Methylmercury and total mercury content in soft tissues of two bird species wintering in the Baltic Sea near Gdansk, Poland

Accepted Manuscript Methylmercury and total mercury content in soft tissues of two bird species wintering in the Baltic Sea near Gdansk, Poland

Małgorzata Rutkowska, Gabriela Bajger-Nowak, Diana Kowalewska, Szymon Bzoma, Elżbieta Kalisińska, Jacek Namieśnik, Piotr Konieczka PII:

S0045-6535(18)32270-7

DOI:

10.1016/j.chemosphere.2018.11.162

Reference:

CHEM 22646

To appear in:

Chemosphere

Received Date:

28 June 2018

Accepted Date:

25 November 2018

Please cite this article as: Małgorzata Rutkowska, Gabriela Bajger-Nowak, Diana Kowalewska, Szymon Bzoma, Elżbieta Kalisińska, Jacek Namieśnik, Piotr Konieczka, Methylmercury and total mercury content in soft tissues of two bird species wintering in the Baltic Sea near Gdansk, Poland, Chemosphere (2018), doi: 10.1016/j.chemosphere.2018.11.162

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ACCEPTED MANUSCRIPT 1

Methylmercury and total mercury content in soft

2

tissues of two bird species wintering in the Baltic Sea

3

near Gdansk, Poland

4

Małgorzata Rutkowska1*, Gabriela Bajger-Nowak1, Diana Kowalewska1, Szymon Bzoma2,

5

Elżbieta Kalisińska3, Jacek Namieśnik1, Piotr Konieczka1

6

1

7 8

Gdańsk, 11/12 G. Narutowicza Street, Poland; e-mail: [email protected]; 2

9 10 11

Gdańsk University of Technology, Faculty of Chemistry, Department of Analytical Chemistry, 80-233

Waterbird Research Group KULING, 81-526 Gdynia, 34/7 Świerkowa Street, Poland; e-mail: [email protected];

3

Pomeranian Medical University, Department of Biology and Medical Parasitology, 70-411 Szczecin, Poland, 72 Powstancow Wielkopolskich Street, Poland; e-mail: [email protected];

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* Corresponding author: [email protected]; telephone number: +48 58 347 16 01

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Abstract: Of the various forms of Hg occurring in nature, (mono) methylmercury (MeHg) is an

14

especially toxic form and practically all forms of Hg can be converted into MeHg as a result of

15

natural processes. Total mercury (THg) and MeHg were determined in tissues of two piscivorous

16

birds: razorbill Alca torda and black-throated loon Gavia arctica to provide baseline data on current

17

mercury concentrations for liver, kidneys and pectoral muscle mercury concentrations of birds

18

which winter on the south Baltic Sea coast. Intra and inter-specific comparisons were carried out.

19

The study is conducted between winter and autumn and the distributions of mercury in tissues

20

were compared with data in other studies. The following paper contains discussion of the results

21

based on the statistical analysis and ecology aspect. The highest average Hg content was in the liver

22

(loon ≈ 3.86 mg kg-1 dw; razorbill ≈ 1.57 mg kg-1 dw), then in the kidneys (loon ≈ 3.14 mg kg-1 dw;

23

razorbill ≈ 1.53 mg kg-1 dw) and the lowest concentrations were in pectoral muscles (loon ≈ 1.97 mg

24

kg-1 dw; razorbill ≈ 0.67 mg kg-1 dw).

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Keywords: Mercury; methylmercury; birds; liver; kidney; pectoral muscle. 1

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1. Introduction

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Mercury (Hg) is one of the priority hazardous contaminants in the world (Jackson, 1998;

29

Stenhouse et al., 2018) and it can enter the environment naturally and as a result of human activities.

30

Anthropogenic emissions of Hg include fossil fuels combustion, gold mining, the roasting of sulfide

31

ores, the production of paper and drugs, the chloralkali process, and agriculture whereas natural

32

releases are mainly due to volcanoes (Horowitz et al., 2014; Rutkowska et al., 2014; Valdersnes et al.,

33

2016). Mercury is mainly present in gaseous form in the atmosphere.

34

exclusively of the element Hg with a global residence time in the atmosphere of about 6-24 months.

35

As a result, this Hg species can be transported over long distances in the atmosphere, and the

36

atmosphere is the main route for its introduction into the marine environment (Lamborg et al., 2014;

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Mason et al., 1994; Schroeder et al., 1998). When Hg is introduced in the environment, especially

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aquatic ecosystems, it can be biologically transformed by various methylating microbes into

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methylmercury (MeHg) (Camacho et al., 2015; Valdersnes et al., 2016). MeHg is a dangerous

40

neurotoxin; it can be absorbed by organisms and biomagnify up the food chain (Fox et al., 2017). Hg

41

and MeHg contaminations are not only a problem to aquatic ecosystems but also to land animals

42

occupying higher trophic levels (Fu et al., 2010). Semi-aquatic mammals and piscivorous birds

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accumulate MeHg from their diet due to the consumption of fish and other aquatic biota (Ackerman

44

et al., 2016; Åkerblom et al., 2014; Depew et al., 2013; Eagles-Smith et al., 2016; Houserová et al., 2007;

45

Sullivan and Kopec, 2018; Whitney and Cristol, 2017). High levels of Hg compounds in avian tissues

46

can affect immune, cardiovascular and nervous systems, as well as reproductive capacity (Eagles-

47

Smith et al., 2018, 2016; Fu et al., 2010; Harada, 1995; Morel et al., 1998; Tan et al., 2009; Tartu et al.,

48

2013). Also MeHg is able to cross the blood–brain barrier and can be deposited in eggs (Boening, 2000;

49

Frederick and Jayasena, 2011). That is why marine and other aquatic birds are particularly valuable

50

and effective monitoring tools for assessing contamination of the marine environment (Hothem et

This state includes almost

2

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al., 1998; Kalisińska et al., 2010). Additional, studying marine bird ecology should serve as a proxy

52

and a harbinger of changes in marine ecosystems (Mallory et al., 2006).

53

At present, a number of different analytical methods are used to determine Hg and MeHg in

54

samples with a complex matrix composition. The determination of THg is carried out the vapour

55

generation technique coupled to atomic absorption spectrometry (CV-AAS) (Gonzalvez et al., 2010,

56

2009; Ruelas-Inzunza et al., 2009; Vieira et al., 2009), fluorescence spectrometry (CV-AFS) (Wang et

57

al., 2017). The speciation of mercury is usually carried out by high-performance liquid

58

chromatography (HPLC) (Jagtap et al., 2011; Zhu et al., 2017) and gas chromatography (GC) (Gorecki

59

et al., 2013) coupled with element selective (atomic fluorescence, atomic absorption, atomic emission)

60

and mass spectrometric

61

et al., 2007, 2006; Jagtap et al., 2011; Rodil et al., 2002; Zhu et al., 2017).

detection

technique (Ferreira et al., 2015; Gorecki et al., 2013; Houserová

62

This work reports the concentrations of THg and MeHg in three different tissues (pectoral

63

muscle, liver and kidney), in two seasons (winter and autumn) of two bird species: razorbill (Alca

64

torda) and black-throathed loon (Gavia arctica), both are predominantly fed with fish and both

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wintering in the south part of the Baltic Sea (the Gulf of Gdansk). The razorbill is an Alcidae seabird

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species that breeds in high latitudes and black-throated loon is a migratory aquatic bird living in the

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northern hemisphere, mainly breeding in freshwater lakes in northern part of Europe and Asia. The

68

Baltic Sea is one of the most polluted seas.

69

sides by land (only a few shallow straits link to the North Sea), which poses a high risk to the marine

70

environment due to pollution by toxic compounds. Seabirds are often used as biomonitors of marine

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ecosystem health and have frequently been used to monitor Hg in marine environments via internal

72

tissues (Espín et al., 2012; Monteiro and Furness, 1995). These species are considered as indicators of

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marine ecosystem pollution because they are large, wide-ranging, abundant, long-lived, and easy to

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observe and monitor. In addition, they are of public interest and often at the top of the food chain

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(Burger and Gochfeld, 2004; Espín et al., 2012). As many seabird species return to the same nesting

It is an inland sea of northern Europe, surrounded on all

3

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and colony sites each year and travel long distances to feed, they accumulate contaminants over time

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and space (Burger, 1993; Espín et al., 2012; ).

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2. Materials and methods

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2.1. Sampling site description

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The Gulf of Gdansk (area - 4940 km2) lies in the southern part of the Baltic Sea. The Gulf is

81

partially enclosed, being bordered by the Hel Peninsula and by continental Poland. The three cities

82

of Gdynia, Sopot and Gdansk discharge wastewaters into the gulf and are the three main outlets of

83

the Vistula River, which drains most of Poland, including the major industrial regions and cities. Not

84

surprisingly, the Gulf is considered to be polluted by heavy metals including Hg and its compounds

85

(Glasby and Szefer, 1998; Szefer et al., 2002, 1998, 1990) .

86

2.2. Sample collection and pretreatment

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The examined birds were found in the Baltic Sea water bodies: Gulf of Gdansk and Coastal Zone

88

(Fig. 1). Birds were drowned in fish-nets as a bycatch. There were two bird species: razorbill (n = 37),

89

and black-throated loon (n = 13), which in majority had drowned in fishing nets. Birds were examined

90

in terms Hg content and had been collected from year 2006 up to 2011. Every examined bird had

91

determined gender, age, place and date of finding, and species identification. Some birds were too

92

young to determine their gender, because the gonads were not fully developed. It is also extremely

93

difficult to define the exact bird age. For this study the age of the razorbills was determined by the

94

bow's characteristics and of loons by the characteristics of the feathers based on the available

95

identification keys. In case of the bird species which are objects of our interest, it is possible to divide

96

them into two age groups: juvenile and adult. Before reaching the laboratory, tissue parts were

97

separated through dissection using a stainless steel scalpel (which was disinfected with methanol

98

after each use), including the liver, pectoral muscle and kidney. Skeletal muscle sample was cut out

99

from the upper right part of the pectoral muscle. Kidney sample was cut out from the right kidney. 4

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All tissue samples were weighed (wet mass), placed in Zip-Lock bags and immediately frozen for

101

later analysis.

102

Figure 1. Area of the Baltic Sea where razorbill and black-throated loon were gathered (the size of

103

the dots are related to the number of samples taken in that specific point).

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After being transported to the laboratory, the bird tissues were freeze-dried at -51 °C/0.027

105

mbar/48 h (LABCONCO with a 6 L capacity, USA). Lyophilised samples were weighed (dry mass)

106

on the analytical balance and homogenised in the agate mortar. After preparation, the powdered

107

samples were sealed in polyethylene bags and stored in a -20 °C refrigerator for further analysis.

108

2.3. Reagents and standards

109

All the used reagents were of analytical-reagent grade unless otherwise stated. The solutions

110

were prepared using ultra-pure water Milli-Q. Hg standard-MSHG at a concentration 100.48 ± 0.22

111

µg mL-1 in 3.3% HCl was purchased from Inorganic Ventures, INC (USA). Certified reference material

112

BCR-463 -Tuna fish (MeHg - 3.04 ± 0.16 µg g-1; Hg -2.85 ± 0.16 µg g-1) was obtained from

113

IRMM (Geel, Belgium) and Certified reference material DOLT – 4 - Dogfish liver (MeHg as Hg - 1.33

114

± 0.12 mg kg-1; Hg - total element mass fraction -

115

National Research Council of Canada. L-Cysteine (98%), Buffer Solution Standard (Phosphate pH

116

Standard Equimolar Solution) pH 6.86 (25 °C) and additive B (activated alumina) were obtained from

117

Nacalai Tesque, Inc, Kyoto and Wako pure Chemical Industries, Ltd (Japan). Additive M (sodium

118

carbonate + calcium hydroxide) and buffer solution of pH 7.00 ± 0.05 were purchased from POCh

119

(Poland). Toluene and HBr were obtained from Sigma Aldrich, MO (USA).

120

2.4. Sample preparation for MeHg determination

121

2.58 ± 0.22 mg kg-1) was purchased from the

MeHg in bird tissues was extracted following the method described by Maggi et al. (Maggi et

122

al., 2009) with a few modifications. Approximately 250 mg of homogenized dried

123

samples were hydrolyzed with 5 mL of 48% hydrobromic acid (HBr) by shaking for 5 min. After the

124

hydrolysis process, 10 mL of toluene was added to the samples and organomercury species were

125

extracted by mixing vigorously for 20 min in a mechanical shaker. The extracts were then centrifuged

126

at 3000 rpm for 10 min. The supernatant with organomercury species was collected in a clean

127

centrifuge tube. The samples were double-extracted by repeating the previous toluene extraction

128

process with 5 mL of toluene. The combined organic extracts were double back-extracted using 3 mL

bird tissue

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of 1% (v/v) L-cysteine aqueous solution to draw out MeHg from the collected toluene. The L-cysteine

130

extracts were mixed vigorously for 20 min and centrifuged for 5 min. This process was repeated once

131

more using another 3 mL of L-cysteine. Approximately 200 µL the L-cysteine extracts was collected

132

for immediate analysis using Mercury Analyser (MA-2000) purchased from Nippon Instruments

133

Corporation (Japan).

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2.5. Determination procedure

135

The analyses were carried out with a Mercury Analyser (MA 2000) using cold vapour atomic

136

absorption spectrometry technique (CV-AAS). The extracts and freeze-dried samples (liquid sample

137

for MeHg analysis and solid sample for THg determination, n=3) are thermally decomposed by

138

controlled heating (T=850˚C/4 min). Hg is further atomized and free Hg vapour is collected by a Hg

139

collection agent in the form of gold amalgam. Hg collection agent is heated to release atomic Hg

140

(T=600˚C/1 min). The released Hg is detected using cold atomic absorption method at a wavelength

141

of 253.7 nm in the detector’s absorption cell. As a method of removing part of substances that could

142

interfere with measurement, Nippon Instruments Corporation uses two kinds of additives: additive

143

B (activated alumina) and additive M sodium carbonate + calcium hydroxide). They have to be used

144

in accordance with special procedure which includes the appropriate preparation of the additives

145

(heating them at 750 °C for about an hour) and an appropriate scheme for the addition of additives

146

together with a sample for porcelain boats, depending on the type of sample. The rest of interferes is

147

removed in the scrubber filled with the KOH solution. The procedure for the determination of THg

148

and MeHg is schematically shown in Figure 2.

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149 150 151

Figure 2: Scheme of the procedure for the THg and MeHg determination.

2.6. Method validation

152

The numerical values of the calibration curves regression parameters were the basis for

153

estimating the value of the limit of detection and quantification of the analytical method. The limit of

154

detection (LOD) is defined as the lowest content of the analyte that can be detected (without

155

quantitative determination) by a measuring-apparatus with a certain probability. While the limit of

156

quantification (LOQ) is the minimum amount or minimum concentration for quantification possible

157

by the system with a predetermined accuracy and precision (Konieczka and Namieśnik, 2007).

158

The limit of detection (LOD) was calculated using the equation (1):

159

𝐿𝑂𝐷 =

3.3 𝑠𝑎 𝑏

(1)

160

Sa – the standard deviation of the intercept of calibration curve

161

b – the slope of the calibration line

162

When calculating the numerical value of the LOQ were assumed dependence, described by the

163

equation (2):

164 8

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165

𝐿𝑂𝑄 = 3 ∙ 𝐿𝑂𝐷 (2)

166 167

Obtained numerical values LOD and LOQ were converted to the corresponding value of MDL

168

and MQL - the limits of detection and quantification of the analytical method, assuming that the mass

169

of the sample is 100 mg.

170

The next validation parameters were repeatability and intermediate precision. Repeatability was

171

expressed as a coefficient of variation (CV) test samples results in a single analytical cycle. The

172

intermediate precision was calculated as the coefficient of variation for all the results obtained in all

173

the analyzed samples (Konieczka and Namieśnik, 2007).

174

The trueness of the measurements for T-Hg and MeHg were accompanied by the analysis of two

175

certified reference material BCR-463 (Tuna fish muscles) and DOLT-4 (Dogfish liver). The average

176

recovery of BCR-463 for THg and MeHg were 97.1 and 88.4% respectively and the average recovery

177

of DOLT – 4 for THg and MeHg were 97.0% and 95.0% respectively . Based on the results can be seen

178

that the recovery of the analytical procedure is at a satisfactory level. Acceptable recovery for this

179

type of analysis should be in the range of 80 to 120%. Individual standard uncertainties were

180

determined using a series of test results. For this purpose, a series of results were used to calculate

181

the standard deviation (s), then the relative standard deviation (RSD) and the value of the relative

182

standard uncertainty (u) and the expanded uncertainty (U) according to the following equations:

183

184

185

186

𝑠=

∑𝑛

𝑥𝑚𝑒𝑎𝑛)

𝑛‒1

𝑅𝑆𝐷 =

𝑢=

(𝑥 𝑖 ‒

𝑖=1

𝑅𝑆𝐷 𝑛

𝑠 𝑥𝑚𝑒𝑎𝑛

2

(3)

(4)

(5)

(6)

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where: k – coverage factor (usually 2), c – average concentration of the analyte, x - single result,

188

xmean -measurement average result obtained for a given series of measurements, n - number of

189

obtained results (replicates) for a given series of measurements for a given sample. All of the

190

validation parameters are presented in Table 1 (based on Konieczka & Namieśnik (Konieczka and

191

Namieśnik, 2008)).

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Table 1. Calculated validation parameters for MeHg and THg in birds tissue samples.

Parameter

Value

Analyte 

Hg

MeHg

10 measuring points (10. 20. 31. 41. 51. 62. 72. 82. 92. 103 [ng]),

Linearity



0.999

3 repetitions, f(m) = 1.0006m* – 0.15



6 measuring points (0.10. 0.31. 0.51. 0.71. 0.91. 1.02[ ng]),



1.000

3 repetitions, f(m) = 0.9987m* + 1.1 (LOD) [ng]

0.096

LOQ [ng]

0.29

MDL [ng/g]

0.96

1.0

MQL [ng/g]

2.9

3.1

Measuring range [ng/g]

2.9 ÷ 102.5

3.1 ÷ 110.0

Repetability CV [%]

2.8

1.4

Intermediate precision CV [%]

4.7

3.9

BCR-463 (n=3)

97.1 ± 2.4

88.4 ±1.1

DOLT-4 (n=3)

97.0 ± 1.9

95.0 ± 1.0

Recovery ± Uncertainty (k=2) [%]

193

*m

= mass of the total Hg [ng]

194 195

2.7. Statistical analysis 10

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Median (Med), arithmetic mean (AM), standard deviation (SD), THg and MeHg concentrations

197

and the percentage of MeHg in THg (%MeHg) in soft tissues of razorbill and black-throated loon

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were calculated. Due to the fact that mercury tends to accumulate in the internal tissues of birds with

199

age, the division of birds into two age categories (Ad, adult - adults and Im, immature - young) was

200

taken into account in the calculations. Since the concentration distribution of mercury deviates from

201

the expected normal distribution, non-parametric

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compare the two parameters, and the Kruskal-Wallis test to compare three parameters (K - kidney, L

203

- liver, M - muscle).

tests were used: U test and Mann-Whitney test to

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Intraspecific comparisons were carried out which include:

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• age categories (Ad, Im);

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• types of biological material (K, L, M);

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• seasons: A, autumn (October - December) and W, winter (January - March).

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Interspecific comparisons were carried out which include:

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both bird species and age categories.

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3. Results and discussion

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The aim of this study was to provide baseline data on current mercury concentrations for liver,

212

kidneys and pectoral muscle Hg concentrations of birds which winter on the south Baltic Sea coast,

213

which had drowned in fishing nets, in order to assess exposure to Hg, to determine the impact of age

214

and sex of the specimens analysed. Intra and inter-specific comparisons were carried out.

215

Bioaccumulation of Hg species in the in tissues of razorbills and black-throathed loons living in the

216

vicinity of the Baltic Sea ecosystem have also been investigated. To show statistically significant

217

differences and correlations between the contents of analytes in some of the analysed tissues and bird

218

age or season when the samples were acquired, xenobiotic content statistical analysis has been used.

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3.1. Intraspecific comparisons

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Table 2 summarizes the concentrations of THg, MeHg and %MeHg in the biological samples for

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both species of birds. The mean values were calculated for juveniles, adults, and for all birds collected

222

for analysis (for some birds it was impossible to determine the age category). Water content in

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individual sample types was determined. Water content in the liver, kidneys and pectoral muscles

224

was about 70%.

225

3.2. Razorbill

226

Taking into consideration all the analyzed individuals (n = 37), it was found that both the

227

concentration of THg and MeHg was similar in the liver and kidney whereas significantly smaller in

228

pectoral muscle. Statistically significant differences in the concentration of THg and MeHg in liver vs

229

muscle and kidney vs muscle (K-W test: H=49.57, p<0.0001; H=42.91, p<0.0001, respectively) were

230

observed. Juveniles relative to adults had a significantly lower concentration of THg and MeHg in

231

kidneys and a significantly lower concentration of THg in the liver. Concentrations for both THg and

232

MeHg in muscles were similar in both age groups. Lower MeHg proportion in the liver of the adults

233

compared to younger birds can be result of demethylation of MeHg by selenium (Se) which occurs

234

over a long period of time in adults compared to young birds. These differences are influenced also

235

by variations in condition of the examined individuals, removal of a significant amount of MeHg

236

during moulting, and often different content and proportions of various forms of Hg and Se in food

237

intaken from water. Many waterbirds associated with the Se-rich environment use a different method

238

of Hg detoxification. In their tissues and organs, especially in the liver, various forms of Hg and Se

239

may form biologically inactive complexes at the end of the detoxification process (Kalisinska et al.,

240

2014). Se is considered to be a natural MeHg and inorganic Hg antagonist that potently counteracts

241

or eliminates symptoms of toxicity that would otherwise accompany high MeHg/Hg exposures

242

(Arcagni et al., 2017; Frederick and Jayasena, 2011; Ralston et al., 2007; Ralston and Raymond, 2010;

243

Yamashita et al., 2013). Interactions between Se and Hg have previously been observed in fish and

244

other aquatic biota (Arcagni et al., 2017; Ralston and Raymond, 2010).

12

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There were no significant differences in the values of %MeHg between age groups in any of the

246

tested tissues (Table 2). For the analysis in autumn, 24 individuals, and in winter 10 specimens, were

247

collected (for 3 birds the month of collection was not reported). The analyses showed that in all types

248

of samples median concentrations of THg and MeHg were significantly higher in winter than in

249

autumn (kidney: 1.444 vs 0.782 mg THg kg-1 and 1.171 vs 0.656 mg MeHg kg-1, M-W test Z=3.38,

250

p<0.001 and 3.80, p<0.0001, respectively; liver: 1.608 vs 0.852 mg THg kg-1, M-W test Z=3.55, p<0.0001

251

and Z=2.58, p<0.01 respectively; muscle: 1.608 and 0.852 mg THg kg-1, and 1.318 and 0.776 mg MeHg

252

kg-1, M-W test Z=3.86, p<0.0001 and Z=3.60, 0.0001, respectively).

13

253

Table 2. Concentrations (in mg kg-1 dw) of total mercury (THg), methylmercury (MeHg) and the percentage of MeHg in THg (%MeHg) in soft tissues of the razorbill Alca

254

torda and the black-throated loon Gavia arctica wintering on the Polish Baltic coast as well as and comparisons of THg, MeHg, %MeHg/THg between age groups (im

255

immature, ad adult, Med median, AM arithmetic mean, SD standard deviation, M-W Mann-Whitney test, NS difference non-significant) Kidney

Species

Liver

Muscle

THg

MeHg

%MeHg

THg

MeHg

%MeHg

THg

MeHg

%MeHg

n

12

12

12

12

12

12

12

12

12

Med

0.944

0.759

82.1

1.177

0.844

82.8

0.401

0.378

90.3

AM±SD

0.98±0.41

0.81±0.34

82.8±9.1

1.15±0.56

0.91±0.54

77±17

0.49±0.27

0.41±0.26

79±24

Range

0.376-1.750

0.328-1.482

70.8-99.5

0.484-2.424

0.330-2.123

28.4-96.4

0.191-1.057

0.036-0.965

16.4-97.6

n

7

7

7

7

7

7

7

7

7

Med

1.423

1.127

79.4

1.731

1.299

81.8

0.613

0.557

90.8

AM±SD

1.53±0.51

1.18±0.45

78±16

1.57±0.44

1.21±0.36

78±10

0.67±0.18

0.54±0.14

82±17

Alca torda Im

Ad

Range

0.730-2.299

0.527-2.011

49.0-99.3

0.660-1.953

0.540-1.652

57.0-85.0

0.430-0.970

0.311-0.769

51.4-98.0

Im vs Ad

M-W

Z=2.155

Z=1.986

NS

Z=1.986

NS

NS

NS

NS

NS

p<0.05

p<0.05

All specimens1

n

37

37

37

37

36

36

37

36

36

Med

0.873

0.667

82.1

1.109

0.822

84.3

0.454

0.393

90.8

AM±SD

1.05±0.43

0.81±0.36

78±13

1.18±0.47

0.93±0.40

79±13

0.52±0.21

0.42±0.19

80±19

Range

0.376-2.299

0.328-2.011

31.3-99.5

0.484-2.424

0.330-2.123

28.4-96.4

0.191-1.057

0.036-0.965

16.4-99.3

n

9

9

9

8

8

8

9

9

9

Med

1.439

1.073

70.7

2.047

1.110

63.1

1.119

0.673

74.8

AM±SD

2.5±1.8

1.27±0.56

62±19

3.0±2.4

1.31±0.54

57±21

2.0±2.3

0.89±0.57

65±23

Range

0.891-6.358

0.711-2.129

33.5-81.6

1.091-7.091

0.665-2.398

15.3-75.7

0.543-7.384

0.410-2.215

14.2-93.1

n

3

3

3

3

3

3

3

3

3

p<0.05

(p<0.09)

Gavia arctica Im

Ad

1

Im vs Ad All

256

specimens2

1unknown

Med

1.256

0.822

65.4

1.568

1.048

63.9

0.573

0.466

81.4

AM±SD

3.1±3.4

1.5±1.3

59±14

3.9±4.1

1.9±1.6

61 ±16

1.5±1.7

1.3±1.6

80±14

Range

1.154-7.007

0.798-3.027

43.2-69.2

1.412-8.597

1.002-3.734

43.4-74.3

0.494-3.516

0.336-3.155

68.0-89.7

M-W

NS

NS

NS

NS

NS

NS

NS

NS

NS

n

13

13

13

12

12

12

13

13

13

Med

1.352

1.015

69.2

2.002

1.110

63.1

0.774

0.665

74.8

AM±SD

2.6±2.1

1.31±0.71

62±17

3.2±2.6

1.47±0.84

58±18

1.2±2.0

0.96±0.83

69±20

Range

0.891-7.007

0.711-3.027

33.5-81.6

1.091-8.597

0.665-3.734

15.3-75.7

0.494-7.384

0.336-3.155

14.2-93.1

age category of 18 specimens.

2unknown

age category of one specimen

2

ACCEPTED MANUSCRIPT 257

3.3. Black-throated loon

258

In the total group (n = 13) some differences were detected between the concentrations of THg

259

and MeHg in the liver, kidneys and muscles (M-W test: H = 7.06, p <0.05, H = 7.63, p <0.05,

260

respectively). The lowest median concentrations of THg and MeHg were detected in muscles (Table

261

2) and they were only significantly different from corresponding concentrations found in the liver of

262

black-throated loon. The median values for MeHg and THg content in the three types of the analyzed

263

samples do not differ in a statistically significant way. Between percentage medians of MeHg in THg

264

set for the three types of samples studied, there were no statistically confirmed differences. In this

265

species, a small number of specimens (n = 13) were available, the age category was defined for 12

266

birds (Ad n = 3, Im n = 9). Comparative analysis between young and adult birds has shown no

267

differences in the concentrations of THg, MeHg and %MeHg. However, it has been shown that

268

individuals obtained in the autumn season had lower levels of hepatic THg than those collected in

269

the winter season: 1.508 vs 4.472 mg kg-1 (M-W test: Z = 1.95, p <0.05). The difference between seasons

270

could also be influenced by the use of the energetic reserves and for instance, a decrease of the size

271

of the liver leads to an increase of Hg concentration just because of its mass variation (Fort et al.,

272

2015).

273

3.4. Interspecific comparisons

274

In the pectoral muscle, kidney and liver of the examined birds of the razorbill species from

275

Poland, THg concentrations ranged from 0.191 to 1.057; 0.376 to 2.299; 0.484 to 2.424 mg kg-1 dw

276

respectively (Table 2). The mercury content in individual tissues is higher than the mercury content

277

in fish from the Baltic Sea (Table 3), as confirmed by the conclusion of mercury bioaccumulation

278

ability in food chain (Árvay et al., 2017). Also the most important factor governing the level of Hg

279

and organomercury compounds in the tissues of an animal appears to be the diet (Arcagni et al.,

280

2017).

281 1

ACCEPTED MANUSCRIPT 282

Table 3. Literature data on the content Hg in biological samples from different parts of the world. SPECIES

GEOGRAPHICAL REGION

TYPE OF

INDIVIDUALS

SAMPLE

Sprat -

(Sprattus sprattus)

Poland (coastal

Herring

zone of the

(Clupea harengus)

Baltic Sea)

Cod (Gadus morhua)

-

-

-

-

Razorbills (Alca torda)

(Mediterranean coastline, La Marina, Elche, Alicante)

USA (Minnesota)

-1]

(Polak-

0.022 ± 0.013[µg g

-

1]

0.031 ± 0.022 [µg g -1]

1.8 ± 0.65[µg g -1] juvenile

1.38 ± 0.49 [µg g -1]

Brain

1.22 ± 0.40 [µg g -1]

Vane

1.03 ± 0.59 [µg g -1]

Shaft

0.48 ± 0.15 [µg g -1]

(Espín et

Liver

3.00 ± 0.87 [µg g

-1]

al., 2012)

2.54 ± 0.82 [µg g

-1]

Kidney Muscle

adult

1.68 ± 0.51 [µg g -1] 1.67 ± 0.52 [µg g -1]

Vane

3.76 ± 0.97 [µg g -1]

Shaft

1.95 ± 0.44 [µg g -1]

Liver

8.0 ± 1.9 (3.6 - 23.1) [µg g -1] 39.3 ± 29.2

adult

(3.4 - 103.0) [µg g 1]

Common Loons

Canada (Quebec)

(Gavia immer) Goosander (Mergus merganser)

Goosander (Mergus merganse)

Finland (Lake Päijänne)

Feather

Muscle

males

17.6 [µg g -1]

females

8.9 [µg g -1]

-

18.1 [µg g -1]

Liver

14.7 [µg g -1]

Kidney

9.9 [µg g -1]

Poland (River Odra

Brain

estuary)

Breast

-

Bone

torda)

(Atlantic Ocean)

Kidney

albatrosses

Southern Pacific and Indian Oceans

Liver

Pichner, W. E. Braselt et al., 2002) (Champoux et al., 2006) (Sarkka et al., 1978)

(Kalisińska et al., 2010)

10.13 ± 4.71 [µg g 1] -

6.48 ± 2.14 [µg g -

(Fort et al.,

1]

2015)

3.99 ± 1.56 [µg g -

Muscle Wandering

(Bischoff, J.

0.08 [µg g -1]

Liver Bay of Biscay

1.3 [µg g -1] 2.3 [µg g -1]

muscle

Razorbills (Alca

Juszczak, 2009)

Kidney

juvenile (Gavia immer)

0.014 ± 0.005 [µg g

2.68 ± 0.86 [µg g -1]

Brain

Common Loons

REFERENCES

(RANGE) d/w *

Liver Muscle Spain

-

Hg MEAN

1] adult

920.0 ± 794.1

(Hindell et

[µg g -1]

al., 1999) 2

ACCEPTED MANUSCRIPT (Diomedea exulans) Shy albatrosses

36.3 ± 21.4

(Thalassarche

[µg g -1]

cauta)

283

∗The numerical values are given as originally stated in the cited literature.

284 285

These results were similar to northern gannet (Morus bassanus) from the Portuguese Atlantic

286

coast where THg concentrations were 0.473 – 0.851; 0.952 – 3.423; 1.291 – 2.603 µg g-1 dw for muscle,

287

kidney and liver respectively [40]. For these results, it can be observed that the THg concentration in

288

the liver is lower than in the kidney in comparison to the results obtained for the birds from Poland.

289

Comparable results were also obtained during the determination of Hg content in tissues of razorbills

290

living in Mediterranean coastline (Table 3) (Espín et al., 2012).

291

Higher THg concentrations were reported in razorbills species from the Portuguese Atlantic

292

coast where mean THg contents for muscle, kidney and liver were 2.669; 3.939; 6.094 µg g-1 dw

293

respectively (Ribeiro et al., 2009) and populations of the species from Scandinavia and North America

294

in the 1960– 1980 (concentration in the breast muscle was 6.094 µg g-1dw) when agricultural use of

295

MeHg-pesticides was on a large scale (Barr, 1986).

296

In our study THg concentration in the pectoral muscle kidney and liver of black-throated loon

297

were even higher and ranged from 1.091 to 8.597; 0.494 to 7.384 and 0.891 to 7.007mg kg-1 dw

298

respectively (Table 2). Total mercury concentrations in muscle, kidney and liver in populations of

299

loons (specifically Gavia immer) from eastern Canada was found to be 2.9; 15; 19 µg g-1 dw and in

300

mergansers (Mergus merganser) 3.0; 11; 15 µg g-1 dw respectively (Scheuhammer et al., 1998), which

301

does not go beyond the typical concentrations for species of predatory birds from different areas of

302

the world (Evers et al., 2005). Significant higher mercury concentrations in the tissues of birds of the

303

same species as birds described in this paper were observed in birds living in the Minnesota State

304

(USA) (Bischoff, J. Pichner, W. E. Braselt et al., 2002). For adults, the concentration of mercury in the

305

liver in the range 3.4 to 103.0 mg kg-1 dw (Table 3). However, these levels may related not only to the

306

diet of these animals, but also by the fact that the north-eastern part of North America is characterized 3

ACCEPTED MANUSCRIPT 307

by high Hg content in the geological surface and significant anthropogenic pollution of the

308

environment by this metal (Bischoff, J. Pichner, W. E. Braselt et al., 2002). Therefore, it can be

309

suggested that THg concentrations in birds depend on the Hg contamination in their habitats, but

310

also on their position in the food chain.

311

Recently, levels that may be indicative of adverse effects were suggested for THg concentrations

312

in the liver and kidneys of nonmarine birds (Shore et al., 2011). Bird death may be expected when

313

either hepatic or nephric concentrations were greater than 20 mg kg-1 or 40 mg kg-1 wet weight (more

314

than 67 mg kg-1 and 133 mg kg-1 dry wt), respectively. A conservative threshold for toxic effects of

315

Hg in waterbirds are 5 mg kg-1 wet weight or 16.7 mg g-1 dry weight in the liver (Bearhop et al., 2000;

316

Burger, 1993; Burger and Gochfeld, 2004; Pillatzki et al., 2011; Zillioux et al., 1993).

317

4. Conclusions

318

This study, having regard to the statistical analysis of all the collected individuals of razorbill

319

and black-throated loon, showed that in the compared similar tissues (kidney, liver and muscle)

320

median concentrations of THg and MeHg are significantly higher in the black-throated loon than in

321

razorbill. This may indicate that demethylation by Se in this species is effective.

322

On the other hand the percent MeHg in THg (%MeHg) it is significantly higher in the razorbill

323

than in black-throated loon. For example in razorbill, pectoral muscle MeHg accounted for about 91

324

% of total mercury and in black-throated loon for about 75% of total mercury (Table 2). Similar %

325

MeHg has been found in great cormorant and great crested grebe (Podiceps cristatus) from the Czech

326

Republic (Houserová et al., 2007), osprey (Pandion haliaetus) from Norway (Norheim and Froeslie, A.

327

(Veterinaerinstituttet, 1978), and brown pelican (Pelecanus occidentalis) from the Gulf of California

328

(Ruelas-Inzunza et al., 2009).

329

Muscle MeHg fraction of THg in freshwater and coastal piscivorous birds is generally higher

330

than 80% because demethylation process in the muscle tissue is very weak (Kalisinska et al., 2014).

331

This type of difference was not found when compared to adults belonging to the studied species.

4

ACCEPTED MANUSCRIPT 332

However, among young representatives of razorbill and black-throated loon some differences have

333

been shown. Nephric, hepatic and muscular THg and the concentration MeHg in muscle was

334

markedly higher in the black-throated loon compared to razorbill (MW test: Z = 2.31, p <0.05; Z = 2.43,

335

p <0.02; Z = 2.74 p <0.01; Z + 2.67, p <0.01, respectively).

336

In groups of analyzed common birds from Poland, the average hepatic THg concentration did

337

not exceed lethal concentration, compared to the Canadian population of this species where total

338

mercury content was higher than this specified value.

339

Consumption of fish is the main pathway to methylmercury exposure for birds. It can cause

340

adverse effects on reproductive success, behaviour and cell development. Methylmercury is able to

341

cross the blood – brain barrier and can be passed from the mother to the eggs. Our results help us to

342

better understand the accumulation of mercury in the selected tissues of two species of birds (Alca

343

torda and Gavia arctica), showing significant differences between the contents of MeHg in the selected

344

tissues and the close correlations between the contents of methylmercury and inorganic mercury in

345

some analysed tissues.

346 347

Acknowledgments: The authors would like to thank to Ewelina Kołodziejczak and Dominika Michalska for

348

their assistance in performing chemical analyses.

349

Conflicts of Interest: The authors declare no conflict of interest.

350 351

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ACCEPTED MANUSCRIPT Highlights    

Concentrations of Hg and MeHg in Alca torda and Gavia arctica tissues were measured; The highest average content of Hg was in liver in comparison to the other tissues; The average hepatic THg concentration did not exceed lethal concentration. Intra and inter-specific comparisons were carried out.