In order to ease the control of weeds, some crops have been genetically engineered to be resistant to the herbicide glyphosate (GLY). This feature has boosted the use of this systemic, wide spectrum herbicide around the world (Green, 2018; Székács and Darvas, 2012). GLY inhibits the 5-enolpyruvylshikimate-3-phosphate synthase, which is responsible for the biosynthesis of aromatic amino acids in plants (Duke and Powles, 2008; Shilo et al., 2016); since animals lack this enzyme, GLY is considered one of the least toxic pesticides for them (Duke and Powles, 2008). However, some studies suggest that it does affect organisms other than plants; for example, it reduces the reproduction of soil-dwelling earthworms (Gaupp-Berghausen et al., 2015), affects the growth of microalgae and aquatic bacteria, and has detrimental effects on fish, amphibians, mammals and birds (Benachour and Séralini, 2009; Relyea, 2005; Richard et al., 2005). GLY is also associated with negative effects on soil rhizosphere-associated bacterial communities (Newman et al., 2016) and with a reduction of mycorrhizal colonization (Helander et al., 2018). Bees are insects with the highest risk of exposure due to the multiple routes to which they can be exposed when collecting nectar and pollen from blooming plants, carrying any contaminants in those resources to the hive (Agrebi et al., 2019; Coupe et al., 2012; Krupke et al., 2012). The main exposure routes include glyphosate-treated crops, drift, and the wide use of this herbicide in urban areas for domestic and minor applications, such as weed control on railways, parks, and home gardens (Pasquale et al., 2013; Silva et al., 2018; Simon-delso et al., 2017). In fact, multiple pesticide residues have been reported in honey, pollen, propolis, wax, royal jelly and honey bread (Calatayud-Vernich et al., 2017; de Oliveira et al., 2016; Matin et al., 2016; Pohorecka et al., 2012; Ruiz-Toledo et al., 2018; Tosi et al., 2018; Valdovinos-Flores et al., 2017; Zawislak et al., 2019). However, since 1990, due to the introduction and rapid acceptance of herbicide-resistant crops worldwide, Mexico included (James, 2016), applications of the herbicide glyphosate have intensified, bringing with it a greater health risk to honey bees (Agrebi et al., 2019; Bohan et al., 2005; Foulk, 2009; Rubio et al., 2014), due to the accumulation of pesticide residues inside the hives with chronic consequences, (Boily et al., 2013; Crenna et al., 2020; Herbert et al., 2014; Weisbrod, 2020; Wu et al., 2012; Zawislak et al., 2019), even though it is considered not toxic for adult bees (Lewis et al., 2016); for example, young adult bees chronically exposed to GLY formulations showed impaired associative learning and reduced sucrose sensitivity (Gonalons and Farina, 2018; Herbert et al., 2014; Luo et al., 2021) and forager bees exposed to sublethal doses of such formulations showed poor navigation back home (Balbuena et al., 2015).
Regarding human wellbeing, various regulatory agencies and scientific institutions worldwide have concluded that there is not sufficient evidence supporting that glyphosate causes health problems (EFSA, 2015a; European Commission, 2002; USEPA, 1993). However, there are some works that show that residues found in the environment could be toxic to humans (Agrebi et al., 2019), and cause teratogenic, tumorigenic and hepatorenal effects, supposedly due to endocrine disruption and oxidative stress. The risk of exposure is even greater since bee products are part of the supplementary diet of humans; such is the case of pollen, which is considered an excellent dietary supplement for nutrition found in different forms in the market (granules, capsules, tablets, granules and powders) (Komosinska-Vassev et al., 2015; Kostić et al., 2020), which could represent a greater risk for human health.
In our study area, beekeepers commonly place their apiaries in non-cultivated plots in which plant succession is allowed; however, they are surrounded by a landscape consisting of soybean, mango, bean, pumpkin, maize and sesame crops (authors’ observation). Soybean is the only genetically modified crop in the area, but non-transgenic soybean varieties are cultivated as well. Therefore foraging honey bees are potentially exposed to a variety of pesticides, GLY included, through water, pollen and nectar (Hladik et al., 2016; Krupke et al., 2012). Also, since most farmers switched from non-transgenic varieties, it is supposed that this herbicide is used in higher amounts, so transgenic soybean contributes largely to contamination by GLY. Thus we hypothesize that colonies located in places in which transgenic soybean pollen is found have higher amounts of GLY. The goal of this work was to quantify to glyphosate residues in pollen samples from honey bee Apis mellifera L., and assess the risk that it could represent for the honey bee and consumers health.