Veterinary Treatments

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Veterinary Treatments

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Contents

As far as European "traditional" bee pathologies or parasites are concerned and in most cases, either enough efficient organic methods are known, or the beekeepers can trust the natural defence mechanisms developed by Apis mellifera over millennia of coevolution. Despite of this, some beekeepers still do use pesticides or repellents as a remedy to beehive intruders, like, e.g., the wax moth. As far as "new" pathologies or parasites are concerned, that is to say the ones that were recently introduced in Europe under the influence of the human being (see Bee Trading and Global Trading, and became invasive, as this is e.g. the case for varroa, organic methods are still under development and information on these methods spread very slowly. In response to the amplitude of the damage caused by those "new" pathologies and parasites and in the absence of known alternative methods, beekeepers have mostly resorted to chemotherapy.

What is the Problem about the "Medicine" Used in Beekeeping?

Roughly, beekeepers use two kinds of "medicine":

  1. Pesticides or antibiotics: most acaricides have e.g. originally been used in agriculture and found application as treatment against bee pest. Some of them, like amitraz that used to be applied on fruit trees, have been forbidden in the European Union for their ecotoxicity, but are still available in countries that grant a "marketing authorisation" for special applications, like this is e.g. the case for varroa control. The active substances fluvalinate and its derivates, amitraz, and coumaphos have been most commonly used. Also, common insect repellents like PDCB are used e.g. for wax moth control.
  2. "Natural" substances: the most commonly used are organic acids like formic, lactic and oxalic acid, and thymol. Since these substances are highly irritant, thus present manipulation constraints, beekeepers often prefer getting back to pesticides.

Overview of Pesticides and Antibiotics Used in Beekeeping (with their effects on bees, humans and the wider environment)

Lack of Efficiency

Beekeepers have often complained about the lack of actual efficiency of pesticides. A Canadian beekeeper and researcher, for example, found out that 60% of the varroa mites knocked down by pesticides were not killed and were able to climb back in the beehive to parasite the bees again.[1]

Development of Resistance by Pests

The lack of efficiency may partly result from the well-known natural development resistance that pest are able to develop by pests against poisons.

Varroa was for example able to develop successively a resistance more and more rapidly against all acaricides up to now: Amitraz was first used until varroa developed a resistance in 1986. Fluvalinate succeeded in 1998, to which varroa became resistant within seven years. Coumaphos, an extremely toxic substance, was first applied in 1988 and the first resistance cases were mentioned by 2001: Varroa became this time resistant within only three years. With the use of fluvalinate, varroa developed a cross-resistance against all pyrethoids, a family of pesticides that comprise acrinathrin, flumethrin and amitraz.[2][3][4][3][5]

The development of new active substances is only a race forward, as it will be necessary to develop steadily new and more virulent formulations with increased environmental and health risks for the users. As stated in a report by Vita, a company that develops honeybee "health" products: "The chemical family of the active ingredient used for varroa treatment must be changed regularly in order for these substances to remain effective."[6]

It is commonly admitted that pests are not be able to develop a resistance against organic acids, since these naturally occur in the metabolic process of all organisms, thus cannot be rendered harmless through enzymatic effects.[7]

Toxicity in Bees

With the exception of flumethrin - for which no obvious adverse effect has been demonstrated up to now - all chemotherapeutic substances have shown some degree of toxicity in bees.[7][8]

Fluvalinate and amitraz have been reputed to have low toxicity in bees. Nevertheless, new formulations of fluvalinate to overcome the resistance developed by varroa, like tau-fluvalinate, are highly toxic for bees.[9] More recent studies have revealed that amitraz might be more toxic in bees than formerly assumed.[2] Regardless of this, high toxicity of fluvalinate and amitraz has been demonstrated in young bees[10], and adults and larvae mortality appears to be higher than normal after an amitraz or coumaphos treatment.[7]

If some pesticides are reputed to be of low toxicity for bees, sublethal effects are more difficult to demonstrate. Researchers of the University of Annaba, Algeria, however observed a decrease in the body sizes of the workers resulting from the stress by increased production of specific enzymes needed for desintoxication by the bees after an acaricide treatment.[11] Bees in the larval stage are particularly vulnerable, while studies have detected acaricide residues in the larval feeding jelly and e.g. coumaphos is known to affect larval development.[2] Some acaricides, like Coumaphos, have shown to reduce the viability and/or fertility of queens.[4][12]

The fact that a substance is "natural" does not mean that it is harmless: Among the chemotherapies used against varroa, formic acid is most fatal to bees, with a death rate of 35.3 bees/hive/day. Brood and hatching bees are particularly vulnerable to formic acid. After a lactic acid treatment, the workers remove 60% of the eggs from the hive and bee mortality increases by four. Oxalic acid affects significantly larval development and queen survival.[7] Formic acid is most effective at temperatures between 12 and 25°C. Above those temperatures, bees may become agitated and may leave the hive[13] (while the normal temperature inside a hive is 32-36°C).

Pesticides at sublethal levels have also shown to impair the immune system and the "learning" ability of bees, delaying thereby any capacity toward developing defence mechanisms against varroa.[9]

Bees that have been exposed to pesticides are more sensitive to diseases and show higher infection rates.[14] The application of coumaphos, for example, have shown to multiply exponentially the Black Queen Cell Virus (BQCV) leading to colony collapse.[15]

Increased mortality and weakening of workers deprive a colony of precious labour, thus increase the colony's vulnerability to further environmental influences.

Inhibition of the Immune System

A study on bumblebees[16] showed that bacteria living in bee guts protect their hosts against harmful parasitic bacteria, exactly as this is the case in humans. These useful bacteria are transmitted socially by eating other bees' faeces, while the mechanism of the resulting resistance to diseases in bees is not known. However sub-lethal doses of veterinary chemical treatments on bees damages the bees' gut flora, contributing to reducing bees’ immunity, thereby leaving an open a door to infectious diseases.

Inhibition of Coevolution

A Comparison Case

Gypsy moths were imported from Europe to the United State in 1869 to cross them with the silkworm in the aim of creating a more productive species. Gypsy moths escaped from the laboratory successfully reproduced with disastrous consequences for the Northern-American oak forests. First organic control trials were performed in 1910, with the introduction of a fungus, Entomophaga maimaiga, which was known to infect a closely related Lepidoptera species in Japan. This first did not bring any remediation and E. maimaiga was considered as extinct in North America after some time. Insecticide use from the 1940s also remained inefficient, then progressively abandoned after the publication of Rachel Carson's "Silent Spring"[17] triggered general public disapprobation of the use of pesticides. Gypsy moth infestation showed a peak in 1981 on which their populations suddenly dropped. The following peaks remained largely moderate. This was due to two reasons. First, after the oak forests had been decimated, the surviving oaks were the one that owned a higher toxicity, which cause a gypsy moth population decreased due to malnutrition. The second was that the suddenly "resurrected" E. maimaiga had finally been successful in infecting the gypsy moth: According to the environmentalists, the pesticides were responsible for the delayed spreading of E. maimaiga. The application of pesticides to fight the gypsy moth had decimated numerous other non-targeted other insect species, which were potential hosts for E. maimaiga. This reduced the opportunities for E. maimaiga to rapidly adapt to new host and thereby to contaminate progressively the gipsy moth.[18]

This story shows an example on how the use of pesticide may delay environmental adaptative response to new situations.

Cases of Successful Coevolution with the Varroa Mite

An experience have been performed from 2000 to 2005 in the South of the Swedish Island Gotland, after a coevolution between bees and varroa mites had been observed on a tropical island in Brazil where bee colonies had been left untreated. The experience consisted in leaving varroa-infested bee colonies unmanaged and without treatment. After a steady increase of the varroa infestations and important losses in the bee population during the first thee years, the curve reversed from the third year, and the colonies that had been able to survive were observed to have reached a balanced relationship with the varroa mite. The mite populations fell considerably and the bee population begun again to swarm after inhibited colony reproduction for several years.[19]

A subsequent study[20] comparing the evolution over one year of treated colonies and colonies that had survived varroa infestation for 6 years without treatment suggested that natural selection pressures in untreated colonies had led to an adaptative evolution of the bees. The treated colonies experienced a much steeper increase of varroa infestations through the summer than the untreated colonies. The untreated colonies were observed to produce fewer drones and worker brood and the proportion of mites in the sealed brood (rather than on adult bees) was much smaller in the untreated colonies, while the success of varroas to enter brood cell is considered to be an important factor for the further development of varroa populations. The authors of the study, Fries and Bommarco, concluded that these aspects may be traits developed in honeybees in response to the varroa phenomenon.

According to Fries, Imdorf, and Rosenkranz[19]: "the problems facing the apicultural industry with mite infestations probably is linked to the apicultural system, where beekeepers remove the selective pressure induced from the parasitism by removing mites through control efforts."

However, as Fries and Bommarco point out[20], it must be admitted that relying uniquely on the natural selection strategy is likely to result in massive bee population losses in a first phase, which would threaten the livelihood of beekeepers and the industries based on bee products, lead to massive losses in agriculture and horticulture and jeopardize the wider ecological systems. It appears thus important to work at developing alternative and softer control methods (see e.g. Organic Varroa Control on this topic) of invasive organisms that for example promote adapted hygienic behaviours in bees or promote varroa predators or pathologies rather than attempting to control the varroa mite population, which will probably only result in an endless and unavailing fight.

Residues in Bee Products

It is a common practice in beekeeping to recycle wax to make "comb foundations". The recycling work is usually given to beekeeping supply specialists. Pesticides are lipophilic, thus accumulate in bee wax. Bee wax suppliers may mix the wax from different beekeepers, thus different treatments used by different beekeepers that have accumulated in the wax.[21][13]

Stored in the wax, acaricides or acaricide metabolites are released slowly into the larval jelly and the honey. This benefits varroa, in which low doses create favourable conditions to become rapidly resistant[4] while impairing the bees' health as explained above and jeopardizing the quality of honey both as a source of food for bees and as a commercial product. The older the wax, the higher the level of contamination.[13]

Coumaphos and other acaricides remain very stable in wax and do not degrade.[22] Acaricides with short half-lives like amitraz are reputed not to accumulate in bee wax, but as studies begun to investigate also the presence of their metabolites in wax, these have been detected.[9] Amitraz metabolites are more persistent than the parent substance.[23][24]

If beekeepers decide to change the treatment after its efficiency has decreased, it can last up to 12 years until the contamination level in the wax sinks under the detection level.[22] The new substance is thus added to the residual molecules of the former treatment. Moreover, bee workers bring back to the hive further pesticides from treated fields where they gathered contaminated pollen and nectar (see also the Agricultural Pesticides section) and further contaminants may enter the hive and bee products due to inadequate construction material used for hives, the atmospheric pollution in the surrounding of the hives or the presence of contaminants in the water collected by the workers (see also the Atmospheric and Aquatic Pollution section). Up to 17 pesticides could be identified in one single pollen sample, while acaricides made out the greatest proportion.[9] The "cocktail" of all those different chemicals may have additive or synergistic effects.

The effect of metabolites and the synergy of several pesticides and pollutants from different origins on the health of bees are unpredictable and have been insufficiently studied up to now. Nevertheless, it is allowed to assume on the base of available studies on chemical synergies that the combination of several chemicals, even in low doses of each, moreover in chronic exposure, may affect bees harder than one single pesticide at high dose.[25][9][26]

Pest treatment residues have been found in all bee products: like wax, pollen, honey and propolis.[9][22][13]

There are no international norms concerning acaricide Maximum Residue Limits (MRL) in honey, thus the legal permitted level can vary from country to country. For some substances, no MRL have been determined at all.[27][24] While most studies on the contamination of honey by acaricides have rather been unalarming, a considerable number of samples did exceed the most stringent MRLs (corresponding to the levels permitted in Germany and Italy) and even, in relatively few but some cases, the less stringent EC and EPA standards. Some pesticides, like tau-fluvalinate and flumethrin, have shown to be very stable in honey.[22][28][29][27] No amitraz in its undegraded form have been detected in honey, this substance remains nevertheless a significant source of pesticide residues in honey in its metabolite forms, as these do remain stable in honey. Pesticide metabolites should therefore be also taken into account in determining MRLs of an active substance.[24]

Only by the disparities about MRLs adopted by different national and supranational governments, it is allowed to question what can be accepted as "safe" residue level in honey for human consumption, if there is any. Due to multiple pesticides that may have accumulated in wax over the different treatments, the honey may be also contaminated with a pesticide mix for which again additive and synergistic effects should be taken in account in estimating risks for human consumption of honey or other bee products contaminated by pesticides, especially for chronic bee product eaters and sensitive population groups like unborn and born children and the elderly, while statistics have shown that infants and young children have the highest honey daily intake relatively to their body weight.[24]

Organic acids are natural components of bee products and do not accumulate, but they can only be applied after the honey harvest and before the winter, unless time would not be sufficient for them to evaporate, thus excessive proportions would affect the organoleptic properties of the honey and make them unfit for commercialisation, since taste-altering additives are prohibited in honey in most countries.[13][7][30][31]

Inappropriate Use by Beekeepers

Another cause of concern is the manipulation of pesticides by persons that are insufficiently informed about the hazards of pesticides. Most pesticide package inserts give instructions about protection measures to be taken during the manipulation and on how to discard the product residues, but users often read the inserts superficially or even completely disregard it. Moreover, pesticide packaging largely play down the hazards of pesticides with either an attractive or neutral (pharmaceutical) presentation of the product. (See also my works on private gardening about common prejudices about the use of pesticides in the private sphere.)

Some beekeepers, due also among others to the high costs and the restricted access by veterinary prescription, disregard the instructions given with the pesticide and either leave diffuser strips for too long in the hive, leave them over the winter, sometimes even completely forget them in the hive, make too frequent or incorrect applications of the chemicals and reuse strips or spray the strips over with other formulations. Some beekeepers also divert other products which are based on the same active substances and normally used in agriculture or for other purposes like tick control in pets to manufacture their own treatments, while those products may have an inadequate dosage for the purpose.[13][29][15] Studies detected in honey samples residues above MRLs of substances of which use is forbidden in the frame of pest treatment in beehives, such as tetracycline.[27]

While pesticides used in veterinary treatments are regulated and mostly available on prescription only, their discarding is submitted to neither regulation nor control, while most pesticide users dump diffuser media in household waste rather than bringing them to the hazardous waste site, and wash out material used for pesticide application in the domestic sink. Those practices represent a source of environmental contamination.

Finally, if instructions are not properly respected, the manipulation is hazardous to the beekeepers themselves and the people in their environment, since most pesticides are contact poisons or very irritant, can be inhaled or get into the eyes during manipulation. See the Overview of Pesticides and Antibiotics Used in Beekeeping table to know potential hazard of the pesticides used in beekeeping in humans.

Even if these statements do not allow making generalisations and the cases mentioned certainly not concluding that all beekeepers make an abusive use of pesticides, they represent nevertheless a symptom that 1. highlights that beekeepers are often not conscious of the fact that the "medicine" they get from the vet are actually hazardous pesticides – this point appeared fairly clearly during the interviews conducted in the frame of the survey – and 2. confirms that the wider public is insufficiently informed about the hazards linked with commercially available pesticides (see my works on private gardening about common prejudices about the use pesticides in the private sphere on this topic).

Side Effects on the Environment of the Beehive

Observations have shown that other arthropods cohabit with the bees and do play a role in the hive's hygiene, among others as varroa control is concerned (see Varroa Predators on this topic). The role of these cohabitants is poorly known, but it is allowed to consider that the use of pesticides may eliminate these cohabitants thereby weakening the hygiene and defence mechanisms of bees.

Pesticides may contaminate the environment of the beehive, by dispersion of the substance or transport by water evaporated from the hive. Even if this local application may be considered as only a small pollution factor, the soil in the direct vicinity of the beehive and water (either by infiltration or evaporation) can be contaminated, while soil and aquatic animal are particularly sensitive to pesticides. Local applications do contribute to the global pollution burden in several ways, especially if the complete life cycle of a pesticide is considered. (See the Overview of Pesticides and Antibiotics Used in Beekeeping table on the ecotoxicity of the pesticides used in beekeeping and my works on private gardening for comparative impacts on the local application of pesticides.)

Conclusion

There is growing concern that chemical pest treatment contribute to the current honeybee mass mortality in the world. The current bee extinction phenomenon is reputed as multifactorial and those pesticides obviously add to the current plight and generally to the introduction of pollutants into the environment.

Moreover, the use of pesticides in beekeeping jeopardizes the reputation of beekeeping as a handicraft and honey as a natural product. Even if there are official tolerances of pesticides residues in honey, the presence of pesticides does not meet the expectations of honey consumers and contamination levels may exceed MRLs adopted by some countries, thus reduce opportunities for beekeepers to export their products. On the other hand, there is no regulation concerning residues in beeswax.[13] Bee products contaminated with pesticides present then a supplementary problem since these are used in considerable quantities in the pharmaceutical, food and cosmetic industries. Beekeepers are not yet submitted to strict laws and Good Manufacturing Practices since methods depend on bee races and local circumstances.[32] It is thus in the hands of beekeepers to rule out methods that may be detrimental to both bees, their main resource of business, and the image of their activity.

The extended use of pesticides by beekeepers may have been a first desperate reaction in front of their rapidly declining hives as a result of the uncontrolled development of invasive pests, but also reflects in my opinion the lack of information of the wider public about the hazards linked by commercially available pesticides or pesticides available on prescription. Moreover, information on different methods of organic pest control (see e. g. Organic Varroa Control) invented or discovered to fight the pandemics that have newly spread geographically or extended to Apis Mellifera diffuses too slowly and these methods lack extended experimentation to confirm their efficiency or refine the methods in order to gather the conditions for their success while minimising risks for the bees. This sluggishness can be at least partly explained by the lack of funds for the development of alternatives to pesticides and antibiotics, as organic methods do not bring immediate financial profit. However, as I tried to demonstrate in this article, pesticides and antibiotics can bring a solution only on the short term. As we should consider the costs of the current bee mortality, it is of crucial importance we should stop thinking in terms of immediate financial benefits but rather in terms of ecosystem services on which humans depend thus that funds may be raised for more holistic approaches.

The varroa problem is a phenomenon that found its origin in globalisation (see Bee Trading and Global Trading) but would also be better controlled with the possibilities offered by globalisation, that is:

  1. Intensified networking nationally and internationally between beekeepers, researchers and governments in order to promote knowledge exchange and experiences, early opportunity recognition and exploitation, the intensification of research & development as well as field experimentations, raise on funds for theses purposes, and
  2. International laws or standards to control sanitary conditions in bee trade and beekeeping for the prevention of epidemics.

References

  1. Chapleau, J.-P., 2003: Experimentation of an Anti-Varroa Screened Bottom Board in the Context of Developing an Integrated Pest Management Strategy for Varroa Infested Honeybees in the Province of Quebec. Accomplished within the framework of the "Appui au développement de l'agriculture et de l'agroalimentaire en région 2000-2003" programme of the "Ministère de l'Agriculture, des Pêcheries et de l'Alimentation du Québec, Canada" Regional district of l’Estrie), Final Report. http://www.countryrubes.com/images/AV-BOTTOM_BOARD.pdf; French version under: http://www.reineschapleau.wd1.net/articles/anti-varoa.pdf
  2. 2.0 2.1 2.2 Faucon J.-P., 2002: La varroase, une situation alarmante. Apiservices. http://www.apiservices.com/sante-de-labeille/articles/varroase.htm
  3. 3.0 3.1 Shahrouzi R., 2009: La résistance de varroa aux pyréthrinoïdes en Iran. http://www.apiculture.com/articles/fr/resistance_varroa_iran_pyrethrinoides.htm
  4. 4.0 4.1 4.2 Hamida T. B., 1997: Chemotherapy against varroa jacobsoni : Efficiency and side effects. Institut de la recherche vétérinaire de Tunisie. http://ressources.ciheam.org/om/pdf/c21/97605909.pdf
  5. Pettis J. S., 2003: A scientific note on Varroa destructor resistance to coumaphos in the United States. USDA-ARS Bee Research Laboratory, Beltsville 2003. http://ressources.ciheam.org/om/pdf/c21/97605909.pdf
  6. Vita, 2009: Monitoring varroa resistance. http://www.vita-europe.com/Map_enscript/frmbuilder.php?dateiname=%2Fen%2Fmonitoring.htm
  7. 7.0 7.1 7.2 7.3 7.4 Ministery of Agriculture and Forestry of New Zealand, 2001: A Review of Treatment Options for Control of Varroa Mite in New Zealand. http://www.biosecurity.govt.nz/files/pests/varroa/papers/varroa-treatment-options.pdf
  8. PAN, 2009: The PAN Pesticide Database, the Pesticide Action Network of North America. http://www.pesticideinfo.org/Index.html
  9. 9.0 9.1 9.2 9.3 9.4 9.5 Frazier M., Mullin C., Ashcraft S., 2008: What have pesticides got to do with it? Department of Entomology; Penn State University. http://maarec.psu.edu/CCDPpt/WhatPesticidesToDoWithItJune08ABJ.pdf
  10. Fakhimzadeh K., 2001: Detection of major mite pests of Apis mellifera and development of non-chemical control of varroasis. University of Helsinki, Department of applied biology. http://ethesis.helsinki.fi/julkaisut/maa/selai/vk/fakhimzadeh/detectio.pdf
  11. Loucif-Ayad W., Aribi N., Soltani N., 2008: Evaluation of Secondary Effects of some Acaricides on Apis Mellifera Intermissa (Hymenoptera, Apidae): Acetylcholinesterase and Glutathione S-Transferase Activities. European Journal of Scientific Research, ISSN 1450-216X Vol.21 No.4 (2008), pp.642-649, http://www.eurojournals.com/ejsr_21_4_07Wahida.pdf
  12. van Engelsdorp D. et al., 2009.pdf: Colony Collapse Disorder: A Descriptive Study. PLoS One, August 2009, Volume 4, Issue 8. http://www.plosone.org/article/info:doi/10.1371/journal.pone.0006481
  13. 13.0 13.1 13.2 13.3 13.4 13.5 13.6 Wallner K., Fries I., 2003: Control of the Mite Varroa Destructor in honey Bee Colonies. Pesticide Outlook. http://www.rsc.org/delivery/_ArticleLinking/DisplayArticleForFree.cfm?doi=b301510f&JournalCode=PO
  14. Milius S., 2009: No one Vilain behind Honey-Bee Collony Collapse. ScienceNews, Web edition of December 15th, 2009. http://www.sciencenews.org/view/generic/id/50824/title/No_one_villain_behind_honey-bee_colony_collapse
  15. 15.0 15.1 Benjamin A., McCallum B., 2008: A World Without Bees, Chapter 6. Guardian Books, 2009. ISBN-10: 0852651317, ISBN-13: 978-0852651315
  16. Burns T., 2011: Social bees use faecal diet to fight parasites. Cosmos Online, Cambridge 2011. http://www.cosmosmagazine.com/news/4972/bee-sociality-defends-against-deadly-parasites?page=0%2C0
  17. Carson R., 1962: Silent spring, Mariner Book edition, Houghton Mifflin Company, Boston/New York, 2002. ISBN: 0 618 24906 0
  18. Stein S., 1993a: Noah's Garden: Restoring the Ecology of you Garden, Chapter 6; Houghton Mifflin Company, New York 1993. ISBN-13: 978-0-395-70940-5, ISBN-10: 0-395-70940-7
  19. 19.0 19.1 Fries I., Imdorf A., Rosenkranz P., 2005: Survival of mite infested (Varroa destructor) honey bee (Apis mellifera) colonies in a Nordic climate; Department of Entomology, Swedish University of Agricultural Sciences, Uppsala, Sweden / Swiss Apicultural Institute, FAM, Liebefeld / State Institute of Apiculture, University of Hohenheim, 2005. http://www.apidologie.org/index.php?option=article&access=standard&Itemid=129&url=/articles/apido/pdf/2006/05/m6039.pdf
  20. 20.0 20.1 Fries I., Bommarco R., 2007: Possible host-parasite adaptations in honey bees infested by Varroa destructor mites; Department of Entomology, Swedish University of Agricultural Sciences, Uppsala, 2007. http://www.apidologie.org/10.1051/apido:2007039
  21. Martel A.-C. et al., 2007: Acaricide residues in honey and wax after treatment of honey bee colonies with Apivar® or Asuntol®50. Agence Française de Sécurité Sanitaire des Aliments (AFSSA), Site de Sophia Antipolis, Laboratoire d’Études et de Recherches sur les Petits Ruminants et les Abeilles (LERPRA), Unité de Pathologie de l’Abeille. Sophia Antipolis, 2007 http://www.apidologie.org/index.php?option=article&access=standard&Itemid=129&url=/articles/apido/pdf/2007/06/m6116.pdf
  22. 22.0 22.1 22.2 22.3 Bogdanov S., Kilchenmann V., Imdorf A., 1999: Acaricide residues in honey, beeswax and propolis. Swiss Bee Research Center, Diary Research Station. Liebefeld, Bern, 1999. http://www.agroscope.admin.ch/imkerei/01810/01822/index.html?lang=en&download=NHzLpZeg7t,lnp6I0NTU042l2Z6ln1ad1IZn4Z2qZpnO2Yuq2Z6gpJCDeHt7f2ym162epYbg2c_JjKbNoKSn6A--
  23. EPA, 1996: R.E.D. facts: Amitraz. U.S. Environmental Protection Agency. http://www.epa.gov/oppsrrd1/REDs/factsheets/0234fact.pdf
  24. 24.0 24.1 24.2 24.3 Kay J., Arnold D., Ellis R., 2009: Residues of Veterinary Drugs in Honey and Possible Approaches to Derive MRLs for this Commodity. First Draft. 2009. ftp://ftp.fao.org/docrep/fao/011/i0659e/i0659e01.pdf
  25. Beyond Pesticides, Pesticide Action Network North America, et al., 2009: Transforming Government's Approach to Regulating Pesticides to Protect Public Health and the Environment. Beyond Pesticides, 2009. http://www.beyondpesticides.org/transformingpesticidepolicy/
  26. Calestrémé N., 2009: Disparition des abeilles : la fin d'un mystère. Mona Lisa Production, Mandavara Production, 2009
  27. 27.0 27.1 27.2 Sabatini A. et al., 2003: Presence of Acaricides and Antibiotics in Samples of Italian Honey. Istituto Nazionale di Apicoltura, Bologna, 2003. http://www.apimondiafoundation.org/cgi-bin/index.cgi?sid=&zone=download&action=download_file&file_id=267&categ_id=115
  28. Lodesani M., Costa, C, 2008: Residues in beeswax after conversion to organic beekeeping. http://orgprints.org/11602/1/Lodesani_11602_ed.doc
  29. 29.0 29.1 Kamel A., Al-Ghamdi A., 2005: Determination of Acaricide residues in Saudi Arabian Honey and Beeswax Using Solid Phase Extraction and Gas Chromatography. Journal of Environmental Science and Health, Part B. Taylor & Francis Inc., 2006; ISSN: 1532-1234. http://colleges.ksu.edu.sa/FoodsAndAgriculture/PlantProtection/Academic%20Research/Papers/Determination%20of%20acaricide%20residues%20al-ghomdy%20full%20paper.pdf
  30. Imdorf A. et al., 2003: Strategie zur alternativen Bekämpfung von Varroa Destructor in Zentraleuropa. Swiss Bee Research Center, Diary Research Station. Liebefeld, Bern, 2003. http://www.apimondia.org/apiacta/articles/2003/imdorf_1_ge.pdf
  31. Bogdanov S. et al., 1998: Einfluss von organischen Säuren und Komponenten ätherischer Öle auf den Honiggeschmack. Swiss Bee Research Center, Diary Research Station. Liebefeld, Bern, 1998. http://www.agroscope.admin.ch/imkerei/01810/01822/index.html?lang=de&download=NHzLpZeg7t,lnp6I0NTU042l2Z6ln1acy4Zn4Z2qZpnO2Yuq2Z6gpJCDeHt7fGym162epYbg2c_JjKbNoKSn6A--
  32. Wikibooks, 2009: Beekeeping/Leading practices. http://en.wikibooks.org/wiki/Beekeeping/Leading_practices




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