Perfluoroalkyl Acids in European Starling Eggs Indicate Landfill and

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Characterization of Natural and Affected Environments

Perfluoroalkyl Acids in European Starling Eggs Indicate Landfill and Urban Influences in Canadian Terrestrial Environments Sarah B Gewurtz, Pamela A. Martin, Robert J. Letcher, Neil M Burgess, Louise Champoux, John E. Elliott, and Abde Idrissi Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b06623 • Publication Date (Web): 17 Apr 2018 Downloaded from http://pubs.acs.org on April 17, 2018

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Environmental Science & Technology

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Perfluoroalkyl Acids in European Starling Eggs

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Indicate Landfill and Urban Influences in Canadian

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Terrestrial Environments

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Sarah B. Gewurtz,† Pamela A. Martin,*, ‡, Robert J. Letcher,*,§ Neil M. Burgess,ǁ Louise

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Champoux,┴ John E. Elliott,# Abde Idrissi,∇ †

6 7

‡

310 Normandy Avenue, Waterloo, Ontario N2K 1X7, Canada

Ecotoxicology and Wildlife Health Division, Wildlife and Landscape Science Directorate,

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Science and Technology Branch, Environment and Climate Change Canada, Burlington, Ontario

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L7S 1A1, Canada

10

§


11

Science and Technology Branch, Environment and Climate Change Canada, National Wildlife

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Research Centre, Carleton University, Ottawa, Ontario K1A 0H3, Canada

13

ǁ

14

Science and Technology Branch, Environment and Climate Change Canada, Mount Pearl,

15

Newfoundland A1N 4T3, Canada


ACS Paragon Plus Environment

1


16

┴


17

Science and Technology Branch, Environment and Climate Change Canada, Québec City

18

Québec G1J 0C3, Canada

19

#


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Science and Technology Branch, Environment and Climate Change Canada, Pacific Wildlife

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Research Centre, Delta, British Columbia V4K 3N2, Canada

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∇

Laboratory Services, Wildlife and Landscape Science Directorate, Science and Technology Branch, Environment and Climate Change Canada, Ottawa, Ontario K1A 0H3, Canada

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ABSTRACT: Perfluoroalkyl acids (PFAAs) were determined in European starling (Sturnus

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vulgaris) eggs collected between 2009 and 2014 from industrial, rural/agricultural, and landfill

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locations within five urban centers across Canada. Within each urban center, perfluoroalkyl

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sulfonic acid (PFSA) concentrations were generally greater in starling eggs collected from

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urban/industrial locations and PFSAs and perfluoroalkyl carboxylic acids (PFCAs) were

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generally greater at landfills compared to rural and remote locations. However, the relative

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importance of urban/industrial versus landfill locations as potential sources was chemical- and

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location-specific. PFSA concentrations in eggs collected from non-landfills were positively

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correlated with human population. Despite the 2000 to 2002 phase-out of perfluorooctane

34

sulfonic acid (PFOS) and its C8 precursors, leaching from consumer products during use likely

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continues to be a major source to the environment. In comparison, the concentrations of most

36

PFCAs in eggs were not related to population, which supports the hypothesis that atmospheric

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transport and degradation of precursor chemicals are influencing their spatial trends. PFAA

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concentrations in eggs from landfills were not correlated with the quantity of waste received by a

39

given landfill.

40

composition of waste items.

The variability in PFAAs between landfills may be due to the specific


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TABLE OF CONTENTS (TOC)/ABSTRACT ART

42 43

Landfill Industrial 10 km from urban center 40 km from urban center Remote

PFOS (ng/g wet weight)

Method Limit of Quantification Vancouver

103

103

102

102

101

101

100

100

10-1

10-1

104 103 102 101 100 10-1

Halifax

Calgary 102

103

101 100 10-1

Redcliff

104 103 102 101 100 10-1

Hamilton

Montreal

102 101 100 10-1


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INTRODUCTION

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Concern over perfluoroalkyl acids (PFAAs) has increased dramatically since 2016 due in part

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to the lowering of the United States Environmental Protection Agency (USEPA) drinking water

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advisory level to 70 ng/L for perfluorooctane sulfonic acid (PFOS) and perfluorooctanoic acid

48

(PFOA).1 Several U.S. States and other countries, including Canada, have also recently released

49

new guidance and/or regulatory standards for a variety of media.2 Despite regulatory and

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voluntary actions for these chemicals,3-6 a recent study found that the drinking water supply of

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approximately six million U.S. residents may have concentrations of PFOS and PFOA above the

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USEPA advisory level of 70 ng/L.7

53

Identification of sources of PFAAs to the environment is important for controlling

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environmental releases. Although several large-scale studies have examined sources to surface

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and drinking water and aquatic biota,7-9 comparable information is not available on a continental

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scale for the terrestrial environment and biota, which may differ from water.10 This information

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is needed for risk and hazard assessments on PFAAs as well as development of regulatory

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guidelines and standards that are focused on terrestrial-based ecological receptors, which are

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known information gaps.2,11-13

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In Canada, where PFAAs were not historically and are not currently manufactured,14,15 release

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from currently used commercial materials that were manufactured prior to phase-outs and

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regulations16,17 as well as following disposal, e.g., in landfills,18-20 are expected to be major

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environmental sources. Landfills are known sources of PFAAs to the aqueous environment20-22

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and the atmosphere.19,23 However, the impact of landfills is not clear as to PFAA concentrations

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observed in the terrestrial environment and in comparison to non-point sources related to human

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population.


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Large geographical scale monitoring programs using European starling (Sturnus vulgaris) eggs

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are effective in evaluating spatial trends and identification of contaminant sources on local,24

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national,25 and international26 scales. Starlings live up to 15 years in the wild and produce, on

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average, five eggs per season.27 They feed primarily on invertebrates in the upper few

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centimeters of soil during nesting season.28 This species is an income breeder and uses daily

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food intake to provide energy for eggs.29 Their home range is typically between 5 to 40 km,30

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but can be reduced by as much as 10-times during breeding season when the starlings forage

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closer to the nest site.31,32 Therefore, PFAA concentrations in starling eggs reflect recent and

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local exposure.26 They prefer habitats close to humans,28 nest in man-made boxes, and breeding

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populations can be readily established.24,26

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The objective of this study was to use a large North American transcontinental dataset of

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European starling eggs to test the hypothesis that the waste sector and non-point sources related

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to human population influence the spatial variability of PFAA concentrations in the terrestrial

80

environment. Particularly, we collected starling eggs from urban/industrial, rural/agricultural,

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and landfill locations associated with five Canadian urban centers to evaluate the overall

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influence of human activity and proximity to landfills on PFAAs found in the terrestrial

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environment. To our knowledge, this is the first study to assess PFAA concentrations in a

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terrestrial organism on a continental scale.

85 86

MATERIALS AND METHODS

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Sample Collection. Freshly laid starling eggs were collected between 2009 and 2012 and in

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2014 from nest boxes established within, adjacent to, and distant from five major urban centers

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across Canada, namely Vancouver, BC, Calgary, AB, Hamilton, ON, Montreal, QC, and Halifax,


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NS (Figure SI1 and Table SI1). Within each urban center, locations were categorized as one of

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four location type: urban industrial (districts of industrial activity within city limits), landfill

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(adjacent to cities), and rural sites located 10 and 40 km from major urban centers (typically in

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agricultural areas). It should be noted that the industrial location in Vancouver was close to the

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city limits in a light industrial area with agricultural activity nearby. A more suitable industrial

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area that would support a sufficient starling population could not be found in Vancouver due to

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the absence of grassed areas within industrial parks. A non-urban/non-landfill prairie location

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(Redcliff, AB) was chosen as an overall national reference location given that starlings do not

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nest in more remote locations. Starling nest boxes (25-30 per location) had been established at

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each location in 2008 and monitored each year for occupancy and onset of egg laying. On each

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sampling event, one to five eggs were randomly collected per nest box after at least three eggs

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had been laid, depending on the number of occupied boxes available to select from at the

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location.

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Upon collection, the eggs were transported to Environment and Climate Change Canada's

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National Wildlife Specimen Bank (ECCC-NWSB, Ottawa, ON, Canada), homogenized, and

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stored at -40 ºC until analysis. The eggs were homogenized in pools of up to 13 and we aimed

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for five or more pools, depending on the number of starling eggs collected (Table SI1). Pools

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were created from adjacent nest boxes.

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Chemical and Instrumental Analysis. The PFAAs and isotopically labeled surrogates that

109

were evaluated in this study are listed in Table SI2. The sample extraction and cleanup and

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instrumental analysis have been described previously in extensive detail.33-36 Eggs collected in

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2009 to 2012 were analyzed by the Organic Contaminants Research Laboratory (OCRL) at

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ECCC's National Wildlife Research Center (NWRC) and the instrument used was a Waters 2695


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HPLC that was coupled to a Waters Quattro Ultima triple quadrupole mass spectrometer. Eggs

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collected in 2014 were analyzed by the Lab Services section at ECCC's NWRC and the

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instrument used was an Agilent/AB-Sciex HPLC-MS/MS system. PFAA concentrations are

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presented on wet weight basis since PFAAs were not correlated to extractable lipid content in the

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eggs. Full details of the PFAA sample analyses, quality control, and calculation of the method

118

limits of detection (MLODs) and quantification (MLOQs) can be found in the Supporting

119

Information.

120

Data Analysis. Data analysis was performed on PFAAs detected in greater than 60 % of the

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samples, namely perfluorohexane sulfonic acid (PFHxS), PFOS, perfluorodecane sulfonic acid

122

(PFDS),

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perfluoroundecanoic acid (PFUnDA), perfluorododecanoic acid (PFDoDA), perfluorotridecanoic

124

acid (PFTrDA), and perfluorotetradecanoic acid (PFTeDA) (Table SI4). Robust Regression on

125

Order Statistics (ROS) were used for non-detect handling, as recommended by Helsel37 for

126

relatively small sample sizes and datasets containing up to 80 % censoring.

PFOA,

perfluorononanoic

acid

(PFNA),

perfluorodecanoic

acid

(PFDA),

127

Principal component analysis (PCA) on log-normalized concentrations was conducted to

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explore overall spatial patterns. Factor loadings were rotated using the Varimax normalized

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rotation. Two factors were retained based on the results of the Scree test, which accounted for

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87 % of the variance in the model.

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Linear mixed effect models (LMEMs) were used to assess PFAA concentration patterns in

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starling eggs with location type and urban center as fixed variables and year as a random

133

variable.38-40 Parameter concentrations were log-transformed to approximate normality (Shapiro-

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Wilk, p > 0.05). The Vancouver urban center was not included in the LMEM analysis given that

135

the 10 km rural location type was not evaluated within this urban center (Table SI1). The


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optimal model was selected on the basis of consistency with Zuur et al.39 For each PFAA, we

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started with a model where the fixed component contained the two explanatory variables and the

138

interaction term.

139

identified using the restricted maximum likelihood (REML) estimation likelihood ratio test and

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Akaike’s Information Criterion (AIC). We then identified the optimal/most parsimonious fixed

141

structure using the maximum likelihood estimation likelihood ratio test and AIC.39 After model

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selection, the optimal/most parsimonious model was refitted using REML estimation. The

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residuals of candidate and optimal models were inspected for homogeneity and normality. For

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each PFAA, the optimal/most parsimonious model contained location type and urban center and

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their interaction as fixed factors. Therefore, simple main effects ANOVAs were used to test for

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significant differences in log-transformed PFAA concentrations between locations within each

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urban center. In addition, within each location, simple main effects ANOVAs were used to test

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for significant differences between years for locations/years with three or more pooled replicate

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samples. Unplanned multiple comparisons were performed using the Tukey test. Log-linear

150

regression on annual mean concentrations was used to determine if concentrations increased or

151

decreased with time.

The optimal/most parsimonious structure of the random component was

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In order to explore the influence of human activity on PFAA concentrations, the Pearson

153

correlation coefficient (r) was used to test the significance of log-log linear correlations between

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human population and median PFAA concentrations in starling eggs. The estimated population

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of each non-landfill location is presented in Table SI5. Landfill locations were excluded from

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this analysis due to their potential to act as point sources distinct from the influence of

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population, as discussed below. The Pearson correlation coefficient was also used to test the


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significance of log-log correlations between landfill fill rate (Table SI6) and median PFAA

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concentrations in starling eggs.

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The LMEMs were constructed in R Version 3.2.3 using the lme function (nlme package).41,42

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All other statistical analyses were performed using Statistica 7.0 (Stats Soft Inc., Tusla, OK,

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USA) at the α = 0.05 significance level. Additional technical details of the statistical analyses are

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presented in the Supporting Information.

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RESULTS AND DISCUSSION

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Overall Spatial Assessment. The spatial distribution of PFAAs in European starling eggs

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collected across Canada is presented in Table SI7 and Figure SI2. Figure 1 summarizes the

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results for five representative PFAAs for all sampling years combined. The concentrations of

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PFAAs in starling eggs were consistently elevated at the Brantford landfill (ON). The PCA

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conducted on log-normalized concentrations (Figure 2) grouped the Brantford landfill separately

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from the other locations, with relatively high scores for both factor 1 and factor 2, which were

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generally associated with perfluorinated carboxylic acids (PFCAs) and perfluoroalkyl sulfonic

173

acids (PFSAs), respectively. Interestingly, other than the Brantford landfill, the PCA conducted

174

on log-normalized concentrations (Figure 2) grouped locations within each urban center,

175

indicating spatially distinct sources.

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The results of the LMEM showed that the optimal/most parsimonious model contained the

177

interaction term for urban center and location type for all PFAAs (see Supporting Information for

178

detailed information on model selection including AIC values and results of likelihood ratio

179

tests). The random factor of year was included in the optimal/most parsimonious model, which

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explained between 1.3 and 36 % of the total variation in the model (see Supporting Information


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for presentation of results). The simple main effects ANOVAs within urban center with location

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as a fixed factor showed that PFSA concentrations were generally greater at industrial location

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types and both PFSAs and PFCAs were generally greater at landfills compared to rural location

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types, especially in Vancouver, Calgary, and Halifax, although the specific patterns varied

185

between urban center. A detailed description of PFAA concentrations within each urban center

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and discussion of composition patterns of PFAAs are presented in the Supporting Information.

187

Groffen et al.13 recently compiled data from previous studies (including their own) that

188

evaluated PFAA concentrations in passerine birds. PFAA concentrations observed in the present

189

starling eggs from the Brantford landfill were higher than any previously reported levels in

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passerine birds except for eggs of great tits (Parus major) collected near a fluorochemical plant

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in Flanders, Belgium in 2011.13 The median PFOS concentration of 10,380 ng/g found in eggs

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of great tits near this fluorochemical plant was among the highest ever recorded in bird eggs

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(including aquatic and terrestrial) and almost an order of magnitude greater than the present

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Brantford landfill starling eggs (median across all years = 1,018 ng/g). The median PFHxS

195

concentration of 99.3 ng/g in the same great tit eggs was also approximately an order of

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magnitude greater than in starling eggs at the Brantford landfill (median across all years = 7.8

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ng/g). However, the median PFDS and PFOA concentrations were comparable between the two

198

studies. Concentrations of the other longer-chain PFCAs at the fluorochemical plant were less

199

than at the Brantford landfill and comparable to those observed at the other landfill and industrial

200

location types in the current study.

201

fluorochemical plant was owned by the 3M Company, and likely produced PFOS, PFHxS,

202

PFOA, PFDS and related precursors, prior to their phase-outs.3,43,44 In comparison, emissions

203

from landfills are impacted by domestic, commercial, and industrial products.45 The PFAA

This result is likely explained by the fact that the


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concentrations in starling eggs at other locations in this study fell within the range of previously

205

observed levels.13

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Significant differences in log-transformed PFAA concentrations were observed among

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sampling years for most locations/chemicals (ANOVA, 0.0017 ≤ F ≤ 549; n = 6 to 41, p-values

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range from less than 0.001 to 0.99; see Supporting Information for specific values and degrees of

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freedom of F-statistic). Despite these time-differences, the overall spatial trends were consistent

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between years (Figure SI2). The use of PFOS and PFOA and related precursors have been

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phased-out and regulated beginning in 2000 and 2006, respectively. However, significant

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increasing or decreasing trends between the 2009 and 2014 time period were observed for some

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chemicals/locations but not others (log-linear regression, 0.001 ≤ p ≤ 0.99; 0.07 ≤ r2 ≤ 0.99 - see

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Supporting Information for exact values and additional information). More than five years of

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data are typically required to detect the changes in PFAA concentrations observed in the

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environment.36,46 Continued monitoring of PFAAs in starling eggs is required to achieve a

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database capable of detecting long-term temporal trends.

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Influence of Human Population. For PFHxS, PFOS, and PFDS, when south of Indus (AB)

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was qualitatively excluded as an outlier following review of Figure 3 and Figure SI4,47,48 there

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was a significant (p < 0.05) correlation between median starling egg concentration and human

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population (see Supporting Information for specific results). The median PFHxS, PFOS, and

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PFDS concentrations in starling eggs collected from south of Indus were relatively high (2.69,

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162, and 27 ng/g, respectively) compared to the assumed population for Indus of 45 as reported

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by Statistics Canada49 in the 2011 census. However, as discussed in the Supporting Information,

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the starling eggs collected from south of Indus had PFAA concentrations that were comparable

226

to the industrial and landfill location types in Calgary, which has a much greater population of


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1,096,833 (Table SI5).49 The south of Indus location is 10 km east of Calgary, which is within

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the home range of the starlings.50 Furthermore, the prevailing wind direction in this area is west

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to east which could lead to atmospheric transport of PFAAs (either from their precursors in the

230

gas phase or PFAAs on particles) from Calgary to south of Indus.50,51 However, in our previous

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study,25 the range of the sum of polybrominated diphenyl ether (ΣPBDE) concentrations (20 ng/g

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to 95 ng/g) determined in 15 pooled starling eggs collected from south of Indus in

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2009/2010/2011 was lower than in five pooled starling eggs collected from Calgary (95 ng/g to

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135 ng/g). Given that PBDEs are also influenced by non-point sources associated with human

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population,25 the elevated PFHxS, PFOS and PFDS in starling eggs collected from south of Indus

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were not likely due to sources originating from Calgary as this would have a similar influence on

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both classes of chemicals. It should be noted that south of Indus is an agricultural area southeast

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of a small airport. However, to our knowledge, there have been no fire training activities or

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accidents at this airport that could have released PFOS-containing aqueous film-forming foam

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(AFFF) to the environment.13,52,53 Therefore, our results suggest that starling eggs from south of

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Indus are influenced by an unidentified point source and this requires further study.

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The r-value for the correlation between population size and concentrations of PFHxS (0.55),

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PFOS (0.64), and PFDS (0.62) in starling eggs, even with the exclusion of south of Indus, may

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be influenced by the fact that PFSA emissions are not always connected to the assumed

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population of a given location (see Supporting Information for specific results). For example,

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although St. George (ON) has a relatively small population of 3,124,49 this town is located in

247

highly urbanized southern Ontario that is 10 km from Hamilton. In addition, due to lack of

248

information, the populations of Oakfield and Graves Island Provincial Parks (NS) of 3,892 and

249

10,599, respectively, were estimated from Enfield and Chester, which are located 5 km and 3 km


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away, respectively. However, it is likely that emissions of PFHxS, PFOS, and PFDS to the

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environment in these Provincial Parks are over-estimated by their assumed population. As

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discussed in the Supporting Information, PFAA concentrations were comparable across the

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Montreal urban center, which also weakened the PFHxS/PFOS/PFDS relationship with

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population. The fact that a significant correlation was found between population size and

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concentrations of PFHxS, PFOS, and PFDS (0.55 ≤ r ≤ 0.64; p < 0.05; see Supporting

256

Information for specific results), despite these potential outliers that were not considered in the

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analysis, provides strong evidence of human population being a substantial factor influencing the

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extent of PFHxS, PFOS, and PFDS released to the terrestrial environment. Human population

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was also found to influence PBDE concentrations in starling eggs collected between 2009 and

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2011 at the same locations as this study.25 In addition, the spatial distribution of PFOS in air,

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water, sediment, fish, and birds across Canada between 2006 and 2011 was generally related to

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urbanization.54 Route et al.55 also found elevated PFOS and PFDS in blood plasma of bald eagle

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(Haliaeetus leucocephalus) nestlings collected near urban compared to remote locations, which

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they attributed to effluent from municipal wastewater systems and industrial waste. Although

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regulatory action and phase-outs for PFOS and its precursors began in 2000 in North America,

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ongoing releases from consumer products likely continue to be sources to the environment.17,56,57

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Less is known about PFHxS and PFDS compared to PFOS. However, PFHxS and PFDS are

268

commercially relevant, have been found in PFOS formulations as impurities, and were included

269

in the 2000-2002 voluntary phase-out by the 3M Company.3,44,58

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In contrast to PFSAs, the correlation between population size and concentrations of all PFCAs

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(-0.051 ≤ r ≤ 0.42; p > 0.05), except PFDA (r = 0.58, p = 0.03) in starling eggs was not

272

significant with or without including south of Indus in the regression (see Supporting


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Information for specific results). These results are surprising given that PFCAs, like PFOS and

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PFDS, also continue to be present in commercial products,16,56,57 which are likely sources to the

275

environment. However, they are consistent with PFAA trends reported in our previous studies

276

on Canadian air, surface water, sediment, top predator fish, and gull (Larid) eggs.36,54 We

277

hypothesize that atmospheric transport and degradation of precursor chemicals, such as

278

fluorotelomer alcohols (FTOHs), are influencing the spatial trends of PFCAs in the Canadian

279

terrestrial environment. FTOHs are released from commercial products57,59-61 and are commonly

280

detected in ambient air.19,62,63 FTOHs are degraded atmospherically and biologically64-66 to

281

PFCAs and are sufficiently volatile and persistent in the atmosphere to reach remote locations

282

from source regions in a period of days to weeks.67,68

283

Influence of Landfills. In our previous complementary study, ANOVA revealed significant

284

differences in ΣPBDE concentrations between location types in starling eggs collected from the

285

same locations as this study (F3,44 = 7.4, p < 0.001).25 Scheffe’s post hoc analysis further

286

indicated that eggs collected from landfills contained significantly greater (p < 0.001) ΣPBDE

287

concentrations than those from other location types.25 In a second complementary study, median

288

volatile methylsiloxane concentrations in starling eggs collected from the same locations as this

289

study were one to two orders of magnitude greater at landfills compared to other location types.69

290

The impact of landfills on PFAAs detected in starling eggs was not as clear as for PBDEs and

291

volatile methylsiloxanes. For example, the concentrations of PFAAs in starling eggs were

292

consistently elevated at the Brantford landfill compared to all other locations, as illustrated by

293

the results of the PCA (Figure 2; also see discussion on PFAA concentrations within each urban

294

center in the Supporting Information). The PCA also grouped the Delta landfill (BC) and Otter

295

Lake Waste Facility (NS) separately from other land use types, illustrating that they were sources


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of PFSAs/PFCAs (Delta landfill) or PFCAs only (Otter Lake Waste Facility) to the terrestrial

297

environment. However, PFAA concentrations and patterns in pooled starling egg samples from

298

the Calgary (AB), Halton (ON), and Stoney Creek (ON) landfills were comparable to those

299

measured in industrial areas. In addition, PFAAs in starlings from the Lachenaie landfill (QC)

300

were similar to those measured at other land use types in the Montreal urban center.

301

The source of PFAAs emitted from landfills is likely from disposed commercial products

302

containing PFAAs and/or their precursors.18 The PFAAs and/or precursors at landfill locations

303

are released to the atmosphere,19,23 which may be subsequently deposited and bioaccumulated in

304

starlings. PFAAs can also leach from solid waste particles into open air.23 Biotransport from the

305

landfills may influence contaminant concentrations in starling eggs since the organic material in

306

landfills could attract a variety of organisms seeking food25,70 which could then be consumed by

307

starlings. Chen et al.25 found that PBDE concentrations in starling eggs collected at the landfills

308

were correlated with the quantity of waste received. However, PFAA concentrations in the

309

starling eggs and the rate at which landfills are filled were not correlated (-0.59 ≤ r ≤ -0.27; p >

310

0.05; see Supporting Information for specific results) for any of the PFAAs (Figure 4, Figure

311

SI5, Table SI6), which is similar to what was observed for volatile methylsiloxanes.69 PFAA

312

concentrations in air and leachate samples were also highly variable between landfills.19,21,23,45,54

313

Therefore, the variability observed in starling eggs collected at landfills is not surprising and may

314

depend on the specific composition of waste objects received and/or the years since the waste

315

was added to the landfill.45

316

methylsiloxanes in starling eggs collected at the Brantford landfill were either comparable or less

317

than at the other landfills.25,69 This suggests that the sources of PFAAs to the Brantford landfill

318

did not contain similarly elevated levels of flame retardants and volatile methylsiloxanes.

Interestingly, concentrations of flame retardants and volatile


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Furthermore, factors such as the size of the active dumping area, presence of engineering

320

features within the landfill (e.g., liner or cover material), and/or local climate conditions are not

321

likely responsible for the relatively elevated PFAA concentrations observed at the Brantford

322

landfill since these factors would have an effect on PFAAs and at least some flame retardants

323

and/or volatile methylsiloxanes (depending on their physical-chemical properties).

324

Toxicological Considerations. PFOS concentrations in the starling eggs were below the Draft

325

(Canadian) Federal Environmental Quality Guideline (FEQG) of 1900 ng/g developed by ECCC

326

at all locations except for the Brantford landfill (Figure 1). At the Brantford landfill, there was

327

one sample (analyzed in 2010) that contained a PFOS concentration of 1998 ng/g, which is

328

marginally above the FEQG. However, a field-based study on tree swallows reported decreased

329

hatching success at a PFOS concentration as low as 150 ng/g in eggs.71 This level was exceeded

330

in 17 % of the starling egg samples, particularly those collected at industrial and landfill location

331

types. There is less toxicological information available for PFAAs other than PFOS. However,

332

O'Brien et al.72 determined a no observed adverse effect level of 10,000 ng/g for PFUnDA and

333

PFDS for pipping success in chicken eggs, which was not exceeded in any of the starling eggs.

334

Implications. In this first evaluation, to our knowledge, of PFAA concentrations in terrestrial

335

biota on a continental scale, we found that non-point sources associated with human population

336

influence the concentrations of PFSAs and landfills influence the concentrations of PFSAs

337

and/or PFCAs in the terrestrial environment. However, the relative importance of these two

338

sources varies between location and chemical. The difference in the relative contribution of

339

landfills to the PFAA concentrations found in the terrestrial environment was not correlated with

340

landfill fill rate, similar to what was observed for volatile methylsiloxanes but not PBDEs,25,69

341

and likely relates to the specific composition of waste objects received and/or the years since the


17


Page 18 of 35

342

waste was added to the landfill. We predict that the relative importance of landfills as a source

343

of PFAAs to the terrestrial environment will increase as in-use consumer products reach the end

344

of their lifetime and are disposed of in landfills.45,73

345

For non-landfill locations, our study found that sources of PFSAs and PFCAs to the terrestrial

346

environment differ. PFHxS, PFOS, and PFDS concentrations in starling eggs collected from

347

non-landfill locations were positively correlated with human population. Despite the 2000-2002

348

phase-out of PFOS and its precursors, ongoing losses from consumer products likely continue to

349

be major sources to the environment and impact concentrations in populated regions.

350

comparison, concentrations of most PFCAs in starling eggs were not related to population,

351

indicating that atmospheric transport and degradation of precursor chemicals are influencing the

352

spatial trends of PFCAs in terrestrial wildlife.

In

353

PFOS concentrations in starling eggs collected from some of the landfills and industrial areas

354

exceeded concentrations that are associated with decreased hatching success. Continued long-

355

term monitoring is recommended in order to achieve a dataset with sufficient power to track the

356

impact of voluntary and regulatory measures on PFAA concentrations observed in the terrestrial

357

environment, particularly in urban areas and by landfill locations.


18

Page 19 of 35


358

ASSOCIATED CONTENT

359

Supporting Information.

360

The Supporting Information is available free of charge on the ACS Publications website at DOI:

361

Additional analytical details, technical details on the application and selection of the optimal

362

LMEM, discussion on PFAAs within each urban center, compositional patterns of PFAAs, time

363

trends, correlation between PFAAs and population and landfill fill rate, tabulation of locations,

364

PFAAs examined in this study, MLODs and MLOQs, estimated human population for non-

365

landfill location types, fill rates for landfills, summary statistics of PFAA concentrations,

366

locations of the five urban centers, box and whisker plots, compositional profiles of PFAAs,

367

PFAA concentrations versus human population and landfill fill rate.

368

AUTHOR INFORMATION

369

Corresponding Authors

370

*(P.M.) Phone: 905-336-4879; email: [email protected]

371

*(R.J.L) Phone: 613-998-6696; email: [email protected]

372

Notes

373

The authors declare no competing financial interest.

374 375

ACKNOWLEDGMENT

376

This study was financially supported by the Chemicals Management Plan (CMP; ECCC) (to

377

P.A.M). ECCC staff and all those involved in egg collections and processing are thanked,

378

especially Sandi Lee, Glenn Barrett, Kimberly O’Hare and Kyna Intini of Ecotoxicology and


19


Page 20 of 35

379

Wildlife Health Division of ECCC. Other field partners include Dr. Pauline Brousseau and

380

students from INRS – Institut Armand Frappier (Laval, QC), Dr. Colleen Barber and students of

381

St. Mary’s University (Halifax, NS), and Rob Wapple of Kingbird Consulting (Medicine Hat,

382

AB). Shane de Solla of ECCC is thanked for statistical advice. We thank Kimberley Hughes

383

(on contract to ECCC) for data management as well as David Blair in the OCRL /Letcher Group

384

and François Cyr in Lab Services at the NWRC for PFAA analysis.


20

Page 21 of 35


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O'Brien, J. M.; Crump, D.; Mundy, L. J.; Chu, S.; McLaren, K. K.; Vongphachan, V.; Letcher, R. J.; Kennedy, S. W. Pipping success and liver mRNA expression in chicken


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embryos exposed in ovo to C8 and C11 perfluorinated carboxylic acids and C10

610

perfluorinated sulfonate. Toxicol. Lett. 2009, 190 (2), 134-139.

611

(73)

Wang, Z.; Boucher, J. M.; Scheringer, M.; Cousins, I. T.; Hungerbuhler, K. Toward a

612

comprehensive global emission inventory of C4-C10 perfluoroalkanesulfonic acids

613

(PFSAs) and related precursors: focus on the life cycle of C8-based products and ongoing

614

industrial transition. Environ. Sci. Technol. 2017, 51 (8), 4482-4493.

615 616 617


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10000 1000

619

100

PFOS

10

620

1 0.1 1000

621

100

PFDS

1

623 624 625 626

PFNA

627 628 629

PFDoDA

630

633

0.1 0.01 1000 100 10 1 0.1 0.01 1000 100 10 1 0.1 0.01 1000

631 632

10

Concentration (ng/g wet weight)

622

100

PFTeDA

10 1

638 639 640 641 642 643 644 645 646 647

British Columbia Landfill

Alberta Industrial

Ontario 10 km from urban center

Quebec 40 km from urban center

Otter Lk Landfill Dartmouth Refinery Oakfield Park Graves Is. Park

637

Lachenaie Landfill Parc-Nature Repentigny Lanoraie

636

Brantford Landfill Halton Landfill Stoney Creek Landfill Hamilton St. George Delhi

635

0.01

Calgary Landfill Calgary Industrial South of Indus South of Strathmore Redcliff

634

Delta Landfill Abbotsford Langley

0.1

Nova Scotia

Remote (Alberta only)

Figure 1. Box and whisker plots of the concentrations (ng/g wet weight) of five representative PFAAs (PFOS, PFDS, PFNA, PFDoDA, and PFTeDA) in European starling eggs collected across Canada in 2009-2012 and 2014. The line within the boxes indicates median, the boxes indicate 25th and 75th percentiles, the whiskers (error bars) below and above the boxes indicate 10th and 90th percentiles, and the closed circles indicate outliers. The method limits of quantification for 2009 to 2012 data are shown as solid blue lines and for 2014 as dash blue lines. For PFOS, the Draft (Canadian) Federal Environmental Quality Guideline (FEQG) for bird eggs of 1900 ng/g is displayed as a dashed brown line.


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648 649 650

652 653 654 655 656 657 658 659 660 661 662 663 664 665 666 667 668

b) Factor Scores

1.0

PCA – axis 2 (39%)

651

a) Factor Loadings PFHxS PFDS

0.8

2.0

PFOS

CLf CInd C10

PFTeDA

0.6

HLf1

1.0

PFDoA

VLf HxInd

PFDA PFTrDA

0.4

PFOA PFUnDA

0.0 C40 Rem V40

0.2 PFNA

0.0 0.0

0.4

0.8

-1.0 1.2

VInd

-2.0

Hx10

HInd HLf2 M10 HLf3 MLf MInd M40

HxLf

H40 H10 Hx40

0.0

2.0

PCA – axis 1 (48%) Vancouver, BC Calgary, AB Hamilton, ON Montreal, QC Halifax, NS VLf – Vancouver landfill (BC); VInd – Abbotsford (BC); V40 – Langley (BC) CLf – Calgary landfill (AB); CInd – Calgary (AB); C10 – South of Indus (AB); C40 - South of Strathmore (AB); REM – Redcliff (AB) HLf1– Brantford landfill (ON); HLf2 – Halton landfill (ON); HLf3 – Stoney Creek landfill (ON); HInd – Hamilton (ON); H10 - St. George (ON); H40 - Delhi (ON) MLf – Lachenaie landfill (QC); MInd – Parc-Nature (QC); M10 – Repentigny (QC); M40 – Lanoraie (QC) HxLf – Otter Lake Waste Facility (NS); HxInd – Dartmouth Refinery (NS); ); Hx10 – Oakfield Provincial Park (NS); Hx40 – Graves Island Provincial Park (NS)

Figure 2. PCA (a) factor loadings and (b) mean factor scores for factor 1 and factor 2 conducted on log-normalized PFAA concentrations in European starling eggs collected across Canada in 2009-2012 and 2014. Location types are defined in Table SI1. This figure illustrates that locations within urban centers often (but not always) group together with similar factor scores.

669


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670 671 10000

672

674 675 676 677 678 679 680 681 682 683 684 685 686 687 688

(b) PFDS

r = 0.548, p = 0.043


673

1000

(a) PFOS

r = 0.643, p = 0.013

1000

100

CInd

C10 (outlier) HxInd

10

100 M40 Hx40

H10

10

H40

H10

Hx40

H40

MInd HInd

V40

V40

0.1

1

104

M10

M40

1

VInd

0.1 101103

CInd HxInd

HInd MInd

M10

C40

Hx10 Rem

100

C10 (outlier) Hx10

105

106

107

(c) PFOA

0.01 101103 100

r = 0.207, p = 0.458

Rem

C40

VInd

104

105

106

107

(d) PFUnDA r = 0.173, p = 0.537

Hx10 CInd

10

HxInd C10

H10 M40 Hx40

10

CInd

M10

C10

M40

Hx40

M10 HxInd

H40 H10

1

1

MInd HInd

Hx10

MInd V40

0.1

H40

Rem

C40 V40

VInd

HInd

0.1 Rem

0.01 101103

104

105

106

107

0.01 101103

VInd

C40

104

105

106

107

Human Population Vancouver, BC

Calgary, AB

Montreal, QC

Hamilton, ON

Halifax, NS

VInd – Abbotsford (BC); V40 – Langley (BC) CInd – Calgary (AB); C10 – South of Indus (AB); C40 - South of Strathmore (AB); REM – Redcliff (AB) HInd – Hamilton (ON); H10 - St. George (ON); H40 - Delhi (ON) MInd – Parc-Nature (QC); M10 – Repentigny (QC); M40 – Lanoraie (QC) HxInd – Dartmouth Refinery (NS); ); Hx10 – Oakfield Provincial Park (NS); Hx40 – Graves Island Provincial Park (NS)

689 690 691 692 693 694 695 696 697 698 699

Figure 3. Correlation between median (a) PFOS, (b) PFDS, (c) PFOA, and (d) PFUnDA concentrations in European starling eggs (ng/g wet weight) and human population. The starlings were collected from industrial (Ind), rural locations located 10 km and 40 km away from major urban centers, and a remote (REM) location. The results are shown for eggs collected in 20092012 and 2014 combined. The error bars represent the minimum and maximum values. The method limits of quantification are displayed as dashed (2014) and solid (2009 to 2012) lines. PFDS and PFOA were not detected in eggs collected from Oakfield Provincial Park (NS) and the population of this location is indicated with an "×". Location types are defined in Table SI1. For PFOS and PFDS, an outlier (south of Indus, Alberta; median concentrations = 162 and 27 ng/g wet weight, respectively; population = 45) was excluded from the correlation analysis.

700


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10000

1000

PFOS

1000


701 702 703 704 705 706 707 708 709 710 711 712 713 714 715 716 717 718 719 720 721 722 723 724 725 726 727 728 729 730 731 732 733


PFDS

100

100

10

10 1

1

0.1

0.1 0.01

0.01 0.0

1000

2.0e+5 4.0e+5 6.0e+5 8.0e+5 1.0e+6 1.2e+6 1.4e+6

0.0

1000

PFOA

100

100

10

10

1

1

0.1

0.1

0.01

2.0e+5 4.0e+5 6.0e+5 8.0e+5 1.0e+6 1.2e+6 1.4e+6

PFUnDA

0.01 0.0

2.0e+5 4.0e+5 6.0e+5 8.0e+5 1.0e+6 1.2e+6 1.4e+6

0.0

2.0e+5 4.0e+5 6.0e+5 8.0e+5 1.0e+6 1.2e+6 1.4e+6

Fill Rate (tonnes/year) Vancouver, BC

Calgary, AB

Montreal, QC

Hamilton, ON

Halifax, NS

Figure 4. Median (a) PFOS, (b) PFDS, (c) PFOA, and (d) PFUnDA concentrations in European starling eggs (ng/g wet weight) collected from landfill locations across Canada versus landfill fill rate (tonnes/year). The results are shown for eggs collected in 2009-2012 and 2014 combined. The error bars represent the minimum and maximum values. The method limits of quantification are displayed as dashed (2014) and solid (2009 to 2012) lines.


35

Perfluoroalkyl Acids in European Starling Eggs Indicate Landfill and

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