Hexabromocyclododecane contamination of herring gulls in the coastal area of the southern Baltic Sea

Hexabromocyclododecane (HBCD) is a bromo-organic compound belonging to the group of polybrominated diphenyl ethers (PBDE) and its presence in the environment is closely related to human activity. HBCD was used in expanded polystyrene (EPS), extruded polystyrene (XPS) and in high impact polystyrene (HIPS), as well as to reduce textile inflammability (de Wit 2002; Alaee et al. 2003; Kajiwara et al. 2009). Its composition is dominated by the γ-HBCD diastereoisomer (about 70%), while α- and β-HBCD constitute from 10 to 30%, and other isomers do not exceed 1% (Heeb et al. 2005). In accordance with the Stockholm Convention on Persistent Organic Pollutants, the use of HBCD is conditionally admissible. Pursuant to Regulation (EC) No. 1907/2006 (REACH), HBCD has been included on the candidate list of Substances of Very High Concern (SVHC) as it is stable and able to accumulate in biota (Covaci et al. 2006; Wu et al. 2011). In biological samples, including humans, the α-HBCD isomer dominates and is characterized by high persistence in the environment (Covaci et al. 2006; Kuiper et al. 2007; Janák et al. 2008). This environmental pollutant can be transported over long distances in the atmosphere and is resistant to photo-and chemical degradation (Remberger et al. 2004; Schure et al. 2004; Law et al. 2008). HBCD affects the thyroid hormone receptor-mediated gene expression and is a potential endocrine disruptor (Janák et al. 2008; Kakimoto et al. 2008; de Wit et al. 2010). HBCD can cause skin sensitization and inhibition of plasma membrane uptake of the neurotransmitters dopamine, glutamate and γ-amino-n-butyric-acid (GABA). Furthermore, it may act as a peroxisome proliferator, which is a mechanism involved in non-mutagenic cancer (Sellström et al. 2003).

Sea birds are an early warning of environmental pollutants and the contamination of their habitat may cause unexpected changes in their numbers, health or breeding success. These animals are commonly used as sentinel organisms (Furness 1993; Grove et al. 2009; Van den Stern et al. 2009) and their eggs are often used as a noninvasive tool for environmental pollution monitoring (e.g. Bignert et al. 2016; Miller at al. 2014; Rigét et al. 2016).

Previous studies on aquatic birds from the Baltic Sea region provide information on its contamination with several persistent organic pollutants (e.g. Falandysz 1984; 1986; Falandysz & Szefer 1983; Falandysz et al. 1994a; 2000; Falkowska et al. 2016; Fliedner et al. 2012; Kannan et al. 2003; Lundstedt-Enkel et al. 2006; Reindl et al. 2019; Thyen et al. 2000). Many researchers also confirm the contamination of bird habitats with HBCD isomers, even in areas where they have never been produced or used (Braune et al. 2007; Evenset et al. 2007; Jörundsdóttir et al. 2013). HBCD isomers were found in bird organisms and eggs in different regions of the world (e.g. Chen et al. 2012; Elliott et al. 2005; Herzke et al. 2005; Fernie et al. 2009; Marteinson et al. 2012), including the Baltic Sea (Sellström et al. 2003; Lundstedt-Enkel et al. 2006). Our research to date has shown the ability of HBCD to accumulate and accrue in the marine trophic chain, as well as to be transmitted via maternal transfer in Spheniscus demersus from the Gdansk Zoo. HBCD isomers were found in the Baltic herring, which represented the only food source for penguins, as well as in the penguin muscles, liver and eggs (Reindl & Falkowska 2015). Further research on eggs of aquatic birds has shown that their contamination depends on the source of food. Eggs of birds feeding on marine food are about 50% more contaminated than eggs of omnivores and scavengers (Reindl & Falkowska 2019).

The liver plays a key role in the internal organ distribution and elimination of several toxins. It also participates in the transformation of environmental pollutants, including HBCD (Abdallah et al. 2014). In birds, the liver is also responsible for the synthesis of egg yolk lipoproteins (Vieira et al. 1995). As part of this process, lipophilic pollutants such as HBCD can be transported internally and deposited in egg lipids. With this in mind, the presented study is focused on the determination of the concentration of HBCD isomers and the selective sequestration factor in the livers of herring gulls collected from the southern coast of the Baltic Sea.

HBCD isomers were found in the muscles and livers of the examined birds, irrespective of their sexual maturity. Mean ΣHBCD concentrations in herring gull muscles (42.82 ± 30.65 ng g⁻¹ l.w.) were lower than those of ΣHBCD in the liver (65.51 ± 27.96 ng g⁻¹ l.w.). Among the analyzed isomers, the highest concentrations were determined for the α-HBCD isomer, whose contribution to ΣHBCD was on average 80% in both muscles and liver. The correlations were statistically significant and linear (a-HBCD_Muscle = 0.4660 ΣHBCD_Muscle + 13.0181, p = 0.0000, r = 0.7730; α-HBCD_Liver= 0.9175 ΣHBCD_Liver −7.0279, p = 0.0000, r = 0.8841) for both tissues. The average proportion of β- and γ-HBCD isomers in ΣHBCD was about 20%.

In terms of sexual maturity of birds, the concentrations of HBCD in the muscles of mature males were lower than in mature females, while the concentrations of HBCD and α-HBCD in the liver of males were higher than in females. However, the sex of mature herring gulls had no statistically significant effect on the differences in the concentrations of the studied contaminants (Table 1). A statistically significant effect of sex on varying concentrations of β-HBCD was manifested only in the liver of immature herring gulls (p =0.014). In addition, in this age group, the highest concentrations of the ΣHBCD product and of the α-HBCD isomer were found in females (Table 1). The student’s t-test showed significant differences in the concentrations of HBCD (p = 0.0005) and α-HBCD (p = 0.005) between the muscles and the liver of immature birds.

The HBCD selective hepatic sequestration ratio calculated as the concentration of the assayed parameters in the liver to the concentration in muscles was determined in herring gulls in both sexually mature and immature individuals of both sexes. The highest sequestration rate was found for the α-HBCD isomer in adult and sexually immature males (mean = 7.75 ± 13.70 and mean = 6.18 ± 11.95, respectively), while the lowest in females (Fig. 1).

Figure 1

The presence of HBCD in the environment is closely related to anthropogenic activity as it has been used on a significant scale throughout Europe (Remberger et al. 2004). It enters the sea with industrial wastewater and via atmospheric deposition (Schure et al. 2004; Covaci et al. 2006; Feng et al. 2012) and its presence has been confirmed by studies of bottom sediments of rivers entering the Baltic Sea (Sellström et al. 1998). HBCD was found in red algae (Ceramium tenuicorne) and in blue mussels (Mytilus edulis) from the Baltic Sea (Malmvärn et al. 2005; Bignert et al. 2011). Bignert et al. (2011) indicated temporal and spatial changes in HBCD concentrations in herring (Clupea harengus) and blue mussels, with a general conclusion on decreasing trends in fish. Janák et al. (2008) reported HBCD in herring at the level of 26 ng g⁻¹ l.w., while the average concentration in herring caught from the southern Baltic Proper was 30 ng g⁻¹ l.w. (Korpinen et al. 2010). Remberger et al. (2004) found HBCD (10–20 ng g⁻¹ l.w.) in muscles of herring caught in 2001 in the Gulf of Bothnia. Reindl and Falkowska (2015) reported a relatively low HBCD concentration in muscles of herring caught in the southern Baltic Sea in 2009–2010 (average: 11.68 ± 4.32 ng g⁻¹ l.w.). The same study carried out on penguins from the Gdansk Zoo, feeding on fish from the southern Baltic, showed the presence of ΣHBCD in penguin muscles at the level of 79.9 ± 15.8 ng g⁻¹ l.w. and indicated the diet as the main route of exposure to environmental pollution. The contamination of penguin bodies was similar to other reports on Baltic birds. The concentration of ΣHBCD detected in the muscles of common guillemots (Uria aalge) from a colony on Gotland in the Baltic Sea was at the level of 64.7 ng g⁻¹ l.w. (Lundstedt-Enkel et al. 2006). The present study indicates that the contamination of herring gull muscles with ΣHBCD is at a significantly lower level (42.82 ng g⁻¹ l.w.) than that indicated by previous studies. This shows a significant effect of diet on bird muscle contamination and may also suggest a decreasing trend for these contaminants in the Baltic Sea environment.

This research complements the current knowledge about the HBCD concentration in birds from the Laridae family inhabiting the southern Baltic coastal area (Table 2). Studies of the muscles and livers of the herring gull prove the presence of HBCD assayed as a mixture of isomers of the technical product, as well as the three main isomers of its composition (α-, β- and γ-HBCD), of which the α-HBCD isomer was predominant. Seagulls from the southern Baltic coastal area supplement their marine diet with anthropogenic food (Meissner & Betleja 2007; Szumiło-Pilarska et al. 2017), which would indicate that the diet of marine origin is richer in HBCD than the food available in landfills. The reason for such findings may be the possibility of HBCD accumulation in the trophic chain. HBCD enters the Baltic Sea with sewage and as a result of wet and dry deposition of pollutants emitted into the air. These pollutants are partially accumulated in the sediment and, as a dissolved form, accumulate in fish that are part of seagulls’ diet.

With the exception of the Baltic Sea region, HBCD has been found in birds’ organs worldwide and the results of studies concerning HBCD concentrations in muscles of aquatic birds (Table 2) from regions with varying degrees of contamination indicate the influence of feeding habits and trophic position on contaminant burdens. The highest levels of HBCD were found in the muscles of large birds of prey, such as the sparrowhawk (Accipiter nisus) from the UK (de Boer et al. 2003). Concentrations of ΣHBCD in the Chinese pond heron (Ardeola bacchus) periodically inhabiting an electronic waste recycling area in the Pearl River delta in China were in a wide range from 460.0 to 5058.0 ng g⁻¹ l.w., with the predominance of the α-HBCD isomer (He et al. 2010). The study of the glaucous gull (Larus hyperboreus) from Bjørnøya in the Barents Sea indicated the presence of the α-HBCD isomer in the liver of birds at a low level of 1.1±4.3 ng g⁻¹ l.w. (Sagerup et al. 2009), while livers of cormorants (Phalacrocoracidae) from the British Isles contained 796–1200 ng g⁻¹ l.w. (de Boer et al. 2003).

The carbon stable isotopes (δ¹³C reflecting the feeding habitat) and nitrogen (δ¹5N reflecting the trophic level) detected in the muscles of the herring gull increases with the trophic position (Fig. 2). This confirms the influence of food sources from at least two trophic levels on ΣHBCD and α-HBCD concentrations in bird muscles (ΣHBCD = 13.15 δ¹⁵N–94.31, r = 0.59, p = 0.05; α-HBCD = 15.11 δ¹⁵N–119.31, r=0.76, p=0.006). In the liver of gulls, the effect of the stable isotope ratio on the concentration of hexabromocyclododecane was not statistically significant. Other researchers report a similar finding (de Boer et al. 2003; He et al. 2010).

Figure 2

The bird’s liver plays an important role in the processes of detoxification, redistribution and transformation of xenobiotics due to its ability to accumulate large amounts of external impurities (Braune & Norstrom 1989; Kubota et al. 2013; Abdallach et al. 2014). In three quarters of the examined gulls, the obtained results indicate a higher HBCD burden on the liver than on the muscle tissue (Fig. 1). It is likely that chronic exposure contributes to the selective accumulation of xenobiotics in the liver. The β-HBCD isomer in mature and immature males was characterized by the lowest degree of retention in the liver (liver/muscle ratio < 1). This suggests an advantage of elimination over sequestration, for example by deposition in guano, as was the case with penguin feeding on Baltic fish (Reindl & Falkowska 2015), or horn-like formations of epidermis (feathers, claws), as observed in the case of mercury by Grajewska et al. (2019).

A high sequestration factor was found for females, which suggests that lipophilic contaminants can be transferred from the mother’s liver to the eggs during their formation. As reported by Vieira et al. (1995), the liver of birds during egg formation is responsible for lipids included in the egg yolk synthesis. The process of egg formation promotes the transfer of lipophilic pollutants from the liver to the egg, thus burdening the future generation with environmental pollutants (McIndoe 1971). Since xenobiotics are selectively retained in the liver, the transfer to the next generation can also be selective, but the scale of this process should be further researched.

The fact that the effect of sex and age on the HBCD burden in the system of a gull could not be clearly determined is related to its condition and cause of death. Research on dead birds have some limitations and the effect of sex and age may be difficult to assess. It is likely that in emaciated, starved birds, part of HBCD in the muscles and liver was mobilized into the bloodstream due to a hungry body catabolizing its own tissues. The problem of birds’ condition, related to the condition of their organisms and the level of xenobiotics in their tissues, has been discussed by scientists (Kalisinska et al. 2010; Mallory & Braune 2018). This issue requires further research, as there are no clear opinions, especially in the case of wild organisms.

Herring gulls inhabit the southern Baltic coastal area in quite large numbers, mostly leading a sedentary existence. The abundance of marine and anthropogenic food in the regional environment resulted in a very wide range of concentrations of HBCD and its isomers in the liver and muscles of omnivorous birds. Due to the direct connection between the organism and the environment, these birds can be an excellent indicator of pollution with bromo-organic compounds and serve as an early ecotoxicological warning.

The research conducted on the group of herring gulls from the southern Baltic coast indicated a lower HBCD burden on their organisms than in other birds whose main food is of marine origin.

The authors of the study believe that it is necessary to continue the research along with hepatic sequestration, which affects the level of internal transfer of xenobiotics from the bird’s liver to eggs and determines their transfer to the next generation.