# Exploring the levels of rare earth elements and trace metals in macroalgae from different Antarctic islands

Maria da Graça Landim Bravo, Léa Spitzer, Amandine Adrien, Pio

Colepicolo, Hosana Maria Debonsi, Lorena Rigo Gaspar, Javier

Jiménez-Lamana, Susana C.M. Fernandes

► To cite this version:

Maria da Graça Landim Bravo, Léa Spitzer, Amandine Adrien, Pio Colepicolo, Hosana Maria Debonsi, et al.. Exploring the levels of rare earth elements and trace metals in macroalgae from different Antarctic islands. Marine Pollution Bulletin, 2025, 221, pp.118579. 10.1016/j.marpolbul.2025.118579. hal-05222583

HAL Id: hal-05222583

https://univ-pau.hal.science/hal-05222583v1

Submitted on 18 Sep 2025

HAL is a multi-disciplinary open access
archive for the deposit and dissemination of sci-
entific research documents, whether they are pub-
lished or not. The documents may come from
teaching and research institutions in France or
abroad, or from public or private research centers.

L'archive ouverte pluridisciplinaire HAL, est
destinée au dépôt et à la diffusion de documents
scientifiques de niveau recherche, publiés ou non,
émanant des établissements d'enseignement et de
recherche français ou étrangers, des laboratoires
publics ou privés.

<figure><img src="image_1.png" /></figure>

Distributed under a Creative Commons Attribution 4.0 International License
# Exploring the levels of rare earth elements and trace metals in macroalgae from different Antarctic islands

Maria da Graça Landim Bravo<sup>a,b</sup>, Lea Spitzer<sup>a</sup>, Amandine Adrien<sup>a</sup>, Pio Colepicolo<sup>c</sup>, Hosana Maria Debonsi<sup>b</sup>, Lorena Rigo Gaspar<sup>b</sup>, Javier Jiménez-Lamana<sup>a,*</sup>, Susana C.M. Fernandes<sup>a</sup>

## ARTICLE INFO

### Keywords:

Antarctica

Desmarestia anceps

Palmaria decipiens

Phaeurus antarcticus

Rare earth elements

Trace metals

## ABSTRACT

The Antarctic continent remains one of the most unexplored ecosystems in the world due to its extreme climatic conditions and to the fact that it is the most remote environment. Despite this, it is known that human activities are increasing the contamination of its ecosystems with pollutants, including metals. Algae are considered as important bioindicators for monitoring these kinds of pollutants, since they easily absorb organic and inorganic compounds. In this context, herein we report the presence of rare earth elements (REEs) and trace elements in three Antarctic macroalgae species, i.e., *Desmarestia anceps*, *Palmaria decipiens*, and *Phaeurus antarcticus* collected in different regions. Inductively Coupled Plasma Mass Spectrometry (ICP-MS) was employed to determine the concentration of 33 metals in the algal samples. Our findings revealed that the trace metals and REEs concentrations are dependent on the species and collection site. *P. decipiens* presented the greatest capacity to accumulate REEs; and *D. anceps* and *P. decipiens* presented the highest levels of trace metals, with Fe concentrations ranging from 166 to 6640 µg/g of dry algae biomass. The comparison of collection sites revealed that Deception Island had higher average total levels of REEs and trace metals than the other islands. These results provide an important contribution to the biomonitoring of trace metals and, especially, REEs, which remain poorly studied in the region.

The Antarctic continent remains one of the most unexplored ecosystems in the world due to its extreme climatic conditions, namely low availability of water and organic nutrients, strong winds, and high UV radiation levels (Jordão et al., 2024). However, even under these conditions, Antarctica is not free from the presence of deleterious effects induced by human activity (Santos et al., 2005). Local anthropogenic activities or long-distance oceanic activities can release organic contaminants and highly toxic metals such as copper (Cu), lead (Pb), chromium (Cr), cadmium (Cd), arsenic (As), and mercury (Hg) (Bargagli, 2008; Szopińska et al., 2016). The presence of these heavy metals in the environment has raised concerns, especially due to their potential effects on biota. Recent evidence indicates that climate change may be exacerbating the mobility and bioaccumulation of exogenous elements in Antarctic ecosystems, potentially altering ecological dynamics and affecting the health of biological communities (da Silva

et al., 2023; Marina-Montes et al., 2020; Olalla et al., 2020). Rare Earth Elements (REEs) comprise a group of 17 chemical elements, including the 15 lanthanides, as well as scandium (Sc) and yttrium (Y). These elements are considered emerging contaminants due to their increasing use in electronic components, which may lead to their dispersion in the environment (Costa et al., 2020; Henriques et al., 2021).

The release of these elements into the environment occurs through multiple pathways: deposition in fur shed by top predators of the Antarctic marine food chain (Reindl et al., 2021), immobilization or release due to increasing soil acidity, continuous atmospheric deposition from volcanic eruptions accumulating in snow and entering watercourses via glacier melting (Reindl et al., 2024), and proximity to human activities (Piarulli et al., 2021; Runcie and Riddle, 2004). In example, on Deception Island, metals primarily originate from local rock and soil dust, sea salt spray, volcanic activity, and anthropogenic influences from South

<footnote><sup>a</sup> Université de Pau et des Pays de l'Adour, E2S UPPA, CNRS, IPREM, Institut des Sciences Analytiques et de Physico-chimie pour l'Environnement et les Matériaux, 64 000 Pau, France</footnote>

<footnote><sup>b</sup> University of Sao Paulo, School of Pharmaceutical Sciences of Ribeirao Preto, Department of Pharmaceutical Sciences, Ribeirao Preto, Brazil</footnote>

<footnote><sup>c</sup> University of Sao Paulo, Chemistry Institute, Department of Biochemistry, Sao Paulo, Brazil</footnote>

<footnote>* Corresponding author.</footnote>

<footnote>E-mail address: j.jimenez-lamana@univ-pau.fr (J. Jiménez-Lamana).</footnote>
America, South Africa, and Australia (Bargagli and Rota, 2024).

While studies on the impacts of these metals on the Antarctic environment have focused mainly on periglacial terrains (Reindl et al., 2024) ornithogenic sediments (Nie et al., 2014), or organisms such as invertebrates, seabirds, mosses, and lichens (Szopińska et al., 2016), relatively few studies have been dedicated to Antarctic algae (Chu et al., 2019a, 2019b; Elster et al., 2016; Koppel et al., 2017a, 2017b). Algae are often known for their crucial role in the food chain and nutrient cycling of aquatic ecosystems (Duncan and Petrou, 2022), and as promising bioresources of bioactive molecules and biomacromolecules for different application sectors (Castejón et al., 2024; Claverie et al., 2020; Maciel et al., 2018; Samalens et al., 2022; Spitzer et al., 2024).

Nonetheless, algae are also extremely important as bioindicators of environmental conditions, due to their important capacity to absorb organic and inorganic compounds, their sensitivity, and rapid response to environmental changes (Roy et al., 2022). Monitoring trace metal levels in macroalgae has been a key element in using the latter as early bioindicators of environmental pollution (Refat et al., 2021). Algae communities' assessments are recognized as better indicators of water quality than the evaluation using chemical tests. This is because their retention of elements is strong, with minimal exchange between bound metals and those found in the surrounding environment (Chu et al., 2019a, 2019b), allowing them to detect much higher concentrations than those found in the ambient waters (Smichowski et al., 2004a, 2004b).

The available literature on heavy metal content in Antarctic macroalgae and other organisms and its toxicological implications remains limited (Koppel et al., 2017b; la Rocca et al., 2009; Runcie and Riddle, 2007). However, studies have identified areas with elevated metal concentrations, such as Brown Bay, where algae can accumulate Cu, Pb and Hg at levels 10 to 100 times higher than background levels (Chu et al., 2019a, 2019b). Developing new ecological risk assessments and identifying threshold levels of contamination are important aims to protect these ecosystems from the anthropogenic impacts.

Considering the relevance of algae in the Antarctic environment and its biodiversity, in this study we report the levels of REEs and trace metals in different species of macroalgae from the Antarctic continent collected in different regions. This study focuses on 3 species, *Desmarestia anceps*, *Palmaria decipiens* and *Phaeurus antarcticus*. *D. anceps* is a brown alga, widely distributed on the Antarctic Peninsula and the South Shetland Islands, that has a crucial role in the region's ecosystems (Wiencke and Amsler, 2012). *P. decipiens* frequently occurs in sublittoral areas, being one of the most abundant red macroalgae in Antarctica, with a distribution that ranges from the east coast of the continent to the South Shetland Islands (Becker et al., 2011; Quartino et al., 2005). *P. antarcticus* is a brown species characteristic of sub-Antarctic and Antarctic marine habitats, found in a variety of coastal environments along the Antarctic coast (Wiencke and Amsler, 2012). These species are considered one of the ideal biomonitors because it meets prerequisites of relative abundance in the Antarctic territory, easy collection and taxonomic identification, and, mainly, it has high selectivity for the uptake of metals (Smichowski et al., 2004a, 2004b). In order to determine the concentration of elements at the trace level, samples were subjected to an acid digestion followed by analysis by Inductively Coupled Plasma Mass Spectrometry (ICP-MS).

To the best of our knowledge, this is the first study reporting the levels of REEs elements in *D. anceps*, *P. decipiens*, and *P. antarcticus* species. With this, we attempt to better understand the dynamics of metals and REEs in this extreme environment and provide support for conservation strategies and the applicability of these algae.

For this study, three species of algae were used: *P. decipiens*, *D. anceps*, and *P. antarcticus*. *P. decipiens* and *D. anceps* were collected during the expedition coordinated by PROANTAR, OPERANTAR XXXIV, during the months of November and December 2015, while *P. antarcticus* was collected during the operation XXXVI, also coordinated by PROANTAR OPERANTAR, during the month of December

2017. Two samples of the red alga *P. decipiens* were used, collected from different points on Deception Island. As for the brown alga *D. anceps*, three samples collected on Deception and King George Islands were used. Finally, for the brown alga *P. antarcticus*, a sample was collected on King George Island (Fig. 1 and Table 1).

The samples were identified by Dr. Cesar Bertagia Pasqualetti and Dr. Maria Beatriz Barbosa de Barros Barreto, and vouchers were deposited in the herbarium "Maria Eneyda Kauffmann Fidalgo" located at the Botanical Institute of São Paulo (São Paulo, Brazil). The collected algae were kept in plastic bags at a temperature of -20 °C until analysis.

The samples (n = 6) were taken from the previously described storage conditions, washed three times using ultrapure water to remove excess salts, visible epibionts, and sand particles, then were placed to dry at room temperature before being lyophilized. Finally, the entire thallus of each sample, excluding the holdfast, was milled into a fine powder using a RETSCH PM100 ball mill (Haan, Germany) at 400 rpm for 20 min.

Each algal powder was first digested in two steps before being analyzed by ICP-MS. First, the algae were pre-digested by adding 1 mL of HNO₃ to approximately 0.1 g of pounded biomass. Following, they were maintained for 30 min at room temperature, and 1 mL of H₂O₂ was added, and the mixture was left to react at room temperature overnight. Then, the samples were heated at 40 °C for 6 h to successfully remove all the organic material. Finally, the digested samples were diluted with HNO₃ (2 % v/v) according to the concentrations of the elements in the samples. Three replicates were prepared for each sample.

An Agilent 7900 ICP-MS (Agilent, Tokyo, Japan) with a collision cell containing hydrogen was employed. The sample introduction device included a concentric nebulizer and a Scott spray chamber. H₂ gas was injected at a flow rate of 5 mL.min⁻¹ to eliminate known interferences for the detection of some isotopes (indicated between brackets). The monitored isotopes were: ⁴⁷Ti, ⁵¹V, ⁵²Cr (H₂), ⁵⁵Mn, ⁵⁶Fe (H₂), ⁵⁹Co, ⁶⁰Ni (H₂), ⁶³Cu (H₂), ⁶⁴Zn (H₂), ⁷⁵As, ⁸⁰Se (H₂), ⁹⁵Mo, ¹⁰⁷Ag, ¹¹⁴Cd, ¹²¹Sb, ¹³⁹La, ¹⁴⁰Ce, ¹⁴¹Pr, ¹⁴⁶Nd, ¹⁴⁷Sm, ¹⁵³Eu, ¹⁵⁸Gd, ¹⁵⁹Tb, ¹⁶³Dy, ¹⁶⁵Ho, ¹⁶⁶Er, ¹⁶⁹Tm, ¹⁷²Yb, ¹⁷⁵Lu, ²⁰²Hg, ²⁰⁸Pb, ²³²Th and ²³⁸U. Multi-elemental calibration curves (0.1 ng.mL⁻¹ to 20 ng.mL⁻¹) were prepared, and the coefficient of determination R² was >0.99 for all of them.

This digestion protocol followed by ICP-MS analysis for the determination of the metal content in algae has already been used and published by our research group (Sánchez-Quintero et al., 2024). Similarly, the same ICP-MS methodology (including the same ICP-MS instrument) was successfully used recently by our research group to determine the content of REE (among other metals) in environmental microplastics (Elseblani et al., 2023). In addition, method blanks (i.e. a blank subjected to the same two-steps digestion protocol followed by the same dilution and ICP-MS analysis) were prepared each day of analysis. Values below LOQ (<1-20 ng L⁻¹ for all REE) were obtained for all blanks analyzed. LOQ were calculated as 10 times the standard deviation of the blank divide by the slope of the calibration curve for each REE.

Here, we determined the concentration of 14 REEs as listed in Table 3. Among the 3 algae species analyzed, *P. decipiens* presented the highest levels when compared to the other two species. The elements Lanthanum (La), Cerium (Ce), Neodymium (Nd), Samarium (Sm), Gadolinium (Gd) and Dysprosium (Dy) were the only ones quantified above 100 ng.g⁻¹, with concentrations being two to three times higher compared with *D. anceps*. For instance, Ce was the most abundant REEs, with concentrations ranging from 359.7 ± 8.1 to 626.4 ± 4.8 ng.g⁻¹ in *P. decipiens* and from 89.2 ± 2.3 to 251.0 ± 0.8 ng.g⁻¹ in *D. anceps*. In *D. anceps*, these elements were found to be more concentrated in samples collected at Arctowski (except for Gd and Dy). *P. antarcticus* exhibited the lowest concentrations of REEs compared to the other species.

The Earth's crust, despite accounting for only about 0.5 % of the planet's total mass, represents the primary reservoir of REEs, especially in the continental crust (Hoshino et al., 2016). A comparative analysis between the measured mean REEs concentrations and their relative
<figure><img src="image_2.png" /><figcaption>**Fig. 1.** Map representing the Antarctic continent and the collection points of algae *D. anceps*, *P. decipiens* and *P. antarcticus*. Antarctic continent (a), South Shetland Islands (b), King George Island (c) and Deception Island (d), and its collection points (red dots). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)</figcaption></figure>

<table><caption>**Table 1**
Identification of the algae species, location points and collection date.</caption><thead><tr><th>Species</th><th>Collection date</th><th>Location</th><th>Coordinates</th></tr></thead><tbody><tr><td>Palmaria decipiens</td><td>11/11/2015</td><td>Deception Island</td><td>62° 58' 55.6" S 60° 33' 11.5" W</td></tr><tr><td>Palmaria decipiens</td><td>06/12/2015</td><td>Whalers Bay – Deception Island</td><td>62° 59' 18.8" S 60° 33' 46.4" W</td></tr><tr><td>Desmarestia anceps</td><td>08/11/2015</td><td>Machu Picchu – K. George Island</td><td>62° 06' 14.2" S 58° 27' 36.0" W</td></tr><tr><td>Desmarestia anceps</td><td>11/11/2015</td><td>Deception Island</td><td>62° 58' 55.6" S 60° 33' 11.5" W</td></tr><tr><td>Desmarestia anceps</td><td>20/11/2015</td><td>Arctowski – K. George Island</td><td>62° 09' 6.49" S 58° 28' 49.57" W</td></tr><tr><td>Phaeurus antarcticus</td><td>16/12/2017</td><td>Demay Point – K. George Island</td><td>62° 13,14' 0.0 S 58° 26,26' 0.0 W</td></tr></tbody></table>

distribution in the Earth's crust (Hawkesworth and Kemp, 2006; Rudnick and Gao, 2003) was performed, as shown in Fig. 2a.

The observed REEs distribution in the three algae is generally consistent with the pattern found in the Earth's crust. The main deviation is observed in *P. decipiens*, which shows slightly elevated levels of Gd and Dy compared to the crustal trend at both collection sites.

Goecke et al. (2017) reported a similar pattern in *Corallina officinalis* var. *chilensis*, which showed higher levels of REEs such as Nd, La, and Ce, compared to other algae from the Chilean coast. Authors suggest this variability may be due to the ability of some Rhodophyta algae to substitute calcium (Ca) for lanthanides in their structures. Although *P. decipiens* is not a calcareous alga, its higher Gd and Dy levels might reflect a similar preferential uptake of these elements by the algae, or even a higher environmental availability in the collection area (Goecke et al., 2017).

Comparing the Ce/La ratio of approximately 2.09 in the Earth's crust, reported by Hawkesworth and Kemp (2006) and Rudnick and Gao (2003), our findings revealed notable differences, particularly for *D. anceps* from Deception Island, which exhibited a much lower Ce/La ratio of 0.67. Other observed ratios were also below this reference value,

<figure><img src="image_3.png" /><figcaption>**Fig. 2.** a) Comparison of REEs distribution in Antarctic macroalgae with the relative abundance of REEs in the Earth's crust, and b) Post-Archean Australian Shale (PAAS) normalization. Concentrations are expressed as mean values (ng·g⁻¹) for each sampling site. The average continental crust abundance was based on Rudnick and Gao (2003) and Hawkesworth and Kemp (2006), while PAAS normalization was based on Pourmand et al. (2012).</figcaption></figure>
including *D. anceps* from Arctowski (1.30) and Machu Picchu (1.16), *P. antarcticus* from Demay Point (1.42), and *P. decipiens* from Deception Island (1.16). Only *P. decipiens* from Whalers Bay showed a ratio close to that reported by the previously mentioned authors (2.02). This suggests that REEs accumulation in these algae may not directly reflect crustal availability, but rather the influence of environmental and/or biological factors that may have promoted an increase in La concentration in the environment.

REEs levels were also assessed following Post-Archean Australian Shale (PAAS) normalization. The PAAS normalization is a widely adopted reference for enhance the comparability and interpretation of REEs patterns in environmental samples (Rétif et al., 2023). As shown in Fig. 2b, all algae presented a similar normalized distribution, especially when comparing the same species from different collection spots. A general enrichment trend from light to heavy REEs was observed across samples.

The main deviation occurred between Gd and Eu. The brown algae species, *D. anceps* and *P. antarcticus*, shared a similar distribution pattern, with a peak of on Eu. The red alga *P. decipiens*, however, had no peak in Eu, but displayed a marked Gd peak. Thus, the observed deviation may be arising from the algae phylum, and the preferential uptake of some REEs. A high affinity between Eu and alginate, from the cell walls of brown algae, has already been described (Vijayaraghavan et al., 2010). As well, Gd also shows a correlation with Ca (Ryabushko et al., 2022), which resembles the Ca-lanthanide exchange processes described in red algae (Goecke et al., 2017), may explain the observed results.

REEs anomalies were calculated for the main elements that showed changes in Fig. 2 (La, Ce, Gd and Eu), using the PAAS normalized values (REE<sub>SN</sub>), and Eqs. (1) (Barrat et al., 2023) and (2)–(4) (Rétif et al., 2023) (Table 2). Values greater than 1 indicate positive anomalies, while values less than 1 indicate negative anomalies.

$$La / La^* = \frac{Pr_{SN}^3}{Nd_{SN}^2} \qquad (1)$$

$$Ce / Ce^* = \frac{Ce_{SN}}{2Pr_{SN} - Nd_{SN}} \qquad (2)$$

$$Gd / Gd^* = \frac{Gd_{SN}}{0.33Sm_{SN} + 0.67Tb_{SN}} \qquad (3)$$

$$Eu / Eu^* = \frac{Eu_{SN}}{0.67Sm_{SN} + 0.33Tb_{SN}} \qquad (4)$$

All algal samples exhibited negative Ce anomalies alongside positive Gd and Eu anomalies. Positive La anomalies were found for *D. anceps* and *P. decipiens*, but not for *P. antarcticus*. No differences were observed between collection sites, however, Eu in *D. anceps* showed a difference magnitude on anomalies between the collection sites. Although the origin of these patterns remains unclear, these results reinforce the hypothesis of anthropogenic influence on REEs levels in the region.

In the early 2000s, Runcie and Riddle (2004) measured the levels of La, Ce, Pr, Nd, and Sm in four algae species (*Desmarestia menziensii*, *Himantothallus grandifolius*, *Iridaea mawsonii*, and *Prasiola crispa*) collected from Windmill Island. Significant levels of REEs (ranging from 0.033 µg.g⁻¹ Sm to 0.303 µg.g⁻¹ La) were detected near the Brown Bay

region in the algae. However, these findings were attributed to the proximity of this site to the Casey Research Station, where the use of local granite for road construction and heavy vehicle traffic, generated fine particles that were transported to Brown Bay. This process potentially increases the availability of REEs in meltwater, facilitating their uptake by algae in this area (Runcie and Riddle, 2004).

More recently, Reindl et al. (2024) investigated the release and accumulation of REEs in aquatic and terrestrial environments of King George Island. Samples of the green algae *Prasiola crispa* from Admiralty Bay exhibited REEs concentrations one to two orders of magnitude higher than those identified in the present study. Similar to our findings, Ce was the most abundant element (1505 ± 10.43 µg.g⁻¹) not only in *P. crispa* but also in lichens, mosses, and the vascular plant *Deschampsia antarctica*. According to the authors, the green algae were the most responsive in terms of REEs bioaccumulation among the organisms studied (Reindl et al., 2024).

Additionally, their findings revealed that in the surrounding environment, Sc, Ce, and Nd were the most abundant REEs in the soil and bedrock, while La and Ce were predominant in glacial meltwater bodies (Reindl et al., 2024). A study on Ross and Beaufort Islands similarly found Ce, La, and Nd as the most abundant elements in sediments, bedrock, and guano (Nie et al., 2014), reinforcing that the algae studied here reflect the region's predominant elemental composition.

Although the Arctowski collection site being close to the Arctowski Station, and the Machu Picchu (King George Island) site being near the station with the same name, it had the lowest concentrations of these elements. Our collection site on Deception Island, although distant from any functional station, recorded the second-highest concentration of REEs. Further studies are needed to fully understand the presence and distribution of these elements in the Antarctic continent.

The results obtained for the determination of trace metal content in microalgae collected from the Antarctic continent, according to their species and location is shown in Table 4.

In general, the elements were detected at higher levels in the species *D. anceps* and *P. decipiens* than in *P. antarcticus*, with Iron (Fe) and Zinc (Zn) showing the highest concentrations across all species. For instance, Fe levels ranged from 166.56 ± 26.03 to 6640.24 ± 319.22 µg.g⁻¹. These levels are higher than those previously reported for Fe (276 ± 190 µg.g⁻¹) and Zn (62 ± 26 µg.g⁻¹) in *D. anceps*, (260 ± 9 µg.g⁻¹) and Zn (8.02 ± 0.3 µg.g⁻¹) in *P. decipiens*, and for Zn (5.04 ± 0.3 µg.g⁻¹) in *P. antarcticus*, in past studies conducted in the region (Chu et al., 2019a, 2019b; Farías et al., 2002; Lavergne et al., 2022).

Zn concentrations showed significant variations among samples, even within the same species. *D. anceps*, which exhibited the greatest variability, denoted concentrations of 144.93 ± 2.26 and 232.86 ± 85.96 µg.g⁻¹ at Machu Picchu (King George Island) and Deception, respectively, in contrast to 1124.25 ± 32.14 µg.g⁻¹ at Arctowski. Selenium (Se) and Chromium (Cr) also exhibited notable variations compared to earlier studies. Indeed, while *P. antarcticus* maintained Se levels close to 3 µg.g⁻¹, *D. anceps* and *P. decipiens* showed a 20-to-50-fold increase compared to previous works (Farias et al., 2002), with similar values across the collection sites. For Cr, the reported levels in the present study ranged from 6.14 ± 0.70 µg.g⁻¹ in *D. anceps* to 0.28 ± 0.09 µg.g⁻¹ in *P. antarcticus*. Elements such as Titanium (Ti), Manganese (Mn), and Nickel (Ni) exhibited significant fluctuations between species. Ti and Mn presented similar concentrations in *D. anceps* (Ti: 7.20–19.14

<table><caption>**Table 2**
REEs anomalies in macro algae, according to the different collection points.</caption><thead><tr><th rowspan="2">Element</th><th colspan="3">Desmarestia anceps</th><th colspan="2">Palmaria decipiens</th><th>Phaeurus antarcticus</th></tr><tr><th>Deception</th><th>Arctwoski</th><th>Machu Picchu</th><th>Whalers Bay</th><th>Deception</th><th>Demay Point</th></tr></thead><tbody><tr><td>La</td><td>2.33</td><td>3.27</td><td>1.34</td><td>6.28</td><td>4.59</td><td>0.43</td></tr><tr><td>Ce</td><td>0.53</td><td>0.76</td><td>0.67</td><td>0.96</td><td>0.76</td><td>0.93</td></tr><tr><td>Gd</td><td>1.66</td><td>1.68</td><td>1.63</td><td>1.57</td><td>1.65</td><td>1.59</td></tr><tr><td>Eu</td><td>2.78</td><td>3.92</td><td>4.22</td><td>1.55</td><td>1.55</td><td>7.06</td></tr></tbody></table>
<table><caption>**Table 3**
Rare earth elements average concentration (expressed in ng.g⁻¹) in macroalgae from the different places of collection.</caption><thead><tr><th rowspan="2">Element</th><th colspan="3">Desmarestia anceps</th><th colspan="2">Palmaria decipiens</th><th>Phaeurus antarcticus</th></tr><tr><th>Deception</th><th>Arctwoinski</th><th>Machu Picchu</th><th>Whalers Bay</th><th>Deception</th><th>Demay Point</th></tr></thead><tbody><tr><td>La</td><td>192.5 ± 8.4</td><td>193.0 ± 0.8</td><td>77.1 ± 1.8</td><td>309.5 ± 3.2</td><td>309.7 ± 4.0</td><td>28.2 ± 0.8</td></tr><tr><td>Ce</td><td>128.4 ± 9.4</td><td>251.0 ± 0.8</td><td>89.2 ± 2.3</td><td>626.4 ± 4.8</td><td>359.7 ± 8.1</td><td>40.0 ± 1.2</td></tr><tr><td>Pr</td><td>36.4 ± 2.1</td><td>46.1 ± 0.5</td><td>18.3 ± 0.5</td><td>99.4 ± 0.7</td><td>71.3 ± 1.6</td><td>5.9 ± 0.1</td></tr><tr><td>Nd</td><td>165.9 ± 9.0</td><td>199.7 ± 0.8</td><td>78.0 ± 2.2</td><td>456.3 ± 3.8</td><td>324.4 ± 4.4</td><td>25.6 ± 1.1</td></tr><tr><td>Sm</td><td>36.1 ± 2.1</td><td>44.6 ± 1.1</td><td>18.9 ± 0.8</td><td>118.8 ± 1.2</td><td>76.9 ± 1.9</td><td>6.1 ± 0.3</td></tr><tr><td>Eu</td><td>22.0 ± 1.2</td><td>2.8 ± 0.5</td><td>15.7 ± 0.5</td><td>38.7 ± 0.2</td><td>25.4 ± 0.5</td><td>8.2 ± 0.2</td></tr><tr><td>Gd</td><td>78.3 ± 4.1</td><td>74.2 ± 0.2</td><td>33.3 ± 0.4</td><td>225.7 ± 1.3</td><td>157.9 ± 3.1</td><td>9.8 ± 0.3</td></tr><tr><td>Tb</td><td>8.1 ± 0.4</td><td>6.9 ± 0.1</td><td>3.3 ± 0.1</td><td>24.1 ± 0.1</td><td>16.2 ± 0.4</td><td>1.0 ± 0.1</td></tr><tr><td>Dy</td><td>54.1 ± 2.9</td><td>38.2 ± 0.4</td><td>18.2 ± 0.3</td><td>145.2 ± 0.8</td><td>100.4 ± 2.1</td><td>5.3 ± 0.2</td></tr><tr><td>Ho</td><td>13.3 ± 0.6</td><td>8.3 ± 0.1</td><td>4.0 ± 0.1</td><td>30.7 ± 0.2</td><td>22.5 ± 0.2</td><td>1.1 ± 0.1</td></tr><tr><td>Er</td><td>48.5 ± 1.7</td><td>26.0 ± 0.2</td><td>12.5 ± 0.1</td><td>90.3 ± 0.6</td><td>66.5 ± 0.3</td><td>4.0 ± 0.2</td></tr><tr><td>Tm</td><td>6.2 ± 0.3</td><td>3.8 ± 0.1</td><td>1.8 ± 0.1</td><td>12.6 ± 0.1</td><td>19.2 ± 0.2</td><td>0.5 ± 0.1</td></tr><tr><td>Yb</td><td>40.4 ± 1.6</td><td>25.9 ± 0.3</td><td>12.6 ± 0.2</td><td>76.9 ± 0.4</td><td>57.7 ± 0.8</td><td>4.0 ± 0.1</td></tr><tr><td>Lu</td><td>7.0 ± 0.2</td><td>4.6 ± 0.1</td><td>2.2 ± 0.1</td><td>12.1 ± 0.1</td><td>9.2 ± 0.2</td><td>0.8 ± 0.1</td></tr></tbody></table>

<table><caption>**Table 4**
Trace metals average concentrations (expressed in µg.g⁻¹) in macroalgae from different places of collection of the Antarctic continent.</caption><thead><tr><th rowspan="2">Element</th><th colspan="3">Desmarestia anceps</th><th colspan="2">Palmaria decipiens</th><th>Phaeurus antarcticus</th><th>D. anceps</th><th>P. decipiens</th><th>P. antarcticus</th></tr><tr><th>Deception</th><th>Arctwoinski</th><th>M. Picchu</th><th>Whalers Bay</th><th>Deception</th><th>Demay Point</th><th colspan="3">Farías et al., 2002</th></tr></thead><tbody><tr><td>Ti</td><td>19.14 ± 0.48</td><td>8.72 ± 0.21</td><td>7.20 ± 0.53</td><td>182.95 ± 1.98</td><td>88.03 ± 3.07</td><td>10.21 ± 0.29</td><td></td><td></td><td></td></tr><tr><td>V</td><td>22.62 ± 0.61</td><td>1.50 ± 0.02</td><td>1.02 ± 0.02</td><td>10.98 ± 0.07</td><td>22.23 ± 0.78</td><td>0.48 ± 0.003</td><td>3.39 ± 0.12</td><td>6.29 ± 0.28</td><td>15.0 ± 0.6</td></tr><tr><td>Cr</td><td>6.14 ± 0.70</td><td>1.21 ± 0.17</td><td>4.06 ± 0.07</td><td>1.79 ± 0.08</td><td>1.88 ± 0.15</td><td>0.28 ± 0.09</td><td>3.25 ± 0.19</td><td>2.05 ± 0.10</td><td>12.1 ± 0.77</td></tr><tr><td>Mn</td><td>5.90 ± 0.40</td><td>7.19 ± 0.17</td><td>6.29 ± 1.87</td><td>47.78 ± 0.34</td><td>30.99 ± 0.69</td><td>10.59 ± 0.11</td><td>2.00 ± 0.11</td><td>4.01 ± 0.20</td><td>17.1 ± 0.8</td></tr><tr><td>Fe</td><td>4440 ± 113.0</td><td>305 ± 27.91</td><td>225 ± 11.0</td><td>2876 ± 37.0</td><td>6640 ± 319</td><td>166 ± 26.03</td><td>108 ± 4</td><td>260 ± 9</td><td>1400 ± 30</td></tr><tr><td>Co</td><td>0.63 ± 0.01</td><td>0.31 ± 0.10</td><td>0.19 ± 0.01</td><td>0.89 ± 0.01</td><td>0.60 ± 0.02</td><td>0.08 ± 0.004</td><td>155 ± 6</td><td>139 ± 5</td><td>182 ± 7</td></tr><tr><td>Ni</td><td>14.28 ± 0.89</td><td>8.10 ± 0.25</td><td>28.91 ± 0.46</td><td>3.00 ± 0.04</td><td>2.00 ± 0.06</td><td>1.46 ± 0.11</td><td>8.64 ± 0.44</td><td>8.16 ± 0.42</td><td>8.76 ± 0.42</td></tr><tr><td>Cu</td><td>61.50 ± 1.77</td><td>9.48 ± 0.26</td><td>40.01 ± 0.66</td><td>64.06 ± 1.80</td><td>96.11 ± 1.80</td><td>5.37 ± 0.06</td><td>4.05 ± 0.22</td><td>6.03 ± 0.22</td><td>4.11 ± 0.22</td></tr><tr><td>Zn</td><td>232 ± 85.0</td><td>1124 ± 32.0</td><td>144 ± 2.26</td><td>181 ± 68.0</td><td>538 ± 723</td><td>70.55 ± 7.98</td><td>&lt;0.1</td><td>8.02 ± 0.3</td><td>5.04 ± 0.3</td></tr><tr><td>As</td><td>28.80 ± 0.75</td><td>33.58 ± 0.54</td><td>21.93 ± 0.28</td><td>6.35 ± 0.08</td><td>14.78 ± 0.51</td><td>17.02 ± 0.27</td><td>28.7 ± 1.3</td><td>9.80 ± 0.41</td><td>61.4 ± 2.9</td></tr><tr><td>Se</td><td>46.83 ± 1.04</td><td>55.06 ± 1.03</td><td>36.61 ± 3.12</td><td>17.81 ± 0.73</td><td>29.29 ± 0.64</td><td>3.00 ± 0.57</td><td>&lt;0.6</td><td>1.54 ± 0.08</td><td>&lt;0.6</td></tr><tr><td>Mo</td><td>0.30 ± 0.01</td><td>0.41 ± 0.01</td><td>0.35 ± 0.01</td><td>0.36 ± 0.01</td><td>0.26 ± 0.01</td><td>0.37 ± 0.01</td><td>&lt;0.6</td><td>0.80 ± 0.05</td><td>&lt;0.6</td></tr><tr><td>Ag</td><td>0.43 ± 0.04</td><td>0.07 ± 0.09</td><td>0.42 ± 0.05</td><td>0.21 ± 0.003</td><td>0.41 ± 0.01</td><td>0.021 ± 0.001</td><td></td><td></td><td></td></tr><tr><td>Cd</td><td>0.89 ± 0.007</td><td>0.52 ± 0.01</td><td>1.12 ± 0.02</td><td>0.11 ± 0.003</td><td>0.17 ± 0.007</td><td>0.07 ± 0.02</td><td>1.00 ± 0.06</td><td>0.24 ± 0.01</td><td>0.70 ± 0.04</td></tr><tr><td>Sb</td><td>0.01 ± 0.002</td><td>0.04 ± 0.001</td><td>0.02 ± 0.01</td><td>0.008 ± 0.001</td><td>0.01 ± 0.001</td><td>0.01 ± 0.003</td><td></td><td></td><td></td></tr><tr><td>Hg</td><td>0.05 ± 0.004</td><td>0.04 ± 0.001</td><td>0.02 ± 0.001</td><td>0.02 ± 0.001</td><td>0.03 ± 0.001</td><td>0.02 ± 0.002</td><td></td><td></td><td></td></tr><tr><td>Pb</td><td>0.42 ± 0.03</td><td>0.38 ± 0.02</td><td>1.23 ± 0.07</td><td>0.36 ± 0.01</td><td>0.49 ± 0.01</td><td>0.26 ± 0.01</td><td>&lt;0.6</td><td>1.54 ± 0.08</td><td>&lt;0.6</td></tr><tr><td>Th</td><td>0.003 ± 0.001</td><td>0.003 ± 0.001</td><td>0.01 ± 0.001</td><td>0.01 ± 0.001</td><td>0.006 ± 0.001</td><td>0.003 ± 0.001</td><td></td><td></td><td></td></tr><tr><td>U</td><td>0.56 ± 0.01</td><td>0.10 ± 0.003</td><td>0.58 ± 0.006</td><td>0.07 ± 0.002</td><td>0.11 ± 0.006</td><td>0.12 ± 0.0015</td><td></td><td></td><td></td></tr></tbody></table>

µg.g⁻¹; Mn: 5.90–7.19 µg.g⁻¹) and *P. antarcticus* (Ti: 10.21 ± 0.29 µg. g⁻¹; Mn: 10.59 ± 0.11 µg.g⁻¹), but substantially elevated levels in *P. decipiens* (Ti: 88.03–182.95 µg.g⁻¹; Mn: 30.99–47.78 µg.g⁻¹). *D. anceps* displayed higher Ni concentrations (8.10–28.91 µg.g⁻¹) compared to the other species (which ranged from 1.46 to 3.00 µg.g⁻¹).

Although no correlation between those trace elements and these species has been described, it is known that certain algae species preferentially assimilate specific chemical elements (Majer et al., 2014). This selectivity is influenced by several factors, including the physicochemical properties of the elements - such as solubility, pH, and the ability to form soluble complexes - and the metabolic adaptability of algae to their environment (Reindl et al., 2024). The presence of certain compounds on algal cell walls also plays a key role in this process. For instance, the presence of alginates in brown algae contributes to metal ion accumulation, with alginate showing a high affinity for bivalent metals (Davis et al., 2003; Ordóñez et al., 2023).

Environmental conditions like water turbidity, nutrient availability, salinity, and temperature further modulate metal bioaccumulation by altering growth rates and metabolic processes, including metal uptake-excretion mechanisms (Farías et al., 2002; Sanchez-Hernandez, 2000).

Vanadium (V) exhibited significant variations between species, but also between collection sites. Interestingly, algae collected at Deception Island showed higher levels of V compared to other locations (~22 µg. g⁻¹). This finding aligns with previous studies indicating that Deception Island is enriched in elements as Fe, Co, V and Ni, due to its

hydrothermal activity (Belyaev et al., 2024). Although it was not observed for Co and Ni, in the present study, the species *D. anceps* and *P. decipiens* collected on Deception Island displayed higher levels of Fe and V compared to the specimens from other locations.

The elements that showed the lowest concentrations across the three algae species were Cobalt (Co), Molybdenum (Mo), Silver (Ag), Cadmium (Cd), Antimony (Sb), Mercury (Hg), Lead (Pb), Thorium (Th), and Uranium (U). All these elements were quantified at levels below 1 µg. g⁻¹, except for Pb and Cd in *D. anceps* collected at Machu Picchu point, which had concentrations of 1.23 ± 0.07 and 1.12 ± 0.02 µg.g⁻¹, respectively. Previous studies have reported similar concentrations of these elements in King George Island. Farías et al. (2002) found Cd levels ranging from 0.24 to 1.00 µg.g⁻¹, while Lavergne et al. (2022) reported slightly lower values, between 0.37 and 0.42 µg.g⁻¹, for the same algal species analyzed in the present study. In the same study, Farías et al. (2002) observed that Mo and Pb concentrations were generally below the detection limit, except for Pb in *P. antarcticus* (7.59 ± 0.42 µg.g⁻¹). A similar Pb concentration was later reported by Reindl et al. (2024) in the green alga *P. crispa*. Notably, Co was the only of these metals already reported with high concentrations (139–182 µg.g⁻¹), likely influenced by site-specific environmental conditions (Farías et al., 2002). To the best of our knowledge, no other studies have reported the concentrations of Ti, Ag Sb, Hg, Th and U in algae of this region.

Among the metals of toxicological relevance, such as Copper (Cu), Pb, Cd, Hg, and Arsenic (As), the element with the highest concentration
was Cu, detected at levels up to 96.11 ± 1.80 µg.g⁻¹ in *P. decipiens* at Deception point. *D. anceps* exhibited significant variability in Cu levels, for algae collected at Deception Island showing 61.50 ± 1.77, Arctowski 9.49 ± 0.26, and Machu Picchu 40.01 ± 0.66 µg.g⁻¹. As was identified at levels in line with those previously reported for *D. anceps* and *P. decipiens* by Farías et al. (2002, 2007) and Smichowski et al. (2004a, 2004b), but showed a significant decrease in *P. antarcticus* (17.02 ± 0.27 µg.g⁻¹). Farías et al. (2007) reported As levels of 88 ± 20 µg.g⁻¹, while Smichowski et al. (2004a, 2004b) reported significantly higher levels of 447 ± 22 µg.g⁻¹.

This study provides the first report of REEs and 19 trace metals in three macroalgae species from the Antarctic continent, *D. anceps*, *P. decipiens*, and *P. antarcticus*. The analysis revealed that trace metals and REEs concentrations show significant variation depending on the species and collection site. *P. antarcticus* was the species with the lowest concentrations of trace metals (with concentrations between 0.0034 ± 0.0001 µg.g⁻¹ for Th and 166.0 ± 26.03 µg.g⁻¹ for Fe) and REEs (ranging between 0.5 ± 0.1 ng.g⁻¹ for Tm and 40.0 ± 1.2 ng.g⁻¹ for Ce) compared to the other species. *P. decipiens* demonstrated a greater capacity to accumulate rare earth elements than other species, presenting 359.7 ± 8.1–626.4 ± 4.8 ng.g⁻¹ of Ce total content, the most abundant REEs.

Collectively, our results highlight the potential of Antarctic algae as bioindicators for monitoring trace metals and REEs bioavailability in their environment. The variability observed in metal concentrations across species and locations may be driven by biological and environmental factors, emphasizing the challenges in establishing clear correlations. This complexity indicates the need for further studies involving a larger number of algal species and environmental samples (sediment, water, other species, and over time) to better evaluate the linearity of the relationship between metals levels and their surrounding environment and to provide a more comprehensive understanding of the implications of metal accumulation in these ecosystems. Overall, these general findings represent an important contribution to the bio-monitoring of trace metals and, particularly, rare earth elements, which are still poorly studied in the region.

### CRediT authorship contribution statement

**Maria da Graça Landim Bravo:** Resources, Methodology, Investigation, Formal analysis, Conceptualization, Writing – original draft. **Lea Spitzer:** Methodology, Investigation, Formal analysis, Writing – review & editing. **Amandine Adrien:** Formal analysis, Writing – review & editing. **Pio Colepicolo:** Funding acquisition, Writing – review & editing. **Hosana Maria Debonsi:** Funding acquisition, Writing – review & editing. **Lorena Rigo Gaspar:** Funding acquisition, Writing – review & editing. **Javier Jiménez-Lamana:** Supervision, Methodology, Investigation, Formal analysis, Conceptualization, Writing – review & editing. **Susana C.M. Fernandes:** Supervision, Project administration, Investigation, Funding acquisition, Conceptualization, Writing – review & editing.

### Funding

This study had financial support from the Brazilian Antarctic Program PROANTAR/MCTI/CNPq N°64/2013, Brazilian Marine Force, National Institute of Science and Technology (INCT:BioNat), Grant #465637/2014-0, and the State of São Paulo Research Foundation (FAPESP), Grant #2014/50926-0 and 2017/03552-5. This work was carried under the framework of E2S UPPA Partnership Chair MANTA (Marine Materials) funded by the ‘Investissements d’Avenir’ French program managed by ANR, grant number #ANR-16-IDEX-0002 and by the Région Nouvelle-Aquitaine (France).

### Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

### Acknowledgments

The authors would like to thank the University of São Paulo for providing access to essential resources, the research funding agencies: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), for their financial and fellowship support. We would like to thank Dr. Renata Spagolla Napoleão Tavares and Dr. Gustavo Souza dos Santos, for helping in algae collection. Finally, they express their appreciation to the ECOMES and POLYCAT platforms at IPREM/UPPA for providing access to their facilities.

### Data availability

Data will be made available on request.

### References

* Bargagli, R., 2008. Environmental contamination in Antarctic ecosystems. Sci. Total Environ. https://doi.org/10.1016/j.scitotenv.2008.06.062.

* Bargagli, R., Rota, E., 2024. Environmental contamination and climate change in Antarctic ecosystems: an updated overview. Environ. Sci. Adv. 3 (4), 543–560. https://doi.org/10.1039/D3VA00113J.

* Barrat, J.A., Bayon, G., Lalonde, S., 2023. Calculation of cerium and lanthanum anomalies in geological and environmental samples. Chem. Geol. 615, 121202. https://doi.org/10.1016/J.CHEMGEO.2022.121202.

* Becker, S., Quartino, M.L., Campana, G.L., Bucolo, P., Wiencke, C., Bischof, K., 2011. The biology of an Antarctic rhodophyte, Palmaria decipiens: recent advances. Antarct. Sci. 23 (5), 419–430. https://doi.org/10.1017/S0954102011000575.

* Belyaev, O., Huertas, I.E., Navarro, G., Amaya-Vías, S., de la Paz, M., Sparaventi, E., Heredia, S., Sukekava, C.F., Laglera, I.M., Tovar-Sánchez, A., 2024. Hydrothermal alteration of seawater biogeochemistry in Deception Island (South Shetland Islands, Antarctica). Front. Mar. Sci. 11, 1432122. https://doi.org/10.3389/FMARS.2024.1432122/BIBTEX.

* Castejón, N., Adrien, A., Spitzer, L., Fernandes, S.C.M., 2024. Unlocking the full potential of the red seaweed Gelidium corneum: beyond its use as an agar source. J. Appl. Phycol. 36 (1), 291–311. https://doi.org/10.1007/S10811-023-03115-8/METRICS.

* Chu, W.L., Dang, N.L., Kok, Y.Y., Ivan Yap, K.S., Phang, S.M., Convey, P., 2019a. Heavy metal pollution in Antarctica and its potential impacts on algae. In: Polar Science, vol. 20. Elsevier B.V, pp. 75–83. https://doi.org/10.1016/j.polar.2018.10.004.

* Chu, W.L., Dang, N.L., Kok, Y.Y., Ivan Yap, K.S., Phang, S.M., Convey, P., 2019b. Heavy metal pollution in Antarctica and its potential impacts on algae. Pol. Sci. 20, 75–83. https://doi.org/10.1016/J.POLAR.2018.10.004.

* Claverie, M., McReynolds, C., Petitpas, A., Thomas, M., Fernandes, S.C.M., 2020. Marine-derived polymeric materials and biomimetics: an overview. Polymers 12 (5). https://doi.org/10.3390/POLYM12051002.

* Costa, M., Henriques, B., Pinto, J., Fabre, E., Dias, M., Soares, J., Carvalho, L., Vale, C., Pinheiro-Torres, J., Pereira, E., 2020. Influence of toxic elements on the simultaneous uptake of rare earth elements from contaminated waters by estuarine macroalgae. Chemosphere 252, 126562. https://doi.org/10.1016/J.CHEMOSPHERE.2020.126562.

* da Silva, J.R.M.C., Bergami, E., Gomes, V., Corsi, I., 2023. Occurrence and distribution of legacy and emerging pollutants including plastic debris in Antarctica: sources, distribution and impact on marine biodiversity. Mar. Pollut. Bull. 186, 114353. https://doi.org/10.1016/J.MARPOLBUL.2022.114353.

* Davis, T.A., Volesky, B., Mucci, A., 2003. A review of the biochemistry of heavy metal biosorption by brown algae. Water Res. 37 (18), 4311–4330. https://doi.org/10.1016/S0043-1354(03)00293-8.

* Duncan, R. J., & Petrou, K. (2022). Biomolecular Composition of Sea Ice Microalgae and Its Influence on Marine Biogeochemical Cycling and Carbon Transfer through Polar Marine Food Webs. *Geosciences 2022*, *Vol. 12*, *Page 38*, 12(1), 38. doi:https://doi.org/10.3390/GEOSCIENCES12010038.

* Elseblani, R., Cobo-Golpe, M., Godin, S., Jimenez-Lamana, J., Fakhri, M., Rodríguez, I., Szpunar, J., 2023. Study of metal and organic contaminants transported by microplastics in the Lebanese coastal environment using ICP MS, GC-MS, and LC-MS. Sci. Total Environ. 887 (May), 164111. https://doi.org/10.1016/j.scitotenv.2023.164111.

* Elster, J., Nedbalová, L., Vodrážka, R., Láska, K., Haloda, J., Komárek, J., 2016. Unusual biogenic calcite structures in two shallow lakes, James Ross island, Antarctica. *Biogeosciences* 13 (2), 535–549. https://doi.org/10.5194/BG-13-535-2016.

* Farías, S., Perez Arisnabarreta, S., Vodopívez, C., Smichowski, P., 2002. Levels of essential and potentially toxic trace metals in Antarctic macro algae. Spectrochim. Acta Part B. 57.
Farías, S., Smichowski, P., Vélez, D., Montoro, R., Curtosi, A., Vodopívez, C., 2007. Total and inorganic arsenic in Antarctic macroalgae. Chemosphere 69 (7), 1017–1024. https://doi.org/10.1016/j.chemosphere.2007.04.049.

Goecke, F., Aránguiz-Acuña, A., Palacios, M., Muñoz-Muga, P., Rucki, M., Vítová, M., 2017. Latitudinal distribution of lanthanides contained in macroalgae in Chile: an inductively coupled plasma-mass spectrometric (ICP-MS) determination. J. Appl. Phycol. 29 (4), 2117–2128. https://doi.org/10.1007/S10811-017-1106-6. /METRICS.

Hawkesworth, C.J., Kemp, A.I.S., 2006. Evolution of the continental crust. Nature 446:7113–713 (7113), 811–817. https://doi.org/10.1038/nature05191.

Henriques, B., Morais, T., Cardoso, C.E.D., Freitas, R., Viana, T., Ferreira, N., Fabre, E., Pinheiro-Torres, J., Pereira, E., 2021. Can the recycling of europium from contaminated waters be achieved through living macroalgae? Study on accumulation and toxicological impacts under realistic concentrations. Sci. Total Environ. 786, 147176. https://doi.org/10.1016/J.SCIOTENV.2021.147176.

Hoshino, M., Sanematsu, K., Watanabe, Y., 2016. REE Mineralogy and Resources. Handbook on the Physics and Chemistry of Rare Earths 49, 129–291. https://doi.org/10.1016/BS.HPCRE.2016.03.006.

Jordão, A.C., dos Santos, G.S., Teixeira, T.R., Gluzezak, A.J.P., de Souza Azevedo, C.B., de Castro Pereira, K., Tonani, L., Gaspar, L.R., von Zeska Kress, M.R., Colepicolo, P., Debonsi, H.M., 2024. Assessment of the photoprotective potential and structural characterization of secondary metabolites of Antarctic fungus *Arthrinium* sp. Arch. Microbiol. 206 (1), 1–16. https://doi.org/10.1007/S00203-023-03756-W. /FIGURES/9.

Koppel, D.J., Gissi, F., Adams, M.S., King, C.K., Jolley, D.F., 2017a. Chronic toxicity of five metals to the polar marine microalga Cryothecomonas armigera – application of a new bioassay. Environ. Pollut. 228, 211–221. https://doi.org/10.1016/J. ENVPOL.2017.05.034.

Koppel, D.J., Gissi, F., Adams, M.S., King, C.K., Jolley, D.F., 2017b. Chronic toxicity of five metals to the polar marine microalga Cryothecomonas armigera – application of a new bioassay. Environ. Pollut. 228, 211–221. https://doi.org/10.1016/J. ENVPOL.2017.05.034.

la Rocca, N., Andreoli, C., Giacometti, G.M., Rascio, N., Moro, I., 2009. Responses of the Antarctic microalga Koliella Antarctica (Trebuouxophyceae, Chlorophyceae) to cadmium contamination. Photosyntheticna 47 (3), 471–479. https://doi.org/ 10.1007/S11099-009-0071-Y/METRICS.

Lavergne, C., Celis-Plá, P.S.M., Chenu, A., Rodríguez-Rojas, F., Moenne, F., Díaz, M.J., Abello-Flores, M.J., Díaz, P., Garrido, I., Bruning, P., Verdugo, M., Lobos, M.G., Sáez, C.A., 2022. Macroalgae metal-biomonitoring in Antarctica: addressing the consequences of human presence in the white continent. Environ. Pollut. 292, 118365. https://doi.org/10.1016/J.ENVPOL.2021.118365.

Maciel, O.M.C., Tavares, R.S.N., Caluz, D.R.E., Gaspar, L.R., Debonsi, H.M., 2018. Photoprotective potential of metabolites isolated from algae-associated fungi Annulohypoxylon stygium. J. Photochem. Photobiol. B Biol. https://doi.org/ 10.1016/j.iphotobiol.2017.11.018.

Majer, A.P., Petti, Mó.A.V., Corbisier, T.N., Ribeiro, A.P., Theophilo, C.Y.S., Ferreira, P.A. de L., Figueira, R.C.L., 2014. Bioaccumulation of potentially toxic trace elements in benthic organisms of Admiralty Bay (King George Island, Antarctica). Mar. Pollut. Bull. 79 (1–2), 321–325. https://doi.org/10.1016/j.MARPOLBUL.2013.12.015.

Marina-Montes, C., Pérez-Arribas, L.V., Escudero, M., Anzano, J., Cáceres, J.O., 2020. Heavy metal transport and evolution of atmospheric aerosols in the Antarctic region. Sci. Total Environ. 721, 137702. https://doi.org/10.1016/J. SCITOTENV.2020.137702.

Nie, Y., Liu, X., Emslie, S.D., 2014. Distribution and sources of rare earth elements in ornithogenic sediments from the Ross Sea region, Antarctica. Microchem. J. 114, 247–260. https://doi.org/10.1016/J.MICROC.2014.01.010.

Olalla, A., Moreno, L., Valcárcel, Y., 2020. Prioritisation of emerging contaminants in the northern Antarctic peninsula based on their environmental risk. Sci. Total Environ. 742, 140417. https://doi.org/10.1016/J.SCIOTENV.2020.140417.

Ordóñez, J. I., Cortés, S., Maluenda, P., & Soto, I. (2023). Biosorption of heavy metals with algae: critical review of its application in real effluents. *Sustainability* 2023, Vol. 15, page 5521, 15(6), 5521. doi:https://doi.org/10.3390/SU15065521.

Piarulli, S., Hansen, B.H., Giesielski, T., Zocher, A.L., Malzahn, A., Osvik, P.A., Sonne, C., Nordtug, T., Jenssen, B.M., Booth, A.M., Farkas, J., 2021. Sources, distribution and effects of rare earth elements in the marine environment: current knowledge and research gaps. Environ. Pollut. 291, 118230. https://doi.org/10.1016/J. ENVPOL.2021.118230.

Pourmand, A., Dauphas, N., Ireland, T.J., 2012. A novel extraction chromatography and MC-ICP-MS technique for rapid analysis of REE, Sc and Y: revising CI-chondrite and post-Archean Australian shale (PAAS) abundances. Chem. Geol. 291, 38–54. https:// doi.org/10.1016/j.CHEMGEO.2011.08.011.

Quartino, M.L., Zaixso, H.E., De Boraso Zaixso, A.L., 2005. Biological and environmental characterization of marine macroalgal assemblages in Potter Cove, South Shetland Islands, Antarctica. Bot. Mar. 48 (3), 187–197. https://doi.org/10.1515/ BOT.2005.029. /MACHINEREDABLECITATION/RIS.

Refat, M., Rakib, J., Jolly, Y.N., Dioses-Salinas, D.C., Pizarro-Ortega, C.I., De-La-Torre, G. E., Khandaker, M.U., Alsubaie, A., Almalki, A.S.A., Bradley, D.A., 2021. Macroalgae in biomonitoring of metal pollution in the bay of Bengal coastal waters of Cox's Bazar and surrounding areas. Sci. Rep. 11, 20999. https://doi.org/10.1038/s41598- 021-99750-7.

Reindl, A.R., Saniewska, D., Grajewska, A., Falkowska, L., Saniewski, M., 2021. Alimentary exposure and elimination routes of rare earth elements (REE) in marine mammals from the Baltic Sea and Antarctic coast. Sci. Total Environ. 754, 141947. https://doi.org/10.1016/J.SCIOTENV.2020.141947.

Reindl, A.R., Wolska, L., Piotrowicz-Ciesłak, A.I., Saniewska, D., Bolatek, J., Saniewski, M., 2024. The impact of global climate changes on trace and rare earth elements mobilization in emerging periglacial terrains: insights from western shore of Admiralty Bay (King George Island, Antarctic). Sci. Total Environ. 926 (March). https://doi.org/10.1016/j.scitotenv.2024.171540.

Rétif, J., Zalouk-Vergnoux, A., Briant, N., Poirier, L., 2023. From geochemistry to ecotoxicology of rare earth elements in aquatic environments: diversity and uses of normalization reference materials and anomaly calculation methods. Sci. Total Environ. 856, 158890. https://doi.org/10.1016/J.SCIOTENV.2022.158890.

Roy, A., Gogoi, N., Yasmin, F., Farooq, M., 2022. The use of algae for environmental sustainability: trends and future prospects, 1, 3. Environ. Sci. Pollut. Res. https://doi.org/10.1007/s11356-022-19636-7.

Rudnick, R. L., & Gao, S. 2003. Composition of the continental crust. Treatise on Geochemistry, 3–9, 1–64. https://doi.org/10.1016/B0-08-043751-6/03016-4.

Runcie, J.W., Riddle, M.J., 2004. Metal concentrations in macroalgae from East Antarctica. Mar. Pollut. Bull. 49 (11–12), 1114–1119. https://doi.org/10.1016/J. MARPOLBUL.2004.09.001.

Runcie, J.W., Riddle, M.J., 2007. Assessing the toxic effects of dissolved copper on the Antarctic macroalga *Desmarestia menziesii* using chlorophyll fluorescence imaging in ecotoxicological tests. Toxicol. Environ. Chem. 89 (4), 641–653. https://doi.org/ 10.1080/02772240701561627.

Ryabushko, V.I., Gureeva, E.V., Kapranov, S.V., Bobko, N.I., Prazukin, A.V., Nekhoroshhev, M.V., 2022. Rare earth elements in brown algae of the genus *Cystoseira* (Phaeophyceae) (Black Sea). Eur. J. Phycol. 57 (4), 433–445. https://doi.org/ 10.1080/09670262.2021.2016985. /ASSET/03CF2121-EBCE-4729-BA87- 0F761C5D0DCE/ASSETS/IMAGES/TEJP_A_2016985_F0005.OC.JPG.

Samalens, F., Thomas, M., Claverie, M., Castejon, N., Zhang, Y., Pigot, T., Blanc, S., Fernandes, S.C.M., 2022. Progresses and future prospects in biodegradation of marine biopolymers and emerging biopolymer-based materials for sustainable marine ecosystems. Green Chem. 24 (5), 1762–1779. https://doi.org/10.1039/ D1GC04327G.

Sanchez-Hernandez, J.C., 2000. Trace element contamination in Antarctic ecosystems. Rev. Environ. Contam. Toxicol. 166, 83–127. https://europepmc.org/article/med/ 10868077.

Sánchez-Quintero, Á., Parsy, A., Adrien, A., Spitzer, L., Jiménez-Lamana, J., Fernandes, S.C.M., Beigbeder, J.B., 2024. Effects of CO₂ and liquid Digestate concentrations on the growth performance and biomass composition of Tetradesmus Obliquus and chlorella vulgaris microalgal strains. Front. Bioeng. Technol. 12 (January), 1–15. https://doi.org/10.3389/fbioe.2024.1459756.

Santos, I.R., Silva-Filho, E.V., Schaefer, C.E.G.R., Albuquerque-Filho, M.R., Campos, L.S., 2005. Heavy metal contamination in coastal sediments and soils near the Brazilian Antarctic Station, King George Island. Mar. Pollut. Bull. 50 (2), 185–194. https://doi.org/10.1016/j.MARPOLBUL.2004.10.009.

Smichowski, P., Farías, S., Valiente, L., Iribarren, M.L., Vodopívez, C., 2004a. Total arsenic content of nine species of Antarctic macro algae as determined by electrothermal atomic absorption spectrometry. Anal. Bioanal. Chem. 378 (2), 465–469. https://doi.org/10.1007/s00216-002-2275-5.

Smichowski, P., Farías, S., Valiente, L., Iribarren, M.L., Vodopívez, C., 2004b. Total arsenic content of nine species of Antarctic macro algae as determined by electrothermal atomic absorption spectrometry. Anal. Bioanal. Chem. 378 (2), 465–469. https://doi.org/10.1007/S00216-002-2275-5/TABLES/5.

Spitzer, L., Adrien, A., Veettil, U.T., Olza, S., Alonso-Varona, A., Fernandes, S.C.M., 2024. Exploring marine-based compounds as cross-linkers to improve the biocompatibility and sustainability of chitosan-based hydrogels. Carbohydr. Polym. Technol. Appl. 8, 100541. https://doi.org/10.1016/J.CARPTA.2024.100541.

Szopińska, M., Namieśnik, J., Polkowska, Ż., 2016. How important is research on pollution levels in Antarctica? Historical approach, difficulties and current trends. Rev. Environ. Contam. Toxicol. 239, 79–156. https://doi.org/10.1007/398_2015_ 5008.

Vijayaraghavan, K., Sathishkumar, M., Balasubramanian, R., 2010. Biosorption of lanthanum, cerium, europium, and ytterbium by a brown marine alga, turbinaria conoides. Ind. Eng. Chem. Res. 49 (9), 4405–4411. https://doi.org/10.1021/ IE1000373. ;JOURNAL:JOURNAL:IECRED;PAGE:STRING:ARTICLE/CHAPTER.

Wiencke, C., & Amsler, C. D. 2012. Seaweeds and their communities in polar regions. 265–291. https://doi.org/10.1007/978-3-642-28451-9_13.