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Parasite-insecticide interactions: a case study of Nosema ceranae and fipronil synergy on honeybee

New study in Nature - Scientific Reports finds strong evidence for pesticide + pathogen hypothesis as key explanation for bee disorders.

ABSTRACT: In ecosystems, a variety of biological, chemical and physical stressors may act in combination to induce illness in populations of living organisms. While recent surveys reported that parasite-insecticide interactions can synergistically and negatively affect honeybee survival, the importance of sequence in exposure to stressors has hardly received any attention. In this work, Western honeybees (Apis mellifera) were sequentially or simultaneously infected by the microsporidian parasite Nosema ceranae and chronically exposed to a sublethal dose of the insecticide fipronil, respectively chosen as biological and chemical stressors. Interestingly, every combination tested led to a synergistic effect on honeybee survival, with the most significant impacts when stressors were applied at the emergence of honeybees. Our study presents significant outcomes on beekeeping management but also points out the potential risks incurred by any living organism frequently exposed to both pathogens and insecticides in their habitat.

Imidacloprid in Melon Guttation Fluid: A Potential Mode of Exposure for Pest and Beneficial Organisms

ABSTRACT ELISA techniques were used to detect imidacloprid in guttation fluid of young cantaloupe plants in Arizona. Imidacloprid was detected at up to 4.1 micro g/ml (ppm) in a coincidental guttation collection 3 d after a top label rate soil application and at 37 micro g/ml one d after a separate top label rate soil application study. These imidacloprid titers exceed reported median oral toxicities for several insect species by factors of 10 or more. Pesticides in guttation fluid are a relatively unexplored route of exposure for both pest and beneficial insects, and could represent an important risk for both of these groups in guttation-prone environments.

Ecologically Appropriate Xenobiotics Induce Cytochrome P450s in Apis mellifera

Abstract
Background: Honey bees are exposed to phytochemicals through the nectar, pollen and propolis consumed to sustain the colony. They may also encounter mycotoxins produced by Aspergillus fungi infesting pollen in beebread. Moreover, bees are exposed to agricultural pesticides, particularly in-hive acaricides used against the parasite Varroa destructor. They cope with these and other xenobiotics primarily through enzymatic detoxificative processes, but the regulation of detoxificative enzymes in honey bees remains largely unexplored.
Methodology/Principal Findings: We used several approaches to ascertain effects of dietary toxins on bee susceptibility to synthetic and natural xenobiotics, including the acaricide tau-fluvalinate, the agricultural pesticide imidacloprid, and the naturally occurring mycotoxin aflatoxin. We administered potential inducers of cytochrome P450 enzymes, the principal biochemical system for Phase 1 detoxification in insects, to investigate how detoxification is regulated. The drug phenobarbital induces P450s in many insects, yet feeding bees with phenobarbital had no effect on the toxicity of taufluvalinate, a pesticide known to be detoxified by bee P450s. Similarly, no P450 induction, as measured by tau-fluvalinate tolerance, occurred in bees fed xanthotoxin, salicylic acid, or indole-3-carbinol, all of which induce P450s in other insects.
Only quercetin, a common pollen and honey constituent, reduced tau-fluvalinate toxicity. In microarray comparisons no change in detoxificative gene expression was detected in phenobarbital-treated bees. However, northern blot analyses of guts of bees fed extracts of honey, pollen and propolis showed elevated expression of three CYP6AS P450 genes. Diet did not influence tau-fluvalinate or imidacloprid toxicity in bioassays; however, aflatoxin toxicity was higher in bees consuming sucrose or high-fructose corn syrup than in bees consuming honey.
Conclusions/Significance: These results suggest that regulation of honey bee P450s is tuned to chemicals occurring naturally in the hive environment and that, in terms of toxicological capacity, a diet of sugar is not equivalent to a diet of honey.

Honey bees (Apis mellifera) reared in brood combs containing high levels of pesticide residues exhibit increased susceptibility to Nosema (Microsporidia) infection.

Abstract: Nosema ceranae and pesticide exposure can contribute to honey bee health decline. Bees reared from brood comb containing high or low levels of pesticide residues were placed in two common colony environments. One colony was inoculated weekly with N. ceranae spores in sugar syrup and the other colony received sugar syrup only. Worker honey bees were sampled weekly from the treatment and control colonies and analyzed for Nosema spore levels. Regardless of the colony environment (spores+syrup added or syrup only added), a higher proportion of bees reared from the high pesticide residue brood comb became infected with N. ceranae, and at a younger age, compared to those reared in low residue brood combs. These data suggest that developmental exposure to pesticides in brood comb increases the susceptibility of bees to N. ceranae infection.

Assessment of the Environmental Exposure of Honeybees to Particulate Matter Containing Neonicotinoid Insecticides Coming from Corn Coated Seeds

ABSTRACT: Since seed coating with neonicotinoid insecticides was introduced in the late 1990s, European beekeepers have reported severe colony losses in the period of corn sowing (spring). As a consequence, seed-coating neonicotinoid insecticides that are used worldwide on corn crops have been blamed for honeybee decline. In view of the currently increasing crop production, and also of corn as a renewable energy source, the correct use of these insecticides within sustainable agriculture is a cause of concern. In this paper, a probable - but so far underestimated - route of environmental exposure of honeybees to and intoxication with neonicotinoid insecticides, namely, the atmospheric emission of particulate matter containing the insecticide by drilling machines, has been quantitatively studied. Using optimized analytical procedures, quantitative measurements of both the emitted particulate and the consequent direct contamination of single bees approaching the drilling machine during the foraging activity have been determined. Experimental results show that the environmental release of particles containing neonicotinoids can produce high exposure levels for bees, with lethal effects compatible with colony losses phenomena observed by beekeepers.

Bee Exposure to Treated Seed Dust During Planting Confirmed

[Viewpoint Beyond Pesticides] Washington, DC--(ENEWSPF)--February 28, 2012. A study by researchers at the University of Padova in Italy and published in the journal Environmental Science and Technology has confirmed the findings of previous research showing that honey bees are exposed to toxic neonicotinoid insecticides during spring seed planting. Neonicotinoids are known to be highly toxic to honey bees and, yet, are used on millions of acres through North America every year. These findings lend even greater urgency to the need to take these chemicals off the market and ensure the continued survival of honey bees and the essential pollination services that they provide for our food system.

Sub-Lethal Effects of Imidacloprid Exposure on Honey Bee Queen Egg-Laying and Activity

Wu, J., V. Krischik and M. Spivak, Department of Entomology, University of Minnesota; St. Paul, MN 55108
Abstract for the 2012 American Bee Research Conference, February 7-8 2012 Greenbelt.

Pesticides such as neonicotinoid insecticides have been implicated as a contributing factor to honey bee losses. The objective of this study is to examine sub-lethal effects of imidacloprid on honey bee queen egg-laying and activity. Observation hives, containing about 1500 bees and a laying queen on newly drawn comb, were given 80 ml of sugar syrup with various imidacloprid treatments (0, 20, 50, 100 ppb) every other day. A total of 16 observation hives, or 4 colonies per treatment, were set-up in July and August of 2011. Queen egg-laying rate and activity were recorded in 15-minute intervals and quantified over 3 weeks. After 3 weeks, colonies were quantified for total adult and brood population, nectar and pollen stores, presence of disease, and weight of newly emerged bees. Preliminary results show that queen laying rates were affected at each imidacloprid treatment dose (20, 50, and 100 ppb). This study will be repeated in the summer of 2012. The findings will improve our understanding of known imidacloprid studies on honey bee colonies and workers. In addition, this study will highlight the need to focus future risk assessment studies on sub-lethal effects of neonicotinyl insecticides on honey bee queen health and behavior.

A Quantitative Model of Honey Bee Colony Population Dynamics

Abstract
Since 2006 the rate of honey bee colony failure has increased significantly. As an aid to testing hypotheses for the causes of colony failure we have developed a compartment model of honey bee colony population dynamics to explore the impact of different death rates of forager bees on colony growth and development. The model predicts a critical threshold forager death rate beneath which colonies regulate a stable population size. If death rates are sustained higher than this threshold rapid population decline is predicted and colony failure is inevitable. The model also predicts that high forager death rates draw hive bees into the foraging population at much younger ages than normal, which acts to accelerate colony failure. The model suggests that colony failure can be understood in terms of observed principles of honey bee population dynamics, and provides a theoretical framework for experimental investigation of the problem.

Worldwide honey bee colony losses continue

International Bee Research Association Press Release 1 February 2012
Since 2006 there has been concern worldwide about losses of honey bee colonies, especially the phenomenon of “Colony Collapse Disorder” in the USA. Information about the extent of these losses has,to date, been patchy, unsystematic and difficult to compare year on year and from country to country. Today, for the first time, the results of systematic surveys in Europe, north America, China, Israel and Turkey are published together in the Journal of Apicultural Research.

Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema

Abstract: Global pollinator declines have been attributed to habitat destruction, pesticide use, and climate change or some combination of these factors, and managed honey bees, Apis mellifera, are part of worldwide pollinator declines. Here we exposed honey bee colonies during three brood generations to sub-lethal doses of a widely used pesticide, imidacloprid, and then subsequently challenged newly emerged bees with the gut parasite, Nosema spp. The pesticide dosages used were below levels demonstrated to cause effects on longevity or foraging in adult honey bees. Nosema infections increased significantly in the bees from pesticide-treated hives when compared to bees from control hives demonstrating an indirect effect of pesticides on pathogen growth in honey bees. We clearly demonstrate an increase in pathogen growth within individual bees reared in colonies exposed to one of the most widely used pesticides worldwide, imidacloprid, at below levels considered harmful to bees. The finding that individual bees with undetectable levels of the target pesticide, after being reared in a sub-lethal pesticide environment within the colony, had higher Nosema is significant. Interactions between pesticides and pathogens could be a major contributor to increased mortality of honey bee colonies, including colony collapse disorder, and other pollinator declines worldwide.

Multiple Routes of Pesticide Exposure for Honey Bees Living Near Agricultural Fields

Abstract
Populations of honey bees and other pollinators have declined worldwide in recent years. A variety of stressors have been implicated as potential causes, including agricultural pesticides. Neonicotinoid insecticides, which are widely used and highly toxic to honey bees, have been found in previous analyses of honey bee pollen and comb material. However, the routes of exposure have remained largely undefined. We used LC/MS-MS to analyze samples of honey bees, pollen stored in the hive and several potential exposure routes associated with plantings of neonicotinoid treated maize. Our results demonstrate that bees are exposed to these compounds and several other agricultural pesticides in several ways throughout the foraging period. During spring, extremely high levels of clothianidin and thiamethoxam were found in planter exhaust material produced during the planting of treated maize seed. We also found neonicotinoids in the soil of each field we sampled, including unplanted fields. Plants visited by foraging bees (dandelions) growing near these fields were found to contain neonicotinoids as well. This indicates deposition of neonicotinoids on the flowers, uptake by the root system, or both. Dead bees collected near hive entrances during the spring sampling period were found to contain clothianidin as well, although whether exposure was oral (consuming pollen) or by contact (soil/planter dust) is unclear. We also detected the insecticide clothianidin in pollen collected by bees and stored in the hive. When maize plants in our field reached anthesis, maize pollen from treated seed was found to contain clothianidin and other pesticides; and honey bees in our study readily collected maize pollen. These findings clarify some of the mechanisms by which honey bees may be exposed to agricultural pesticides throughout the growing season. These results have implications for a wide range of large-scale annual cropping systems that utilize neonicotinoid seed treatments.

Current toxicological risk assessment can lead to serious underestimates of actual risk of neonicotinoids

The traditional approach to toxicity testing is to consider dose (concentration)-effect relationships at arbitrarily fixed exposure durations which are supposed to reflect ‘acute’ or ‘chronic’ time scales. This approach measures the proportion of all exposed individuals responding by the end of different exposure times. Toxicological databases established in this way are collections of endpoint values obtained at fixed times of exposure. As such these values cannot be linked to make predictions for the wide range of exposures encountered by humans or in the environment. Thus, current toxicological risk assessment can be compromised by this approach to toxicity testing, as will be demonstrated in this paper, leading to serious underestimates of actual risk. This includes neonicotinoid insecticides and certain metallic compounds, which may require entirely new approaches.

Urgent call for EU-wide action to halt bee deaths

On 15 November 2011 the EU parliament voted for a resolution on honeybee health. Rising bee mortality could have a serious impact on Europe's food production and environmental stability, as most plants are pollinated by bees, warned MEPs on Tuesday. Parliament's resolution calls on the EU to step up investment in research on new medicines and coordinate its efforts to protect what is fast becoming an endangered species.

New directions in crop protection

Current Biology, Volume 21, Issue 17, 13 September, 2011
The spread of herbicide-resistant weeds, progress in genomics, climate change and the continuing worries about pollinator decline are forcing companies to rethink their approach to crop protection. Michael Gross reports.

Save The Bees Petition in New Zealand by MP

Thursday, 08 Sep 2011
Report by Sue Kedgley MP in New Zealand to the Local Government and Environment Select Committee

1. An urgent reassessment by the ERMA [now EPA] of Neonicotinoid insecticides, and the use of other pesticides that are highly toxic to bees

The petition calls for an urgent reassessment by the Environment Protection Agency of the use of Neonicotinoid insecticides in New Zealand-and in particular their use as a seed coating on seeds such as grass and maize, as there is mounting evidence that Neonicotinoids may be contributing to unacceptable levels of bee deaths and to the phenomenon of Colony Collapse Disorder overseas.

Exposure to Sublethal Doses of Fipronil and Thiacloprid Highly Increases Mortality of Honeybees Previously Infected by Nosema ceranae

ABSTRACT: 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.

Contribution of Pollinator-Mediated Crops to Nutrients in the Human Food Supply

ABSTRACT: The contribution of nutrients from animal pollinated world crops has not previously been evaluated as a biophysical measure for the value of pollination services. This study evaluates the nutritional composition of animal-pollinated world crops. We calculated pollinator dependent and independent proportions of different nutrients of world crops, employing FAO data for crop production, USDA data for nutritional composition, and pollinator dependency data according to Klein et al. (2007). Crop plants that depend fully or partially on animal pollinators contain more than 90% of vitamin C, the whole quantity of Lycopene and almost the full quantity of the antioxidants β-cryptoxanthin and β-tocopherol, the majority of the lipid, vitamin A and related carotenoids, calcium and fluoride, and a large portion of folic acid. Ongoing pollinator decline may thus exacerbate current difficulties of providing a nutritionally adequate diet for the global human population.

UCSF Finds New Bee Viruses, Offers Baseline to Study Colony Collapse

A 10-month study of healthy honey bees by University of California, San Francisco (UCSF) scientists has identified four new viruses that infect bees, while revealing that each of the viruses or bacteria previously linked to colony collapse is present in healthy hives as well.

Authorities Say Pesticide Caused Bee Deaths, Announce Lawsuits

Ljubljana, 3 June (STA) - Slovenian agriculture authorities have confirmed that a pesticide suspected of causing massive bee deaths in NE Slovenia in late April was indeed a leading cause of the deaths and announced new measures, including lawsuits against producers of the pesticide.

Wild bees and not honeybees the main pollinators of UK crops

Researchers from the University of Reading have shown that wild bees are the unsung heroes for our food security and not honeybees as previously thought.

Beehive must wake up to honey bee crisis

[NGO viewpoint, Wednesday, 25 May 2011 Sue Kedgley]
Unless we take decisive action to protect our bees, we could be faced with massive bee deaths, a horticultural industry in crisis, food shortages and escalating food prices.

The honey bee is indispensable to our horticulture, our ecology and our economy. Yet the honey bee is in crisis all around the world, with bee populations being decimated by a phenomenon known as Colony Collapse Disorder, where entire colonies of bees disappear.

Slovenia bans neonicotinoids after massive bee deaths in Pomurje region

Treated Corn Seed and Pesticide Banned as Bee Deaths Continue
Ljubljana, 28 April 2011 (STA) - The government of Slovenia issued a temporary ban Thursday on seeds treated with neonicotinoid pesticides which have caused massive bee deaths in the northeastern Pomurje region in the recent weeks. The use of Biscay, a pesticide, will also be limited.

Neonicotinoid implicated in Honeybee mass poisoning incidents

An investigation by Buglife – the Invertebrate Conservation Trust has revealed that contrary to statements made by Government scientists from the National Bee Unit on yesterday’s Channel 4 News item - http://www.channel4.com/news/bee-decline-not-caused-by-pesticides -, there is evidence of an increasing link between Neonicotinoid pesticides and bee deaths in Britain.

Spotlight falls on pesticide over bee deaths

HELEN MURDOCH , Nelson Mail, 1-Apr-2011
It is used for seed dressings, on agricultural crops, soil treatment, compost products, in wood preservatives and in animal flea treatments. But the synthetic neonicotinoid pesticide family is under the spotlight of beekeepers and the Green Party for its possible bee-killing properties.

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