Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites

Abstract

Since their discovery in the late 1980s, neonicotinoid pesticides have become the most widely used class of insecticides worldwide, with large-scale applications ranging from plant protection (crops, vegetables, fruits), veterinary products, and biocides to invertebrate pest control in fish farming. In this review, we address the phenyl-pyrazole fipronil together with neonicotinoids because of similarities in their toxicity, physicochemical profiles, and presence in the environment. Neonicotinoids and fipronil currently account for approximately one third of the world insecticide market; the annual world production of the archetype neonicotinoid, imidacloprid, was estimated to be ca. 20,000 tonnes active substance in 2010. There were several reasons for the initial success of neonicotinoids and fipronil: (1) there was no known pesticide resistance in target pests, mainly because of their recent development, (2) their physicochemical properties included many advantages over previous generations of insecticides (i.e., organophosphates, carbamates, pyrethroids, etc.), and (3) they shared an assumed reduced operator and consumer risk. Due to their systemic nature, they are taken up by the roots or leaves and translocated to all parts of the plant, which, in turn, makes them effectively toxic to herbivorous insects. The toxicity persists for a variable period of time-depending on the plant, its growth stage, and the amount of pesticide applied. A wide variety of applications are available, including the most common prophylactic non-Good Agricultural Practices (GAP) application by seed coating. As a result of their extensive use and physicochemical properties, these substances can be found in all environmental compartments including soil, water, and air. Neonicotinoids and fipronil operate by disrupting neural transmission in the central nervous system of invertebrates. Neonicotinoids mimic the action of neurotransmitters, while fipronil inhibits neuronal receptors. In doing so, they continuously stimulate neurons leading ultimately to death of target invertebrates. Like virtually all insecticides, they can also have lethal and sublethal impacts on non-target organisms, including insect predators and vertebrates. Furthermore, a range of synergistic effects with other stressors have been documented. Here, we review extensively their metabolic pathways, showing how they form both compound-specific and common metabolites which can themselves be toxic. These may result in prolonged toxicity. Considering their wide commercial expansion, mode of action, the systemic properties in plants, persistence and environmental fate, coupled with limited information about the toxicity profiles of these compounds and their metabolites, neonicotinoids and fipronil may entail significant risks to the environment. A global evaluation of the potential collateral effects of their use is therefore timely. The present paper and subsequent chapters in this review of the global literature explore these risks and show a growing body of evidence that persistent, low concentrations of these insecticides pose serious risks of undesirable environmental impacts.

Fig. 1

Common names and molecular structures of the systemic insecticides

Fig. 2

a Trend in the agricultural use of neonicotinoid insecticides in Britain from 1990, measured in tonnes of active ingredient applied per year. Data from http://pusstats.csl.gov.uk/index.cfm. b Trend in the quantities of neonicotinoid insecticides sold in Sweden from 1998, measured in tonnes of active ingredient per year. Data from Swedish Chemicals Agency, KEMI, quoted in (Bergkvist 2011). c Trend in the domestic shipment of neonicotinoid insecticides and fipronil in Japan from 1990, measured in tonnes of active ingredient per year. Data from Japan’s National Institute for Environmental Studies database, provided by Mizuno, R. in litt., . d Trend in the quantity of neonicotinoid insecticides and fipronil used in California from 1990, measured in tonnes of active ingredient applied per year. Data taken from http://www.cdpr.ca.gov/docs/pur/purmain.htm. Also shown are the total quantities sold, from http://www.cdpr.ca.gov/docs/mill/nopdsold.htm

Fig. 3

Trend in the sales (Sweden), domestic shipment (Japan), use (California) and agricultural use (Britain) of all neonicotinoid insecticides and fipronil. See Figs. 2a–d for further details. All measured in tonnes of active ingredient per year. Note the separate vertical axes for California//Japan, and Britain//Sweden

Fig. 4

Trend in the agricultural use of neonicotinoid insecticides as seed treatments in Britain from 1990, measured in tonnes of active ingredient per year (bars). The total usage of all insecticidal seed treaments (solid line) is also shown. Data from http://pusstats.csl.gov.uk/index.cfm