Vidau C, Diogon M, Aufauvre J, Fontbonne R, Vigues B, Brunet JL et al.. Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PLoS ONE 6: e21550

Clermont Université, Laboratoire Microorganismes: Génome et Environnement, BP 10448, Clermont-Ferrand, France.
PLoS ONE (Impact Factor: 3.23). 06/2011; 6(6):e21550. DOI: 10.1371/journal.pone.0021550
Source: PubMed


The honeybee, Apis mellifera, is undergoing a worldwide decline whose origin is still in debate. Studies performed for twenty years suggest that this decline may involve both infectious diseases and exposure to pesticides. Joint action of pathogens and chemicals are known to threaten several organisms but the combined effects of these stressors were poorly investigated in honeybees. Our study was designed to explore the effect of Nosema ceranae infection on honeybee sensitivity to sublethal doses of the insecticides fipronil and thiacloprid.

Five days after their emergence, honeybees were divided in 6 experimental groups: (i) uninfected controls, (ii) infected with N. ceranae, (iii) uninfected and exposed to fipronil, (iv) uninfected and exposed to thiacloprid, (v) infected with N. ceranae and exposed 10 days post-infection (p.i.) to fipronil, and (vi) infected with N. ceranae and exposed 10 days p.i. to thiacloprid. Honeybee mortality and insecticide consumption were analyzed daily and the intestinal spore content was evaluated 20 days after infection. A significant increase in honeybee mortality was observed when N. ceranae-infected honeybees were exposed to sublethal doses of insecticides. Surprisingly, exposures to fipronil and thiacloprid had opposite effects on microsporidian spore production. Analysis of the honeybee detoxification system 10 days p.i. showed that N. ceranae infection induced an increase in glutathione-S-transferase activity in midgut and fat body but not in 7-ethoxycoumarin-O-deethylase activity.

After exposure to sublethal doses of fipronil or thiacloprid a higher mortality was observed in N. ceranae-infected honeybees than in uninfected ones. The synergistic effect of N. ceranae and insecticide on honeybee mortality, however, did not appear strongly linked to a decrease of the insect detoxification system. These data support the hypothesis that the combination of the increasing prevalence of N. ceranae with high pesticide content in beehives may contribute to colony depopulation.

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    • "For example, pesticide exposure can increase pathogen loads and jeopardize colony survival (Alaux et al. 2010, Vidau et al. 2011, Aufauvre et al. 2012, Pettis et al. 2012, Wu et al. 2012, Di Prisco et al. 2013). Honey bee behavior also can be altered by pesticides (El Hassani et al. 2005, Aliouane et al. 2009), and these compounds can increase colony susceptibility to loss from parasites such as Nosema or from queen failure (Vidau et al 2011; Wu et al. 2012; DeGrandi- Hoffman et al. 2013a; Pettis et al. 2012, 2013). While insecticides, especially neonicotinoids, often are implicated in pollinator losses (e.g., Blacquiere et al. 2012, Gill et al. 2012), honey bees and other pollinators are more likely to encounter fungicides. "
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    ABSTRACT: Sublethal exposure to fungicides can affect honey bees (Apis mellifera L.) in ways that resemble malnutrition. These include reduced brood rearing, queen loss, and increased pathogen levels. We examined the effects of oral exposure to the fungicides boscalid and pyraclostrobin on factors affecting colony nutrition and immune function including pollen consumption, protein digestion, hemolymph protein titers, and changes in virus levels. Because the fungicides are respiratory inhibitors, we also measured ATP concentrations in flight muscle. The effects were evaluated in 3- and 7-d-old worker bees at high fungicide concentrations in cage studies, and at field-relevant concentrations in colony studies. Though fungicide levels differed greatly between the cage and colony studies, similar effects were observed. Hemolymph protein concentrations were comparable between bees feeding on pollen with and without added fungicides. However, in both cage and colony studies, bees consumed less pollen containing fungicides and digested less of the protein. Bees fed fungicide-treated pollen also had lower ATP concentrations and higher virus titers. The combination of effects we detected could produce symptoms that are similar to those from poor nutrition and weaken colonies making them more vulnerable to loss from additional stressors such as parasites and pathogens. Published by Oxford University Press on behalf of Entomological Society of America 2015. This work is written by US Government employees and is in the public domain in the US.
    Journal of Economic Entomology 08/2015; DOI:10.1093/jee/tov251 · 1.51 Impact Factor
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    • "A second species named Nosema ceranae was more recently described and is now the predominant microsporidian species in Apis mellifera. Interestingly, N. ceranae has been shown to have more negative impacts on honey bees than N. apis (Williams, Shutler, Burgher-MacLellan, & Rogers, 2014) and some studies provided evidence of a role of N. ceranae in colony losses alone (Higes et al., 2008), or in combination with other stressors such as pesticides (Aufauvre et al., 2012; Vidau et al., 2011), viruses (Bromenshenk et al., 2010). It has also been demonstrated that infection of honeybee colonies by Nosema may decrease the efficacy of acaricide treatment used to fight the mite Varroa destructor (Botías et al., 2012). "
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    ABSTRACT: Nosemosis is one of the most common and widespread diseases of adult honeybees. The causative agents, Nosema apis and Nosema ceranae, belong to microsporidia some obligate intracellular eukaryotic parasites. In this study, 10 sulphated polysaccharides from algae were evaluated for their antimicrosporidian activity. They were first shown to inhibit the in vitro growth of the mammal microsporidian model, Encephalitozoon cuniculi. The most efficient polysaccharides were then tested for their ability to inhibit the growth of Nosema ceranae in experimentally-infected adult honeybees. Two polysaccharides extracted from Porphyridium spp. did not show any toxicity in honeybees and one of them allowed a decrease of both parasite load and mortality rate due to N. ceranae infection. A decrease in parasite abundance but not in mortality rate was also observed with an iota carrageenan. Our results are promising and suggest that algal sulphated polysaccharides could be used to prevent and/or control bee nosemosis.
    Carbohydrate Polymers 07/2015; 133:213-220. DOI:10.1016/j.carbpol.2015.07.022 · 4.07 Impact Factor
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    • "In contrast to previously reported synergistic effects between neonicotinoid pesticides and N. ceranae (Alaux et al., 2010; Vidau et al., 2011; Aufauvre et al., 2012; Pettis et al., 2012), our data provided no such evidence. A potential explanation for this difference may be that previous studies were carried out under laboratory conditions . "
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    ABSTRACT: Interactions between pesticides and parasites are believed to be responsible for increased mortality of honey bee (Apis mellifera) colonies in the northern hemisphere. Previous efforts have employed experimental approaches using small groups under laboratory conditions to investigate influence of these stressors on honey bee physiology and behaviour, although both the colony level and field conditions play a key role for eusocial honeybees. Here, we challenged honey bee workers under in vivo colony conditions with sub-lethal doses of the neonicotinoid thiacloprid, the miticide tau-fluvalinate, and the endoparasite Nosema ceranae, to investigate potential effects on longevity and behaviour using observation hives. In contrast to previous laboratory studies our results do not suggest interactions among stressors, but rather lone effects of pesticides and the parasite on mortality and behaviour, respectively. These effects appear to be weak due to different outcomes at the two study sites, thereby suggesting that the role of thiacloprid, tau-fluvalinate, and N. ceranae and interactions among them may have been overemphasized. In the future, investigations into the effects of honey bee stressors should prioritize the use of colonies maintained under a variety of environmental conditions in order to obtain more biologically relevant data. This article is protected by copyright. All rights reserved.
    Environmental Microbiology 03/2015; DOI:10.1111/1462-2920.12825 · 6.20 Impact Factor
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