Linking trace element variations with macronutrients and major cations in marine mussels Mytilus edulis and Perna viridis (original) (raw)

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Division of Life ScienceThe Hong Kong University of Science and Technology Clearwater Bay, Kowloon Hong Kong China

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04 February 2015

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18 March 2015

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Fengjie Liu, Wen‐Xiong Wang, Linking trace element variations with macronutrients and major cations in marine mussels Mytilus edulis and Perna viridis, Environmental Toxicology and Chemistry, Volume 34, Issue 9, 1 September 2015, Pages 2041–2050, https://doi.org/10.1002/etc.3027
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Abstract

Marine mussels have long been used as biomonitors of contamination of trace elements, but little is known about whether variation in tissue trace elements is significantly associated with those of macronutrients and major cations. The authors examined the variability of macronutrients and major cations and their potential relationships with bioaccumulation of trace elements. The authors analyzed the concentrations of macronutrients (C, N, P, S), major cations (Na, Mg, K, Ca), and trace elements (Al, V, Mn, Fe, Co, Ni, Cu, Zn, As, Se, Mo, Cd, Ba, Pb) in the whole soft tissues of marine mussels Mytilus edulis and Perna viridis collected globally from 21 sites. The results showed that 12% to 84% of the variances in the trace elements was associated with major cations, and the tissue concentration of major cations such as Na and Mg in mussels was a good proxy for ambient seawater concentrations of the major cations. Specifically, bioaccumulation of most of the trace elements was significantly associated with major cations, and the relationships of major cations with trace cations and trace oxyanions were totally opposite. Furthermore, 14% to 69% of the variances in the trace elements were significantly associated with macronutrients. Notably, more than half of the variance in the tissue concentrations of As, Cd, V, Ba, and Pb was explained by the variance in macronutrients in one or both species. Because the tissue macronutrient concentrations were strongly associated with animal growth and reproduction, the observed coupling relationships indicated that these biological processes strongly influenced the bioaccumulation of some trace elements. The present study indicated that simultaneous quantification of macronutrients and major cations with trace elements can improve the interpretation of biomonitoring data. Environ Toxicol Chem 2015;34:2041–2050. © 2015 SETAC

INTRODUCTION

Mussel Watch Programs are designed to monitor the status and trend of contamination of metals and other contaminants in regional or national coastal water settings, and the programs are based on the analysis of tissue concentrations of contaminants in soft tissues of bivalves [1, 2]. Marine mussels, such as the common mussel Mytilus edulis and the green mussel Perna viridis, are frequently employed in regional or international biomonitoring programs [1, 3]. Mussels take up trace metals from water and suspended particles. Interpretation of tissue metal concentration requires consideration of many biological and environmental factors, such as animal size, reproductive cycle, age, salinity, temperature, and season [3]. These documented and other unknown factors make direct comparisons of metal bioavailability in time and space difficult. No strategy or method corrects the integrated bias of these factors.

Marine mussels live over a wide range of salinity, and salinity should be taken into account when interpreting metal bioavailability from samples collected from different sites or times. Specifically, salinity can directly affect the speciation and bioavailability of some trace elements in ambient seawaters and subsequently affect their bioaccumulation [4, 5, 6]. Meanwhile, salinity variation can cause ecophysiological changes (e.g., apparent water permeability, feeding physiology, and growth) in the animals and subsequently affect bioaccumulation of trace elements [7, 8]. Little is known, however, about combined effects of salinity‐induced speciation and ecophysiological changes, as well as their relative contribution to trace element bioaccumulation. Marine mussels are well‐known osmoconformers, and the internal concentrations of major cations such as Na and Mg vary linearly with external salinity [9, 10, 11]. The tissue concentration of the cations in mussels should be a good proxy for ambient seawater salinity. Therefore, we hypothesize that one way to quantify the integrated effects of salinity (i.e., a combined effect of chemical speciation and animal ecophysiology) on trace metals bioaccumulation is to analyze the relationships between major cations and trace elements in mussel tissues.

Similar to salinity, macronutrients such as C, N, and P vary temporally and spatially in seawaters, and significant variation in their concentrations in organisms may be associated with some aspects of animal physiology (e.g., trace metal bioaccumulation, growth rate, and reproduction) [12, 13, 14]. That biogeochemical cycling of macronutrients is closely related to that of trace metals such as Zn/Cd/Co and C, Mo and N, and Cd and P in a diverse array of microorganisms is well documented [15, 16, 17, 18]. Significance of macronutrients (e.g., N, P, and Si) in the accumulation kinetics of several trace elements (e.g., Zn, Cd, Cr, and Se) by marine phytoplankton and their subsequent transfer along marine food webs are also documented [19, 20, 21]. Whether macronutrients are significantly associated with trace element bioaccumulation by marine mussels remains unclear. In other words, knowing whether macronutrient variation in biomonitors should be taken into account when interpreting the tissue concentration of trace elements is of significance.

In the present study, mussel samples collected from 21 sites worldwide were analyzed 1) to quantify the variability of macronutrients (C, N, P, S), major cations (Na, Mg, K, Ca), and trace elements (Al, V, Mn, Fe, Co, Ni, Cu, Zn, As, Se, Mo, Cd, Ba, Pb) in 2 representative marine mussels, M. edulis and P. viridis; 2) to examine the magnitude of possible associations of macronutrients and major cations with trace elements; and 3) to identify trace elements that are sensitive to variation in macronutrients or major cations. The 2 species are distributed widely in coastal waters all over the world. Specifically, M. edulis is mainly found in coasts of the North Atlantic (including the Mediterranean) and of the North Pacific in temperate to polar waters, as well as in coasts of similar conditions in the Southern Hemisphere, whereas P. viridis occupies the coastal waters of the Indo‐Pacific region. The results of the present study will be relevant to the data interpretation of biomonitoring programs including other biomonitors and the understanding of trace element bioaccumulation by marine mussels.

MATERIALS AND METHODS

Mussel collection

We analyzed mussel samples from 2 species of marine mussels (M. edulis and P. viridis) collected from 21 sites from 8 countries or regions (Table 1). Marine mussels other than the 2 species from 6 more countries or regions were also analyzed but not reported in the present study, simply because of difficulty in species identification and limited replicates. The hydrology, chemistry, climate, and contamination history of these sites are given in the references listed in Table 1. For a given site, 8 individuals of similar size were selected; however, the Scotland samples were pooled samples of 2 to 6 replicated pools for each site (each pool had 25 homogenized individuals). After collection, mussels were depurated for 2 d in nearby laboratories before elemental analyses. Mussels were rinsed with distilled, deionized water, and whole soft tissues were removed with plastic forceps and rinsed with Milli‐Q water. Finally, individual tissues were freeze‐dried at –80 °C, weighed, homogenized, and then shipped to the Coastal Marine Laboratory of The Hong Kong University of Science and Technology. Alternatively, the fresh mussel samples were shipped on dry ice to the Coastal Marine Laboratory and then freeze‐dried for further elemental analyses [22].

Table 1.

General information on sampling locations and marine musselsa

a

Data for shell length and dry weight of soft tissue are mean ± standard deviation (See Materials and Methods for sample size). See reference in last column for local water quality of the sampling sites.

NA = not available.

Table 1.

General information on sampling locations and marine musselsa

a

Data for shell length and dry weight of soft tissue are mean ± standard deviation (See Materials and Methods for sample size). See reference in last column for local water quality of the sampling sites.

NA = not available.

Elemental analyses

Subsamples of the freeze‐dried homogenates were microwave digested in Teflon vials (speedwavefour, BERGHOF) with trace metal grade 70% HNO3 (Fisher Scientific), and subsequently the digests were diluted to appropriate concentration ranges with a 1% HNO3 solution. All elements except C, N, and S were determined by inductively coupled plasma–mass spectrometry (Agilent 7700x). Briefly, the instrument was calibrated using multi‐element standard solutions (Agilent) and a P solution, and internal standardization was also performed by addition of the Internal Standard Mix solution (Part# 5183‐4681; Agilent) to account for instrument drift and change in sensitivity. One of the diluted external standards was reanalyzed after every 20 samples, and deviations from the reference value were less than 10%. Analyses of 2 bivalve reference materials (i.e., mussel tissue‐SRM® 2976 and oyster tissue‐SRM® 1566b) gave acceptable recoveries (Supplemental Data, Table S1). The levels of the detection limit for the elements were generally several orders of magnitude lower than those determined in the samples. Total element concentrations were normalized by dry weight of soft tissue.

To determine tissue concentrations of macronutrients (i.e., C, N, and S), subsamples of homogenized tissues were placed into preweighed tin capsules (Elemental Microanalysis, UK), weighed, and analyzed using a CHNS Analyzer (Series II 2400, PerkinElmer). The recovery percentage from the standard (Cystine, N241‐0324, PerkinElmer) ranged from 100% to 102% (Supplemental Data, Table S1).

Statistical analyses

The software SPSS (Ver 16.0) and SigmaPlot 12.5 for Windows were used for data analyses. Data of individual and pooled samples were computed, and the significance level was set at p < 0.05 unless otherwise specified.

First, the interrelationships among macronutrients and major cations were analyzed by linear and exponential regression models (SigmaPlot). Second, the difference in stoichiometry between marine mussel and marine plankton (i.e., the Redfield ratio C:N:P:S = 106:16:1:1.7) was compared by 1‐sample t test (SPSS). Third, multiple regression analysis (SPSS) was used to relate the tissue concentration of trace elements in marine mussels to macronutrients or major cations. Specifically, the “forced entry” method was used to test the hypothesis, and the test made no decision about the order in which variables were entered [23]. The tested hypothesis was that macronutrients (or major cations) correlate with trace elements. Roles of macronutrients and major cations in the variations of trace elements were separately analyzed simply because of their distinguished biology functions and chemical behaviors. However, complicated correlations exist between macronutrients and major cations, and they share part of their variation in explaining trace element variance. Only tissue concentrations of Na, K, and Ca were used to relate the tissue concentration of trace elements to major cations, because Na linearly varied with Mg. Multiple regression results showed that the values of variance inflation factor were all well below 6, and the tolerance statistics were all above 0.2. The Durbin‐Watson statistic indicated that the assumption of independent errors was met as well (i.e., 1 < Durbin‐Watson < 3).

Finally, further partial correlation coefficients (i.e., controlling for tissue weight) were also calculated to show the correlations between each of the macronutrients or major cations and each trace element in each mussel species (2‐tailed test) [23]. Tissue element concentration of all samples was computed, although the data of tissue weight of the Scotland samples are not available.

RESULTS

Concentration and variation of major cations

The measured concentrations of major cations (Na, Mg, K, and Ca) in M. edulis and P. viridis are presented in Figure 1 and Supplemental Data, Table S1. The tissue concentrations of major cations varied among the sampling sites, with factors of 13.0, 5.6, 11.9, and 16.4, respectively. Tissue concentrations of Na, K, and Ca ranged over more than 1 order of magnitude; tissue Mg was least variable among the cations.

Figure 1.

Tissue concentrations of macronutrients and major cations (percentage dry wt) in marine mussels. The data are mean ± standard deviation.

The concentrations of Na and Mg linearly covaried in the mussels (Figure 2), and the mass ratio of tissue Mg to Na was 0.11. The concentration of tissue K also linearly covaried with that of tissue Na/Mg when tissue Na concentration was less than 6% (or Mg < 1%; Figure 2). The tissue K reached a plateau when the tissue Na was higher than 6% (or Mg > 1%). Alternatively, the relationship between K and Na/Mg was well fitted by an exponential regression model (Figure 2). No significant relationship was seen between tissue Ca and tissue Na in marine mussels (data not shown).

Figure 2.

Correlations of tissue concentrations of macronutrients and major cations (percentage dry wt) in marine mussels. Each dot represents 1 replicate, and only significant correlations are shown (p < 0.05, n = 133 or 135).

Concentration and variation of macronutrients

The measured concentrations of macronutrients (i.e., C, N, P, and S) in M. edulis and P. viridis are also presented in Figure 1 and Supplemental Data, Table S1. The concentrations of tissue C, N, P, and S varied among the sampling locations, but with small differences, by factors of 1.5, 1.8, 2.0, and 2.3, respectively (Figure 1).

Tissue concentrations of N, P, and S were more variable than that of C, and the concentrations ranged from 8.4% to 15.3%, from 0.7% to 1.4%, and from 1.1% to 2.5%, respectively. Interrelationships among C, N, and S were significant (Figure 2), and tissue C/N/S concentration also was correlated with tissue concentration of Na (Figure 2). Macronutrient stoichiometry of M. edulis or P. viridis was significantly different from that of its diet (i.e., the Redfield ratio; Figure 3).

Figure 3.

Stoichiometry of tissue concentrations of macronutrients (molar ratio) in marine mussels Mytilus edulis and Perna viridis. The data are mean ± standard deviation (n = 87 and 46, respectively). *Significant differences in stoichiometry between each mussel species and the Redfield ratio of plankton (p < 0.05).

Concentration and variation of trace elements

The measured concentrations of 14 trace elements in M. edulis and P. viridis are presented in Figure 4 and Supplemental Data, Table S1. The abundance of trace elements in the mussels were highest for Fe, Al, Zn, and Mn at the average levels of 40 μg/g to 420 μg/g, intermediate for Ni, Cu, and As at the average levels of 5 μg/g to 12 μg/g, and lowest for V, Co, Se, Mo, Cd, Ba, and Pb at the average levels of 1 μg/g to 4 μg/g, on a dry weight basis.

Figure 4.

Tissue concentrations of trace elements (microgram per gram dry wt) in marine mussels. The data are mean ± standard deviation.

The variability in the tissue concentrations of the elements was element specific; variation was lowest in V, Co, Cu, Zn, As, Se, and Mo, with factors of 2.4 to 7.5; intermediate in Mn, Fe, Cd, and Pb, with factors of 20 to 25; and highest in Al, Ni, and Ba, with factors of 43 to 128.

Correlations of trace elements with major cations

Of the variances in trace elements, 12% to 84% were associated with major cations, and the magnitude of the associations depended on species and metals (Table 2). In the mussel M. edulis, for all of the 14 trace elements except Ni, Cu, and Cd, regression against all of the 4 major cations was significant, explaining between 12% and 42% of the spatial variation in trace elements. Specifically, more than a third of the variance in tissue As, Se, and Mo was a consequence of the variation in major cations, and most of the explained variance was attributable to Na or Mg. Significantly positive relationships between As and Na/Mg were observed in both M. edulis and P. viridis.

Table 2.

Multiple and partial correlation coefficients for regression of trace element concentration against major cation concentration in marine musselsa

a

See Materials and Methods for statistics.

b

Values of R or R2 are only shown for those of p < 0.05, and absolute values of _p_ > 0.05 are ≤0.20.

Table 2.

Multiple and partial correlation coefficients for regression of trace element concentration against major cation concentration in marine musselsa

a

See Materials and Methods for statistics.

b

Values of R or R2 are only shown for those of p < 0.05, and absolute values of _p_ > 0.05 are ≤0.20.

In the mussel P. viridis, for all of the 14 trace elements except for Mo, regression against all of the 4 cations was significant, explaining between 20% and 84% of the variance. Notably, more than 50% of the variance in tissue As and Ba was associated with major cations. In contrast to As, tissue concentration of Se was negatively correlated with Na/Mg and Ca in P. viridis. Tissue concentration of Cd was negatively correlated with major cations, and the partial correlation coefficients indicated that Ca was the only significant variable affecting tissue concentration of Cd.

Negative relationships between major cations and most of the positively charged trace metals (i.e., Al, Mn, Fe, Co, Cu, Zn, Cd, and Ba) were observed in the mussel P. viridis. In M. edulis, only 3 of the positively charged metals (Al, Mn, and Ba) were negatively correlated with major cations. Conversely, positive relationships between major cations and trace oxyanions (As, Se, and Mo) were observed in M. edulis, and so were As and V in P. viridis.

Correlations of trace elements with macronutrients

Multiple regression analyses indicated that a significant portion (14–69%) of the variances in tissue trace element concentration was associated with the tissue concentrations of macronutrients, and the magnitude of the associations depended on species and metals (Table 3).

Table 3.

Multiple and partial correlation coefficients for regression of trace element concentration against macronutrient concentration in marine musselsa

a

See Materials and Methods for statistics.

b

Values of R or R2 are only shown for those of p < 0.05, and absolute values of _p_ > 0.05 are ≤0.20.

Table 3.

Multiple and partial correlation coefficients for regression of trace element concentration against macronutrient concentration in marine musselsa

a

See Materials and Methods for statistics.

b

Values of R or R2 are only shown for those of p < 0.05, and absolute values of _p_ > 0.05 are ≤0.20.

In the mussel M. edulis, for all of the 14 trace elements except Pb, regression against all 4 macronutrients was significant, explaining between 14% and 59% of the variance (Table 3). Specifically, more than 50% of the variance in tissue As and Cd was associated with tissue macronutrients, as was approximately one‐third of the variance in tissue Mn, Ni, Cu, and Ba and 14% to 25% of the variance in tissue Al, V, Fe, Co, Zn, Se, and Mo. Inspection of the partial correlation coefficients within each trace element provided insight to the relative importance of C, N, P, and S on the observed intersite differences of trace elements. For As, most of the explained variance was attributable to C and S, but the 2 macronutrients had contrasting roles. A negative partial correlation coefficient was obtained for C with As, whereas a positive partial correlation coefficient was obtained for S with As. Conversely, variation in Cd was related to the variations in N and C and to a lesser extent P.

In the mussel P. viridis, for all 14 trace elements, 33% to 69% of the variance was significantly associated with tissue macronutrient concentration (Table 3). Specifically, more than 50% of the variance in tissue concentrations of V, As, Ba, and Pb was explained by macronutrient variation, and so was 33% to 47% of the variance in tissue concentrations of the other 10 elements. For V and As, the 2 elements were negatively correlated with C, N, and P but positively correlated with S. Barium was negatively correlated with S but positively correlated with C and N, and Pb was positively correlated with S. Moreover, a positive relationship between Se and S was observed in M. edulis, and their relationship in P. viridis was not significant.

DISCUSSION

Linking trace element variations with major cations

Little is known about the quantitative relationship between salinity and trace elements in marine biomonitors, although salinity is well documented for its significant role in bioaccumulation of several trace metals [3, 5]. Tissue concentration of major cations in mussels is a well‐known proxy for seawater salinity [9, 10, 11], which is further confirmed by the covariation of Na and Mg in mussels and their similar mass ratio with seawater (seawater Mg/Na = 0.12 [24]) in the present study. In waters with dramatically fluctuating salinity, tissue concentration of major cations may or may not be a good proxy of ambient salinity because of their unknown relationships in mussels. However, it should be a good proxy for ambient salinity for mussels living in waters of a relatively constant salinity. The present study quantitatively documented significant coupling relationships between trace element bioaccumulation and salinity.

Negative relationships between most trace cations (i.e., Al, Mn, Fe, Co, Cu, Zn, Cd, and Ba) and major cations were observed in the mussel P. viridis. Consistent with the present study, the negative relationships between tissue concentration of Cu, Zn, or Cd and salinity are frequently observed in both laboratory‐exposed and field‐collected marine mollusks, including P. viridis [5, 25, 26]. Several explanations are possible for Cu, Zn, and Cd, none of which is mutually exclusive. First, a correlation might occur between freshwater inflow and a freshwater metal source, and thus mussels collected from a relatively low salinity site show relatively high concentrations of the metals. Second, increasing complexation with Cl and competition with major cations at higher salinities reduce the bioavailability of dissolved metals such as Cd and Cu [25, 27]. However, Ca was likely the most important contributor in reducing Cd bioaccumulation by P. viridis (Table 2). Conversely, higher tissue concentration of Zn in mussels collected from lower salinities would not be expected from salinity‐induced Zn speciation changes, because free ion [Zn2+] is relatively constant (∼48%) in salinity ranges from 5 psu to 30 psu [25]. Third, the metal concentrations in the mussels' diets, such as phytoplankton and other particles, may be higher in waters of lower salinities. Finally, influences of salinity on animal gut physiology [26], dietary metal uptake, and metal turnover rate are possible, although little work has been conducted on this aspect.

The present study's results demonstrated for the first time that salinity plays a significant and negative role in the bioaccumulation of Al, Mn, Fe, Co, and Ba in the mussel P. viridis. The results may be similarly explained by the underlying mechanisms for salinity‐induced effects on bioaccumulation of Cd, Cu, and Zn, but the dominant mechanisms for these metals are likely different from those of Cu, Zn, and Cd. For instance, precipitation and removal of Al, Mn, and Fe increased with salinity in estuarine mixing zones [28, 29], and thus both dissolved and dietary sources of the metals are less available to mussels at sites of higher salinities. In case of Ba, the dissolved concentration at low salinity is relatively high because of low‐salinity desorption of particulate Ba [30]; meanwhile, the uptake competition with Ca and Mg should be weak at low salinities. This might partly explain the negative relationship between Ba and salinity in P. viridis.

Another interesting point is the positive relationships between major cations and trace oxyanions (i.e., As, Se, and Mo) in M. edulis, as well as for V in P. viridis. First, arsenobetaine, a dominant form of As in marine animals [31], is considered to be involved in osmotic regulation. The accumulation of arsenobetaine by the mussel Mytilus edulis depended on seawater salinity in a manner leading to higher concentrations at higher salinities [32]. Similarly, in 3 teleost species [33], a positive linear relationship between tissue As concentration and salinity was observed, and the underlying mechanism may be related also to osmoregulation of these animals. Thus, the coupling relationship of As and salinity suggested that tissue concentration of As in these biomonitors was highly dependent on salinity‐dependent osmoregulation other than ambient As concentrations. Second, to our knowledge, no data have been reported on the interactions of Se and salinity. Possibly the bioaccumulation of Se was related to osmotic regulation as well, given that Se was also predominantly presented as organic Se species in mussels [34]. Almost all Se in M. edulis was predicted to be obtained from ingested food [35]; thus, investigating the role of salinity in the dietary uptake of Se will be interesting for a better understanding of the observed positive relationships. Third, little is known about salinity‐induced changes in bioaccumulation of Mo, but the present study's results highlighted a significant coupling relationship in bioaccumulation of Mo and salinity in M. edulis. Finally, salinity also appeared to influence the bioaccumulation of V by P. viridis but not M. edulis. One study showed that salinity played a minor role in the biokinetics of V in Mytilus galloprovincialis [36].

Interspecies differences in salinity‐induced effects on trace metals bioaccumulation were observed between M. edulis and P. viridis. For example, the relationships between major cations and Cu, Zn, and Cd in M. edulis were not as significant as those observed in P. viridis. Interestingly, the relationships between major cations and Se or V were positive in M. edulis but negative in P. viridis. Because the salinity‐induced chemical changes of 1 metal in ambient waters were constant, the salinity‐induced ecophysiological change of 1 mussel species was totally different from that of the other. In the case of Cu, Zn, Cd, Se, and V, species (i.e., biotic factors) may play a more important role in their bioaccumulation than the ambient salinity‐induced chemical changes (i.e., abiotic factors).

Given that salinity is a global regulator of many chemical and biotic processes in estuary and marine waters, the present study has important implications for interpreting data of Mussel Watch Programs. First, bioaccumulation of many trace elements—including the well‐documented Cd, Cu, and Zn—by mussels was indeed significantly associated with seawater salinity, which indicated that salinity certainly should be taken into account when mussels are employed as biomonitors. Second, salinity effects on bioaccumulation of cations and oxyanions of trace elements seem to be totally opposite, although the correlations vary with mussel species and trace elements. Third, salinity‐induced effects on bioaccumulation of some trace elements are highly species specific, and bioavailability of these trace elements is dominantly controlled by animal biology instead of marine chemistry. Overall, quantitative comparisons of salinity‐induced chemical and biological effects on metal bioaccumulation under controlled field or laboratory conditions are necessary to correctly interpret the biomonitoring data.

Linking trace element variations with macronutrients

That many micronutrients (e.g., Zn, Fe, Co, and Mn) are involved in metabolism or biogeochemical cycle of macronutrients by marine phytoplankton is well documented; however, little work is done on their associations in marine invertebrates, including mussels. Unlike major cations, both types of mussels in the present study tightly regulate tissue concentrations of macronutrients, even though macronutrient bioavailability may vary much in ambient waters. In the present study, even though the variations in tissue macronutrients' concentrations were relatively small, some significant correlations were observed between macronutrients and trace element concentrations in marine mussels. The underlying mechanisms can be complicated, but any significant relationship has important implications in understanding the bioaccumulation of trace elements and thus in interpreting data of Mussel Watch Programs.

Among the trace elements, As showed the strongest relationships with macronutrients in both species. Specifically, 59% variation in As concentrations of M. edulis and 69% of that in P. viridis were associated with macronutrients; moreover, most of the explained variance was attributable to C and S. Given that tissue C is a basic element of cells, why an increase in As concentration in the mussels was associated with a decrease in tissue C concentration is unclear. Likely, their relationship partly resulted from tissue Na variation, because tissue Na was strongly correlated with tissue C. Partial correlation analysis indicates that Na plays a more important role in the As variation than C (As vs Na, controlling C, R = 0.29, p < 0.01; As vs C, controlling Na, _R_ = –0.09, _p_ > 0.05). The negative relationship between Na and C also indicated that mussels grown at low salinities might have relatively high concentrations of lipid (i.e., high C concentration), which is an important factor for determining hydrophobic compound accumulation [37]. Conversely, observing that tissue As concentration in the 2 species was highly correlated with its S concentration was very interesting. The results suggested that S played an unknown but significant role in the storage and detoxification of As; at the molecular level, the presence of predominantly As‐S compounds were recently revealed in As‐contaminated M. edulis tissues [38].

Cadmium was sensitive to the variation in tissue macronutrients concentration of M. edulis, and tissue N and P concentrations were positively related to Cd concentration. Their relationships can be partly explained by the size‐dependent N/P concentration and the Cd biokinetics. First, fast‐growing individuals (e.g., sufficient food, warm temperature, and low abiotic stress) generally have relatively high tissue concentrations of N or P [12]. Second, these fast‐growing individuals take up Cd at a relatively high rate in comparison with slow‐growing individuals [39]. Thus, the observed positive relationships between N/P and Cd in M. edulis are reasonable. On the contrary, somatic growth dilution may occur when rapid individual growth causes a disproportional gain in biomass relative to gain of Cd [14]. This explains why no positive relationship between Cd and N/P was observed in P. viridis, a faster‐growing species found predominantly in the Indo‐Pacific region. Overall, the relationship of tissue Cd concentration and growth rate is significant but variable, and tissue N/P concentrations may be used as an indicator of growth‐dependent Cd bioaccumulation. In other words, if significant differences in tissue N/P are found among mussel samples, the growth effect shall be considered in interpreting tissue Cd concentration.

The coupling relationship between Cd and P also indicates that Cd bioaccumulation is likely to be influenced by the sexual or reproduction cycle, because P is a variable element in reproduction. Sexual maturation has been identified as a source of variation in the tissue Cd concentration of M. edulis [40]. Thus, P should be measured when mussels are sampled around their sexual cycle in the Cd‐monitoring programs.

Vanadium also covaried with macronutrients in P. viridis; it is positively correlated with tissue S concentration and negatively correlated with tissue C/N/P concentrations. First, the association between V and S can be explained by the functional link between metallothionein (SH‐rich proteins) induction and V exposure [41]. Second, the negative relationships between N/P and V may point out that growth plays an important role in tissue V concentration. For example, in contaminated seawaters where fossil oils and fuels are dominant sources of V, the growth of mussels under the stress of these anthropogenic pollutants had decreased (i.e., reduced tissue N/P). Consequently, V would have been more concentrated in mussel tissues. Marine mussels have a low capability of V bioaccumulation [36], and tissue concentrations of V in mussels are generally low, with a mean of 1.5 μg g–1 dry weight according to the data of the French Mussel Watch and other studies [41]. In the present study, tissue concentration of V in all mussels on average was 1.7 μg g–1 dry weight, but a part of samples reached up to 3.5 μg g–1 to 4.7 μg g–1, indicating possible oil spills and thus V pollution in these sampling regions [42].

Like other organisms, coupling relationships among elements of similar physicochemical properties may be observed in marine mussels as well, because they are considered to share the same transport systems. In the present study, the negative relationship between As and P was observed in P. viridis, indicating that uptake of As may be inhibited by ambient P. Thus, ambient P bioavailability shall be taken into account when interpreting tissue As concentration of the species. No significant relationship was found, however, between As and P in M. edulis. Besides, a negative relationship was expected between tissue concentration of Se and its chemical analog S [43]. A positive relationship between Se and S was observed in M. edulis, however, and their relationship in P. viridis was not significant. Overall, at present little is known about the possible influences of ambient macronutrients on bioaccumulation of their trace chemical analogs, let alone the underlying mechanisms for these observed relationships in the present study.

Element stoichiometry of marine mussels

Data on elemental composition in mussels beyond several trace elements are very limited, and nearly all biomonitoring programs only focus on several targeted trace elements [44, 45]. The means and ranges of trace elements in the present study are comparable to those reported by World Mussel Watch Programs [44, 45], and the present study covers a few elements other than macronutrients and major cations. The means and ranges of macronutrients are also comparable to those reported by the only available study on C, N, and P [46]; meanwhile, no data are available on tissue concentrations of S and major cations in marine mussels. In addition, our mussel samples approximately cover a salinity ranging from 2.6 psu to 34 psu based on the 13‐fold change in tissue Na and the highest salinity of 34 psu at site 16 [47]. Mussels from regions with higher salinity levels (e.g., the Mediterranean Sea, Arabian Sea, South Atlantic) should be further investigated to get an overall tissue pattern of major cations.

Putting the data of all mussel samples (including unidentified mussel species) together, the average stoichiometry in marine mussels was C129N27P1S1.9Na5.3Mg0.73K0.85Ca0.77 (mol:mol P) for macro elements and Al272V1.2Mn18Fe243Co0.46Ni3.5Cu5.2Zn52As5.5Se1.2Mo0.29Cd0.57Ba0.87Pb0.35 (μmol:mol P) for trace elements. Three interesting points are found by comparing mussels with marine particulate seston (i.e., mussel diet) [48, 49] and seawater in elemental composition. First, the macronutrient stoichiometry of marine mussels was close to those of marine particulate seston (i.e., the Redfield ratio C:N:P:S = 106:16:1:1.7; Supplemental Data, Figure S1), but tissue N:P in mussels is clearly higher than that in marine particulate seston (Figure 3). Second, the stoichiometry of major cations in marine mussels was also similar to those of either marine particulate seston or seawater (Supplemental Data, Figures S1 and S2). Third, the average concentrations of trace elements in mussels were 1 to 2 orders of magnitude lower than those in their diet, but they were 2 to 7 orders of magnitude higher than those in seawater (Supplemental Data, Figures S1 and S2). The elemental pattern not only is relevant to the data interpretation of biomonitoring programs but also improves understanding of the elemental biogeochemical cycling in aquatic ecosystems.

In conclusion, the present study's data show that the variations in trace elements concentration were significantly associated with those macronutrients and major cations, and for the first time many interesting relationships among elements were observed in marine mussels. The significant correlations have important implications in interpretation of mussel biomonitoring data. For instance, osmoregulation of these biomonitors can cause a significant variation in tissue As concentration even when the ambient As concentration is relatively constant. Second, simultaneous measurement of tissue N and P will be useful in improving data interpretation of trace elements, because N and P are well‐documented indicators in animal growth and reproduction, which can strongly affect the bioaccumulation of some trace elements. Third, the variation in S in marine mussels may indicate their enhanced exposure to V and As. Overall, simultaneous quantification of macronutrients and major cations together with monitored trace elements can result in a better data interpretation of Mussel Watch Programs.

SUPPLEMENTAL DATA

Tables S1.

Figures S1–S2. (60KB DOC).

Acknowledgment

We thank A. Jeffs, Y. Chen, F. Dang, E.P. Espinosa, X.Y. Guo, S.G. Jia, M. Sundbom, O. Trottier, P.S. Rainbow, C. Rouleau, M. Russell, B.D. Smith, C. Tan, S.Z. Wang, H.F. Wu, Y. Lind, and W. Zhang for helping collect mussel samples, Q.G. Tan for advice on statistical analyses, and anonymous reviewers for helpful comments. The present study was supported by a Key Project from the National Natural Science Foundation (21237004) and a General Research Fund grant from the Hong Kong Research Grants Council (662813).

Data availability

Data, associated metadata, and calculation tools are available on request to the corresponding author ([email protected]).

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