Article pubs.acs.org/est
Do Antiparasitic Medicines Used in Aquaculture Pose a Risk to the Norwegian Aquatic Environment? Katherine H. Langford,* Sigurd Øxnevad, Merete Schøyen, and Kevin V. Thomas Norwegian Institute for Water Research, Gaustadaléen 21, NO-0349, Oslo, Norway S Supporting Information *
ABSTRACT: Aquaculture production is an important industry in many countries and there has been a growth in the use of medicines to ensure the health and cost effectiveness of the industry. This study focused on the inputs of sea lice medication to the marine environment. Diflubenzuron, teflubenzuron, emamectin benzoate, cypermethrin, and deltamethrin were measured in water, sediment, and biota samples in the vicinity of five aquaculture locations along the Norwegian coast. Deltamethrin and cypermethrin were not detected above the limits of detection in any samples. Diflubenzuron, teflubenzuron, and emamectin benzoate were detected, and the data was compared the UK Environmental Quality Standards. The concentrations of emamectin benzoate detected in sediments exceed the environmental quality standard (EQS) on 5 occasions in this study. The EQS for teflubenzuron in sediment was exceeded in 67% of the samples and exceeded for diflubenzuron in 40% of the water samples collected. A crude assessment of the concentrations detected in the shrimp collected from one location and the levels at which chronic effects are seen in shrimp would suggest that there is a potential risk to shrimp. It would also be reasonable to extrapolate this to any species that undergoes moulting during its life cycle.
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INTRODUCTION
infestations in salmonid aquaculture are estimated to be greater than US$100 million annually across the globe.6 DIF and TEF are chitin synthesis inhibiting benzoylurea pesticides administered in fish feed. DIF is sold on the Norwegian market as Releeze vet (0.6 g/kg DIF) and TEF is sold as Ektoban vet (2 g/kg TEF). It is estimated that approximately 10% of the dose of the benzoylurea pesticides administered in feed is absorbed into the fish and that the remaining 90% is rapidly excreted in faeces. EMA is also administered through feed and is marketed as Slice (0.2% EMA). It acts through binding the invertebrate glutamate regulated ion channels. DEL and CYP are pyrethroid pesticides used as topical bath treatments where medication is poured directly into the aquaculture cages which are temporarily enclosed using wrap around curtains. DEL and CYP are marketed as AlphaMax (10 mg/mL DEL) and BetaMax (50 mg/mL CYP). Pyrethroid insecticides interfere with the sodium and potassium channels in nerve cells causing paralysis and death of the sea lice. Whatever the mode of action involved, because of the way that antiparasitic medicines are administered to farmed fish, there is the high possibility that
Norway is one of the top 10 aquaculture producing countries in the world (the largest producer in the western world). Despite a stagnation in production in recent years across developed countries, Norway’s share of the European market continues to grow and, in 2010, represented 40% of the European market and 1.5% of the world market.1 Sea lice treatments are required in aquaculture because marine finfish, such as salmon and cod, are typically vulnerable to marine ectoparasitic infections, particularly in fish farming where water quality can be poor, stress factors are typically high, and space is often confined. Sea lice are among the most common parasitic crustacean in fish farming and require treatment since they affect both the economy of the fish farm and the health of the fish. Sea lice browse on the skin causing lesions adding additional stress to the fish and leaving them vulnerable to further infection. In recent years, usage patterns of sea lice treatments have changed as resistance by sea lice to traditional treatments has increased.2,3 In Norway, the use of emamectin benzoate (EMA) has reduced from 81 kg in 2008 to 36 kg in 2012, resulting in a return to the use of benzoylphenylurea insecticides, such as diflubenzuron (DIF) and teflubenzuron (TEF), in 2009, and the heavy use of pyrethroids, such as deltamethrin (DEL) and cypermethrin (CYP), from 2012,4 despite the fact that deltamethrin showed resistance in some locations in Norway.5 Indirect and direct losses due to sea lice © XXXX American Chemical Society
Received: January 31, 2014 Revised: June 4, 2014 Accepted: June 6, 2014
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dx.doi.org/10.1021/es5005329 | Environ. Sci. Technol. XXXX, XXX, XXX−XXX
Environmental Science & Technology
Article
Figure 1. Measured environmental concentrations of DIF and TEF in sediment and water compared to EQS values outside of the allowable zone of effect (AZE).
particulates settle on the sediment surface where they are more persistent, having half-lives of up to 80 days.8 The hydrophobic nature of all 5 antiparasitic compounds means they have the potential to bind to the suspended particulate matter or to the sediment phase and may accumulate in aquatic organisms. The physicochemical characteristics of the medicines, the modes of action, and the pathways into the environment all indicate that nontarget species may be adversely affected by antiparasitic medication. Studies of crab larvae have shown significant adverse effects when exposed to DIF.9,10 Larval development of mud crabs (Rhithropanpeus harrisii) and marsh crab (Sesarma reticulatum) were affected at 1 μg/L. No effects
nontarget crustaceans, such as shrimp, crab, or lobster, will also be exposed. Uneaten food is point source of DIF, TEF, and EMA to the surrounding environment, and it is estimated that approximately 5−15% of the administered food is uneaten,7 while faeces and biliary excretion make up the remaining environmental input. The topical bath treatment method applied for the pyrethroids will most likely result in rapid dilution of the active ingredients. DEL and CYP have a half-life of approximately 5 days in marine waters8 and together with the hydrophobic properties they exhibit, are likely to become sorbed to particulates and distributed in this way before the B
dx.doi.org/10.1021/es5005329 | Environ. Sci. Technol. XXXX, XXX, XXX−XXX
Environmental Science & Technology
Article
Table 1. Measured Environmental Concentrations of DIF and TEF
sediment (ng/g) (dw)* particulate (ng/L) water (ng/L) shrimp (ng/g) (ww)* amphipod (ng/g) (dw) crab (ng/g) (ww) blue mussel (ng/g) (ww) cod filet (ng/g) (ww) cod liver (ng/g) (lipid wt) cod skin (ng/g) (ww)
DIF TEF DIF TEF DIF TEF DIF TEF DIF TEF DIF TEF DIF TEF DIF TEF DIF TEF DIF TEF
farm 1
farm 2
farm 3
reference
DIF and TEF
TEF
DIF
no usage
range
median
range
5.9−42.5 7.2−66.0 1.1−15.2
