Organohalogen contaminants and Blood plasma clinical–chemical parameters in three colonies of North Atlantic Great skua (Stercorarius skua) Christian Sonne a,n , Frank F. Rige ´t a , Eliza H.K. Leat b , Sophie Bourgeon c , Katrine Borg ˚ a d , Hallvard Strøm e , Sveinn A. Hanssen c , Geir W. Gabrielsen e , Aevar Petersen f , Kristin Olafsdottir g , Ellen Magnusdottir f , Jan O. Bustnes c , Robert W. Furness b , Mads Kjelgaard-Hansen h a Aarhus University, Faculty of Science and Technology, Department of Bioscience, Arctic Research Centre (ARC), Frederiksborgvej 399, DK-4000 Roskilde, Denmark b College of Medical, Veterinary and Life Sciences, Graham Kerr Building, University of Glasgow, Glasgow G12 8QQ, UK c Norwegian Institute for Nature Research, FRAM Centre, 9296 Tromsø, Norway d Norwegian Institute for Water Research, Gaustadallee´n 21, 0349 Oslo, Norway e Norwegian Polar Institute, FRAM Centre, 9296 Tromsø, Norway f Icelandic Institute of Natural History, IS-210 Gardabaer, Iceland g University of Iceland, Department of Pharmacology & Toxicology, IS-107 Reykjavik, Iceland h University of Copenhagen, Department of Veterinary Clinical and Animal Sciences, Frederiksberg, Denmark article info Article history: Received 12 October 2012 Received in revised form 8 February 2013 Accepted 18 February 2013 Available online 26 March 2013 Keywords: ALAT Albumin Amylase Blood plasma biochemistry GGT Persistent organic pollutants Total bilirubin Total protein Urea abstract The present study compares blood plasma clinical–chemical parameters (BCCPs) in birds from three geographically distinct North Atlantic Great skua (Stercorarius skua) colonies. Birds from these sites bioaccumulate different POP (persistent organic pollutant) concentrations and that enabled us to compare Great skua BCCPs in different exposure scenarios. Persistent organic pollutants (organochlor- ines: PCB, DDT, chlordanes, HCB, HCH, mirex and brominated flame retardants: PBDEs) and nineteen BCCPs were analysed in 114 adult Great skuas sampled during summer 2009 in North Atlantic colonies at Bjørnøya (n ¼42), Iceland (n ¼57) and Shetland (n ¼15). Specimens from Bjørnøya had the highest blood plasma concentrations of all contaminant groups followed by Iceland and Shetland birds, respectively (ANOVA: p o0.05). Most of the 19 BCCP parameters followed the pattern of colony differences found for contaminants, with Bjørnøya having the highest concentrations. However seven BCCPs, the three liver enzymes ALKP, ALAT and GGT as well as bile acids, cholesterol, sodium and potassium, did not differ between colonies (ANOVA: p 40.05). Therefore correlation analyses of these seven BCCPs vs. POPs were done on the combined colony data while the analyses of the remaining 12 BCCPs were carried out for each colony separately. The analyses of combined colony data showed that the blood plasma concentration of liver enzymes ALAT and GGT increased with increasing concentra- tions of SPBDE and SHCH, HCB and SCHL, respectively (all Pearson’s p o0.05). In Great skuas from Shetland, the important osmotic transport protein albumin increased with increasing concentrations of SPCB and SDDT, while total blood plasma protein increased with SPCB, SDDT, SHCH and HCB concentrations (all Pearson’s p o0.05). In both Bjørnøya and Iceland skuas, blood plasma pancreatic enzyme amylase decreased with increasing SHCH concentrations while the erythrocyte waste product total bilirubin in blood plasma increased with increasing SHCH and SPBDE concentrations in Iceland Great skuas (all Pearson’s p o0.05). In Bjørnøya birds, blood plasma urea from protein metabolism (reflects kidney function) increased with increasing SPBDE concentrations (Pearson’s p o0.05). Furthermore, a redundancy analysis showed that 10.6% of the variations in BCCPs could be explained by the variations in POP concentrations. Based on these results we suggest that liver and renal functions could be negatively affected by different POP compounds. It is, however, uncertain if the colony BCCP differences and their relationship to POP concentrations reflect health effects that could have an overall impact on the populations via reduced survival and reproduction parameters. & 2013 Elsevier Inc. All rights reserved. 1. Introduction Concentrations of persistent organic pollutants (POPs) present in the marine environments of the northern hemisphere are particularly high in the vicinity of industrialized areas such as Contents lists available at SciVerse ScienceDirect journal homepage: www.elsevier.com/locate/ecoenv Ecotoxicology and Environmental Safety 0147-6513/$ - see front matter & 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ecoenv.2013.02.012 n Corresponding author. E-mail address: [email protected] (C. Sonne). Ecotoxicology and Environmental Safety 92 (2013) 245–251
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Ecotoxicology and Environmental Safety 92 (2013) 245–251
Contents lists available at SciVerse ScienceDirect
Ecotoxicology and Environmental Safety
0147-65
http://d
n Corr
E-m
journal homepage: www.elsevier.com/locate/ecoenv
Organohalogen contaminants and Blood plasma clinical–chemicalparameters in three colonies of North Atlantic Great skua (Stercorarius skua)
Christian Sonne a,n, Frank F. Riget a, Eliza H.K. Leat b, Sophie Bourgeon c, Katrine Borga d,Hallvard Strøm e, Sveinn A. Hanssen c, Geir W. Gabrielsen e, Aevar Petersen f, Kristin Olafsdottir g,Ellen Magnusdottir f, Jan O. Bustnes c, Robert W. Furness b, Mads Kjelgaard-Hansen h
a Aarhus University, Faculty of Science and Technology, Department of Bioscience, Arctic Research Centre (ARC), Frederiksborgvej 399, DK-4000 Roskilde, Denmarkb College of Medical, Veterinary and Life Sciences, Graham Kerr Building, University of Glasgow, Glasgow G12 8QQ, UKc Norwegian Institute for Nature Research, FRAM Centre, 9296 Tromsø, Norwayd Norwegian Institute for Water Research, Gaustadalleen 21, 0349 Oslo, Norwaye Norwegian Polar Institute, FRAM Centre, 9296 Tromsø, Norwayf Icelandic Institute of Natural History, IS-210 Gardabaer, Icelandg University of Iceland, Department of Pharmacology & Toxicology, IS-107 Reykjavik, Icelandh University of Copenhagen, Department of Veterinary Clinical and Animal Sciences, Frederiksberg, Denmark
a r t i c l e i n f o
Article history:
Received 12 October 2012
Received in revised form
8 February 2013
Accepted 18 February 2013Available online 26 March 2013
The present study compares blood plasma clinical–chemical parameters (BCCPs) in birds from three
geographically distinct North Atlantic Great skua (Stercorarius skua) colonies. Birds from these sites
bioaccumulate different POP (persistent organic pollutant) concentrations and that enabled us to
compare Great skua BCCPs in different exposure scenarios. Persistent organic pollutants (organochlor-
ines: PCB, DDT, chlordanes, HCB, HCH, mirex and brominated flame retardants: PBDEs) and nineteen
BCCPs were analysed in 114 adult Great skuas sampled during summer 2009 in North Atlantic colonies
at Bjørnøya (n¼42), Iceland (n¼57) and Shetland (n¼15). Specimens from Bjørnøya had the highest
blood plasma concentrations of all contaminant groups followed by Iceland and Shetland birds,
respectively (ANOVA: po0.05). Most of the 19 BCCP parameters followed the pattern of colony
differences found for contaminants, with Bjørnøya having the highest concentrations. However seven
BCCPs, the three liver enzymes ALKP, ALAT and GGT as well as bile acids, cholesterol, sodium and
potassium, did not differ between colonies (ANOVA: p40.05). Therefore correlation analyses of these
seven BCCPs vs. POPs were done on the combined colony data while the analyses of the remaining 12
BCCPs were carried out for each colony separately. The analyses of combined colony data showed that
the blood plasma concentration of liver enzymes ALAT and GGT increased with increasing concentra-
tions of SPBDE and SHCH, HCB and SCHL, respectively (all Pearson’s po0.05). In Great skuas from
Shetland, the important osmotic transport protein albumin increased with increasing concentrations of
SPCB and SDDT, while total blood plasma protein increased with SPCB, SDDT, SHCH and HCB
concentrations (all Pearson’s po0.05). In both Bjørnøya and Iceland skuas, blood plasma pancreatic
enzyme amylase decreased with increasing SHCH concentrations while the erythrocyte waste product
total bilirubin in blood plasma increased with increasing SHCH and SPBDE concentrations in Iceland
Great skuas (all Pearson’s po0.05). In Bjørnøya birds, blood plasma urea from protein metabolism
(reflects kidney function) increased with increasing SPBDE concentrations (Pearson’s po0.05).
Furthermore, a redundancy analysis showed that 10.6% of the variations in BCCPs could be explained
by the variations in POP concentrations. Based on these results we suggest that liver and renal functions
could be negatively affected by different POP compounds. It is, however, uncertain if the colony BCCP
differences and their relationship to POP concentrations reflect health effects that could have an overall
impact on the populations via reduced survival and reproduction parameters.
& 2013 Elsevier Inc. All rights reserved.
ll rights reserved.
1. Introduction
Concentrations of persistent organic pollutants (POPs) presentin the marine environments of the northern hemisphere areparticularly high in the vicinity of industrialized areas such as
Fig. 1. Map identifying Bjørnøya, Iceland and Shetland colonies from where 42, 57
and 15 Great skuas, respectively, were sampled during June–August 2009.
C. Sonne et al. / Ecotoxicology and Environmental Safety 92 (2013) 245–251246
the Baltic Sea (AMAP, 1998, 2004). However, POPs are also trans-ported by atmospheric and sea currents from lower latitudes suchas Eurasia and North America towards the Arctic (AMAP, 1998,2004; Macdonald et al., 2003, 2005; Colborn, 2004). Persistentorganic pollutants are xenobiotics and exert environmental stressthat is suspected to have various health impacts, including neuro-endocrine disruption, immune suppression and organ toxicity inwildlife (Gabrielsen, 2007; Letcher et al., 2010; Sonne, 2010;Verreault et al., 2010). POPs are known to influence homeostasisand allostasis, that is the maintenance of a stable physiology,which is important for vital organ-system functioning and criticalfor survival and reproduction in vertebrate species in general(Schulz et al., 2000; Harr, 2002; Braun, 2003; Richards andProszkowiec-Weglarz, 2007; Sonne, 2010). Due to transportmechanisms and chemical and biological properties, POPs areretained within organisms and biomagnify in marine and terres-trial food webs resulting in high concentrations in top predators(Muir et al., 1992; Norstrom and Muir, 1994; Rocca andMantovani, 2006).
Blood plasma clinical–chemical parameters (BCCPs) are a broadsweep of biochemical endpoints that reflect liver and kidneyfunction, bone diseases and metabolic disorders among others(Harr, 2002; Thrall et al., 2006). Multiple factors influence BCCPsand include infectious diseases, genetic defects and environmentalstressors such as starvation, dehydration and POP exposure (Schulzet al., 2000; Harr, 2002; Braun, 2003; Richards and Proszkowiec-Weglarz, 2007; Sonne et al., 2008, 2010, 2012). Therefore BCCPshave been used as biomarker endpoints for POP exposure in birdsas well as mammals (Dieter, 1974, 1975; Dieter et al., 1976, 1977,1978; Smith et al., 1982; Hayes et al., 1984; Fischbein, 1985;Edqvist et al., 1992; Fox et al., 2007; Kutlu et al., 2007; Sonne et al.,2008, 2010, 2012). The Great skua (Stercorarius skua) is an exampleof a marine top predator feeding on birds and fish (Phillips et al.,1997; Kakela et al., 2007) that due to its high trophic positionpresents high concentrations of POPs including organochlorinesand brominated flame retardants (Bourne and Bogan, 1972;Furness, 1987; Ratcliffe et al., 1998; Fisk et al., 2001; Votier et al.,2004, 2007, 2008; Leat et al., 2011; Bourgeon et al., 2012).
Three colonies of North Atlantic Great skuas located inScotland (Shetland), Iceland and Norway (Bjørneøya) reflecteddifferent levels of POP concentrations (Bourgeon et al., 2012).These are the largest colonies of this scarce species (globalpopulation ca. 16,000 pairs) so span the latitudinal range of majorbreeding sites from 601N to 741N (Furness, 1987; Magnusdottiret al., 2012). Birds from these colonies migrate to lower latitudesto spend the winter, many from all these colonies travelling tosouthern Europe or West Africa, although a proportion of the birdsfrom Iceland and Norway migrate to winter off eastern Canada(Magnusdottir et al., 2012). Recently, Bourgeon et al. (2012)examined how POP concentrations in these colonies may relateto markers of stress (corticosterone), immunity and oxidativestress. Despite contrasted POP concentrations between colonies,Bourgeon et al. (2012) did not report any causal relationshipsbetween POPs and the latter three biomarkers. In this context, thepresent study, conducted on Great skuas from the same colonies,aims to assess the effects of contaminants on health status andhealth risks, particularly in liver and kidney functions using BCCPsas a broader span of biomarker health endpoints.
2. Materials and methods
2.1. Study design and sampling
The study was conducted on breeding adult Great skuas trapped live on the
nest and blood sampled at Bjørnøya (n¼42), Shetland (island of Foula, n¼15) and
Iceland (Breidamerkursandur, SE Iceland, n¼57) ranging from 601N to 751N and
from 251W to 201E (Fig. 1). At all three colonies, breeding adults at least five years
old were caught in the middle of their incubation period in 2009 from 16th of June
to 17th of July at Bjørnøya, from 9th to the 26th of June at Shetland and from 3rd
to 23rd of June at Iceland following the procedure described by Bourgeon et al.
(2012). Blood (maximum 10 mL in heparinized syringes) was sampled from the
brachial or tarsal vein and centrifuged on site at 2000 rpm for 5 min and 1 mL
supernatant plasma was transferred to a sterile 1.5 mL Eppendorfs tube and
frozen at �20 1C the same day and subsequently stored until analyses.
Sampling procedures were approved according to legislation by Norwegian,
UK and Icelandic authorities. The Great skua has been increasing in numbers over
recent decades, especially in Scotland and Norway, and is not a specially protected
species, so no CITES permit was required. Appropriate national import and export
licences for health safety were obtained to permit movement of samples between
countries. The Great skuas analyzed in the present study are the same specimens
as those in the Bourgeon et al. (2012) study despite the sample size of Bjørnøya is
slightly lower and Shetland significantly lower due to limited blood plasma
volumes.
2.2. Analyses of blood plasma clinical–chemical parameters (BCCPs)
The analyses of individual samples were conducted at the Central Clinical
Laboratory at the Department of Veterinary Clinical and Animal Sciences, University
of Copenhagen and included the following nineteen components (Table 1): albumin
(Alb; g L�1), glucose (Glu; mmol L�1), total protein (TP; g L�1), alkaline phosphatase
(ALKP; U L�1), alanine aminotransferase (ALAT; U L�1), total bilirubin (TB; mmol L�1),
(Na; mmol L�1) and potassium (K; mmol L�1). Due to limited plasma volume, GGT
was not analysed in the Icelandic Great skuas. All analyses were routinely conducted
at the laboratory using an automated spectrophotometric analyser also containing
ion-selective electrodes (ADVIA 1800, Siemens). All assays were subjected to daily
internal and quarterly external quality control. Only results from accepted analytical
runs are reported here. Information on the methods and their interpretations in
clinical studies can be found in Sonne et al. (2008, 2010, 2012) and in Table 1.
2.3. Analyses of persistent organic pollutants (POPs)
Analyses of POPs in individual plasma samples were performed at the Great
Lakes Institute for Environmental Research (GLIER), University of Windsor, Canada.
See Leat et al. (2011) for details on the analyses. For each batch of six organochlorine
samples, a reference homogenate, method blank, external PCB standard (Quebec
Ministry of Environment Congener Mix; AccuStandard, New Haven, CT, USA),
OC standards and CB-30 recovery standard were analyzed. Recoveries of CB-30 in
Table 1Summary statistics [median (Min–Max)] of 19 blood plasma clinical–chemical parameters n in adult Great skuas from three North Atlantic colonies sampled
n Three liver enzymes (ALKP, ALAT, GGT), one digestive enzyme (amylase), two protein groups (albumin and total protein), two liver/erythrocyte metabolism products
(bile acid and bilirubin), cholesterol, two carbohydrates (glucose and fructosamine), creatinine/urea/uric acid (muscle and protein metabolism) and five electrolytes/
Nineteen blood plasma clinical–chemical parameters weremeasured in all Great skuas except GGT in the Icelandic birds(Table 1). In summary, these were composed of three liver
Table 3Significant and trend-wise Pearson’s correlation (rp) analyses of BCCPs vs. POPs in adult Great skuas from three North Atlantic colonies sampled June–August 2009. Since
no colony differences were found for ALKP, ALAT, GGT, bile acids, cholesterol, sodium and potassium, the correlation analyses were run on data combined across colonies
while the remaining was done separately for each colony. y: colony data combined. B: Bjørnøya. I: Iceland. S: Shetland.
C. Sonne et al. / Ecotoxicology and Environmental Safety 92 (2013) 245–251248
enzymes (ALKP, ALAT, GGT), one digestive enzyme (amylase), twoprotein groups (albumin and total protein), two liver/erythrocyte metabolism products (bile acid and bilirubin), cho-lesterol, two carbohydrates (glucose and fructosamine), creati-nine/urea/uric acid (muscle and protein metabolism) and fiveelectrolytes/minerals (iorganic phosphate, calcium, magnesium,sodium and potassium) (Table 1). With regard to ALKP, ALAT,GGT, bile acids, cholesterol, sodium and potassium no significantdifferences were found between the three colonies while albu-min, total protein, inorganic phosphate and calcium were sig-nificantly lower in Shetland great skuas, compared to the othertwo colonies (Table 1). Amylase, total bilirubin and glucose weresignificantly higher and urea and creatinine significantly lower inBjørnøya great skuas, compared to the other two colonies(Table 1). Fructosamine and uric acid were significantly higherin Great skuas from Iceland and magnesium significantly lower inGreat skuas from Shetland, compared to the other colonies(Table 1).
3.2. POP concentrations
The dominating POP groups in all three colonies were PCBs,DDT and chlordanes (Table 2). For PCBs, the dominant congenerswere the higher chlorinated CB-138, �153 and �180, while forPBDEs it was the lower brominated BDE-47, �99 and �100.Oxychlordane and trans-nonachlor were the chlordanes found inhighest concentrations in birds from all three colonies. Theconcentrations of all POP groups were highest in Great skuasfrom Bjørnøya being 2–5 times higher than in birds from Icelandand Shetland (Table 2). The POP concentrations were also higherin Iceland Great skuas compared to Shetland specimens except forSPBDE (Table 2).
3.3. Relationship between POPs and BCCPs
Significant and trend-wise results of the linear relationshipsbetween BCCPs and POPs are summarised in Table 3. Twelve ofthe BCCPs differed between colonies and these were thereforetreated separately in the correlation analyses. Seven of the BCCPsdid not differ among colonies and of these, ALAT increased withincreasing concentrations of SCHL and SPBDE concentrations andGGT with increasing concentrations of SPCB, SHCH, HCB andSCHL. Beside these two, also sodium increased with increasingconcentration of HCB.
In Shetland Great skuas, albumin levels increased withincreasing SPCB, SDDT, HCB, SCHL and Mirex concentrations(Table 3). Total protein increased with increasing concentrationsof SPCB, SDDT, SHCH, HCB and SCHL while urea and magnesiumdecreased with increasing SHCH concentrations (Table 3).In skuas from Iceland, amylase decreased with increasing SHCHconcentrations while total bilirubin increased with increasingconcentrations of SHCH and SPBDE (Table 3). In addition, calciumdecreased with increasing SHCH concentrations and fructosa-mine with increasing SPBDE concentrations (Table 3). In skuasfrom Bjørnøya, amylase decreased with SHCH concentrationswhile urea increased with concentrations of SPBDE (Table 3).Inorganic phosphate decreased with increasing SPBDE concen-trations and calcium and albumin decreased with increasingSHCH concentrations (Table 3). Finally, magnesium increased withincreasing SCHL concentrations (Table 3).
3.4. RDAs
The RDA analysis of BCCPs, POPs and colonies divided the totalvariance into two parts; 10.6% constrained by the multivariateregression and 89.4% unexplained in the significant model. Thefirst two canonical axes explained 50.3% and 23.0% of theconstrained 10.6% inertia, respectively. Fig. 2 shows a distancebiplot of the RDA results. Some BCCPs seem to group (bile acids,total protein, albumin and ALAT) while all POP groups, exceptSHCH, are correlated. SHCH and HCB contributed significantly tothe RDA indicating those POPs to be the most important forexplaining the BCCP variations. Total bilirubin was positivelyassociated with only SHCH while glucose was positively asso-ciated with all other POP groups and especially HCB and SPBDE.Fructosamine and ALKP were negatively associated with onlySHCH while urea and creatinine were negatively associated withall other POP groups. In addition to this, Bjørnøyaskuasweregroups with all POPs while Shetland’s were not indicating thatBjørnøya specimens had the highest POP concentrations followedby Icelandic and Shetland skuas, respectively.
4. Discussion
Great skuas from Bjørnøya had POP concentrations that were3–24 folds higher than those found in Shetland birds; also elevenof the nineteen BCCPs were significantly different betweenBjørnøya and Shetland. Such differences point towards POP
Fig. 2. Distance RDA biplot of BCCP (red) and POP (blue arrows) concentrations in
the three colonies Bjørnøya (B), Shetland (S) and Iceland (I) of adult Great skuas.
RDA1 explained 50.3% and RDA2 23.0% of the constrained 10.6% inertia, respec-
tively. Arrows pointing in the same direction indicate that the compounds are
positively correlated while arrows pointing in opposite direction indicate
a negative correlation. Lines with an angle of 90 degrees indicate no correlation.
Consult Tables 1 and 2 for abbreviations. Black circles¼95% for location centres.
(For interpretation of the references to colour in this figure legend, the reader is
referred to the web version of this article.)
C. Sonne et al. / Ecotoxicology and Environmental Safety 92 (2013) 245–251 249
exposure being a co-factor for the colony differences in BCCPconcentration while time from last prey digestion and differencesin diet should also be considered as possible causes of BCCPcolony variation (AMAP, 1998, 2004; Schulz et al., 2000;Van Loveren et al., 2001; Harr, 2002; Braun, 2003; Thrall et al.,2006; Richards and Proszkowiec-Weglarz, 2007; Letcher et al.,2010).
In the same colonies, Bourgeon et al., (2012) reported that skuasbreeding at the least contaminated site (Shetland) experienced thehighest levels of corticosterone (25% higher) and oxidative stress(50% higher) and the lowest plasma immunoglobulin levels (15%lower) compared to the two other colonies. They suggested that thelack of consistent relationships between POP concentrations and thelatter biomarkers might be imputable to other ecological factors suchas food availability. Accordingly, while skua numbers are increa-sing in Bjørnøya, skuas at Shetland are declining in numbers, havereduced adult survival rates, and show increased reproductive effortbut reduced breeding success (Votier et al., 2004, 2007, 2008),suggesting that poor food availability at Shetland affects stress levelsmore than pollutant loads.
We found significant correlations between POPs and impor-tant BCCP markers in both combined groups of colonies andwithin the three Great skua colonies, separately. The positiveassociation between ALAT, GGT and five different POP groupsindicate POP-induced liver toxicity. Several other aviary studieshave also reported on PCB, DDT, chlordane, HCH and HCB-inducedliver toxicity with blood plasma increases of ALAT, GGT, bile acid,total bilirubin, albumin, total protein and cholesterol (Dieter,1974,1975; Dieter et al., 1976, 1977, 1978; Hayes et al., 1984;Fischbein, 1985; Edqvist et al., 1992; Kutlu et al., 2007). In GreatLake gulls, however, bilirubin, albumin and total protein were
lower in a group with high POP contamination when compared toa reference site (Fox et al., 2007). The exact mode of action behindthese relationships is unknown but indicates hepatocytic lesionswith abnormal leak of cytoplasmic substances into the bloodstream (Rustad et al., 2004; Klaassen et al., 2007; Sonne et al.,2008, 2010, 2012). Also in mammals for example, Chu et al.(1994) found that bilirubin plasma concentrations were highest ina PCB-exposed rat group and a similar relationship has beenfound in Greenland sledge dogs exposed to a similar POP cocktailas the Great skuas of the present study (Sonne et al., 2008).This was supported by Tryphonas et al. (1984) who foundincreased plasma concentrations of cholesterol and bilirubin inPCB treated cynomolgus monkeys (Macaca fascicularis). That wasalso the case in a study of humans where bilirubin increased withincreasing PCB concentrations (Stehr-Green et al., 1986).
The relationship between renal BCCPs and POP concentrationsindicate an effect on Great skua kidneys. For example, concentra-tions of urea and total protein increased with increasing concen-trations of PCB, DDT, HCH, HCB and PBDEs which may indicateglomerular and/or tubular lesions (Ettinger and Feldman, 1995;Thrall et al., 2006; Sonne et al., 2008). In the study by Chu et al.(1994), a similar increase in urea was found in PCB-exposedfemale rats. How exposure to HCHs (and PBDEs) may affectamylase (and fructosamine) is unknown. For the electrolytesinorganic phosphate, calcium, magnesium and sodium, the rela-tionships may be dietary and/or POP related, while a linkage torenal disorders or bone metabolism cannot be excluded (Harr,2002; Thrall et al., 2006; Musso, 2009).
No normal range for BCCPs was accessible for Great skuas andit was therefore not possible to evaluate the clinical significance ofthe extremes (Harr, 2002; Thrall et al., 2006). Compared to otherseabird species like the Bjørnøya glaucous gull (Larus hyperboreus)carrying high contaminant levels, plasma PCB concentrations wereca. two folds higher in the Great skuas from Bjørnøya (Letcher et al.,2010; Verreault et al., 2010). In the Bjørnøya Glaucous gulls, variousPOPs such as SDDE and SPCB were negatively correlated to bloodplasma thyroid hormone and vitamin A concentrations indicatingsubclinical endocrine-disrupting health effects (Letcher et al., 2010;Verreault et al., 2010). It is therefore likely that also Bjørnøya Greatskuas suffer from immune suppression and lower reproductionrates resulting in impaired fitness, survival and subsequent adapta-tions to ecological changes (Letcher et al., 2010; Verreault et al.,2010).
5. Conclusions
Bjørnøya Great skuas had the highest plasma concentrations ofall POP followed by Iceland and Shetland; and this pattern wasalso found for most of the BCCPs. Correlation analyses of BCCPs vs.POPs reflected that liver lesions and renal function could benegatively affected by different POP compounds. It is, however,uncertain if the colony BCCP differences and their relationship toPOP concentrations reflect health effects that could have anoverall impact on the populations via reduced survival andreproduction parameters.
Acknowledgments
This study was supported by the Research Council of Norway(grant #184830) and the Arctic Research Centre (ARC) at AarhusUniversity is acknowledged for financial support. Licences andpermissions to trap and blood sample from Great skuas inShetland were provided by Scottish Natural Heritage, the BritishTrust of Ornithology (BTO) and the U.K. Home Office. We thank
C. Sonne et al. / Ecotoxicology and Environmental Safety 92 (2013) 245–251250
the late Isobel Holbourn for help with logistics and fieldwork inFoula. Fieldwork in Bjørnøya was carried out under permit fromthe Governor of Svalbard, Stavanger Museum and the Directoratefor Nature Management. Knut Olsen, Veronica Nygard, ArnsteinKnutsen, Tore Nordstad and Lene Ringstad Olsen helped in thefield in Bjørnøya. Halfdan Bjornsson helped in the field in Iceland.Pollutant analysis was carried out at the Great Lakes Institute forEnvironmental Research (GLIER), we thank Aaron Fisk for hisassistance, Nargis Ismail for carrying out PBDE analysis and RogerThiessen and Mary Lynn Mailloux for extraction and clean-up ofsamples for PCBs/OCs/PBDE analyses.
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