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Environmental Pollution 157 (2009) 2282–2290

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Environmental Pollution

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Persistent organic pollutants, heavy metals and parasites in the glaucousgull (Larus hyperboreus) on Spitsbergen

Kjetil Sagerup a,*, Vladimir Savinov b, Tatiana Savinova b, Vadim Kuklin c, Derek C.G. Muir d,Geir W. Gabrielsen e

a Tromsø University Museum, NO-9037 Tromsø, Norwayb Akvaplan-niva, The Polar Environmental Centre, NO-9296 Tromsø, Norwayc Murmansk Marine Biological Institute, Kola Scientific Centre, Russian Academy of Sciences, Murmansk, Russiad Aquatic Ecosystem Protection Research Division, Environment Canada, Burlington ON L7R 4A6, Canadae Norwegian Polar Institute, The Polar Environmental Centre, NO-9296 Tromsø, Norway

Consistent relationships between contaminant level and parasite intens

ity, as an immunotoxic endpoint unit, were not found in the present study.

a r t i c l e i n f o

Article history:Received 15 September 2008Received in revised form23 March 2009Accepted 26 March 2009

Keywords:Glaucous gullPOPsHeavy metalsHelminths

* Corresponding author. Tel.: þ47 77 64 50 92; faxE-mail address: kjetil.sagerup@uit.no (K. Sagerup)

0269-7491/$ – see front matter � 2009 Elsevier Ltd.doi:10.1016/j.envpol.2009.03.031

a b s t r a c t

The prediction of a higher parasite infection as a consequence of an impaired immune system withincreasing persistent organic pollution (POP) and heavy metal levels were investigated in adult glaucousgull (Larus hyperboreus) from Svalbard. The levels of chlorinated pesticides, polychlorinated biphenyls(PCBs), toxaphenes and polybrominated diphenyl ethers (PBDEs) were measured in liver. Cupper,cadmium, lead, mercury, selenium and zinc were measured in kidney samples. An elevated ratio ofPCB-118 was found, suggesting that local contamination from the settlement was detectable in theglaucous gull. Eight cestodes, four nematodes, two acanthocephalan and three trematode helminthspecies were found in the intestine. A positive correlation was found between cestode intensities andselenium levels and between acanthocephalan intensities and mercury levels. No correlation was foundbetween parasite intensities and POP concentrations. It is concluded that the contaminant levels found inglaucous gulls do not cause immune suppression severe enough to affect parasite intensity.

� 2009 Elsevier Ltd. All rights reserved.

1. Introduction

Over the last decades, high levels of persistent organic pollut-ants (POPs) and some heavy metals (HMs) have been detected inbiota from Svalbard area (Daelemans et al., 1992; Knudsen et al.,2007; Savinov et al., 2003, 2005). The levels of ‘‘legacy’’ POPcompounds such as dichloro-diphenyl-trichloroethane (DDT),polychlorinated biphenyl (PCB) and oxychlordane are high in thetop predators of birds and mammals due to the biomagnificationprocess (Borgå et al., 2001). The levels of ‘‘legacy’’ POPs havehowever decreased in the last decades due to the ban and restric-tion in their production and use (Braune et al., 2001; Helgason et al.,2008; Verreault et al., 2005c).

Polybrominated flame retardants have been widely used inelectrical equipment and other flame retarded goods such aspolyurethane foams (Alaee et al., 2003). Most of the use is in urbanareas of eastern Asia, North America and western Europe and arepotential sources for atmospheric transport to the Arctic

: þ47 77 64 55 20..

All rights reserved.

(AMAP, 2004). PBDE is found in air, sediments and biota in Arcticand the levels are increasing (de Wit et al., 2006; Law et al., 2003).Even though the penta- and octa-BDEs have been banned in theEuropean Union, Canada and some US states and withdrawn fromproduction by manufacturers, the levels of PBDE are expected tocontinue to rise in the Arctic (Law et al., 2003). The PBDEs arechemically and structurally similar to PCBs. Potential health effectsfrom PBDE exposure suggest that these new pollutants could havemuch of the same effects as the PCBs (Darnerud, 2003; Vos et al.,2003). The levels of PBDEs are however still less than 2% of the PCBlevels in the glaucous gulls from Bjørnøya (Herzke et al., 2003;Verreault et al., 2005a).

Heavy metals occur naturally in soil and biota and concentra-tions depend on local geology, local addition from mining andindustry and/or globally distributed pollution (Pacyna, 2005). Threemain anthropogenic sources of HM to the Arctic have been iden-tified; fossil fuel combustion, non-ferrous metal production andwaste incineration (Pacyna, 2005). Anthropogenic HMs are trans-ported to the Arctic mainly through the atmosphere (Bard, 1999;Berg et al., 2004; Brooks et al., 2005; Lindberg et al., 2002). Trenddata from sediment and ice cores show that HM concentrations

K. Sagerup et al. / Environmental Pollution 157 (2009) 2282–2290 2283

have increased since the start of the industrial revolution (Brauneet al., 2005). However, data series for mercury (Hg) and cadmium(Cd) in Greenland marine biota from the late-1970s to themid-1990s showed no overall temporal trends (Riget and Dietz,2000). Nevertheless, it is still necessary to monitor HM in Arctic airand biota, since Hg emissions appear to be increasing globally dueto more coal burning in Asia (Pacyna, 2005).

The highest levels of POPs in the European Arctic are found inthe top predators of the marine food chain (Borgå et al., 2005;Johansen et al., 2004; Verreault et al., 2005c). In the EuropeanArctic, the polar bear (Ursus maritimus) and the glaucous gull hasreceived a lot of attention (for review see Gabrielsen (2007)). Theapex predatory feeding behaviour of glaucous gull and its lowcapacity for metabolising organochlorines (Henriksen et al., 2000)makes this species specially susceptible to accumulating high levelsof POPs. Its diet includes marine invertebrates and fish and,seasonally, eggs and chicks from other seabirds, carcasses frompolar bear hunts and sometimes also adult auks (Alcidae) andkittiwakes (Rissa tridactyla) (Bustnes et al., 2000; Erikstad, 1990;Lydersen et al., 1989). On Bjørnøya, in the Barents Sea, high levels ofPOPs have been found in the glaucous gull (Borgå et al., 2001;Henriksen et al., 2000; Savinov et al., 2005) with very high levels insick and dead individuals (Bogan and Bourne, 1972; Gabrielsenet al., 1995). Extensive effect studies of free-living glaucous gulls onBjørnøya have shown negative effects of contamination on thehormone- and immune-systems, on nesting behaviour and repro-duction, on feather development and survival (Bustnes et al., 2002,2003b, 2004, 2006; Sagerup et al., 2000; Verboven et al., 2008;Verreault et al., 2004).

The intestinal helminth fauna of Arctic seabirds includes severalspecies from different classes. However, it is characterised by a lowspecies diversity of trematoda (Kuklin et al., 2004). Several speciesof cestoda, nematoda and acanthocephalans have also been foundin the glaucous gull (Kuklin et al., 2004; Sagerup et al., 2000). Theparasites pose a challenge for the host’s well-being and especiallytheir allocation of resources to immune functions (Sheldon andVerhulst, 1996). The effects of pollution on parasitism might beeither positive or negative for the host. A positive outcome couldarise if the pollutant is fatal for the parasite (Lafferty, 1997) or if itreduces the intermediate hosts’ populations and thereby reducesthe infection rate. Conversely, when the pollutant affects the hostrather than the parasite, as for example through immunotoxicchemicals, the result could be a suppressed immune system andincreased parasites load (Sures, 2006).

The hypothesis of the present study is that high levels ofcontaminants (HMs and POPs) impair the immune system ofglaucous gull. Our objective was to test the prediction that parasiteintensity would increase with POP/HM concentrations.

2. Materials and methods

2.1. Sample collection

A sample of 20 adult glaucous gulls was collected near Barentsburg, Spitsbergen(78.05 �N, 14.2 �E) in August 2001. Immediately after capture, the birds wereweighed with a spring balance (�25 g). Wing length (�1 mm; maximum fattenedcord), bill depth (�0.1 mm) and total head length (�0.5 mm; from neck to the tip ofbill) were measured. All birds were classified to be at least 4 years old (Cramp, 1977).The liver, kidney and the intestinal tract were sampled and frozen at �20 �C untilanalysis. The sex was determined by gonad inspection. The sampling was inaccordance to the current regulation of the Norwegian Animal Welfare Act andpermission to collect glaucous gulls was given by the Governor of Svalbard.

2.2. Sample extraction and analysis

The liver was analysed for chlorinated and brominated contaminants. Chlori-nated pesticides (OCPs), including hexachlorocyclohexanes (HCHs), chlordanerelated compounds (CHLs), and DDTs, as well as chlorobenzenes (CBs) and the PCBs

were analysed at Typhoon, the Centre of Environmental Chemistry, S.P.A. in Obninsk,Russia. PBDEs, hexabromocyclododecane (HBCD) and toxaphenes were analysed atNational Laboratory for Environmental Testing at National Water Research Institute(NWRI) in Burlington, Canada.

The liver tissues for the OCP/PCB analyses were homogenized and recoverystandards were added. The samples were extracted and percent extractable lipidcontent (�0.1%) was determined gravimetrically by evaporation before concentratedH2SO4 was used to remove lipids. The samples were automatically injected into a gaschromatograph (Hewlett Packard 5790A) equipped with an 63Ni electron capturedetector and a 25 m long 0.25 mm HP-1 column. PCBs and pesticides were quantifiedusing certified external standard solutions obtained from the National Laboratoryfor Environmental Testing in Burlington, Canada. A detailed description of extractionand analyses are given in Muir et al. (2003).

PBDEs and toxaphenes were analysed in liver sample extracts and certifiedreference materials previously extracted for PCB and OCPs. Details of the extractionand analyses are given in Verreault et al. (2005c) and Muir et al. (2006). Analyses ofPBDE, HBCD and toxaphene were carried out at NWRI by gas chromatography–lowresolution mass spectrometry (GC–MS) on an Agilent 6890 GC-5973 MSD equippedwith electron capture negative ionization mode (GC-ECNIMS) and HP5-MS capillarycolumn. Quantification of toxaphene homologues (hexa-, hepta-, octa-, nona-) wascarried out using a technical toxaphene standard. Individual chlorobornanecongeners, referred to as either Parlar (‘‘P’’) numbers or bornanes (‘‘B’’), werequantified by a series of authentic external standards of each compound obtainedfrom Ehrenstorfer GmbH (Germany).

The HMs copper (Cu), Cd, lead (Pb), Hg, selenium (Se) and zinc (Zn) wereanalysed from the kidney. The analyses were performed at the Department ofEnvironmental Monitoring and Pollution, Obninsk, Russia using atomic absorptionspectroscopy (AAS). The kidney samples were digested with nitric acid. Levels of Cdand Pb were measured on Perkin Elmer Z-3030 with Zeeman background correction.Levels of Zn and Cu were measured by AAS on Perkin Elmer B-3030 and those of Hgwere measured by cold vapour AAS using the US Environmental Protection Agency(EPA 7471A) method on a Perkin Elmer MAS-50. The extraction of Se was carried outwith a mixture of H2SO4 and HClO4, and a conversion of Se to 5-nitro-2,1,3-benzo-selendiasol and extraction with chloroform. Selenium was measured by cold vapourAAS on a Perkin Elmer Z-3030 with Zeeman background correction.

2.3. Quality assurance

The method detection limit (MDL) for individual analytes was determined as 10times the noise level or, in the case where an analyte was present in blanks, threetimes the standard deviation of the analyte in blanks. Method limits of detection inglaucous gull samples were 0.01 ng/g for toxaphene related compounds, 0.02 ng/gfor most PCBs and PBDEs and 0.02–0.05 ng/g for the other chlorinated compounds.The detection limits for HMs and Se vary for each technique, 0.2 mg/g for Cu and Se,0.1 mg/g for Zn, 0.01 mg/g for Pb, 0.005 mg/g for Hg and 0.001 mg/g for Cd. Blanksamples, consisting of all laboratory reagents, were analysed with every 10 samples.The concentration of analysed congeners was consistently less than 10% of theobserved concentrations in the liver. Results for individual pesticides and PCBcongeners were not blank-corrected. Recoveries of internal standards were good(65–85%) and no recovery corrections were made. One duplicate was analysed atTyphoon, whereas NWRI duplicated the analysis of every fifth sample.

The laboratory at Typhoon has national accreditation within the framework ofRussian Analytical Laboratories Accreditation System for POPs and Hg in abiotic andbiotic samples. Both laboratories had successfully participated in the QUASIMEME(Aberdeen, Scotland) international inter-laboratories comparison. The Typhoonlaboratory also participated in the Department of Energy (MAPEP-2001–2002), USA,the NIST/NOAA-NS&T/EPA-EMAP QA Program, the AMAP ring-test (round 1–2 at2002) and the Second Italian Free Intercalibration Round.

The quality control for the trace elements included analysis of blanks, duplicates,matrix spike recoveries and use of certified reference materials (DORM-1 andDOLT-1) from the National Research Council of Canada.

2.4. Parasite determination

The intestinal helminths were identified and quantified at the MurmanskMarine Biological Institute of Russian Academy of Sciences. The intestinal tract wasremoved from each bird and placed in separate dishes with seawater. The oesoph-agus and gizzard were cut off from the rest of the intestine. The intestine was cutinto segments of about 10 cm. Each segment was cut open and the contents scrapedinto glasses with mixed sea and fresh water (in proportions 1:1) pre-warmed to40 �C. After 30 min, the contents were transferred to Petri dishes and examined forparasites under a stereomicroscope.

The surfaces of the oesophagus, gizzard and ventricle were also examined forparasites under the stereomicroscope. Parasites were fixed in 70% alcohol or 4%formalin in seawater (nematodes).

The trematodes, cestodes and acanthocephalans were stained in mucicarmineand prepared as whole mounts before identification. Nematodes were transferred toglycerine and cleared before examination. The prevalence (% infected), meanabundance (number of parasite individuals/n) and mean intensity (number of

Table 2The mean (�standard deviation) and data range of pesticides (ng/g wet wt.) in liverof adult glaucous gulls from Barentsburg, Spitsbergen. % > MDL ¼ percentage ofsample above method detection limit. n ¼ 20.

Compound % > MDL Mean � SD Range

a-HCH 0 <0.02b-HCH 100 1.9 � 1.5 0.04–6.8g-HCH 5 <0.02–2.2Oxychlordane 100 298.8 � 329.3 11.3–1180.9trans-chlordane 40 <0.02–2.9cis-chlordane 65 0.2 � 0.3 <0.02–1.2Heptachlor 35 <0.05–1.4trans-nonachlor 70 0.2 � 0.3 <0.02–1.4a-Endosulfan 20 <0.02–0.2b-Endosulfan 20 <0.02–6.5o,p0-DDE 100 2.3 � 2.0 0.1–8.8p,p0-DDE 100 270.8 � 251.5 68.2–1073.4o,p0-DDD 95 0.4 � 0.4 <0.05–1.8p,p0-DDD 100 4.2 � 6.1 0.2–27.1o,p0-DDT 100 2.3 � 2.1 0.1–6.6p,p0-DDT 100 7.5 � 5.3 1.4–22.5Endrin 95 0.7 � 0.6 <0.05–2.0Methoxychlor 65 1.0 � 1.2 <0.05–3.6Mirex 95 3.9 � 3.2 <0.05–15.31,3,5 tri-CBa 60 0.2 � 0.2 <0.05–0.91,2,4 tri-CB 70 0.4 � 0.6 <0.05–2.11,2,3 tri-CB 55 <0.05–3.11,2,3,4 tetra-CB 90 1.0 � 1.2 <0.05–5.5Penta-CB 100 1.6 � 1.6 0.1–6.8HCB 100 22.2 � 12.8 6.6–55.4

a Trichlorobenzenes.

K. Sagerup et al. / Environmental Pollution 157 (2009) 2282–22902284

parasite individuals/(prevalence/100)) of infection were calculated for eachhelminth species, following the definitions given by Bush et al. (1997).

2.5. Statistical analyses

The concentration mean for a given compound was only determined if 60% ormore of the samples had concentrations above the MDL (Verreault et al., 2005c), anarbitrary value used to optimize the trade-off between introducing noise (too lowvalue) or loss of data (too high value). Only those compounds were used in thefurther statistical analyses. To avoid missing values in the data computation,analytes below the MDL were assigned a randomly generated value between zeroand the MDL. The fat contents of the liver were considered similar with a smallvariance (mean 3.7%� 0.6). Therefore, concentrations are presented on a wet weightbasis. Natural log transformation (ln) of POP contaminants and parasite intensitiesresulted in residuals with normal distribution and constant variance.

To control for individual difference in size, body mass and sex, a body conditionindex was calculated using a multiple linear regression model with body mass as theresponse variable and sex þ bill length þ total head length þ wing length aspredictor variables for all individuals (Fox et al., 2007). The body condition index wasdefined as the residuals of the regression (Jakob et al., 1996). Linear regressionmodels with each of the summarized parasite groups as response variables and eachof the POP congeners, their summarized groups, or the HMs and the body conditionindex as predictor variable were calculated. Adjustment for multiple comparisonswas not made, since such adjustment could decrease the chances of rejecting thenull hypothesis that are not null (Rothman, 1990). P-values <0.05 were consideredstatistically significant. All statistics were calculated with the free statistical softwareR (R Development Core Team, 2008).

3. Results

3.1. Levels of OCP, PCB, toxaphene and PBDE

The summarized levels of pesticides, toxaphenes, PCBs and BDEsare presented in Table 1. The most abundant organic contaminantswere oxychlordane, PCB-153, p,p0-DDE and PCB-118/149 (Tables 2and 3). The concentrations of the two most abundant pesticides(oxychlordane and p,p0-DDE) were similar and more than 10�higherthan the next highest pesticide, hexachlorobenzene (HCB) (Table 2).

A total of 47 PCB congeners were included in the analyticalprogram (Table 3). All of them were found in at least one (PCB-8)sample. The PCB congeners -6, -8, -16/32, -17, -18, -24/27, -31, -49,-22, -33, -64, -70, -84, -87 and -169 all had levels below detectionlimits for at least 40% of the samples. They were therefore notincluded in the remaining analyses. The SPCB was calculatedfor the remaining 32 congeners (Table 1). The five congenersPCB-153>-118/149>-138>-180>-99 were the most abundantcongeners (Table 3), accounting for 78% of the SPCB32.

Table 1The mean (�standard deviation) and data range of POP concentrations (ng/g wetwt.) in liver of adult glaucous gulls from Barentsburg, Spitsbergen.

Compound Female Male

n Mean � SD Range n Mean � SD Range

Lipid, % 13 3.7 � 0.7 2.5–5 7 3.7 � 0.5 3.2–4.8SCBa 13 26 � 17 8–58 7 26 � 9 14–37SCHLb 13 345 � 386 13–1182 7 215 � 183 15–481SDDTc 13 205 � 86 122–408 7 440 � 393 80–1115SToxaphened 12 83 � 53 7–163 7 133 � 131 37–421SPCB32

e 13 854 � 401 367–1931 7 1363 � 706 386–2347SBDE10

f 12 15 � 9 4–33 7 16 � 7 6–28

a SCB ¼ sum of 1,3,5-trichlorobenzenes (tri-CB), 1,2,4 tri-CB, 1,2,3 tri-CB, 1,2,3,4tetra-CB, penta-CB and HCB.

b SCHL ¼ sum of cis-chlordane, trans-chlordane, trans-nonachlor, oxychlordane,and heptachlor.

c SDDT ¼ sum of o,p0-DDE, p,p0-DDE, o,p0-DDD, p,p0-DDD, o,p0-DDT and p,p0-DDT.d SToxaphene ¼ sum of hexa-, hepta-, octa- and nona-homologues.e SPCB32 ¼ sum of PCB-28, -40, -52, -66/95, -74, -76, -89/101, -97, -99, -132/105,

-110, -114, -118/149, -123, -126, -128/167, -137, -138, -141, -151, -153, -171/156, -157,-158, -170, -174, -180, -187, -189, -193, -194, and -196.

f SBDE10 ¼ sum of BDE-28/33, -47, -66, -99, -100, -138, -153, -154, -183, and -209.One outlier removed (100 ng/g wet wt.).

The octa- and hepta-toxaphenes were the most prevalent toxa-phene homologues (Table 4). Their contributions to the Stoxaphenewere 75% and 17%, respectively. Among the individual chlorobornanecongeners analysed, the octachloroboranes, B8-2229 (P44), B8-1414/B8-1945 (P40/41), B8-810 and B8-1471 had the highest concentra-tions (Table 4).

The SBDE10 concentrations in hepatic tissue of glaucous gullsranged from 3.5 to 100 ng/g wet wt. When removing one extremevalue for BDE-209, the upper range of SBDE10 drops to 32.8 ng/gwet wt (Table 1). Ranking the PBDEs according to their meanconcentrations gives the list, BDE-47>-209>-100>-99>-153(Table 5). The mean concentration of BDE-47 accounts for 49% ofthe SBDE10 after removal of the outlier in BDE-209. BDE-71, -77 and-85 were not found in any of the samples. BDE-17 and -190 werefound in 50% and 5% of the samples, respectively (Table 5).

Female birds may transfer contaminants to their eggs andthereby reduce their body burden compared to males. However,males did tend to have higher mean levels of DDTs, Toxaphenes,and PCBs than females, but these differences were not significant(Table 1).

3.2. Levels of HMs

The highest levels of HMs were found for Zn (mean ¼ 46.3 mg/gwet wt.) and Cd (mean ¼ 13.7 mg/g wet wt.), respectively (Table 6).One outlier for Pb was observed. Its concentration (13.3 mg/g wetwt.) was seven times higher than the next highest (1.9 mg/g wetwt.). When removing this outlier, the mean concentration changedfrom 1.0 mg/g wet wt. to 0.3 mg/g wet wt.

3.3. Intestinal parasites

The parasite intensity was measured as counts of individuals pergull. All gulls were infected with one to seven different parasitespecies and had at least three different individuals in their intes-tine. A total of 17 different species of four different classes were

Table 4The mean (�standard deviation) and data range of concentrations (ng/g wet wt.) oftoxaphene homologs and individual chlorobornanes in liver of adult glaucous gullsfrom Barentsburg, Spitsbergen. Andrews and Vetter (1995) nomenclature withParlar number in brackets. %>MDL¼ percentage of sample above method detectionlimit. n ¼ 19.

Compound % > MDL Mean � SD Range

Toxaphene homologuesa

Hexa-toxaphene 95 0.5 � 0.5 <0.01–1.7Hepta-toxaphene 100 18.0 � 15.8 0.3–62.3Octa-toxaphene 100 75.6 � 70.7 5.2–334.9Nona-toxaphene 100 7.4 � 5.2 1.0–21.7

Chlorobornane congenersB8-1413 (P26) 100 0.5 � 0.4 0.1–1.5B7-515 (P32) 100 0.1 � 0.1 0.01–0.4B8-531 (P39) 5 <0.01–0.01B8-1414/B8-1945 (P40/41) 100 1.4 � 1.7 0.1–7.5B8-806 (P42) 5 <0.01–0.1B8-2229 (P44) 100 8.8 � 10.5 0.5–49.0B9-1679 (P50) 100 0.8 � 0.6 0.1–2.3B9-1046 (P56) 5 <0.01–0.01B9-715 (P58) 68 0.1 � 0.1 <0.01–0.3B9-1025 (P62) 0 <0.01B7-1001 100 0.4 � 0.3 0.03–1.2B8-1412 100 0.9 � 0.6 0.1–2.7B7-1450 89 0.3 � 0.4 <0.01–1.7B8-810 100 1.7 � 1.1 0.1–4.4B8-1471 100 5.3 � 3.4 0.4–11.6B9-718 0 <0.01B9-743/B9-2006 0 <0.01

a Quantified with a technical toxaphene standard.

Table 5The mean (�standard deviation) and data range of PBDE and a-HBCD concentrations(ng/g wet wt.) in liver of adult glaucous gulls from Barentsburg, Spitsbergen.% > MDL ¼ percentage of sample above method detection limit. n ¼ 20.

Compound % > MDL Mean � SD Range

BDE-17 50 <0.02–0.1BDE-28/33 100 0.1 � 0.1 0.02–0.2BDE-47 100 7.4 � 3.3 2.1–12.1BDE-66 85 0.1 � 0.04 <0.02–0.1BDE-71 0 <0.02BDE-77 0 <0.02BDE-85 0 <0.02BDE-99 100 1.4 � 0.9 0.3–3.5BDE-100 100 1.4 � 0.7 0.4–2.4BDE-138 100 0.1 � 0.1 0.03–0.4BDE-153 100 1.1 � 0.9 0.2–3.9BDE-154 100 0.6 � 0.3 0.1–1.3BDE-183 80 0.1 � 0.1 <0.02–0.3BDE-190 5 <0.18–0.2BDE-209a 80 2.8 � 3.5 <0.01–12.7a-HBCD 95 0.1 � 0.04 <0.02–0.2

a One outlier removed (86.5 ng/g wet wt.).

Table 3The mean (�standard deviation) and data range of PCB concentrations (ng/g wet wt.)in liver of adult glaucous gulls from Barentsburg, Spitsbergen. %>MDL¼ percentageof sample above method detection limit. n ¼ 20.

Compound % > MDL Mean � SD Range

PCB-6 35 <0.02–0.3PCB-8 5 <0.02–0.04PCB-16/32 25 <0.04–0.2PCB-17 20 <0.02–0.1PCB-18 25 <0.02–0.1PCB-24/27 25 <0.04–1.3PCB-28 100 6.1 � 4.7 1.3–23.9PCB-31 15 <0.02–3.5PCB-40 95 3.8 � 5.1 <0.02–24.2PCB-49 30 <0.02–14.4PCB-52 65 1.1 � 1.4 <0.02–5.5PCB-22 30 <0.02–5.4PCB-33 35 <0.02–0.2PCB-64 50 <0.02–1.3PCB-66/95 100 4.7 � 3.9 1.6–15.1PCB-70 30 <0.02–1.0PCB-74 100 8.0 � 8.5 2.2–41.2PCB-76 60 5.3 � 10.6 <0.02–46.6PCB-84 35 <0.02–2.7PCB-87 55 <0.02–39.1PCB-89/101 100 9.0 � 21.8 0.2–95.7PCB-97 80 3.9 � 11.0 <0.02–49.7PCB-99 100 44.7 � 36.0 12.6–146.7PCB-132/105 100 12.9 � 16.2 3.6–75.3PCB-110 100 9.6 � 28.9 0.1–128.6PCB-114 100 3.4 � 2.5 0.6–9.1PCB-118/149 100 202.9 � 113.9 70.7–569.1PCB-123 100 1.0 � 0.6 0.1–2.3PCB-126 90 3.4 � 4.3 <0.04–19.6PCB-128/167 100 33.1 � 29.6 0.1–105.2PCB-137 100 6.5 � 5.9 1.7–28.6PCB-138 100 177.9 � 122.5 66.2–546.0PCB-141 65 1.9 � 5.8 <0.02–26.0PCB-151 95 4.9 � 6.7 <0.02–31.4PCB-153 100 275.0 � 155.8 95.5–641.3PCB-171/156 100 21.7 � 16.4 6.3–69.2PCB-157 90 3.5 � 3.3 <0.02–11.5PCB-158 100 4.0 � 5.7 0.7–26.7PCB-169 15 <0.02–0.8PCB-170 100 28.0 � 20.1 8.3–88.5PCB-174 80 1.1 � 1.7 <0.02–74PCB-180 100 108.3 � 74.8 17.6–291.0PCB-187 100 21.2 � 15.4 1.6–49.1PCB-189 85 1.1 � 1.3 <0.02–5.2PCB-193 80 0.8 � 0.9 <0.02–2.9PCB-194 100 13.9 � 12.6 2.4–46.5PCB-196 100 9.1 � 6.1 1.1–23.4

K. Sagerup et al. / Environmental Pollution 157 (2009) 2282–2290 2285

found (Table 7). The most numerous and species-rich class was thecestoda with at least seven species. The cestode Microsomacanthusductilus was the most prevalent and infected 70% of the gulls. Itsmean abundance was 51 individuals per bird.

The most prevalent of the four nematode species was theHysterothylacium aduncum, which infected 25% of the birds, whilethe highest infection was found for the Stegophorus stellaepolariswith seven individuals infecting one bird. The nematodes were onlyfound in the stomach. More than half (17 of 26) had penetrated thecuticula and were found in the connective- or muscle-tissuebeneath the cutiula. The penetrating behaviour of the nematodeswas found for all species.

Three species of digenetic trematodes and two species ofachantocephalan were also found (Table 7).

3.4. POP/HM-parasite associations

A positive correlation between Hg levels and acanthocephalanintensity (Hg partial t17 ¼ 3.53, p ¼ 0.003) was found (Fig. 1).

However, the acanthocephalan infected only 50% of the sample.To ensure that the correlation was valid, the more robust non-parametric Spearman rank test was applied and confirmed thecorrelation between Hg and acanthocephalan intensity (r ¼ 0.54,p ¼ 0.01).

In the multiple linear regression model, the Se explained 25% ofthe variation in cestode intensity (Se partial t17 ¼ 2.34, p ¼ 0.03)(Fig. 2). This positive correlation also held for the summarized totalparasites, but since the cestodes were the most numerous group,the correlation was essentially the same as for the cestodes. None ofthe chlorinated or brominated compounds were correlated toparasite intensity.

Table 6The mean (�standard deviation) and data range of heavy metal concentrations(mg/g wet wt.) in kidney of adult glaucous gulls from Barentsburg, Spitsbergen. n¼ 20.

Compound Mean � SD Range

Cu 4.9 � 1.2 3.0–7.2Cd 13.7 � 7.4 4.9–34.1Pba 0.3 � 0.4 0.1–1.9Hg 0.3 � 0.1 0.1–0.5Se 1.9 � 0.5 1.3–3.4Zn 46.3 � 13.4 30.2–88.5

a One outlier removed (13.3 mg/g wet wt.).

0.0

0.5

1.0

0.0 0.1 0.2 0.3 0.4 0.5

1.5

Hg (µg/g ww)

Ac

an

th

oc

ep

ha

la

n (ln

(in

t+

1))

y = -0.25 + 3.35Hg + 0.002BCI(0.26) (0.95) (0.0003)

Fig. 1. The scatter plot and regression line for intestinal acanthocephalan, natural log ofintensity þ 1 (ln(int þ 1)), and kidney mercury (Hg) concentration (mg/g wet wt.),controlled for body condition index (BCI), in glaucous gull from Barentsburg, Spitsbergen.The regression line is given with its estimated standard errors below the equation.

K. Sagerup et al. / Environmental Pollution 157 (2009) 2282–22902286

4. Discussion

4.1. Levels of pesticides, PCB, toxaphene and PBDE

The POP concentrations in seabirds are influenced by severalfactors such as nutritional status, feeding behaviour, age, sex, stageof breeding, location and season (Bustnes et al., 2000; Fox et al.,1990; Henriksen et al., 1996). Furthermore, the females can transferPOPs into the eggs, and thereby lower their body burden. Thisstudy, however, did not find the levels of PBDEs, pesticides, PCBs ortoxaphenes to be significantly higher in males than in females(Table 1) unlike reported in Bustnes et al. (2001). Age was nota confounder as only adult glaucous gulls were sampled (Bustneset al., 2003a), so why a difference between sexes was not observedin this study while previously observed in this species (Bustneset al., 2001) is not known.

The comparisons of OCP and PCB concentrations were made onlipid weight (lipid wt.) levels due to too high variance of liver lipid %between studies (Henriksen et al., 2000; Savinova et al., 1995). TheSDDT and SPCB lipid wt. levels of this study was about 1/3 ofBjørnøya (Barents Sea) glaucous gull from 1996 (Henriksen et al.,2000) and 2/3 of glaucous gull from Ny-Ålesund (North-WestSpitsbergen) sampled in 1991 (Savinova et al., 1995). These levelsare lower than the highest reported NOEL (no-observed-effects-level) in Arctic bird eggs (AMAP, 2004), and further only about 1/3

Table 7The prevalence (% infected), mean abundance, mean intensity and maximumintensity of intestinal parasites in adult glaucous gulls from Barentsburg, Spitsber-gen. Mean abundance¼ number of parasite individuals/n, mean intensity¼ numberof parasite individuals/ number of infected hosts (Bush et al., 1997). n ¼ 20.

Parasite Prevalence Meanabundance

Meanintensity

Maxintensity

Cestode 100 96.0 96.0Microsomacanthus diorchis 5 12.7 254 254Microsomacanthus ductilus 70 50.7 72.4 242Microsomacanthus microsoma 10 0.6 6.0 9Tetrabothrius erostris 45 7.5 16.7 52Alcataenia dominicana 15 1.6 10.7 28Anomotaenia sp. 5 0.6 12 12Anomotaenia micracantha 35 13.7 39.1 237Arctotaenia tetrabothrioides 10 8.5 85 154

Nematode 50 1.3 2.6Hysterothylacium aduncum 25 0.5 1.8 3Stegophorus stellaepolaris 20 0.6 3 7Streptocara crassicauda 10 0.2 2 3Paracuaria adunca 5 0.1 1 1

Trematode 20 11.2 56Cryptocotyle lingua 15 1.2 7.7 21Microphallus pseudopygmaeus 5 10.0 199 199Gymnophallus sp. 5 0.1 2 2

Acanthocephalan 50 1.2 2.4Corynosoma strumosum 50 1 2 3Polymorphus phippsi 10 0.2 2 2

of the SPCB9 level reported to correlated with nematode intensity(Sagerup et al., 2000).

The oxychlordane level of the present study was, however,higher than from Bjørnøya and Ny-Ålesund (Henriksen et al., 2000;Savinova et al., 1995). Oxychlordane is typically reported at about1/20 the level of p,p0-DDE in glaucous gull (Henriksen et al., 2000;Savinova et al., 1995), but in this study they are of equal levels(Table 2). The high oxychlordane to p,p0-DDE ratio is hard to explainsince local sources of both oxychlordane and p,p0-DDE should beabsent in this remote area. The PCB-118 was also relatively highcompared to other PCBs normally reported in glaucous gull (Clee-mann et al., 2000; Henriksen et al., 2000). The gulls have probablystayed in the area for the lasts 3–4 months since the largest nearby

1.0 1.5 2.0 2.5 3.0 3.5 4.0

0

1

2

3

4

5

6

Se (µg/g ww)

Ce

sto

de

(ln

(in

t))

y = 1.11 + 1.45se - 0.003BCI(1.22) (0.62) (0.003)

Fig. 2. The scatter plot and regression line for intestinal cestode, natural log ofintensity (ln(int)), and kidney selenium (Se) concentration (mg/g wet wt.), controlledfor body condition index (BCI), in glaucous gull from Barentsburg, Spitsbergen. Theregression line is given with its estimated standard errors below the equation.

K. Sagerup et al. / Environmental Pollution 157 (2009) 2282–2290 2287

breeding colony of glaucous gulls is located just across the fjord.The house paint and soil in and around the settlement of Bare-ntsburg was contaminated with PCBs, with the PCB-118 as thedominating congener (Jartun et al., 2007). The leakage of PCB fromthe settlement was reflected in marine macro-benthos from thefjord by a significant higher ratio of PCB-118 compared to otherfjords on Svalbard (Hop et al., 2001). Since a higher ratio of PCB-118was found in potential macro-benthos food and in soil around thesettlement were the glaucous gulls also forage, we suggest thatlocal contamination from the settlement also reached the uppertrophic level glaucous gull.

Toxaphene concentrations have been previously reported inglaucous gull livers from the Svalbard area by Herzke et al. (2003)and in blood and eggs by Verreault et al. (2005b). Herzke et al.(2003) analysed samples for 4 toxaphene congeners and foundmuch higher concentrations of B8-1413 (1.2–70 ng/g wet wt.) andB9-1679 (2.2–116 ng/g wet wt.), but similar low levels of B7-515and B8-1414. The lower B8-1413 and B9-1679 in the present studymay be due to elution of these congeners in the hexane elutionduring extraction, which was not analysed for toxaphene. Verreaultet al. (2005b) found that congeners B8-1412 and B8-2229 wererelatively prominent in glaucous gull blood and eggs, similar toresults from this study. Skopp et al. (2002) also found that B8-2229and B8-1414/B8-1945 (P40/41) were prominent chlorobornanesin osprey and goshawk eggs. The latter authors did not identifyB8-810 and B8-1471, however, they did note several unknownchlorobornanes with GC retention times near the well knownB9-1679 (P50) congener.

The median lipid normalised liver concentrations of BDE-47 and-99 in the present study were lower (192 and 29 ng/g lipid wt.,respectively) than the corresponding liver median from glaucousgulls sampled in August 1999 at Bjørnøya (365 and 143 ng/g wetwt., respectively) and from the Barents Sea in May–July 2004 (452and 74 ng/g lipid wt., respectively) (Haukås et al., 2007; Herzkeet al., 2003). The deca-brominated diphenyl ether BDE-209 wasabove MDL in 80% of our samples, compared to 50% and 36% in maleand female plasma from Bjørnøya glaucous gull (Verreault et al.,2005a). In one of the samples, an extreme outlier (86.5 ng/g wetwt.) was measured for the BDE-209. The bird with the outlier mayhave ingested a contaminated object. The blank samples from thePBDE analyses were clean, but since PBDEs are widely used inhuman equipment such as furniture, computers, etc, we can notdisregard the possibility that the BDE-209 outlier was a result ofcontamination (Knudsen et al., 2007). The risk assessment forPBDEs in wildlife is difficult to assess due to several and importantdata gaps (Darnerud, 2003). Neonatal exposure of mice to tetra-and penta-BDE (BDE-47, 99) caused developmental neurotoxiceffects (Eriksson et al., 2001). In co-exposure with methylmercurya single dosage of 0.8 mg/kg body weight BDE-99 caused behav-ioural and reduced learning effects in mice (Fischer et al., 2008).However, the SPBDE is still less than 2% of SPCB (Table 1) as waspreviously found in glaucous gulls from Bjørnøya (Herzke et al.,2003; Verreault et al., 2005a).

4.2. HM levels

According to the United Nations Economic Commission forEurope Convention on long-range trans boundary air pollution Hg,Cd and Pb are the HM of concern because of their environmentaland human toxicity (UNECE, 2004). Se, Cd, Pb and Hg concentra-tions reported in the AMAPs’ HM report (AMAP, 2005) were withinthe same range as found in the present study. In two other seabirdstudies from the Barents Sea, the concentrations of HM weresimilar to those found in the present study (Borgå et al., 2006;Savinov et al., 2003). Savinov et al. (2003) concluded that the levels

of the most toxic elements, Hg and Cd, are mainly the result ofnatural background levels rather than from pollution input.

The Hg threshold level of biological effects for terrestrial birdeggs was ten times greater than the kidney levels reported inpresent study (Derome et al., 2005). Further, the Cd threshold levelfor adverse renal function was seven times higher and the Pbthreshold level for subclinical poisoning was double the reportedlevels from the present study (Derome et al., 2005). Low levels ofHg can cause reproductive effects, while behavioural and neuro-toxic effect appear with increased exposure (Chan et al., 2003, andreferences therein). However, the Hg level of 0.3 mg/g wet wt.(Table 6) is reviewed as a background level apparently withoutcausing effects (Scheuhammer, 1987, and references therein).

4.3. Parasite infection

The number of helminth species was similar to that previouslyfound in breeding adult glaucous gull collected on Bjørnøya in 1996(Sagerup et al., 2000). The main differences were that cestodeswere more abundant, prevalent and species rich, while there werefewer species and a lower abundance and prevalence of nematodesin the present study than on Bjørnøya (Sagerup et al., 2000).

The cestodes, which were the most prevalent group ofhelminths, are regarded as relatively harmless to the host (Davisand Anderson, 1971). The most abundant trematode Cryptocotylelingua is also regarded as harmless (Bakke, 1972). Acanthocephalanparasites attach to the gut wall by hooks and could thereby harmtheir hosts, but infected only 50% of our sample, with a maximum offour parasites. The adult nematode H. aduncum has fish as hosts(Balbuena et al., 1998; Klimpel et al., 2007), but an infection toa non-host species could be troublesome, as for example in anisa-kiasis (Mehlhorn and Bunnag, 1988). It is not known, however, howvirulent the H. aduncum is for birds. Both H. aduncum and the threeother nematode species were mostly found under the cuticula inthe stomach. When penetrating tissues, the parasites cause woundsand we therefore believe that the nematodes may be costly for theglaucous gull. However, as for the acanthocephalan, the nematodegroup had 50% prevalence and low intensity (Table 7).

4.4. POP/HM-parasite associations

The primary task of the immune system is to fight, and preventestablishment of infection. Since immune responses are costly,hosts should regulate their response to parasites according tovirulence and intensity (Behnke et al., 1992). Even though PCBlevels were lower than NOEL for hatching success in eggs (AMAP,2004), the levels and complexity of the POP cocktail invites foreffect study of the sensitive immune system (Tryphonas, 1994).Parasite intensity effects from a suppressed immune system shouldtherefore be observed on the most prevalent and harmful parasites.The gastrointestinal helminths occupy an extracellular niche, butthey are not completely protected against immune systems defencemechanisms (Michels et al., 2006). The immune system fightshelminths through both increased muscular contraction andwith immunoglobulin E antibody activated mast cells (Abbas andLichtman, 2003). Even though the immune system effects oforganic halogenated compounds have been reviewed as negative(Tryphonas, 1994; Vos and Luster, 1989), and that parasite intensityhas been associated with POPs in a breeding population in glaucousgull (Sagerup et al., 2000), such effect was not found in the presentstudy.

Few experimental studies on helminth infection and POP expo-sure have been done, and the results vary. A single high dose ofdioxin, 2,3,7,8-TCDD, delayed the elimination of the adult nematodeTrichinella spiralis from the intestine of mice (Luebke et al.,1994). No

K. Sagerup et al. / Environmental Pollution 157 (2009) 2282–22902288

effect on infection rates of the acanthocephalan Polymorphus botu-lus was found, however, when single doses of PCB-77 (5 or50 mg/kg) or the technical mixture of Clophen A50 (50 or200 mg/kg) were given to common eider ducklings Somateriamollissima (Rozemeijer et al., 1995). The birds in the present studywere in good body condition and, as discussed above, the pollutionlevels were not exceptionally high.

The glaucous gulls were sampled in August, chicks had fledged(Løvenskiold, 1964) and birds were in better body condition sincethe energy-demanding breeding period was over (Monaghan andMetcalfe,1986). As the harsh winter months had not yet started, thestress levels were reduced and body resources could be channelledto the immune system. In addition, the relatively small sample sizeand the large variation in component levels may have masked anyassociation.

Selenium is a naturally occurring substance and is an essentialmicronutrient for plants and animals. It works in synergy withvitamins in the protective activities of immune cells and is essentialfor antibody production (Maggini et al., 2007). High levels of Se are,however, toxic and accumulation above a certain threshold level ineggs, at least 16 mg/g dry weight, may cause embryo malformationor death (Fairbrother et al., 1999). High levels of Se are also deadlyfor adult birds, but in concentrations much higher than those foundin this study. It is therefore hard to find any good biologicalexplanation for the cestode correlation with Se. However, since theSe is an essential micronutrient, one explanation could be thatthe highest levels of Se in this study resulted in an advantage to thecestodes in their competition for micronutrients (Barnard andBehnke, 1990).

Mercury and most of its compounds, including methylmercury,are extremely toxic and controlled feeding studies have identifiedbehavioural, hormonal and reproductive effect in bird, mammalsand fish (Scheuhammer et al., 2007). It has further been associatedwith a suppressed immune function in common loon (Gavia immer)chicks that received methylmercury chloride in the food (Kenowet al., 2007). These studies suggest that our correlation between Hgand acanthocephalan could be a result of a depressed immunesystem. But since the Hg levels were low and acanthocephalansonly infected half of the gulls with a maximum infection of fourindividuals, it is suggested that the correlation is a coincidence.

5. Conclusions

This study failed to find a consistent relationship between levelsof contaminants and parasite intensities. Long term exposure todifferent POPs did therefore not result in a systematic variation inintensity of parasites in the glaucous gull. An increased number ofparasites, as a consequence of increased POP levels, could havebeen the end result of an impaired immune system. However, wesuggest that a more direct measurement of the immune systemalso is included in this kind of study. It is therefore concluded thatthe POP effects on the immune system of glaucous gulls should befurther investigated.

Acknowledgements

We want to thank Sergey Zyryanov and Sergey Marasaev fortaking part in the field work at Svalbard. We also want to thankLyudmila Alexeeva, Elena Pasynkova and Valery Surnin (Centre ofEnvironmental Chemistry SPA ‘‘Typhoon’’, Obnisnk, Russia) for theirhelp with chemical analysis of persistent organic pollutants andheavy metal samples. We thank Sean Backus (Environment Canada,Burlington ON) for the analysis of PBDEs and toxaphene. RobBarrett, Anne Helene Tandberg and three anonymous reviewersprovided useful comments to drafts of the manuscript. Funding for

this study was provided by the Joint Russian-Norwegian Commis-sion on Environmental Protection, Akvaplan-niva, Norwegian PolarInstitute and Tromsø University Museum.

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