Exposure of honeybees (Apis mellifera) in Saskatchewan, Canada to organophosphorus insecticides

Apidologie (2015) 46:667–678 * INRA, DIB and Springer-Verlag France, 2015 DOI: 10.1007/s13592-015-0357-y Original article Exposure of honeybees (Apis mellifera ) in Saskatchewan, Canada to organophosphorus insecticides Yahya ALNAGGAR1,2 , Anja VOGT2 , Garry CODLING2 , Elsaied NAIEM1 , Mohamed MONA1 , Amal SEIF1 , Albert J. ROBERTSON8 , John P. GIESY, .2,3,4,5,6,7 1 Department of Zoology, Faculty of Science, Tanta University, Tanta 31527, Egypt Toxicology Centre, University of Saskatchewan, 44 Campus Drive, Saskatoon, Saskatchewan S7N 5B3, Canada 3 Department of Veterinary Biomedical Sciences, University of Saskatchewan, Saskatoon, Saskatchewan, Canada 4 Department of Zoology, and Center for Integrative Toxicology, Michigan State University, East Lansing, MI, USA 5 Department of Biology & Chemistry and State Key Laboratory in Marine Pollution, City University of Hong Kong, Kowloon, Hong Kong, SAR, China 6 School of Biological Sciences, University of Hong Kong, Hong Kong, SAR, People’s Republic of China 7 State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University, Nanjing, People’s Republic of China 8 Meadow Ridge Enterprises LTD, Saskatoon, Saskatchewan S7K 3J9, Canada 2 Received 22 September 2014 – Revised 22 January 2015 – Accepted 9 February 2015 Abstract – Concentrations of 14 organophosphorus insecticides (OPs) were measured in Apis mellifera L. (European honeybee) and hive matrices (honey and bee bread). Samples were collected from seven randomly selected colonies in central Saskatchewan during the summer of 2013. LC-MS/MS was used to identify and quantify individual OP by use of a modified quick easy cheap effective rugged safe (QuEChERS) method. Diazinon, dimethoate, and chlorpyrifos-oxon were the only OPs detected in honey with mean concentrations of 0.3, 1.5, and 0.2 ng/g, wet mass (wm), respectively. Fenamiphos, chlorpyrifos, and chlorpyrifos methyl were the only OPs detected in bee bread, with mean concentrations of 0.4, 2.7, and 15.8 ng/g, wm, respectively, while ethoprop, malathion, and dichlorvos were the only OPs detected in bees with mean concentrations of 1.4, 3.7, and 889.2 ng/g, wm, respectively. Total hazard quotients (HQs), based on lethality of bees exposed to OPs in honey and pollen consumed by bees ranged from 0.01 to 0.06 and based on lethality of bees from direct exposure to OPs ranged from 0.3 to 0.4 which suggests little hazard of OPs to Saskatchewan beehives. honey / OPs / risk assessment / agriculture / honeybees 1. INTRODUCTION Honeybees are important for both production of honey and pollination of crop plants. The European honeybee, Apis mellifera L., is an essential pollinator for agricultural crops in many Electronic supplementary material The online version of this article (doi:10.1007/s13592-015-0357-y) contains supplementary material, which is available to authorized users. Corresponding author: Y. ALNaggar, Manuscript editor: Monique Gauthier countries, pollinating $15 to $20 billion worth of crops in the USA alone and more than $200 billion globally (VanEngelsdorp and Meixner 2010). The United States Department of Agriculture (USDA) estimates that one third of food consumed in North America is dependent on pollination by honeybees. Canada is a major food producer combining large areas (415,000 km2) of agricultural land with a low population density. It has the 6th largest area of farmed arable land, with the province of Saskatchewan, making up 40 % of this area, with an estimated 50,000 farms. In 2006, Saskatchewan produced 11.3×106 kg of honey, which accounted for 23 % of all honey produced 668 Y. Al Naggar et al. in Canada. Bees in Saskatchewan produce an average of 88 kg of honey per colony, meaning that the province supports approximately 128,000 commercial hives (http://www.agriculture.gov.sk. ca/Honey-Factsheet). Honeybee colony losses pose a serious threat to both the apiculture industry and food production in crops requiring pollination. Increased colony failure has been estimated to cause losses in the agriculture economy of up to $75 billion USD in 2007 (USDA 2007). It is not uncommon to lose hives during the over wintering period in Canada with an acceptable loss of 15 % being described by Canadian beekeepers. However, over the winter of 2012–2013 in Canada, the average loss of honeybee colonies (colony mortality) or colonies too weak to be commercially productive was 28.6 % (27 % in Saskatchewan; CAPA 2013). Such increased rates of colony losses in Canada and globally has led to concerns that there may not be enough bees to sustain the required levels of pollination for agriculture crops and native species. Although the putative causes of colony loss are still unclear and currently being investigated, results of some studies have suggested that extensive use of insecticides might be a factor in the increased rates of colony failure. Sequencing of the genome of the honeybee provides a possible explanation for their sensitivity to pesticides. Compared to genomes of other insects, that of the European honeybee is deficient in a number of genes encoding detoxification enzymes (Claudianos et al. 2006). As a consequence, honeybees might not be able to detoxify pesticides as rapidly as some other organisms. This might increase the length of time toxicants remain active within the body. Canadian annual usage of pesticides has increased from 9.3 to 12.5 million kilograms from 2003 to 2008 (Health Canada, Consumer Product Safety, Pest Control Products Sales Report 2007 and 2008). The Prairie Provinces use approximately 60 % of the pesticides in Canada, with Saskatchewan having the highest provincial usage (Brimbe 2005). Organophosphates (OPs) are a class of insecticides, which are highly toxic to bees. In the last two decades, they have been the most widely used insecticides. OPs have effective insecticidal properties and are used in Saskatchewan to control pests, such as grasshoppers, aphids, weevils, and crown borers as indicated in Table SI (Online Resource 1). Chlorpyrifos and diazinon are the most widely used in North America (Saskatchewan Usage Inventory 2003; Brimble 2005). In Saskatchewan, the highest atmospheric concentrations were observed for chlorpyrifos as it is the primarily OP used for grasshopper eradication (Raina et al. 2010), control of Bertha army worms, and Diamond back moths in canola and wheat midge. Organophosphates are not only used in agriculture but also in homes, gardens, and in veterinary practices. Determination of OPs in food is a matter of public concern. Due to their global application, their residues constitute a potential risk to human health (Pico et al. 1996). Honeybees are exposed to a range of pesticides during pollination including OPs that have the potential to accumulate in the bees themselves or in their products (i.e., honey and wax). According to Health Canada Environmental Incident Reports in 2012, OPs including chlorpyr (...truncated)