**Pesticide Residues in Bee Products**

Emmanouel Karazafiris1, Chrysoula Tananaki1,

Andreas Thrasyvoulou1 and Urania Menkissoglu-Spiroudi2 *1Laboratory of Apiculture-Sericulture, Faculty of Agriculture, Aristotle University of Thessaloniki, 2 Pesticide Science Laboratory, Faculty of Agriculture, Aristotle University of Thessaloniki, Greece* 

#### **1. Introduction**

88 Pesticides in the Modern World - Risks and Benefits

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*and xeno-estrogens in the aquatic environment of the Netherlands.* RIZA/RIKZ-report

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musk ketone in freshwater fish collected from the Tama River, Tokyo. *Bulletin of* 

"The man has no divine right over the food. He must compete for this with weeds, diseases, insects and other organisms" (Grodner, 1996).

With the above quote, Grodner clearly reflects the situation in the area production and processing of food. More than 10.000 species of insects and mites, 1.500 species of fungi and 600 plant species have been identified as harmful to agriculture (Grodner, 1996; Pimentel et al., 2000). The production of plant and animal products requires the use of large quantities of chemicals (plant protection agents, veterinary drugs, fertilizers, etc.), which could lead to increased production and improved quality, as a consequence. The quality of the final product is usually reflected to particular visual parameters like color, size and general appearance. In the case of food, however, many questions are raising about their safety. The reason is the possible presence of chemical residues detected in the final product. Nowadays, consumer safety is a major priority for governments of developed countries and food safety is a criterion for the trading and prices on the market. Reports in media about alimentary scandals cause anxiety to consumers and turning a part of the market to organic products, which are considered free, or at least less contaminated by hazardous substances. In recent years, reports in media have grown at an alarming rate and any references to the consumer aimed at creating impressions, achieved by overemphasizing the disadvantages of chemical use and mainly problems related to environmental pollution and its impact on human health. In contrast, reports in media referring to the advantages of using chemicals are minimal to nonexistent. For example, the absence of appropriate chemical agents to combat rodents lead to the first epidemic of the bubonic plague disease and the death of 65.000.000 people. Moreover, the starvation in Ireland began due to the fungal disease *Phytophthora infestans*, which destroyed potatoes causing 1.000.000 deaths from 1845 to 1851 (Knutson et al., 1990). Besides health problems that preoccupied humans in the past, the economic impact on different groups of consumers will be significant in case of pesticides withdrawal. Specifically, the weekly expenses for food are expected to rise by 44% for consumers of low average income. The economies of countries with intensive agriculture will be stroke because of the decline in exports of grains and products like cotton. Finally, undesirable environmental effects are expected due to the increasing of cultivated land and the erosion problems that could be observed because of the limited growth of the root

Pesticide Residues in Bee Products 91

Neonicotinoids like imidacloprid were also detected in stored pollen (Gregorc & Bozic, 2004; Chauzat et al., 2006). Also, the type of formulation and application of the pesticide in relation to toxicity caused to the bees proved particularly important. For example, the standardization of the active ingredient methyl parathion in microcapsules kills 13 times more bees than the formulation of the same substance as an emulsified solution. Furthermore, wettable powder or dust proved less dangerous than microcapsules, but also

Under the development of framework concerning consumer safety, the European Union created a warning system called RASFF (Rapid Alert System for Food and Feed), which reports hazardous foods and feeds, identified in the markets of the Member States. Bee products like honey and royal jelly have been reported occasionally. The main reason why they have been reported is the detection of residues of antibiotics that have been used by

There are two ways of contamination of bee products with various chemicals; the indirect and the direct contamination. The indirect way reflects the transporting of toxic substances by foragers bees during the collection of nectar, honeydew, water, pollen and propolis. Many studies concern the contamination of hive products by agrochemicals and heavy metals, while few concern the presence of nitrofurans, toxins and PCBs in beehive products. The direct way, which is the most important, regards the contamination of bee products by

Many researchers supported the theory that the transferring of pesticides from fields to beehive is prevented in various ways. The bees' death at the field, the lost of orientation of the foragers, the reluctance of guard bees to permit the entrance to foragers with contaminated nectar, the retaining of contaminated food in bees' stomach, the stopping of further elaboration of contaminated nectar by hive bees and the removal of affected bees from the hive are natural provisions against general contamination of honey (Johansen & Mayer, 1990; Atkins, 1992). Contrary to the above-mentioned cases, older studies reported that worker bees may carry high concentrations of pesticides into their beehive. In some cases the concentration of pesticides in the load was 25 times greater than the lethal dose of

Pesticides used on various crops are classified into groups based on their chemical structure (organophosphates, pyrethroids, organochlorines, carbamates, neonicotinoids etc.), mode of action (systemic, contact), target (insecticides, acaricides, herbicides, fungicides, bactericides, nematicides) and synthesis (synthetic or natural). The residues of pesticides detected in beehive products are classified in the groups of insecticides (organochlorines, organophosphates, carbamates and neonicotinoids), acaricides, fungicides and herbicides.

This specific group of insecticides is considered particularly hazardous because of its ability to bioaccumulate into the food chain, to remain stable for many years and to move into the

caused more deaths than aqueous or emulsified solutions (Sanford, 1993).

acaricides, antibiotics and volatile pesticides caused by beekeeping practices.

beekeepers to fight various diseases of bees.

**2.1 Indirect contamination of bee products** 

**2.1.1.1 Organochlorine pesticides (OCPs)** 

the bee (Jaycox, 1964).

**2.1.1 Pesticides** 

**2. Contamination of bee products** 

system of plants (Knutson et al., 1990). In contrast to the above, there are few cases of pesticides proved dangerous to public health. A typical example is the chlorinated hydrocarbon DDT, which was previously used against mosquitoes. The active substance DDT contributed greatly to reduce the spread of diseases like malaria, but was withdrawn in 1970 as it was considered dangerous for human and environment safety.

Active substances are classified into five groups according to their toxicity. The first group (Ia) includes the extremely toxic agricultural plant protection agents, while the four other groups of substances are listed in order of decreasing toxicity (Ib, II, III). The fifth group (U) includes substances that are unlikely to become toxic to humans (International Programme on Chemical Safety, 2004). The adverse effects of these compounds may be observed in a short period (acute toxicity) or after a long time (chronic toxicity). In any case, it should be noted that, although the annual reported number of deaths by poisoning is 355.000, only a part of these poisonings, which is not specified in the World Health Report, are due to pesticides (WHO The World Health Report, 2003). Moreover, all cases of poisoning are due to accidents, like accidental ingestion or inhalation of chemicals, and not by food intake. However, the possibility of indication of various effects in consumer health through chronic toxicity cannot be ignored. Toxicity of a plant protection product depends on various factors, including chemical structure, temperature and humidity conditions, dose, duration of exposure, mode of action and the kind of exposure, like ingestion, inhalation, dermal etc. Different groups of pesticides and veterinary drugs are likely to be responsible for causing malaise, sore eyes, abnormalities to skin and respiratory system. Moreover, some pesticides and veterinary drugs are suspected of causing certain types of cancer, teratogenicity, chromosomal abnormalities and the weakening of the immune system of humans (Banerjee, 1999). The toxicity of various active substances, which can be detected in bee products, varies according to their chemical synthesis. In any case, poisoning or deaths due to the presence of toxic substances exclusively to bee products have not been reported. An exception is the death of infants, which was caused by *Clostridium botulinum* (Arnon, 1980). Even in these cases, however, the responsibility of honey has not been proven clearly, as this clostridium appears in the environment widely (Midura, 1996). In addition, 65% of infants that became ill had not eaten honey at all (Arnon et al., 1979). In any case, appropriate infant feeding prohibits the consumption of honey until the age of one year to eliminate possible poisoning from toxins of this micro-organism.

Another way of classification of active substances, relates to the subject of this investigation, and is based on bee toxicity. In general, active substances are classified as very toxic, moderately toxic and non-toxic to bees. The most significant impact on bee colonies has been observed after treatments with plant protection products during the blooming. Most deaths occurred during the stage of forager worker bee that collects nectar and pollen. Moreover, larvae and domestic bees die because of pesticide residues detected in pollen. Although in many cases the concentration of pesticide found in pollen is not lethal, it is however likely to cause paralysis of bees, irritability, killing and replacing of the queen bee and generally abnormal behavior. This behavior can also be caused by substances that do not kill bees directly (e.g. carbaryl as active ingredient of Sevin®) but are transferred into the hive by foragers and affect the entire population (Sanford, 1993). The long–term persistence of many pesticides in stored pollen has also serious impact of bees' survival. Arsenic from paris green and calcium arsenate was present in pollen stored in comb analyzed six months after application. Methomyl residues persisted in honeybee combs for eight months. Methyl parathion from Penncap M, persisted in combs samples of stored pollen for 7 to 14 months after use and carbaryl similarly persisted over winter for 7-9 months (Erickson et al., 1983)

system of plants (Knutson et al., 1990). In contrast to the above, there are few cases of pesticides proved dangerous to public health. A typical example is the chlorinated hydrocarbon DDT, which was previously used against mosquitoes. The active substance DDT contributed greatly to reduce the spread of diseases like malaria, but was withdrawn

Active substances are classified into five groups according to their toxicity. The first group (Ia) includes the extremely toxic agricultural plant protection agents, while the four other groups of substances are listed in order of decreasing toxicity (Ib, II, III). The fifth group (U) includes substances that are unlikely to become toxic to humans (International Programme on Chemical Safety, 2004). The adverse effects of these compounds may be observed in a short period (acute toxicity) or after a long time (chronic toxicity). In any case, it should be noted that, although the annual reported number of deaths by poisoning is 355.000, only a part of these poisonings, which is not specified in the World Health Report, are due to pesticides (WHO The World Health Report, 2003). Moreover, all cases of poisoning are due to accidents, like accidental ingestion or inhalation of chemicals, and not by food intake. However, the possibility of indication of various effects in consumer health through chronic toxicity cannot be ignored. Toxicity of a plant protection product depends on various factors, including chemical structure, temperature and humidity conditions, dose, duration of exposure, mode of action and the kind of exposure, like ingestion, inhalation, dermal etc. Different groups of pesticides and veterinary drugs are likely to be responsible for causing malaise, sore eyes, abnormalities to skin and respiratory system. Moreover, some pesticides and veterinary drugs are suspected of causing certain types of cancer, teratogenicity, chromosomal abnormalities and the weakening of the immune system of humans (Banerjee, 1999). The toxicity of various active substances, which can be detected in bee products, varies according to their chemical synthesis. In any case, poisoning or deaths due to the presence of toxic substances exclusively to bee products have not been reported. An exception is the death of infants, which was caused by *Clostridium botulinum* (Arnon, 1980). Even in these cases, however, the responsibility of honey has not been proven clearly, as this clostridium appears in the environment widely (Midura, 1996). In addition, 65% of infants that became ill had not eaten honey at all (Arnon et al., 1979). In any case, appropriate infant feeding prohibits the consumption of honey until the age of one year to eliminate possible

Another way of classification of active substances, relates to the subject of this investigation, and is based on bee toxicity. In general, active substances are classified as very toxic, moderately toxic and non-toxic to bees. The most significant impact on bee colonies has been observed after treatments with plant protection products during the blooming. Most deaths occurred during the stage of forager worker bee that collects nectar and pollen. Moreover, larvae and domestic bees die because of pesticide residues detected in pollen. Although in many cases the concentration of pesticide found in pollen is not lethal, it is however likely to cause paralysis of bees, irritability, killing and replacing of the queen bee and generally abnormal behavior. This behavior can also be caused by substances that do not kill bees directly (e.g. carbaryl as active ingredient of Sevin®) but are transferred into the hive by foragers and affect the entire population (Sanford, 1993). The long–term persistence of many pesticides in stored pollen has also serious impact of bees' survival. Arsenic from paris green and calcium arsenate was present in pollen stored in comb analyzed six months after application. Methomyl residues persisted in honeybee combs for eight months. Methyl parathion from Penncap M, persisted in combs samples of stored pollen for 7 to 14 months after use and carbaryl similarly persisted over winter for 7-9 months (Erickson et al., 1983)

in 1970 as it was considered dangerous for human and environment safety.

poisoning from toxins of this micro-organism.

Neonicotinoids like imidacloprid were also detected in stored pollen (Gregorc & Bozic, 2004; Chauzat et al., 2006). Also, the type of formulation and application of the pesticide in relation to toxicity caused to the bees proved particularly important. For example, the standardization of the active ingredient methyl parathion in microcapsules kills 13 times more bees than the formulation of the same substance as an emulsified solution. Furthermore, wettable powder or dust proved less dangerous than microcapsules, but also caused more deaths than aqueous or emulsified solutions (Sanford, 1993).

Under the development of framework concerning consumer safety, the European Union created a warning system called RASFF (Rapid Alert System for Food and Feed), which reports hazardous foods and feeds, identified in the markets of the Member States. Bee products like honey and royal jelly have been reported occasionally. The main reason why they have been reported is the detection of residues of antibiotics that have been used by beekeepers to fight various diseases of bees.
