Lethal and Sub-Lethal Effects of Commonly Used Anti-Sea Lice Formulations on Non-Target Crab Metacarcinus Edwardsii Larvae
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Chemosphere 185 (2017) 1019e1029 Contents lists available at ScienceDirect Chemosphere journal homepage: www.elsevier.com/locate/chemosphere Lethal and sub-lethal effects of commonly used anti-sea lice formulations on non-target crab Metacarcinus edwardsii larvae * Paulina Gebauer a, , Kurt Paschke b, d, Claudia Vera b, Jorge E. Toro c, Miguel Pardo c, d, Mauricio Urbina e a Centro i~mar, Universidad de Los Lagos, Casilla 557 Puerto Montt, Chile b Instituto de Acuicultura, Universidad Austral de Chile, Casilla 1327, Puerto Montt, Chile c Instituto de Ciencias Marinas y Limnologicas, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile d Centro FONDAP de Investigacion en Dinamica de Ecosistemas Marinos de Altas Latitudes (IDEAL), Chile e Departamento de Zoología, Facultad de Ciencias Naturales y Oceanograficas, Universidad de Concepcion, Chile highlights Cypermethrin, deltamethrin, and azamethiphos affected 100% crab larvae at concentrations lower than used against sea-lice. Hydrogen peroxide at the concentration used as an anti-sea lice treatment had lethal and sub-lethal effects on M. edwardsii zoea I. À Repeated exposure to azamethiphos (0.0625e0.5 mgL 1) increased mortality, but did not affect zoea I developmental time. À Chronic exposure to hydrogen peroxide (187.5e1500 mg L 1) had a lethal effect on larvae. article info abstract Article history: The pesticides used by the salmon industry to treat sea lice, are applied in situ via a bath solution and are Received 8 February 2017 subsequently discharged into the surrounding medium. The effects of cypermethrin, deltamethrin, Received in revised form azamethiphos and hydrogen peroxide were assessed on the performance of Metacarcinus edwardsii 10 July 2017 larvae, an important crab for Chilean fishery. All larvae were dead or dying after 30 min of exposure to Accepted 19 July 2017 cypermethrin and after 40 min to deltamethrin at concentrations 100 and 20 times lower (0.15 and Available online 24 July 2017 À 0.1 mgL 1, respectively) than the concentrations and exposure times recommended by the manufacturers Handling Editor: Jim Lazorchak (CRM) to treat sea lice. Azamethiphos affected all larvae at a concentration 10 times lower than CRM. Hydrogen peroxide had the lowest detrimental effects, but at the CRM, 100% of the larvae were affected. Keywords: Sub-lethal effects, i.e prolonged developmental time, were observed at concentrations lower than CRM. À À Cypermethrin Repeated exposure to azamethiphos (0.0625e0.5 mgL 1) and hydrogen peroxide (188e1500 mg L 1) had Deltamethrin effects on survival. In conclusion, the pesticides used against parasitic copepod tested here, negatively Azamethiphos affect non-target crustacean larvae. Due to the product’s characteristics, the lethal effects of the pyre- Hydrogen peroxide throids probably are restricted to the time and area of application, while the action of azamethiphos may Organophosphate extend to a wider area. Current data are insufficient to accurately dimension the effects of these com- Crustacean larvae pounds in the field. More research is required to evaluate the consequences of prolonged developmental times and/or reduction in appendage mobility, so as the effects of these compounds on the pelagic and benthic communities. © 2017 Elsevier Ltd. All rights reserved. 1. Introduction farming is susceptible to various bacterial, viral, and parasitic dis- eases, due to the high density of cultivation, requiring the use of In the Southern Hemisphere, salmon and trout are intensively both antibiotic and antiparasitic treatments (Burridge et al., 2010). farmed in the fjords and channels of Chilean Patagonia. Salmon Among them, sea lice pose a serious threat to productivity in both salmon and trout farming (Burridge et al., 2014). In global monetary terms, costs associated to sea lice control equate to around 0.19 V À * Corresponding author. kg 1 of salmon produced (Costello, 2009). In Chile, the E-mail address: [email protected] (P. Gebauer). http://dx.doi.org/10.1016/j.chemosphere.2017.07.108 0045-6535/© 2017 Elsevier Ltd. All rights reserved. 1020 P. Gebauer et al. / Chemosphere 185 (2017) 1019e1029 predominant parasite species is the copepod Caligus rogercresseyi. Sub-lethal effects, such as changes in locomotion, were reported Control measures have included the application of chemical com- after exposing adult American lobster to azamethiphos (Abgrall pounds (Aaen et al., 2015), such as organophosphates (since 1981) et al., 2000), and prawn (Palaemon serratus) to deltamethrin À specifically azamethiphos (since 2013), synthetic pyrethroids (e.g. (0.6 ng L 1)(Oliveira et al., 2012). In several species of free-living cypermethrin and deltamenthrin, used since 2007 (Aaen et al., copepods, both swimming and feeding behaviours are altered by À 2015), and hydrogen peroxide to a lesser degree. Large volumes concentrations of 5 mg L 1 hydrogen peroxide (Van Geest et al., À of these pesticides are discharged into the Chilean marine 2014) and 0.098e0.32 mgL 1 cypermethrin (Barata et al., 2002). ecosystem; for example, 677 kg of active compound cypermethrin Damage by oxidative stress as protein carbonylation were reported À and 197 kg of deltamethrin were discharged in 2012 (Helgesen in H. americanus as a result of chronic exposure to 61 ng L 1 aza- et al., 2014). Despite these levels of discharge, very little is known methiphos, and lipid oxidation was reported in Penaeus monodon À about the potential negative effects on aquatic life. after 4 days of exposure to 0.1 mgL 1 deltamethrin (Dorts et al., These pesticides have a different mechanism of action. Organ- 2009). Both types of damage were observed in Procambarus clar- À ophosphates are neurotoxics that inhibit the enzymatic activity of kii after exposure to 0.005 mgL 1 cypermethrin for 24 h (Burridge acetylcholinesterase (AChE), the enzyme responsible for acetyl- et al., 2014). These previous studies indicate a range of both lethal choline hydrolysis (Intorre et al., 2004). Pyrethroids act on neural and sub-lethal effects on non-target organisms from the applica- transmission by interfering with sodium channels (Miller and tion of the various families of pesticide chemicals. Adams, 1982), resulting in motor neuron depolarisation and re- Our aim was to assess the effects of commercial pesticides, petitive discharge in the nerve endings, which may lead to paralysis commonly used in the treatment of C. rogercresseyi on fish farms, on and death (Crane et al., 2011; Haya et al., 2005). Hydrogen peroxide the larval performance of the South American crab species acts as an oxidising agent generating gaseous oxygen, which re- M. edwardsii. This commercially important crab species is abundant mains trapped inside the cuticle of the crustaceans. These chemical on the coasts of Southern Chile, accounts for nearly 80% of the compounds are applied in situ by enclosing net pens and bathing artisanal crab fishery, and is an important component of the local fish using a tarpaulin. After completion of the chemical treatment, economy (Chilean national fishery statistics, SERNAPESCA, the compound is then, released into the surrounding seawater. 2011e2014). The effects of acute (based on the manufacturers’ Dispersion and dilution rates of the chemicals depend on the recommendations, time and concentration) and chronic exposure characteristics of each pesticide and the hydrographic character- to pesticides on the first larval stage (zoea I) of M. edwardsii were istics of the area. A residual chemical compound concentration investigated. Developmental time and survival were used as persists in the area around the treated pens, which is likely to response variable; we also estimated the 50% lethal and effective impact non-target species. (Burridge et al., 2014; Ernst et al., 2014). concentrations. Given the generality and broad action spectrum of Specifically, concentrations of cypermethrin between 0.185 and the formulations used to treat sea lice in Chilean salmon-farming, À 0.218 mgL 1 have been measured 25 m away from the net pen we hypothesize cypermethrin, deltamethrin, azamethiphos and treated, 25min after final treatment (Hunter and Fraser,1995; Willis hydrogen peroxide will negatively affect the developmental time et al., 2005), while concentrations of deltamethrin between 0.020 and survival of the zoea I of M. edwardsii. À and 0.040 mgL 1 have been detected 4e5 h after treatments with this compounds (Ernst et al., 2014). For azamethiphos concentra- 2. Materials and methods tions between 1 and 25 mgL-1 have being measured from 1 to 1000 m away from the application area (Ernst et al., 2014). 2.1. Larvae collection The majority of research assessing the lethal effects of pesticides used on sea lice have been conducted on adult of non-target Ten ovigerous M. edwardsii females were kept in containers with crustaceans, determining lethal and/or effective concentrations circulating seawater until larvae hatched (~12 C, 32 PSU for 1 (LC50,EC50) (see more detailed Table 1 Ernst et al., 2001; Mayor month). Recently hatched zoea I were collected and actively et al., 2008; see more detailed Table 5 Van Geest et al., 2014). swimming larvae were selected for the exposure to cypermethrin ® ® ® However, very little is known about the lethal effects of these (Betamax ), deltamethrin (Alpha Max ), azamethiphos (Calfree ), ® chemical compounds on the early life stages of decapod crusta- and hydrogen peroxide (Hyperox ). ceans. It is useful to note that LC50 has been calculated for American lobster (Homarus americanus) larvae for cypermethrin (Burridge et al., 2000a, 2000b; Pahl and Opitz, 1999), deltamethrin 2.2. Acute exposures (Burridge et al., 2014), azamethiphos (Burridge et al., 2000b, 2014; Pahl and Opitz, 1999), and hydrogen peroxide (Burridge et al., Four independent experiments were carried out, in which 2014), providing some indication of the expected effects. different groups of zoea I larvae (2800 larvae per experiment) were exposed to each of the four compounds. For each compound Table 1 Nominal concentrations of cypermethrin, deltamethrin, azamethiphos and hydrogen peroxide, and exposure times for the acute experiments in M.