TEMPORAL TRENDS OF HEAVY METAL CONCENTRATIONS IN BROWN MACROALGAE FROM COASTAL ENVIRONMENTS

Heavy metals are one of the major drivers of ecological changes in coastal ecosystems. Macroalgae are primary producers of great relevance for ecosystem structure and functioning in these environments, and play a key role in the trophic transfer of these contaminants in the food web. Here, we present the most extensive assessment until now (>3500 records) of heavy metal concentrations in brown macroalgae (Class Phaeophyceae) sampled between 1933 and 2020 worldwide. The study compiles this information from 420 peer reviewed articles to be used as a proxy of global long-term changes in metal concentrations. We report the first detailed multi-decadal time series of Cd, Co, Cr, Cu, Fe, Hg, Mn, Pb and Zn in algae using generalized additive models (GAMs), confirming a significant decrease in metal contamination in the world’s coastal environments since ca. the 1970s for Pb (84% reduction), Zn (79%), Cd (77%) and Cu (72%), since the 1980s for Mn (75%) and Hg (65%), and since the 1990s for Cr (66%), Fe (64%) and Co (60%). Important environmental consequences for the whole aquatic ecosystem, even for human health, may be expected from these changes. The present results provide a building block for the overall evaluation of the status and trends of marine metal contamination, and will help researchers and policy makers to promote new legal regulations and environmental goals against pollution

Matching times: Trying to improve the correlation between heavy metal levels in mosses and bulk deposition

The relationship between the concentrations of metals in moss tissues and atmospheric deposition is highly complex, resulting in a general lack of correlations between these two matrices. Here, we tried to improve the significance of the moss-bulk deposition (BD) relationship by eliminating the mismatch between the time that the moss tissue selected for analysis is exposed to atmospheric deposition, and the time during which BD is collected. For this, we analysed the concentrations of Cd, Hg and Pb in new grown tissue of Pseudoscleropodium purum and BD collected monthly, for one year, in 21 sampling sites (SS) under different degrees of pollution. Additionally, we assessed how different moss tissues, including native moss (green parts and new grown tissues of P. purum) and moss transplants of Sphagnum denticulatum, reflect BD to find out which moss tissues provide a better estimate of the atmospheric deposition of heavy metals. First of all, our results showed that eliminating the mismatch between native moss exposure time and BD collection period is not enough to improve their correlation. Environmental variation emerged as the main driver of tissue content variation altering the moss-BD relationship unpredictably. Secondly, native P. purum represents BD values better than devitalized transplants by displaying a greater number of significant correlations with BD. Specifically, green parts of P. purum generally represent better BD than new grown tissues. Overall, we conclude that neither native mosses nor transplants are good estimators of atmospheric heavy metal deposition rates. However, they are good qualitative indicators of the atmospheric deposition, by allowing us to differentiate SS subject to a wide range of pollution levels. Additionally, green parts of P. purum, and likely of other mosses with similar growth forms, should be used in passive biomonitoring studies to make results from different studies comparable.Peer reviewe

Unravelling the metal uptake process in mosses: Comparison of aquatic and terrestrial species as air pollution biomonitors

Transplanted mosses have been widely shown to be excellent tools for biomonitoring air pollution; however, it is not clear how the functional groups present on their surfaces affect the uptake of metal cations. In the present study, we examined differences in trace metal accumulation in two terrestrial and one aquatic moss species, and investigated whether the differences depended on their physico-chemical characteristics. In the laboratory, we determined C, N and H contents in their tissues and obtained the ATR-FTIR spectra (to identify the presence of functional groups). We also conducted surface acid-base titrations and metal adsorption assays with Cd, Cu and Pb. In the field, we exposed transplants of each species near different air-polluting industries, and determined the mosses enrichment of Al, Cd, Co, Cr, Cu, Fe, Ni, Pb and V. Laboratory results demonstrated higher metal uptake capacity in the terrestrial mosses Sphagnum palustre and Pseudoscleropodium purum, compared to that in the aquatic moss Fontinalis antipyretica, which can be attributed to a greater abundance of acidic functional groups (i.e. negatively charged binding sites) on the surface of the terrestrial mosses. The affinity of moss for certain elements depends on the abundance and nature of surface functional groups. Accordingly, the metal concentrations generally reached higher levels in S. palustre transplants compared to the other species, except for the uptake of Hg, which was higher in F. antipyretica. However, the findings also suggest an interaction between the type of environment (terrestrial or aquatic) and the moss characteristics that may influence the abovementioned trend. Thus, irrespective of the physico-chemical characteristics, metal uptake varied depending on the environment of origin of the mosses “i.e. atmospheric or aquatic”. In other words, the findings suggest that species that accumulate more metals in terrestrial environments will accumulate lower amounts of metals in aquatic environments and vice versa.R. García-Seoane was supported by a postdoctoral research grant awarded by the Juan de la Cierva-Formación (FJC2019-040921-I), funded by MCIN/AEI/10.13039/501100011033 (Spain) and EU NextGenerationEU/PRTR programmes. S. Fiol and J. Antelo acknowledge financial support provided by the Xunta de Galicia - Consellería de Educación e Ordenación Universitaria (Consolidation of Competitive Research Groups; GI-1245, ED431C 2022/40). J.R. Aboal and J.A. Fernández acknowledge financial support provided by the Xunta de Galicia - Consellería de Educación e Ordenación Universitaria (Consolidation of Competitive Research Groups; GI-1252, ED431C 2020/19).Peer reviewe

Phenotypic differences in heavy metal accumulation in populations of the brown macroalgae Fucus vesiculosus: A transplantation experiment

The concentrations of Al, As, Cd, Co, Cr, Cu, Fe, Hg, Ni, Pb and Zn in the thalli of Fucus vesiculosus transplanted reciprocally among four sites affected by different degrees of metal pollution (two unpolluted and two industrial environments) were measured with the aim of comparing the capacity of the algae to accumulate these elements under such conditions. At the beginning of the experiment, the concentrations of all elements differed significantly between the individuals from at least one of the unpolluted and one of the polluted sites. After exposure of the algae for 90 days, the concentrations of all of the elements except As, Cd and Cu in individuals transplanted from the unpolluted sites to the most polluted site increased to higher levels than in the algae transplanted within the site of origin. The same behaviour was observed for all elements except As and Cd in the thalli transplanted from one of the unpolluted sites to the second most polluted site. By contrast, the concentrations of the elements in transplants from the polluted sites exposed in the unpolluted sites usually decreased to approximately the same levels as in the autotransplants. These results suggest that the heavy metal uptake capacity may be limited in F. vesiculosus populations exposed to long-term pollution as an adaptive response to toxicity by metals. We therefore recommend the use of algal transplants to study water quality in highly polluted sites, rather than of native algae already growing in the sites, to avoid the possible effects of such adaptation

Global decrease in heavy metal concentrations in brown algae in the last 90 years

In the current scenario of global change, heavy metal pollution is of major concern because of its associated toxic effects and the persistence of these pollutants in the environment. This study is the first to evaluate the changes in heavy metal concentrations worldwide in brown algae over the last 90 years (>15,700 data across the globe reported from 1933 to 2020). The study findings revealed significant decreases in the concentrations of Cd, Co, Cr, Cu, Fe, Hg, Mn, Pb and Zn of around 60-84% (ca. 2% annual) in brown algae tissues. The decreases were consistent across the different families considered (Dictyotaceae, Fucaceae, Laminariaceae, Sargassaceae and Others), and began between 1970 and 1990. In addition, strong relationships between these trends and pH, SST and heat content were detected. Although the observed metal declines could be partially explained by these strong correlations, or by adaptions in the algae, other evidences suggest an actual reduction in metal concentrations in oceans because of the implementation of environmental policies. In any case, this study shows a reduction in metal concentrations in brown algae over the last 50 years, which is important in itself, as brown algae form the basis of many marine food webs and are therefore potential distributors of pollutants.C. Pacín was partly supported by funding from the “Bolsa de Investigación Deputación da Coruña”. R. García-Seoane was supported by a postdoctoral research grant awarded by the Juan de la Cierva-Formación (FJC2019–040921-I), funded by MCIN/AEI /10.13039/501100011033 (Spain) and EU NextGenerationEU/PRTR programmes. Z. Varela was supported by a postdoctoral research grant awarded by the autonomous government of Galicia (Xunta de Galicia, Spain).Peer reviewe

Analysis of intra-thallus and temporal variability of trace elements and nitrogen in Fucus vesiculosus: Sampling protocol optimization for biomonitoring

To advance the methodological standardization of the biomonitoring technique using macroalgae, we comprehensively characterized the intra-thallus and temporal patterns of variation in concentrations of a wide set of elements (Al, As, Cd, Co, Cr, Cu, Fe, Hg, Ni, Pb, Zn, N) and δ15N signal in 6 consecutive Fucus vesiculosus apical dichotomous sections collected monthly over a four-year period (2015–2019) at 3 sites on the NW coast of Spain. The concentrations of Al, Co, Fe, Ni, Pb and Zn increased significantly from the youngest to the oldest dichotomies regardless of the sampling time and collection site; As, Cd, N and δ15N showed the opposite trend. Time series analysis revealed a significant and consistent seasonal variation of As, Cd, Co, Cu, Fe, Hg, Ni, Zn, N and δ15N concentrations, with maximum values in winter and minimum values in summer. We discussed the possible mechanisms driving these two sources of variation, and proposed an efficient and effective sampling strategy to minimize their impact in the results of biomonitoring studies, in which the part of the algal thallus selected for chemical analysis and the sampling frequency were carefully considered. This protocol will improve the conclusions and comparability of biomonitoring data from coastal environments.En prens