Bifenthrin Causes Toxicity in Urban Stormwater Wetlands: Field and

May 11, 2017 - All these contaminants have been associated with aquatic ecosystem decline due to their toxicity to biota, the extent of which can be e...
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Bifenthrin causes toxicity in urban stormwater wetlands: Field and laboratory assessment using Austrochiltonia (Amphipoda) Katherine Joanna Jeppe, Claudette Robin Kellar, Stephen Marshall, Valentina Colombo, Georgia May Sinclair, and Vincent J. Pettigrove Environ. Sci. Technol., Just Accepted Manuscript • Publication Date (Web): 11 May 2017 Downloaded from http://pubs.acs.org on May 15, 2017

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Environmental Science & Technology

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Bifenthrin causes toxicity in urban stormwater wetlands: Field and

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laboratory assessment using Austrochiltonia (Amphipoda)

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Katherine J. Jeppe*, Claudette R. Kellar, Stephen Marshall, Valentina Colombo, Georgia M. Sinclair

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and Vincent Pettigrove

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Centre for Aquatic Pollution Identification and Management (CAPIM), School of BioSciences, The University of

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Melbourne, Royal Parade, Parkville, Australia, 3010.

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KEYWORDS: Austrochiltonia subtenuis, Sediment toxicity, Synthetic pyrethroid

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ABSTRACT: Stormwater wetlands are engineered to accumulate sediment and pollutants from stormwater and provide

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environmental value to urban environments. Therefore, contaminated sediment risks causing toxicity to aquatic fauna. This

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research identifies contaminants of concern in urban wetland sediments by assessing sediment toxicity using the amphipod

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Austrochiltonia subtenuis. Sediments from 99 wetlands were analyzed for contaminants and laboratory bioassays were performed

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with A. subtenuis. Wild Austrochiltonia spp. were also collected from wetlands to assess field populations. Random forest

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modeling was used to identify the most important variables predicting survival, growth and field absence of Austrochiltonia spp..

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Bifenthrin was the most frequently detected pesticide and also the most important predictor of Austrochiltonia spp. responses.

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Copper, permethrin, chromium, triclosan and lead were also important. The median lethal effect concentration (LC50) of bifenthrin

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to laboratory-based A. subtenuis (1.09 (±0.08) µg/gOC) exposed to wetland sediments was supported by a bifenthrin-spiked

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sediment experiment, indicating A. subtenuis is a suitable test species. Furthermore, Austrochiltonia spp. were absent from all sites

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that exceeded the calculated bifenthrin LC50, demonstrating the impact of this contaminant on wild populations. This research

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demonstrates the sensitivity of Austrochiltonia spp. to urban sediment contamination and identifies bifenthrin as a contaminant of

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concern in urban wetlands.

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INTRODUCTION

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The construction of stormwater wetlands is widely recognized as an effective measure to abate stormwater runoff and reduce the

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environmental impacts of urbanisation.1 Stormwater wetlands serve several purposes, including sedimentation, chemical adsorption

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and biological filtration (by vegetation and bacteria), while also providing habitat and environmental value to urban environments.2

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By design, stormwater wetlands accumulate sediment and associated contaminants, protecting downstream receiving waters but

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potentially harming biota that live in them.

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Contaminants of concern in urban stormwater wetlands have changed over time.3 In recent decades, the occurrence of pesticides in

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urban environments has increased. Pesticides are not only used in agriculture but also in residential areas and are common in

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structural pest control, landscape maintenance and residential home and garden use. The use of synthetic pyrethroids has increased

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in recent years to replace organophosphate insecticides.4 Since the use of organophosphate insecticides decreased due to high

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mammalian toxicity, synthetic pyrethroid use has increased as they have relatively lower mammalian toxicity.5,

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synthetic pyrethroids have recently been shown to be toxic to non-target biota, such as fish and macroinvertebrates, in receiving

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environments.7-14

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Metal contamination in the urban environment has been relatively constant over recent years,3 although individual metals have

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changed with improved regulation. For example, zinc and copper are ubiquitous in urban environments due to their use in

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manufacturing processes, production of tires and brake pads and galvanization of metal surfaces. Lead has decreased since the

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phase out of leaded petrol and metals like cadmium, mercury and silver are generally restricted to industrial point sources.15

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Furthermore, background metal levels are often associated with geology, for example, nickel and chromium concentrations are

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often higher in basalt than in clay soils but can have a relatively lower bioaccessible fraction and toxicity.16 Hydrocarbons are often

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associated with road run off and, like zinc, are ubiquitous in urban environments. All these contaminants have been associated with

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aquatic ecosystem decline due to their toxicity to biota, the extent of which can be established with sediment toxicity tests.6, 17-20

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Amphipoda are one of the main groups used in sediment toxicity testing.21 Toxicity tests have been developed for several

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amphipod species, such as Hyalella azteca (in North America) and Gammarus spp. (in Europe) for the assessment of freshwater

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bodies, and Melita plumulosa for marine environments.22-24 None of these freshwater species, however, occur in Australia.

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Importation is possible but problematic due to strict biosecurity regulation, meaning that these tests could only be run in certified

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laboratories with strict biocontainment. Furthermore, the responses observed in international species are unlikely to accurately

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represent indigenous species responses. Indigenous species have physiologically adapted to local conditions (e.g. higher salinity

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and low phosphorus) and their responses better predict contaminant impacts, as they are not affected by local environmental factors

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that could confound or mask the effect of a toxicant in non-local species.25 It is also possible that the environmental fate and

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However,

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bioavailability of chemicals differ under local environmental conditions. Therefore a native amphipod species is essential for

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ecologically meaningful bioassays.

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A common amphipod that occurs in southern Australian is Austrochiltonia subtenuis.26 This species is a benthic shredder and by

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consuming algae and detritus it provides an important ecological function in freshwater ecosystems. It also provides a food source

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to many invertebrate and vertebrate species. Given that A. subtenuis is one of the most abundant taxonomic groups in these

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freshwater ecosystems and is crucial to the function and structure of invertebrate communities it is pertinent to investigate potential

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toxicity of contaminants to this species. Recently, A. subtenuis has been shown to be sensitive to fungicide contamination in water,

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however there is little research to date on the impacts of sediment contamination on this species.27

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This study investigated the toxicity of stormwater wetland sediments using laboratory-based sediment tests with A. subtenuis and

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field assessment of Austrochiltonia spp. This research aimed to identify sediment contaminants of concern in urban wetlands and to

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validate Austrochiltonia spp. as a sensitive indicator of environmentally relevant sediment toxicity.

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EXPERIMENTAL MATERIAL AND METHODS

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Study area and sample collection. Sediment and field amphipods were collected from 99 constructed wetlands in the Greater

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Melbourne metropolitan Area (GMA) between February and May 2015 (Figure 1). The geographic coordinates of the sampled

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wetlands are listed in Supporting Information Table S1. For sediment collection, deposited sediments (top 2 cm) were collected and

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sieved on site through 63 µm nylon mesh.18 Sediments were then allowed to settle in 10 L buckets, the overlying water decanted,

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and stored in clean glass jars in the dark at 4 °C until chemical analysis and toxicity testing. For field amphipod collection, the

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types of aquatic habitat (vegetated, leaf litter or bare substrate) were assessed at each site and each habitat was sampled for 2

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minutes with a 250 µm dip net. The samples were combined across habitats and picked on site for 30 minutes. Resulting

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amphipods were then stored in 70% ethanol for later identification. Once in the laboratory, amphipods were identified to genus and

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counted under a dissecting microscope.

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Chemical analyses. Sediments were analyzed for a number of chemical parameters, including metals, pesticides, total organic

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carbon, petroleum hydrocarbons, polycyclic aromatic hydrocarbons (PAHs). University of Melbourne Chemistry Department

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analyzed the sediment for organic contaminants by Gas Chromatography Mass Spectrometry (GC-MS), including personal care

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products and selected pesticides. This analysis was selected to target the semi- and non-polar contaminants that associate with

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sediment. Detailed methods for the GC-MS analysis of sediments, including mass spectrometer ion monitoring program and quality

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control and assurance procedures are presented in Supporting Information 2 (Table S2-S4). Australian Laboratory Services

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analyzed the sediment for total metals by ICP-AES (method: EG005T), total mercury by FIMS (method: EG035T), total

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recoverable hydrocarbons (C10-C40) (method: EP080/071), total organic carbon (TOC) (method: EP003) and moisture content

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(method: EA055). Quality assurance and control for metal and hydrocarbon analysis are displayed in Supporting Information Table

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S5.

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Laboratory-based bioassay. Laboratory-based amphipod bioassays, using Austrochiltonia subtenuis were used to assess the

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toxicity of wetland sediments compared to reference sediment (Deep Creek, Bulla Rd, Bulla, Victoria). The A. subtenuis culture

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used in these exposures originated from the reference site. The culture was maintained in glass aquaria containing cotton gauze as

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substrate and a standard artificial media (SAM) modified from Borgmann.28 The SAM consisted of reverse osmosis water with

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4.71 mM of NaCl, 2.3 mM of NaHCO3, 1.73 mM MgCl2 hydrous, 0.61 mM of CaCl2 hydrous, 0.48 mM NaBr, 0.32 mM of MgSO4

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and 0.09 mM of KCl. Cultures were maintained at 21 ± 1°C under a 16:8 h light:dark photoperiod. The culture was fed powdered

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fish food (Tetramin®) and supplemented with conditioned Pomaderris sp. leaves. Leaves were air-dried for 7 days at room

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temperature and conditioned in nutrient-enriched water at a rate of 1 g/L (reference site water with 5 mg/L phosphorous as

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K2HPO4 and 20 mg/L nitrogen as (NH4)2SO4) for 2 weeks, with water renewed after 7 days.

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For the experiment, ten 7-14 day old juveniles were added to each experimental replicate. Each replicate was composed of a 450

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mL beaker containing 40 g (wet weight) of sieved (< 63 µm) sediment and ~350 mL SAM. The bioassays were run in 4 batches of

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25 sites each, with 4 replicates for each site and 8 for the reference (Deep Creek, Bulla Rd, Bulla, Victoria). Batches were timed so

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that sediment was never held for more than 3 weeks between collection and bioassay commencement. The bioassays were run on a

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semi-automated flow-through system, which renewed approximately 120 ml of water twice daily. Amphipods were fed three times

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a week with powdered fish food and ground Pomaderris sp. leaves at a rate of 0.5 mg of each food type per amphipod per day. For

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quality assurance and control, electrical conductivity, pH, dissolved oxygen and total ammonia concentrations were measured at

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the end of the assay. Copper reference toxicity tests were also run for A. subtenuis larvae from the same cultures used in the

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laboratory test to ensure that cultures were appropriately sensitive to a standard stressor. Water quality and copper reference test

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results are displayed in in Supporting Information, Table S6 and Table S7, respectively. After the 21 d exposure, amphipods were

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removed from each replicate by sieving the sediment and water through a 250 µm sieve. If less than ten amphipods were retrieved,

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the remaining sediment (>250 µm) was stained with Rose Bengal and sorted under a dissecting microscope to locate any remaining

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survivors. Amphipod head length was then measured under a dissector microscope to establish growth during the 3-week exposure.

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Validation experiment. The results from the laboratory-based bioassay prompted a validation experiment to demonstrate the

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toxicity of bifenthrin to Austrochiltonia subtenuis. Sediment from an uncontaminated wetland (Bittern Reservoir, Bittern) was

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spiked to a high concentration (100 mg/kg dry weight bifenthrin, 99% purity, ChemService, USA) using acetone as the solvent

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carrier (2 mL in 1 kg wet weight sediment). This sediment was mixed open in a fume hood for 10 min per day with a stainless steel

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spatula to evaporate the acetone and then rolled for 1 h per day for a week. The stock sediment was then diluted with unspiked

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sediment to provide 13 treatments (measured concentrations: 57 µg/kg, 27 µg/kg, 22 µg/kg, 11 µg/kg, extrapolated concentrations

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(below detection of analysis) 8.25 µg/kg, 6.19µg/kg, 4.64 µg/kg, 3.48 µg/kg, 2.61 µg/kg, 1.96 µg/kg, 0.98 µg/kg, 0.49 µg/kg). The

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TOC of spiked sediment was 2.1% and field sediments ranged from 1.07% to 13.91%). Treatment sediments were shaken for 30

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seconds each day and rolled for 1 h per day for 5 days before experiment setup. A solvent control (2 mL in 1 kg wet weight

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sediment), treated as the stock sediment, and an unspiked control, treated as diluted sediments, were included. Four replicates were

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conducted for each spiked treatment and eight replicates were conducted for the two control treatments. Before the experiment

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commenced, water was renewed twice in all beakers and the experiment was run on a semi-automated flow-through system under

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conditions described for the laboratory-based bioassays. Water quality and copper reference test results for the validation

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experiment are displayed in Supporting Information, Table S8 and Table S9, respectively.

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Statistical analysis. All statistical analysis was performed in R (version 3.3.0, The R Foundation for Statistical Computing). For

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modeling, sediment contaminant concentrations were adjusted for limits of detection (LOD). Values below the LODs were reported

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as 50% of the LOD and trace detects were reported as 75% the LOD. To account for differences in bioavailability due to organic

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carbon in the