Elucidating the Behavior of Cyclic Volatile Methylsiloxanes in a

Subscriber access provided by UNIVERSITY OF ADELAIDE LIBRARIES

Article

Elucidating the Behavior of Cyclic Volatile Methylsiloxanes in a Subarctic Freshwater Food Web: A Modeled and Measured Approach Ingjerd Sunde Krogseth, Emma Maria Undeman, Anita Evenset, Guttorm N. Christensen, Mick J. Whelan, Knut Breivik, and Nicholas A. Warner Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b03083 • Publication Date (Web): 05 Oct 2017 Downloaded from http://pubs.acs.org on October 9, 2017

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

Environmental Science & Technology is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 21

Environmental Science & Technology

3

Elucidating the Behavior of Cyclic Volatile Methylsiloxanes in a Subarctic Freshwater Food Web: A Modeled and Measured Approach

4

Dr. Ingjerd S. Krogseth,1,* Dr. Emma Undeman,2,3 Dr. Anita Evenset,4,5 Cand. Scient. Guttorm N.

5

Christensen,4 Dr. Mick J. Whelan,6 Dr. Knut Breivik,7,8 Dr. Nicholas A. Warner1

1 2

6 7 8 9 10 11 12 13

1 2

NILU – Norwegian Institute for Air Research, The Fram Centre, P.O. Box 6606 Langnes, 9296 Tromsø, Norway; Baltic Sea Centre, Stockholm University, SE-106 91 Stockholm, Sweden; 3Department of Environmental Science and Analytical Chemistry, Stockholm University, Svante Arrhenius väg 8, SE-106 91, Stockholm, Sweden; 4 5 Akvaplan-niva AS, The Fram Centre, P.O. Box 6606 Langnes, 9296 Tromsø, Norway; Faculty of Biosciences, Fisheries and Economics, UiT the Arctic University of Norway, Hansine Hansens veg 18, 9019 Tromsø, Norway; 6 School of Geography, Geology and the Environment, University of Leicester, Leicester LE1 7RH, United 7 8 Kingdom; NILU – Norwegian Institute for Air Research, P.O. Box 100, 2027 Kjeller, Norway; Department of Chemistry, University of Oslo, P.O. Box 1033, Blindern, 0315 Oslo, Norway.

14 15

*Corresponding author: NILU – Norwegian Institute for Air Research, The Fram Centre, P.O. Box 6606 Langnes, 9296 Tromsø, Norway, tel: +47 63 89 80 00, [email protected]

16 17

Abstract

18

environments through wastewater effluents, and their bioaccumulation potential is debated. Here, a

19

new bentho-pelagic version of the ACC-HUMAN model was evaluated for polychlorinated biphenyls

20

(PCBs) and applied to cVMS in combination with measurements to explore their bioaccumulation

21

behavior in a subarctic lake. Predictions agreed better with measured PCB concentrations in Arctic

22

char (Salvelinus alpinus) and brown trout (Salmo trutta) when the benthic link was included than in

23

the pelagic-only model. Measured concentrations of decamethylcyclopentasiloxane (D5) were 60 ±

24

1.2 (Chironomidae larvae), 107 ± 4.5 (pea clams Pisidium sp.), 131 ± 105 (three-spined sticklebacks:

25

Gasterosteus aculeatus), 41 ± 38 (char), and 9.9 ± 5.9 (trout) ng g-1 wet weight. Concentrations were

26

lower for octamethylcyclotetrasiloxane (D4) and dodecamethylcyclohexasiloxane (D6), and none of

27

the cVMS displayed trophic magnification. Predicted cVMS concentrations were lower than

28

measured in benthos, but agreed well with measurements in fish. cVMS removal through ventilation

29

was an important predicted loss mechanism for the benthic-feeding fish. Predictions were highly

30

sensitive to the partition coefficient between organic carbon and water (KOC) and its temperature

31

dependence, as this controlled bioavailability for benthos (the main source of cVMS for fish).

Cyclic volatile methylsiloxanes (cVMS) are used in personal care products and emitted to aquatic

1 ACS Paragon Plus Environment


Page 2 of 21

1. Introduction

32 33

Cyclic

34

decamethylcyclopentasiloxane (D5), and dodecamethylcyclohexasiloxane (D6), are used as

35

ingredients in personal care products and are emitted to aquatic environments through wastewater

36

effluents.1-3 D4 has been classified as a persistent, bioaccumulative, and toxic (PBT) substance and D5

37

as a very persistent and very bioaccumulative (vPvB) substance in a European Chemical Agency

38

Member State Committee opinion.4 A restriction on use in wash-off products is currently underway

39

in Europe.5 However, their hazardous properties, particularly their bioaccumulation potential, are

40

uncertain.6-8 Field studies of cVMS in aquatic food webs have demonstrated both trophic dilution9-12

41

and trophic magnification,13,14 and the explanation(s) for this variability remains unclear. Possible

42

influencing factors include behavioral and physiological characteristics of the investigated taxa, food

43

chain composition, and the nature of the physical environment (including possible confounding

44

effects such as spatial gradients in concentration).7,15

45

As well as being very volatile, cVMS are very hydrophobic, and are expected to partition significantly

46

to organic phases. Although it is now well established that the organic carbon (OC) to water partition

47

coefficients (KOC) for cVMS are lower than those expected from their octanol to water partitioning

48

(KOW),16-19 there is uncertainty in the temperature dependence of KOC which currently constrains our

49

understanding of the behavior of cVMS in cold aquatic environments.20 Although a positive

50

relationship between KOW and temperature has been reported (suggesting lower hydrophobicity at

51

low temperatures),19,21,22 a negative relationship between KOC and water was recently reported

52

(suggesting higher hydrophobicity at low temperatures).23 This will influence the behavior of these

53

compounds in systems with low temperatures. In aquatic systems without continuous wastewater

54

emissions, the exposure of pelagic organisms to these compounds is likely to be primarily via benthic

55

links in the food web, as cVMS may be rapidly removed from water between emission events.20

56

The combination of fugacity-based models and measurements has proved useful for developing an

57

understanding of the environmental behavior of cVMS and the identification of key knowledge

volatile

methyl

siloxanes

(cVMS),

such

as

octamethylcyclotetrasiloxane


(D4),

Page 3 of 21


58

gaps.24-27 However, this approach has rarely been used for cVMS behavior in food webs. Exceptions

59

include applications of the AquaWeb6 and ACC-HUMAN models.24,28 ACC-HUMAN predicted trophic

60

dilution of cVMS in zooplankton, herring, and cod from the Inner Oslofjord (which receives high

61

wastewater emissions), in accordance with measurements.24 However, given the importance of

62

sediments as a reservoir of cVMS, there is a need for a benthic link in the model. This is particularly

63

important for systems such as Storvannet where fugacities in sediment often exceed those in the

64

water column due to intermittent emission events and rapid advection of the water column.20 Here,

65

we explore the bioaccumulation behavior of cVMS using the ACC-HUMAN model, which was

66

expanded to include a benthic link. Model performance was first evaluated for well-known PCBs, and

67

the model was subsequently applied to explain measured cVMS concentrations in biota sampled

68

from Lake Storvannet in Northern Norway. Lake Storvannet was chosen as (i) the lake and its food

69

web is relatively well-studied,29,30 (ii) measurements of PCBs from lake water, sediments, and biota

70

are available for model evaluation purposes,31 and (iii) a study of cVMS behavior in the physical

71

environment of the lake has already been carried out.20

72

2. Methods

73

2.1. Study site

74

Lake Storvannet is a small (0.2 km2, maximum depth 17 m), oligotrophic lake, located in a residential

75

area of the town of Hammerfest in Northern Norway (70°N 23°E; 7000 inhabitants).20 The lake has a

76

long history of local contamination with organic contaminants including PCBs.31 Untreated

77

wastewater from Hammerfest is now emitted into the sea. However, sewers run along both sides of

78

Storvannet, and the lake unintentionally receives wastewater through leaking pipes and combined

79

sewer overflow events (CSOs), particularly during the snowmelt season and after heavy rainfalls.20 As

80

a result, cVMS are present in sediments of the lake with concentrations comparable to much more

81

populated areas (207 ± 30, 3775 ± 973, and 848 ± 211 ng g-1 OC for D4, D5, and D6, respectively).20

82

However, cVMS were not detected in water samples from the lake (LOQ 19-40 ng L-1, 12-54 ng L-1,

83

and 42-74 ng L-1 for D4, D5, and D6, respectively).20 The lake is ice covered for approximately six



84

months of the year and the summer season and the plankton bloom is short. Benthic Chironomidae

85

larvae (hereafter; chironomids) and pea clams (Pisidium sp.) are, consequently, important dietary

86

items for resident fish.29,32,33 Populations of both stationary and anadromous Arctic char (Salvelinus

87

alpinus) (hereafter; char) and brown trout (Salmo trutta) (hereafter; trout), as well as three-spined

88

sticklebacks (Gasterosteus aculeatus) (hereafter; sticklebacks) inhabit the lake.29,30 While char mostly

89

feed on benthos, the trout has a more pelagic diet including aquatic insects.29,34,35 Both the trout and

90

char may be cannibalistic, but the trout tends to be more piscivorous than the char and also feed on

91

sticklebacks (Figure 1, Table 1, Supporting Information (SI) 2.2). The sticklebacks feed on plankton

92

and benthos in the littoral zone of the lake. Only stationary fish were included in this study.

93 94

Char (n = 11) and trout (n = 13) were caught opportunistically in March, May, and June 2014 (Table

95

S1). In March and May, the fish were caught with lines and hooks. In June, gill nets were used. In

96

addition, traps, baited with fish roe (wrapped in fine mesh so the fish could not eat it), were

97

deployed in shallow areas of the lake for collection of sticklebacks (n = 5). Benthic fauna

98

(Chironomidae and Pisidium sp.) were collected by hauling a 500 µm trawl along the bottom. All

99

samples were wrapped in aluminum foil, placed in zip-lock bags, and transported in chilled boxes to

100

the lab where they were stored at -20 °C until sample preparation. All use of personal care products

101

was avoided by field and lab personnel. Muscle and liver tissues from Atlantic cod (Gadus morhua)

102

caught off the Norwegian coast were utilized as blank material. Prior to sample collection, the cod

103

tissues were split into three separate portions to serve as field blanks, dissection blanks, and

104

reference blanks, in order to assess if any contamination occurred during field work or sample

105

dissection.

106

Strict quality control procedures were enforced to limit cVMS contamination of samples (SI 1.1). The

107

bodyweight and total length of each fish were recorded, gender and maturity were determined

108

through visual inspection of the gonads, and stomach content was visually examined (Table S1, S2).

109

Otoliths were retrieved to determine the age of the char and trout (Table S1). Liver and dorsal

2.2. Sample collection, preparation and analysis


Page 4 of 21

Page 5 of 21


110

muscle tissue was taken out for analysis of cVMS, extractable organic matter (assumed

111

representative for lipids),36 and stable isotope analysis (muscle only; δ15N, δ13C, δ14S) (SI 1.2, Table 2).

112

Prior to analyses, both liver and muscle samples were homogenized with a metal scalpel on a clean

113

glass surface. Due to the small size of the sticklebacks, the whole fish was homogenized and the

114

homogenate was analyzed for cVMS and stable isotopes. The collected chironomids were pooled and

115

homogenized in a mortar, giving two replicates for cVMS analysis and one for stable isotopes. The

116

same procedure was followed with whole Pisidium samples (including the carbonaceous shell).

117

All samples were extracted for cVMS using a biphasic cold solvent extraction, based on a previously

118

published method for sediments,20 but adapted to biotic tissues (SI 1.3). Analysis of cVMS was carried

119

out on an Agilent 7890A GC connected to an Agilent 5975C MS detector and a Gerstel MPS3

120

autosampler. Method details have previously been published.20 Calculation of limits of detection

121

(LOD) and quantification (LOQ) from blank samples is described in SI 1.1.

122

2.3. Bioaccumulation modeling

123 124

2.3.1. Development of the bentho-pelagic ACC-HUMAN The aquatic part of the original ACC-HUMAN model represents a pelagic Baltic Sea food web

125

consisting of zooplankton, a planktivorous fish (herring) and a piscivorous fish (cod).28 Here, a benthic

126

link was included in the model by adding a sediment compartment, a benthic filter feeder, a benthic

127

predator/deposit feeder, and up to three prey items for the latter. The model does not simulate

128

chemical transfer between lake water and sediment. Rather, time-resolved concentrations or

129

fugacities in sediment and lake water is provided as input to the model. Sediment pore water and

130

sediment solids are assumed to be in equilibrium.

131

The prey items are defined by their biochemical composition (fractions of water, lipid, and non-lipid

132

organic matter), the fraction of time they spend buried in sediments, and assumed thermodynamic

133

equilibrium with their surroundings. Bioaccumulation in the predator/deposit feeder and filter feeder

134

are predicted using a dynamic version of the steady-state model of Arnot and Gobas.37 The fugacity

135

capacity (Z-value) of the organism is calculated based on its biochemical composition. Chemical 5 ACS Paragon Plus Environment


136

uptake occurs through feeding and ventilation (of sediment pore water and/or overlying water).

137

Elimination of chemicals can occur through ventilation, fecal egestion and/or biotransformation. The

138

predator/deposit feeder may feed on the prey items and/or sediment particles, while the filter

139

feeder may feed on suspended or settled sediment particles and/or zooplankton. The fish in the

140

model may prey on the benthic filter feeder and the deposit feeder, in addition to zooplankton and

141

fish. The model assumes annual constant growth rate, lipid content, and dietary composition.

142

However, a seasonal feeding pattern for the fish was included in the model, in which the fish are

143

assumed not to eat during wintertime (November – February) as is the case in Storvannet. All

144

equations, parameters, and assumptions for the new model are described in SI 2.1 and 2.2.

145

To adapt the bentho-pelagic ACC-HUMAN to Storvannet, the model organisms were parameterized

146

as key species of the Storvannet food web. Benthos were parameterized as chironomid larvae

147

(deposit feeder) and Pisidium clams (filter feeder). The pelagic fish was re-parametrized based on

148

sticklebacks, while the piscivorous fish was re-parametrized to represent either char or trout (SI 2.2,

149

Table 1). Dietary composition of the organisms and overall structure of the food web was based on

150

existing knowledge about the system aided by analysis of stable isotopes and gut content.

151

Measurements of water temperatures (Table S11),38 fraction of solids in sediments (18 % v/v) and

152

fraction of OC in sediment solids (5 % w/w)20 from Storvannet were used as model input.

153 154

2.3.2. Model evaluation and application Many model aspects are independent of the compounds studied and are best constrained on the

155

basis of data-rich chemicals like PCBs. To evaluate the performance of the new bentho-pelagic model

156

version, it was compared with the pelagic-only version of ACC-HUMAN parameterized for the taxa

157

present in Storvannet. Predicted concentrations in char and trout were compared to measurements

158

from Storvannet for five PCB congeners (SI 2.3).

159

Empirical data for exposure-relevant physical media are restricted to sediment for cVMS. Hence, only

160

the bentho-pelagic model version was applied to cVMS, as the pelagic-only model needs


Page 6 of 21

Page 7 of 21


161

concentrations in water as input. Average measured concentrations of cVMS in surface sediments (0-

162

1 cm, OC-normalized) of Storvannet in 2014 were used as input to the model (Table S13).20 cVMS

163

concentrations in Storvannet lake water sampled at the same time were below limits of

164

quantification (LOQ).20 Given the lack of measured concentrations, a range of values for the fugacity

165

in water was evaluated, and expressed relative to the fugacity in sediment derived by the model

166

from the concentration in sediment (SI 2.4).

167

Measured partition coefficients (KOW and KAW (air-water partitioning)) and their temperature

168

dependencies (ΔUOW and ΔUAW) were used as input (Table S13).19,20,39 The KOC values for cVMS are

169

known to be significantly overestimated by empirical relationships with KOW.19,39 This deviation may

170

also apply for ΔUOC versus ΔUOW. The most recently measured values of KOC and ΔUOC for cVMS were,

171

therefore, used as direct inputs, rather than relying on relationships based on affinity to octanol

172

(Table S13).18,23 That said, partitioning to lipids was still assumed to be represented by partitioning to

173

octanol,40,41 although there is limited evidence to justify this assumption. cVMS may undergo

174

biotransformation in aquatic biota, but few measurements are available. Here, a fish

175

biotransformation rate constant (kM) of 4 · 10-4 h-1 (corresponding to a half-life of 72 days) was

176

applied for all cVMS (Table S13), following Whelan and Breivik.24,42 In the absence of evidence, cVMS

177

were assumed to not biotransform in benthos or zooplankton.

178

The model was run for 10 years with a 1 hour simulation time step. Predicted median lipid-

179

normalized concentrations in year 10 across all age classes at the time of year when the samples

180

were collected, as well as the annual range (min-max), were compared to measured lipid-normalized

181

concentrations in whole-body homogenates (chironomids, Pisidium, and sticklebacks) and in muscle

182

tissue (char and trout). As the model does not provide gender- and/or maturity-specific results for

183

fish, measurements were grouped irrespective of gender and maturity for comparison to model

184

results. Additional simulations were carried out to test the sensitivity of model results to changes in



185

cVMS physical-chemical properties and biotransformation rates (properties were changed

186

individually by ± 10 % and ± 20 %).

187

3. Results and discussion 3.1. Measured concentrations of cVMS

188 189

All cVMS concentrations in benthos were above LOQ (Table S3). The D4, D5, and D6 whole body

190

concentrations (pooled duplicates) in chironomids were 9.9 ± 0.3, 60 ± 1.2, and 9.3 ± 0.1 ng g-1 wet

191

weight (ww), and in Pisidium 4.7 ± 0.4, 107 ± 4.5, and 11.8 ± 1.2 ng g-1 ww, respectively (Table 2). The

192

measured concentrations in benthos are within the range of measured concentrations in benthos

193

reported elsewhere, including chironomids and burrowing mayfly in Lake Pepin, ragworm in the

194

Humber Estuary, and polychaets from the Oslofjord (Table S8).9,10,43,44 Lipid content for benthos was

195

not measured due to insufficient sample material. Instead this was derived from literature (Table 2).

196

Hence, the lipid-normalized concentrations have added uncertainty, particularly for Pisidium which

197

has a very low lipid content. This does not matter for model comparison purposes as the lipid

198

content assumed for normalization was used as model input and hence errors in lipid-content will

199

cancel out in model-measurement comparisons. The benthic samples may also have contained traces

200

of sediment particles, as they were not depurated after sampling. This means that measured

201

concentrations of (i) D4 in chironomids and D5 in Pisidium could have been diluted by presence of

202

sediment particles (concbenthos > concsed (ng g-1 ww)), while (ii) D5, D6 in chironomids and D4, D6 in

203

Pisidium could have been contaminated by presence of sediment particles (concbenthos ≤ concsed (ng g-1

204

ww)).20 Hence, cVMS concentrations in benthos should be considered approximate and are only used

205

for model-measurement comparison.

206

All cVMS concentrations in whole-body homogenates of sticklebacks were above LOQ (Table S3),

207

with concentrations of 12.6 ± 9, 131 ± 105, and 6.3 ± 3.6 ng g-1 ww for D4, D5, and D6, respectively

208

(309 ± 226, 3203 ± 2584, and 155 ± 89 ng g-1 lipid weight (lw)) (n = 5) (Table 2). In muscle of char and

209

trout, D4, D5, and D6 were above LOQ in 37 %, 97 %, and 14 % of the samples, respectively (Table

210

S3). D4 and D6 were below LOQ in trout, while D5 ranged between 3.9 – 22.0 ng g-1 ww (383 – 2434 8 ACS Paragon Plus Environment

Page 8 of 21

Page 9 of 21


211

ng g-1 lw) (n = 13). In char, D4, D5, and D6 ranged between

Elucidating the Behavior of Cyclic Volatile Methylsiloxanes in a

Recommend Documents