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Posted 8 June 07

Parasitic Fungi and Pesticides Act Synergistically to Kill Honeybees?

Prof. Joe Cummins presents evidence that parasitic fungi can kill insects when low, otherwise non-lethal concentrations of pesticides are present.

Co-operating culprits

Honeybees are facing an unparalleled threat from something that’s causing them to leave their hives, never to return. Scientists call it “colony collapse disorder” (CCD) [1] (Mystery of Disappearing Honeybees, SiS 34). The major suspects in the murder of honeybees appear to be systemic insecticides (the neonicotinoid systemic pesticides used worldwide to treat seeds and crops), including genetically modified (GM) crops [1, 2] (Requiem for the Honeybee, SiS 34), parasitic fungi [3] (Parasitic Fungus and Honeybee Decline SiS 35), and radiation associated with wireless phones [4] (Mobile Phones and Vanishing Bees, SiS 34).

It is unlikely, however, that the suspects act independently of one another, and there is evidence suggesting that parasitic fungi and pesticides interact synergistically in killing honeybees.

Parasitic fungi for biocontrol enhanced by sub-lethal levels of neonicotinoid pesticide.

Parasitic fungi are used extensively as biocontrol agents. Fungal spores are applied in sprays or baits, and it has been observed that the parasites frequently interact synergistically with neonicotinoid pesticides, particularly imidacloprid, in killing insects. When the spores are delivered as a suspension together with low, non-lethal levels of the pesticide, the insect-killing activity of the fungal spores is significantly enhanced. The spores of Beauveria bassinia used to treat the brown leafhopper rice pest, when accompanied by a sublethal dose of imidacloprid, killed the pest earlier and in larger numbers [5]. The fungus Lecanicillium muscarium in sublethal levels of imidacloprid gave satisfactory control of the sweet potato whitefly, and merited inclusion in integrated control programmes [6]. Beauveria bassinia spores combined with imidacloprid at a level one tenth the lethal dose was found to significantly enhance control of the leaf cutting ant [7]. Similarly, termites were controlled by imidacloprid at sub-lethal levels that enhanced the killing activity of the fungal parasite Metarhizium anisopliae [8]. The presence of the insecticides at sub-lethal level appears to interfere with the insect’s immune system, making the insect more susceptible to fungal pathogens.

Bees become exposed to sub-lethal levels of pesticide and biocontrol parasitic fungi

The neonicotinoid insecticides used to dress seeds are systematic, and accumulate in plant parts including the flowers. Hence honeybees collecting pollen will become exposed to the pesticide, and become more susceptible to fungal pathogens. The parasitic fungus, Nosema ceranae, a single celled parasite was indeed found in CCD-affected bee hives from around the USA [3].

Nosema locustae has been a commercial biocontrol fungus to control locusts and grasshoppers. An integrated pest management strategy with an emphasis on the use of Metarhizium, an ascosporic fungus, incorporates low levels chemical pesticides with additional biological options such as the microsporidian Nosema locustae and the hymenopteran egg parasitoids Scelio spp. [9]. Nosema bombycis has been a major pest of the silkworm but it has been used to control Diamondback moth. Another microporidian, Vairimorpha sp., isolated from the Diamondback moth in Malaysia caused 100 percent mortality when applied to moth larvae at 1500 spores per larva [10]. Nosema pyrausta infects the European corn borer and can be used in biocontrol of the pest.

Parasitic fungi increases the killing power of Bt biopesticide

Evidence implicating Bt biopesticides from GM crops has also emerged. Purified Bacillus thuringiensis Cry1Ab toxin was fed to Nosema infected and uninfected borer larvae. Nosema infection reduced the lethal dose of Cry1Ab toxin to one third the lethal dose of the uninfected larvae [11]. When Bacillus thuringiensis kurstaki (Dipel) formulations were used to treat Nosema pyrausta infected and uninfected corn borer larvae. The infected larvae had a lethal dose 45 times lower than the uninfected larvae [12].

I am not suggesting that biocontrol agents pose a threat to the honeybee, rather, the exposure to sub-lethal levels of systemic insecticides used in seed treatment of both conventional and GM crops and in widespread soil and foliar applications can affect beneficial insects by reducing their immunity to parasitic fungi. Furthermore, bees that otherwise are unaffected by exposure to Bt toxins in GM crops may succumb much more readily when they are infected with parasitic fungi, as reported in an experiment carried out at the University of Jena, Germany(13).

Tests have been carried out on one agent at a time.

Regulators have allowed extensive deployment of systemic insecticides for seed treatment and they have allowed extensive use of foliar sprays of the systemic insecticides on a wide array of food and feed crops. The impact of such pesticides on honeybees has been evaluated using measurements of lethal dose of the pesticides alone, ignoring the clear evidence that sub-lethal doses of the insecticides act synergistically with fungal parasites of the insects. The honeybees may be falling victim to “friendly fire” directed to exterminating insect pests. Unfortunately, regulators around the world have dealt with decline of honeybees through tunnel vision, ignoring well-established pesticide-fungal parasite interactions. It is time for the regulators to wake up and impose a ban on the systemic pesticides before more bees succumb.

1.Ho,M-W and Cummins,J. Mystery of disappearing bees Science in Society 2007 34 in press
2.Cummins,J. Requiem forthe honey bee Science in Society 2007 in press
3.Cummins,J. A parasitic fungus Nosema ceranea and honey bee decline in press
4. Ho,M-W Mobile phones and vanishing bees Science in Society 2007 , 34 in press
5. Feng MG and Pu XY. Time-concentration-mortality modeling of the synergistic interaction of Beauveria bassiana and imidacloprid against Nilaparvata lugens. Pest Manag Sci. 2005 Apr;61(4):363-70.
6. Cuthbertson AG, Walters KF and Deppe C. Compatibility of the entomopathogenic fungus Lecanicillium muscarium and insecticides for eradication of sweetpotato whitefly, Bemisia tabaci. Mycopathologia. 2005 Aug;160(1):35-41.
7. Santos AV, de Oliveira BL and Samuels RI. Selection of entomopathogenic fungi for use in combination with sub-lethal doses of imidacloprid: perspectives for the control of the leaf-cutting ant Atta sexdens rubropilosa Forel (Hymenoptera: Formicidae). Mycopathologia. 2007 Apr;163(4):233-40.
8. R Ramakrishnan, DR Suiter, CH Nakatsu, RA Humber and Bennett,G. Imidacloprid-Enhanced Reticulitermes flavipes (Isoptera: Rhinotermitidae) Susceptibility to the Entomopathogen Metarhizium anisopliae J. Econ. Entomol, 1999,92(5): 1125-32
9. Lomer CJ, Bateman RP, Johnson DL, Langewald J and Thomas M. Biological control of locusts and grasshoppers. Annu Rev Entomol. 2001;46:667-702.
10. Sarfraz, M. Keddie, A and Dosdall, L. Biological control of the diamondback moth, Plutella xylostella : A review Biocontrol Science and Technology 2005, 15,763-89
11. Reardon BJ, Hellmich RL, Sumerford DV and Lewis LC. Growth, development, and survival of Nosema pyrausta-infected European corn borers (Lepidoptera: Crambidae) reared on meridic diet and Cry1Ab. J Econ Entomol. 2004 Aug;97(4):1198-201.
12. Pierce CM, Solter LF and Weinzierl RA. Interactions between Nosema pyrausta (Microsporidia: Nosematidae) and Bacillus thuringiensis subsp. kurstaki in the European corn borer (Lepidoptera: Pyralidae). J Econ Entomol. 2001 Dec;94(6):1361-8.
13. Professor Hans-Heinrich Kaatz at the University of Jena found that the gene used to modify oil-seed rape had transferred to bacteria living inside honey bees.

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