⁹⁰Sr in Zostera marina from the Gulf of Gdańsk (southern Baltic Sea)

The Baltic Sea is one of the most polluted marine areas with radioactive isotope ⁹⁰Sr. Nuclear weapons testing in the atmosphere, carried out in the 1950s and 1960s, were the main source of ⁹⁰Sr in the marine environment (HELCOM 2013). At present, the major input pathways changed into surface run-off and atmospheric fallout (Saniewski, Zalewska 2016). Because of a relatively long half-life of 28.8 years and chemical similarity to calcium, ⁹⁰Sr is considered one of the most dangerous radioactive isotopes of anthropogenic origin (Kryshev 2006). Despite the fact that ⁹⁰Sr is currently becoming the most important element in the radioactivity field of the Baltic Sea (Saniewski, Zalewska 2016), information on its distribution in various elements of the marine environment is scarce. It is, however, well established that ⁹⁰Sr is bioaccumulated by marine flora and fauna (Solecki, Chibowski 2002; Zheleznov et al. 2002; Outola et al. 2009; Starichenko 2011).

This article presents an attempt to investigate the bioaccumulation efficiency of ⁹⁰Sr in the eelgrass (Zostera marina) tissues. Zostera marina is a common vascular plant in the southern Baltic Sea region (Kruk-Dowgiałło 1998; Pliński, Jóźwiak 2004). It occurs in large number also in other seas, e.g. the North Sea and along the Atlantic from the northern Norwegian coasts down to Spain (Barum et al. 2004). Interestingly, the plant plays the role of an environmental engineer – seagrasses provide a substrate for the attachment of epiphytic organisms, stabilize the sediment and facilitate the process of organic matter accumulation in the sediment. As a result they form a habitat for a large set of organisms (Gacia et al. 2003; Barum et al. 2004; Bouma et al. 2005). The abundance and diversity of the fauna and flora living in seagrass meadows are consistently higher than those of adjacent unvegetated areas. A number of animals feed on Zostera marina – from invertebrates to mute swan and mallard (Barum et al. 2004). It is estimated that in the previous century, the global loss of seagrass from the direct and indirect human impact amounted to 18% of the documented bottom area covered with seagrass (Barum et al. 2004). In 1957-1988, dense seagrass meadows in the Puck Lagoon (the southern Baltic Sea) were nearly completely replaced by other vascular plants e.g. Zanichellia palustris and filamentous brown algae species like Pylaiella litoralis and Ectocarpus siliculosus (Kruk-Dowgiallo 1991). Currently, a growing tendency of eelgrass recovery is observed and its expanding distribution at many sites in the Gulf of Gdańsk (Jankowska et al. 2014).

Taking into account the ecological importance of Zostera marina for the functioning of the Gulf of Gdańsk ecosystem and relatively high concentrations of ⁹⁰Sr in the marine environment of the southern Baltic Sea, the study was conducted with the objective to determine the radioactivity concentration of this isotope in the eelgrass, with a special focus on its distribution in various parts of the plant, like roots and blades, as well as to determine spatial and temporal differences in ⁹⁰Sr content in plant tissues.

In the period of 2008-2012, the mean concentration activity of ⁹⁰Sr in Z. marina from Jama Kuźnicka reached 1.69 Bq kg⁻¹ d.w. in the whole plant (blades and root). The minimum activity of 0.83 Bq kg⁻¹ d.w. was measured in June 2010, while the maximum activity of 3.78 Bq kg⁻¹ d.w. was recorded in September of the same year (Fig. 2).

Figure 2

In the Klif Orłowski area, the mean ⁹⁰Sr activity concentration was slightly higher and reached 2.40 Bq kg⁻¹ d.w., however, the overall range of activity concentrations was nearly twice as high compared to plants from Jama Kuźnicka; this difference was not statistically significant (test U-W, p = 0.34). In the Klif Orłowski area, the minimum concentration activity of ⁹⁰Sr, 0.68 Bq kg⁻¹ d.w. in the whole plant, was measured in September 2008, and the maximum one – 4.95 Bq kg⁻¹ d.w. – in June 2010 (Fig. 2). The levels of radioactive activities of ⁹⁰Sr in Z. marina at both sampling locations were somewhat lower or comparable to those observed in other vascular plants from the Gulf of Gdańsk, e.g. Potamogeton sp. – 4.56 Bq kg⁻¹d.w. in June and 6.27 Bq kg⁻¹ d.w. in September, Zannichellia palustris – 3.92 Bq kg⁻¹ d.w. (September) (Zalewska 2015). Analogically, the mean ⁹⁰Sr concentrations in Z. marina were not significantly different compared to the concentrations observed in macroalgae species growing in the same areas, e.g. the mean value (range) – Ectocarpus siliculosus – 3.67 Bq kg⁻¹ d.w. (2.02 Bq kg⁻¹d.w. – 8.71 Bq kg⁻¹ d.w.), Furcellaria lumbricalis – 2.76 Bq kg⁻¹ d.w. (0.62 Bq kg⁻¹ d.w. – 5.93 Bq kg⁻¹ d.w.), Polysiphonia fucoides 3.66 Bq kg⁻¹ d.w. (0.81 Bq kg⁻¹ d.w. – 15.24 Bq kg⁻¹ d.w.) and Cladophora glomerata 1.36 Bq kg⁻¹ d.w. (0.36 Bq kg⁻¹ d.w. – 2.61 Bq kg⁻¹ d.w.) (Zalewska 2015).

⁹⁰Sr activity concentrations in Z. marina showed a statistically significant correlation (r = 0.63, p = 0.009) with the isotope content in seawater in the study period, despite the data pool being not very abundant (n = 16). Higher activity concentrations of ⁹⁰Sr in Z. marina measured in 2010 are most probably related to the enhanced strontium activity in surface water of the Gulf of Gdańsk, reaching 8.3 mBq dm⁻³ as compared to 6.4 mBq dm⁻³ – a mean in the other years of the study period.

Salinity is considered another important factor in ⁹⁰Sr bioaccumulation in Z. marina. Despite the meagre data set (n=16), a statistically significant correlation was determined between ⁹⁰Sr activity concentrations in the whole Z. marina plant and salinity: r = - 0.56, p < 0.02.

The inverse proportionality seems to result directly from the concentrations of Ca²⁺ cations, amounting to ca. 1.2% of the total ion mass in seawater. Although Sr is apparently not a plant micronutrient, it is absorbed following the plant’s metabolic requirements for Ca. Interactions between Sr and Ca are complex, and the elements can compete with each other. Multiple experiments demonstrated strong antagonistic interactions between ⁹⁰Sr bioaccumulation and calcium ions concentration in water (Kabata-Pendias, Pendias 2001; Kabata-Pendias, Mukherjee 2007; Smith et al. 2009), supporting the assumption that a salinity increase results in the decline of strontium phytoavailability.

In 2011 and 2013, ⁹⁰Sr activity was determined in particular parts of Z. marina: in blades and roots. The highest activities of ⁹⁰Sr were determined in eelgrass roots collected in June of both years (Fig. 3) – they amounted to 7.75 Bq kg⁻¹ d.w. and 11.44 Bq kg⁻¹ d.w., respectively. The minimum concentration of 1.09 Bq kg⁻¹ d.w. in Z. marina roots was measured in October 2011.

Figure 3

As regards the eelgrass leaves, the lowest activity concentration, i.e. 0.68 Bq kg⁻¹ d.w., was recorded in October 2011. On the other hand, the maximum activity (3.77 Bq kg⁻¹) was measured at the beginning of December 2011. In vascular plants, assimilation of nutrients is accomplished via the root system as well as via leaves (Barum et al. 2004). However, it is assumed that nutrient uptake by roots prevails over the uptake by leaves (Carignan, Kalff 1980). Taking into account the main transport route of nutrients assimilated from the aquatic environment and the huge difference between ⁹⁰Sr concentrations in seawater (6.4 mBq dm⁻³) and in the substrate [sand] (376 mBq kg⁻¹ d.w.) where the root system is fixed, root uptake may be regarded as the main reason for higher strontium concentrations in the roots than in the Z. marina blades. It should be emphasized, however, that such considerable differences were found in June, i.e. they can be related also to the plant seasonal development cycle. In spring and summer, metabolic and growth processes in plants reach the peak intensity, hence the efficiency of nutrient assimilation from the surrounding aquatic environment and the accumulation in plant tissues intensify as well. Already in July, the mean ⁹⁰Sr activity in the eelgrass roots decreased to only 1.58 Bq kg⁻¹ d.w. It is highly likely that the observed decrease was caused by transport both macroelements and metals to newly developed plant tissues. In summer, ⁹⁰Sr decreased also in blades – to 2.49 Bq kg⁻¹ d.w. in July and even 0.96 Bq kg⁻¹ d.w. in August. Consequently, ⁹⁰Sr concentration in eelgrass leaves increased from October to December. A similar observation was made for ¹³⁷Cs bioaccumulation in the whole Z. marina plant (Zalewska 2015). The observed final result of the bioaccumulation efficiency is a result of a number of processes, frequently of opposite directions. In summer, the increase in the bioaccumulation rate results from the intensified life processes – the plant biomass increases, and this may cause the so-called dilution effect, manifested as a decrease in the element’s concentration in plant tissues. In autumn, when the plant metabolism is still intense, the biomass declines and this may result in the concentration increase (Zalewska 2015).

Despite the fact that ⁹⁰Sr activities in eelgrass leaves are lower than in the roots, their specific concentration coefficient (CF = concentration in tissue/concentration in water) reached 200 and was much higher than in the roots (CF = 10). This observation proves that the transfer of the isotope occurs from the roots to plant leaves.

The mean activity concentrations of ⁹⁰Sr in the whole Z. marina plant were 1.69 Bq kg⁻¹ d.w. in Jama Kuźnicka and 2.40 Bq kg⁻¹ d.w. in Klif Orłowski. The measured activities were lower or similar to activity levels observed in other vascular plants and macroalgae occurring in the Gulf of Gdańsk in the study period (2008-2013).

⁹⁰Sr concentrations in Z. marina tissues are affected by the element’s availability in the plant habitat

(seawater, interstitial water of the substrate), as well as the plant physiological activity (metabolism, growth processes) closely related to the sampling season and external conditions. Bioaccumulation efficiency of Z. marina can be affected by salinity and inherent change in Ca²⁺ concentration, as calcium is the natural analogue of strontium.

The maximum activities of radioactive ⁹⁰Sr isotope were recorded in eelgrass roots in spring time. In summer, strontium activity in plant roots significantly decreased, probably due to the transportation of macroelements to the newly developed shoots.

The maximum concentrations of ⁹⁰Sr in the blades of Z. marina were measured in late autumn and winter, probably because of the plant biomass reduction and the concentration effect. In summer, due to the biomass increase, ⁹⁰Sr activity in eelgrass leaves decreased as a result of the dilution effect.