Science in Society Archive

Parasitic Fungus and Honeybee Decline

Prof. Joe Cummins says systemic pesticides undermine the bee's immune system, leaving it susceptible to the parasitic fungus Nosema

The decline of honeybees has become a global issue of grave concern. The symptoms of colony collapse disorder (CCD) of the honeybee include failure of foraging bees to return to their hive, the inability of infected hives to attract healthy bees and the infection of bees from affected hives by parasites and viruses. A United States National Research Council report focused on introduced parasitic mites, the bacterial foul brood disease and viruses; but made no mention of other possibilities besides pesticides and genetically modified (GM) crops, if only to dismiss them [1]. We have drawn attention to the sub-lethal effects on bees of pesticides and GM crops [2, 3] ( Mystery of Disappearing Honeybees , Requiem for the Honeybee , SiS 34) and the serious disorienting effects of radiation from mobile phone base stations [4] ( Mobile Phones and Vanishing Bees , SiS 34)..

Recently, a parasitic fungus was implicated as a potential culprit, but those results were admittedly highly preliminary. The fungus Nosema ceranae was found in affected hives around the USA as well as in some hives where the bees survived [5]. Nosema is a single-cell parasite belonging to the Microsporidia family that infects invertebrates and vertebrates including humans. Nosema infection of honeybees has been known for over a century as Nosema apis , which is relatively benign. The oriental honeybee Apis cerana was infected with Nosema ceranae , but in 2005-2006 the parasite was found in Apis mellifera in a highly virulent form [6, 7]. Nosema ceranae was identified in Apis mellifera honeybees collected from around the world and its importance as an emerging pathogen for beekeeping was highligted [8]. The increase in virulence of Nosema ceranae as it shifted from cerana bees to mellifera bees may be related to mutations or to environmental factors such as pesticides, which decreased immunity in mellifera bees. Microsporidia infections in humans, for example, are associated with suppression of the immune system by viruses or drugs [9].

Nosema ceranae causes bees to die within eight days after infection. Foraging bees seem to be the most infected. They leave the colony but become too weak to return, leaving behind a small cluster and a fragile colony. The antibiotic fumagillin is the only effective treatment of infected hives [10]. Fumagillin treatment is applied dissolved in sugar solution, and pollen and hive frames are irradiated with electron beams [11]. Fumagillin has genotoxic (chromosome damaging) effects on humans [12]. In spite of the genotoxic potential, fumagillin is the drug of choice for the treatment of microsporidia infection in AIDS patients, organ transplant recipients, contact lens wearers and the elderly [13]. Fumagillin is also used as a cancer treatment drug because it inhibits angiogenesis (blood vessel formation and blood flow) to tumours [14].

Until 2006, microsporidia were often deemed to be protozoa but in 2006 they were demoted to the kingdom of the fungi. The basis for the demotion was molecular data from a number of genes [15]. Microsporidia are obligate intracellular parasites, their spores have thick walls and are highly resistant. Within the spores, there is a coiled polar extrusion tube; and when the spore contacts a cell, the extrusion tube is uncoiled and pierces the membrane of the target cell, injecting spore plasma into the cell and initiating the reproductive cycle and release of further spores [16]. The parasite cells lack mitochondria, and depend on their hosts for aerobic respiration. However, some mitochondrial genes are present in the nuclei of the parasite and in some cases, mitochondrial relics can be found, made up of tiny double membrane vesicles containing enzymes but lacking respiratory functions [17].

Nosema ceranae may be a contributor to CCD, but it seems likely that the virulence of the parasite may depend on the bee's immune system being compromised by pesticides such as the systemic insecticides and fungicides used in seed treatment or as sprays, or by a combination of exposures that create immunodeficiency [18] ( Parasitic Fungi and Pesticides Act Synergistically to Kill Honeybees? SiS 35).

Article first published 18/06/07


References

  1. Committee on the Status of Pollinators in North America American National Research Council Status of Pollinators in North America 2006 ISBN:978-0-309-10289-6
  2. Ho MW and Cummins J. Mystery of disappearing honeybees. Science in Society 34 , 35-36, 2007.
  3. Cummins J. Requiem for the honeybee Science in Society 34 , 37-38, 2007.
  4. Ho MW. Mobile phones and vanishing bees. Science in Society 34 , 34, 2007.
  5. Chong J and Maugh T. Experts may have found what's bugging the bees Los Angeles Times 2007, http://www.latimes.com/news/la-sci-bees26apr26,0,2135129,print.story
  6. Higes M, Martin R and Meana A. Nosema ceranae , a new microsporidian parasite in honeybees in Europe. J Invertebr Pathol. 2006 Jun;92(2):93-5
  7. Higes M, Garcia-Palencia P, Martin-Hernandez R and Meana A. Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). J Invertebr Pathol. 2007; 94(3):211-7
  8. Klee J, Besana AM, Genersch E, Gisder S, Nanetti A, Tam DQ, Chinh TX, Puerta F, Ruz JM, Kryger P, Message D, Hatjina F, Korpela S, Fries I and Paxton RJ. Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J Invertebr Pathol. 2007 Mar 12; [Epub ahead of print] doi:10.1016/j.jip.2007.02.014
  9. Samie A, Obi CL, Tzipori S, Weiss LM and Guerrant RL. Microsporidiosis in South Africa: PCR detection in stool samples of HIV-positive and HIV-negative individuals and school children in Vhembe district, Limpopo Province. Trans R Soc Trop Med Hyg. 2007, 101(6):547-54.
  10. Wikepedia Nosema ceranae 2007 http://en.wikipedia.org/wiki/Nosema_ceranae
  11. Manitoba Agriculture, Foods and Rural Initiatives Recommendations for administering antibiotics to honey bee colonies 2006 http://www.gov.mb.ca/agriculture/crops/honey/bha01s00.html
  12. Stanimirovic Z, Stevanovic J, Bajic V and Radovic I. Evaluation of genotoxic effects of fumagillin by cytogenetic tests in vivo. Mutat Res. 2007, 628(1):1-10.
  13. Didier ES, Maddry JA, Brindley PJ, Stovall ME and Didier PJ. Therapeutic strategies for human microsporidia infections. Expert Rev Anti Infect Ther . 2005, 3(3), :419-34.
  14. Chen GJ, Weylie B, Hu C, Zhu J and Forough R FGFR1/PI3K/AKT signalling pathway is a novel target for antiangiogenic effects of the cancer drug Fumagillin (TNP-470). J Cell Biochem. 2007 Feb 12; [Epub ahead of print]
  15. James TY, Kauff F, Schoch CL, et al Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature . 2006, 443, 818-22.
  16. Franzen C. How do microsporidia invade cells? Folia Parasitologica 2005, 52,36-40.
  17. Roger AJ and Silberman JD. Cell evolution: mitochondria in hiding. Nature 2002; 418, :827-9.
  18. Cummins J. Parasitic fungi and pesticides act synergistically to kill honeybees? Science in Society 35 (in press).

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