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Quantification of Neonicotinoid Pesticides in Six Cultivable Fish Species from the River Owena in Nigeria and a Template For water Article Quantification of Neonicotinoid Pesticides in Six Cultivable Fish Species from the River Owena in Nigeria and a Template for Food Safety Assessment Ayodeji O. Adegun 1, Thompson A. Akinnifesi 1, Isaac A. Ololade 1 , Rosa Busquets 2 , Peter S. Hooda 3 , Philip C.W. Cheung 4, Adeniyi K. Aseperi 2 and James Barker 2,* 1 Department of Chemical Sciences, Adekunle Ajasin University, Akungba Akoko P.M.B. 001, Ondo State, Nigeria; [email protected] (A.O.A.); [email protected] (T.A.A.); [email protected] (I.A.O.) 2 School of Life Sciences, Pharmacy and Chemistry, Kingston University, Kingston-upon-Thames KT1 2EE, UK; [email protected] (R.B.); [email protected] (A.K.A.) 3 School of Engineering and the Environment, Kingston University, Kingston-on-Thames KT1 2EE, UK; [email protected] 4 Department of Chemical Engineering, Imperial College, London SW7 2AZ, UK; [email protected] * Correspondence: [email protected] Received: 17 June 2020; Accepted: 24 August 2020; Published: 28 August 2020 Abstract: The Owena River Basin in Nigeria is an area of agricultural importance for the production of cocoa. To optimise crop yield, the cocoa trees require spraying with neonicotinoid insecticides (Imidacloprid, Thiacloprid Acetamiprid and Thiamethoxam). It is proposed that rainwater runoff from the treated area may pollute the Owena River and that these pesticides may thereby enter the human food chain via six species of fish (Clarias gariepinus, Clarias anguillaris, Sarotherodon galilaeus, Parachanna obscura, Oreochromis niloticus and Gymnarchus niloticus) which are cultured in the river mostly for local consumption. This work aims to establish a working method to quantify the likely levels of the insecticides in the six species of fish, firstly by undertaking a laboratory-based study employing the QuEChERS method to extract the four neonicotinoids from fish purchased in marketplace in the UK, spiked with known quantities of the pesticide and using liquid chromatography coupled with tandem mass spectrometry (LC-MS-MS) as the detection method; secondly, by using these samples to optimise the detection method for very low levels of pesticides, then applying the optimised techniques to the analysis of three of each six species of fish taken from the Owena River. A significant benefit of this combined technique is that only small samples of fish are required. Success with this part of the study showed that very low concentrations of the insecticides could be detected in fish muscle. The third aim is to apply a simple quantitative risk assessment model using the data sets obtained, together with information about daily diet, human body weight and recommended safety limits of pesticides in food to illustrate how human health may be affected by the consumption of these fish. The multiple determinations of neonicotinoids in edible fishes in Nigeria are pioneer research and fill a gap in addressing the relationship between waterborne pesticides and food quality in the country. Fundamentally, this work is an exercise to demonstrate the applicability of the aforementioned instrumental method of analysis to fish muscle, which requires only a small sample size of fish; a large number of fish is not required for a proof of concept, in this case. Although not a monitoring programme for the whole Owena River Basin ecosystem per se, this work successfully demonstrates the technical feasibility of a system of chemical analysis and establishes the foundation for ecological surveys in the immediate future. Parameters involving exposures to xenobiotics in ecotoxicological modelling can now be expressed in terms of both mass and molar concentrations of a chemical in animal tissues if so desired. Water 2020, 12, 2422; doi:10.3390/w12092422 www.mdpi.com/journal/water Water 2020, 12, 2422 2 of 41 Water 2020, 12, x FOR PEER REVIEW 2 of 51 Keywords: Owena River fish; neonicotinoids; QuEChERS; liquid chromatography-tandem mass Keywords: Owena River fish; neonicotinoids; QuEChERS; liquid chromatography-tandem spectrometry mass spectrometry 1. Introduction Introduction 1.1. Neonicotinoid Neonicotinoid Insecticides Insecticides as Potential Water Pollutants and Food Contaminants The cocoacocoa tradetrade is is important important to to the the national national economy economy of Nigeria. of Nigeria. In 2019, In the2019, country the country was ranked was rankedthe fourth the largestfourth largest exporter exporter of cocoa of cocoa products products in the in world, the world, with with fermented fermented cocoa cocoa beans beans being being the thesecond second most most important important cash cash crop crop [1,2]. [1,2]. The OwenaThe Owena River River runs runs along along the major the major cocoa-producing cocoa-producing areas areasof Ondo of StateOndo inState Nigeria in Nigeria where neonicotinoidwhere neonicotinoi insecticidesd insecticides (hereafter (hereafter called “neonics”) called “neonics”) are sprayed are sprayedonto Theobroma onto Theobroma cacao L. (cocoa cacao L. trees) (cocoa to trees) control to pests control such pests as mirids,such as a mirids, major problema major problem facing farmers. facing farmers.However, However, when sprayed when in sprayed plantations, in plantations, no more than no 10%more of than applied 10% pesticides of applied are pesticides taken up are by plants,taken upat leastby plants, 50% end at least up in 50% soil end and up in to 30%soil and enter up into to 30% the atmosphere enter into the as vapoursatmosphere and as spray vapours droplets, and sprayaccording droplets, to estimates according/research to estimates/research undertaken by under the U.S.taken EPA by the [3]. U.S. The EPA drift [3]. of The airborne drift of pesticides airborne pesticidesinto rural andinto urbanrural and populations urban populations has also become has also a become public health a public issue health recently issue [ 4recently–6]. Globally, [4–6]. Globally,the tug-of-war the tug-of-war between the between reduction the ofreduction pesticide of use pesticide and the needuse and to satisfy the need food to demands satisfy food (and demandstherefore the(and application therefore the of more application pesticides) of more still exists,pesticides) and nationalstill exists, governments and national struggle governments to keep strugglethat balance—one to keep that example balance—one being France example [7]. being France [7]. Pesticides can also be transported into natural bo bodiesdies of of water water such such as as rivers rivers and and groundwater; groundwater; for example, insecticides from from a a corn corn field field may end up in a nearby stream due to runoff, runoff, or they can seep into groundwatergroundwater byby leaching leaching [8 ].[8]. The The fallout fallout from from airborne airborne pesticides pesticides can can also also contribute contribute to this to thispollution. pollution. These These transport transport phenomena phenomena do not do occur not independently occur independently of each otherof each but other are intimately but are intimatelylinked in a linked cyclic networkin a cyclic of processesnetwork of observed processes and observed proposed and by proposed Majewski by and Majewski Capel [9 ],and based Capel on [9],the U.S.based Geological on the U.S. Survey Geological and depicted Survey and in Figure depicted1[10 ].in Figure 1 [10]. Figure 1. PathwaysPathways of of pesticides pesticides transport transport to streams and groundwater [9,10]. [9,10]. Neonics are soluble in water and can be transported long distances by waterways, polluting Neonics are soluble in water and can be transported long distances by waterways, polluting aquatic ecosystems [11]. It has been suspected that pesticides which enter a river system can cause aquatic ecosystems [11]. It has been suspected that pesticides which enter a river system can cause public health problems. For example, if a river is the main source of drinking/cooking water and if water public health problems. For example, if a river is the main source of drinking/cooking water and if treatment facilities fail to reduce hazardous substances substantially or remove them completely, it is water treatment facilities fail to reduce hazardous substances substantially or remove them unsanitary and harmful to the population. By the end of the last century, agriculturalists accumulated completely, it is unsanitary and harmful to the population. By the end of the last century, so much knowledge about the problem of the pollution of natural bodies of water by pesticides agriculturalists accumulated so much knowledge about the problem of the pollution of natural that they were able to build sophisticated mathematical models to perform detailed ecological risk bodies of water by pesticides that they were able to build sophisticated mathematical models to Water 2020, 12, 2422 3 of 41 Water 2020, 12, x FOR PEER REVIEW 3 of 51 performassessments detailed [12]. ecological Moreover, risk pesticides assessments can also [12] enter. Moreover, the human pesticides body from can fish also eaten enter from the the human same bodynatural from bodies fish ofeaten water from [13 the]. same natural bodies of water [13]. 1.2.1.2. Aims Aims of of the the Present Present Work Work ThisThis study hashas threethree objectives.objectives. The The first first is is to to detect, detect, identify identify and and quantify quantify neonics neonics that that may may have haveaccumulated accumulated in six in cultivable six cultivable fishes fishes from from
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