, but other developmental deformities are often present.

<span class="mw-page-title-main">East African lowland honey bee</span> Subspecies of honey bee native to Africa

The East African lowland honey bee is a subspecies of the western honey bee. It is native to central, southern and eastern Africa, though at the southern extreme it is replaced by the Cape honey bee. This subspecies has been determined to constitute one part of the ancestry of the Africanized bees spreading through North and South America.

<span class="mw-page-title-main">Western honey bee</span> European honey bee

The western honey bee or European honey bee is the most common of the 7–12 species of honey bees worldwide. The genus name Apis is Latin for "bee", and mellifera is the Latin for "honey-bearing" or "honey carrying", referring to the species' production of honey.

<span class="mw-page-title-main">Colony collapse disorder</span> Aspect of apiculture

Colony collapse disorder (CCD) is an abnormal phenomenon that occurs when the majority of worker bees in a honey bee colony disappear, leaving behind a queen, plenty of food, and a few nurse bees to care for the remaining immature bees. While such disappearances have occurred sporadically throughout the history of apiculture, and have been known by various names, the syndrome was renamed colony collapse disorder in early 2007 in conjunction with a drastic rise in reports of disappearances of western honey bee colonies in North America. Beekeepers in most European countries had observed a similar phenomenon since 1998, especially in Southern and Western Europe; the Northern Ireland Assembly received reports of a decline greater than 50%. The phenomenon became more global when it affected some Asian and African countries as well. From 1990 to 2021, the United Nation’s FAO calculated that the worldwide number of honeybee colonies increased 47%, reaching 102 million.

<i>Apis cerana</i> Species of insect

Apis cerana, the eastern honey bee, Asiatic honey bee or Asian honey bee, is a species of honey bee native to South, Southeast and East Asia. This species is the sister species of Apis koschevnikovi and both are in the same subgenus as the western (European) honey bee, Apis mellifera. A. cerana is known to live sympatrically along with Apis koschevnikovi within the same geographic location. Apis cerana colonies are known for building nests consisting of multiple combs in cavities containing a small entrance, presumably for defense against invasion by individuals of another nest. The diet of this honey bee species consists mostly of pollen and nectar, or honey. Moreover, Apis cerana is known for its highly social behavior, reflective of its classification as a type of honey bee.

<i>Apocephalus borealis</i> Species of fly

Apocephalus borealis is a species of North American parasitoid phorid fly that attacks bumblebees, honey bees, and paper wasps. This parasitoid's genus Apocephalus is best known for the "decapitating flies" that attack a variety of ant species, though A. borealis attacks and alters the behavior of bees and wasps. These flies are colloquially known as zombie flies and the bees they infect are colloquially known as zombees. Association with honey bees has so far only been documented from California, South Dakota, Oregon, Washington, British Columbia, and Vermont.

Nosema bombi is a microsporidian, a small, unicellular parasite recently reclassified as a fungus that mainly affects bumble bees. It was reclassified as Vairimorpha bombi in 2020. The parasite infects numerous Bombus spp. at variable rates, and has been found to have a range of deleterious effects on its hosts.

Apicystis bombi is a species of parasitic alveolates in the phylum Apicomplexa. It infects bees, especially bumblebees. It is believed to have a cosmopolitan distribution in bumblebees and a sporadic occurrence in honey bees, and causes disease symptoms in nonresistant bee species.

<span class="mw-page-title-main">Chronic bee paralysis virus</span> Virus which infects bees

Chronic bee paralysis virus (CBPV) commonly affects adult Apis mellifera honey bees and causes a chronic paralysis that can easily spread to other members of a colony. Bees infected with CBPV begin to show symptoms after 5 days and die a few days after. Chronic bee paralysis virus infection is a factor that can contribute to or cause the sudden collapse of honeybee colonies. Since honeybees serve a vital role in ecological resilience, it is important to understand factors and diseases that threaten them.

Bartonella apis is a bacterium from the genus Bartonella. Bartonella apis was first isolated from the gut of the honey bee in 2015 by Swiss researchers at the University of Lausanne. To date, it has been found only as a gut symbiont of honey bees, including the Western honey bee, and the Eastern or Asiatic honey bee.

<i>Black queen cell virus</i> Species of virus

The black queen cell virus (BQCV) is a virus that infects honey bees, specifically Apis mellifera, Apis florea, and Apis dorsata. Infection of the latter two species is more recent and can be attributed to genetic similarity and geographical closeness.

<i>Malpighamoeba mellificae</i> Species of protozoan

Malpighamoeba mellificae is a single-celled parasite which affects excretory organs of adult bees, causing the contagious disease called amoebiasis, which ultimately leads to death of the host. Worker bees are most prone to being infected. It is commonly found in collaboration with nosemosis. In order to diagnose the 3 - 15 μm size parasite, removal of the malphigian tubule is necessary. Because of there being no viable treatment against this parasite, preventional measures such as providing a clean food supply for the hive are crucial.

Commensalibacter is a genus of Gram-negative, aerobic and rod-shaped bacteria from the family of Acetobacteraceae which was originally isolated from Drosophila melanogaster. The complete genome of the type strain C. intestini A911T has been sequenced.

<i>Snodgrassella alvi</i> Species of bacterium

Snodgrassella alvi is a species of Gram-negative bacteria within the Neisseriaceae and was previously the only known species of the genus Snodgrassella. It was isolated and scientifically described in 2012 by Waldan K. Kwong and Nancy A. Moran, who named the bacteria after the American entomologist Robert Evans Snodgrass.

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. (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).
  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. Bibcode:2009EnvMR...1..131P. 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. Bibcode:2013JInvP.114..114G. 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 [ dead link ]
  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. Martín-Hernández, Raquel; Bartolomé, Carolina; Chejanovsky, Nor; Le Conte, Yves; Dalmon, Anne; Dussaubat, Claudia; García-Palencia, Pilar; Meana, Aranzazu; Pinto, M. Alice; Soroker, Victoria; Higes, Mariano (2018-03-24). "Nosema ceranae in Apis mellifera : a 12 years postdetection perspective: Nosema ceranae in Apis mellifera". Environmental Microbiology. 20 (4): 1302–1329. doi:10.1111/1462-2920.14103. hdl: 10198/18545 . PMID   29575513.
  12. Schüler, Vivian; Liu, Yuk-Chien; Gisder, Sebastian; Horchler, Lennart; Groth, Detlef; Genersch, Elke (2023-03-01). "Significant, but not biologically relevant: Nosema ceranae infections and winter losses of honey bee colonies". Communications Biology. 6 (1): 229. doi:10.1038/s42003-023-04587-7. ISSN   2399-3642. PMC   9977864 . PMID   36859713.
  13. Higes, Mariano; Martín-Hernández, Raquel; Botías, Cristina; Bailón, Encarna Garrido; González-Porto, Amelia V.; Barrios, Laura; del Nozal, M. Jesús; Bernal, José L.; Jiménez, Juan J.; Palencia, Pilar García; Meana, Aránzazu (2008-10-09). "How natural infection by Nosema ceranae causes honeybee colony collapse: Natural Nosema ceranae infection". Environmental Microbiology. 10 (10): 2659–2669. doi:10.1111/j.1462-2920.2008.01687.x. PMID   18647336.
  14. Blot, Nicolas; Clémencet, Johanna; Jourda, Cyril; Lefeuvre, Pierre; Warrit, Natapot; Esnault, Olivier; Delatte, Hélène (2023-07-26). "Geographic population structure of the honeybee microsporidian parasite Vairimorpha (Nosema) ceranae in the South West Indian Ocean". Scientific Reports. 13 (1): 12122. Bibcode:2023NatSR..1312122B. doi:10.1038/s41598-023-38905-0. ISSN   2045-2322. PMC   10372035 . PMID   37495608.
  15. Sabin Russell (2007-04-26). "UCSF scientist tracks down suspect in honeybee deaths". San Francisco Chronicle.
  16. "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.[ verification needed ]
  17. Jia-Rui Chong and Thomas H. Maugh II (2007-04-26). "Experts may have found what's bugging the bees". Los Angeles Times .
  18. 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.
  19. Paul Boring (2007-04-25). "Whidbey hives collapse". Whidbey News-Times. Archived from the original on 2007-09-27.
  20. 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. Bibcode:2009EnvMR...1..110H. doi:10.1111/j.1758-2229.2009.00014.x. PMID   23765741.
  21. 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.
  22. (Higes et al. 2006)
  23. Higes; et al. (2009). "Honey bee colony collapse due to Nosema ceranae in professional apiaries". Environmental Microbiology Reports. 1 (2): 110–113. Bibcode:2009EnvMR...1..110H. doi:10.1111/j.1758-2229.2009.00014.x. PMID   23765741.
  24. 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.
  25. 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. 5 (6). Sciencedaily.com: e1000466. doi: 10.1371/journal.ppat.1000466 . PMC   2685015 . PMID   19503607 . Retrieved 2014-03-05.
  26. 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.