Contamination pattern, in Guadeloupe and in Martinique, involves both (1) Sargassum offshore contaminated by oceanic As, mainly resulting from the human activities at global or local scale, and (2) Sargassum contamination by chlordecone in coastal environment due to water resource and soil pollution by banana weevil control during 70’s and 80’s (Bocquené and Franco, 2005). All the results are detailed in the Appendix 1.
As content offshore has been ensured by Atlantic Ocean samplings in front of Santa Lucia Channel (identified as “Transect” in Table A1 of Appendices): As(V) was the dominant form of arsenic (mean ± standard deviation, 58.2±18.0% of total As), corroborating international literature (Michel, 1985). Climactic As content (125.7 mg/kg dw) is observed since pelagic sampling sites and higher As concentrations in Sargassum ashore, whatever island or sampling sites, are related to drifting algae in opposition to dried ones (Figure 2). We found significantly less total As, As(V), MMA and AsBet in the dried samples from the beach than in the floating algae (P < 0.05). For the As(III) and DMA species, no significant differences were observed (Figure 2). Sargassum are floating algae and beaching often involve a first step of compression of massive Sargassum biomass along the shoreline, during which Sargassum density will exceed the density in the mat. At this step, which have to be more studied to properly understand the inducting parameter(s), Sargassum will be stressed and will transudate. Transudation content is poorly known but authors identified that chlordecone and As are significantly transudate in few hours for floating and sank algae (Devault et al., 2021). Due to tide, gravity waves and wind, a part of Sargassum could beach and be dried in the sun: due to rain and tissue degradation, Sargassum will leach: this leach can reach 22,000 µg/L (Chevalier, pers. com.). Another part can sink and, in case of cup-shaped dent from which Sargassum could not drift away, Sargassum biomass could form a pseudo-vase by sedimentation in shallows. In the present study, authors did not focus in such environments, but limited them to floating Sargassum, beached and fresh ones, beached and dried ones, and piled ones, but two sampling sites correspond to such extreme accretion situation.
Comparing the results of our study with the current literature is delicate because the analysis proposed elsewhere about As were mainly performed on total As content, even including inorganic As species (Maher et al., 1983), focuses on the protocol enhancement (Han et al., 2009), or on the metabolic pathways (Edmonds et al., 2009 ; Pichler et al., 2006 ; Leal-Acosta et al., 2013) not about detailed environmental monitoring (Devault et al., 2020a) or did not include As speciation detail Rodríguez-Martínez et al. (2019). As such, the detailed protocol proposed in the present article provided new insights into As dynamics in algae. Total As concentrations into Sargassum exceed the concentration known for the other algal species ut are in agreement with previous results for those species (Michel, 1985; van Tussenbroek et al., 2017). This upper (at least double) As concentration could be due to pelagic conditions: the other Sargassum species are benthic ones and phosphate concentration in shallows is higher than in deep-sea so the phosphate need is higher.
Benson (1984) and fellows hypothesized that orthophosphate and As are competitive for phosphate transporter and that S. natans and fluitans overuse of phosphate transporter to compensate the phosphate lack in the open ocean, increasing As accumulation. Total As content heterogeneity is limited: if piled Sargassum presents a significantly lower As content than other (26.6±20.9 µg/g and 80.9±29.8 µg/g dw, respectively), piled Sargassum sampling sites, located in Martinique, are scarce. Total concentration, at 80.9±29.8 µg/g dw (minimum 28.8 and maximum 127 µg/g dw) is very in agreement with Rodríguez-Martínez et al. (2019) who reported a median of 80 and a minimum 24 and and maximum of 172 µg/g dw. -This statement has to be limited to total As but, based on the 20 million tons estimation per year of floating Sargassum drifted to Caribbean shores (Wang et al., 2019), even in considering a minimized 50 µg/g dw concentration, the total flux of As is yearly about 1 000 tons. Considering the sites where algae were not piled, a significant distinction could be made between the two places where “pseudo-vase” (defined as densely accreted, Sargassum amounts decay in shallow waters) were sampled: At surface of the amounts, algae will be parched by sun, forming a few centimeters-thick compact crust (able to support a crawling adult but not a walking one) covering decimeters-thick wet rotten algae. They are stuck in place due to the limited tidal range (about 40 cm) and permanent trade winds and currents. Such sites have total As content not significantly different to piled ones but significantly different with other non-piled Sargassum (respectively 22.6±13.5 µg/g and 83.4±27.7 µg/g); in such clogged places, interstitial water into the pseudo-vase reaches more than 1000 µg/L due to As transudate from Sargassum but also due to limited water circulation. For such concentrations, sanitary impact of As is unknown: dermic way contamination has only be studied until 200µg/L (Mink et al., 2008; Tsuji et al., 2014) for intact skin when Sargassum sp. lugs which harsh the skin: impact at 200 µg/L are controversial for intact skin and have to be comforted for scratched one. Progressive accumulation of Sargassum, sank or accumulated as pseudo-vase, is a threat for coastal environment because of this As input at each Sargassum event.
As speciation has been detailed for arsenate, arsenite, methylarsonic acid (MMA), dimethylarsinic acid (DMA), arsenobetaine and arsenocholine. All the organic forms are based on pentavalent As. As(V) prevails in oxic conditions (Michel, 1985; Muse et al., 1989; Nekk, 2002; Pell et al., 2013) (41.8±25.2 mg/kg dw for whole samples: 55.7±18 µg/kg dw in Guadeloupe and 33.0±26.04 µg/kg dw in Martinique (but 39.7±25 µg/kg dw without piled Sargassum) minimum 0.025 µg/kg dw (0.8 µg/kg dw without piled Sargassum) and maximum 106.5 µg/kg dw). Considering the other species of As, they are formed under anoxic conditions (Brown et al., 2010) by reduction of As(V) into As(III), inorganic both but in a reversible process, and microbial pathways to form arseno-organic molecules which lead to a non-reversible speciation (Muse et al., 1989). Comparing Martinique and Guadeloupe results, the presence and abundance of such non-As(V) species are the more segregating: non-As(V) are, in Martinique, more present than in Guadeloupe: As(III) concentration was about 3.8±5.2 µg/kg dw for whole samples: 2.4±2.2 µg/kg dw in Guadeloupe and 4.9±6.4 µg/kg dw in Martinique (but 4.3±6.3 µg/kg dw without piled Sargassum), minimum 0.03 µg/kg dw and maximum 29.9 µg/kg dw, to compare to concentration in MMA (8.5±10.8 µg/kg dw for whole samples: 3.7±4.6 µg/kg dw in Guadeloupe and 12.2±12.4 µg/kg dw in Martinique -but 14.8±12.5 µg/kg dw without piled Sargassum), minimum 0.1 µg/kg dw and maximum 42.9 µg/kg dw (40.3 µg/kg dw without off-sampled Sargassum) and concentration in DMA (8.5±10.8 µg/kg dw for whole samples: 3.7±4.6 µg/kg dw in Guadeloupe and 12.2±12.4 µg/kg dw in Martinique -but 14.8±12.5 µg/kg dw without piled Sargassum), minimum 0.01 µg/kg dw and maximum 28.1 µg/kg dw. In other words, non-As(V) species concentration in Martinique are at least twofold of the corresponding concentration in Guadeloupe, and this ratio often reaches fourfold for the organoarsenic species, even if they are based on As(V). Concentration of arsenite, MMA, DMA are in the same order, and arsenobetaine and arsenocholine in an order less, but with the same higher concentrations in Martinique samples (respectively. 1±1 µg/kg dw in Guadeloupe and 2.9±3.5 µg/kg dw in Martinique and 0.5±0.4 µg/kg dw in Guadeloupe and 1.3±2.2 µg/kg dw in Martinique). Those differences are not significant due to wide standard deviation associated to the spatial heterogeneity and suggest that the fate of As speciation is related to sites. The wide standard deviation is related to spatial heterogeneity, about which the first campaign focused on, but this result is not satisfying and led the authors to sample depending to location on the beach: in water, grounded but still wet, and grounded and desiccated (Figure 2). However, if the ratios between As(V) and the other as form is island-dependent, the considered ratios from the same island are comparable, whatever the location on the shore, i.e. all the As forms are transuding with the same intensity whatever the island. Such inter-island difference might be explained by the presence of the genes driving the organoarsenial metabolisation (Héry et al., 2008) but a dedicated study to state is needed. This inter-island difference might also be related to geomorphologic patterns; Guadeloupe shoreline being straight but Martinique shoreline being rugged in front of Sargassum inputs, authors could hypothesize that Sargassum trend to be more often under anaerobic condition in Martinique than in Guadeloupe. Further studies about current and water column oxygenation have to test this hypothesis, including the frequency of the genes driving the organoarsenial metabolisation.
Considering As fate for drifted Sargassum, authors observed that As content decreases dramatically between floating Sargassum to dried ones (Figure 2). This phenomenon cannot be explained by volatilization (As and organoarsenial compounds studied having a volatilization temperature upper than 350°C) nor degradation –not pertinent for elements. If photolysis of organic forms of arsenic is reported (authors only found Howard and Comber, 1992 as reference), this aspect is too weakly studied to decide, and, whatever, it cannot justify the total As decrease. Figure 2 informs about the temporal process because dried Sargassum are the oldest, but is this arsenic leaching due to rain, due to daily dipping by tide, or both? The dataset does not allow to determine but further studies have to be performed to understand. Nevertheless, Devault et al. (2021) highlighted that Sargassum transudate the main part of their As content in few hours in water column when stressed, addressing the environmental managers reactivity. Considering the second campaign, during which authors distinguished dried and wet algae, the ratios between As species are not modified whatever the concentration decrease level but As species sums still represented 105.1±10.1% of total As measurement, discarding the hypothesis of an apparent decrease due to formation of no-analyzed As species. The homogeneous decrease for most of the measured As species (except DMA and As(III)) is in favor with leaching in opposition to a species-dependant metabolisation. As consequence, As leaching, as leachate on beach sand as transudate in the water column, is an As input which can affect the coastal environment in a Caribbean environment where As were never reported as critical in geochemical background.
3.2 C, N, P
We also performed an elemental analysis of the C, N and P contents (Figure 3). No significant difference was observed for the C/N ratio of the sample from different drifted status (Figure 3A). It is noteworthy that this C/N ratio (mean 24.85) would make Sargassum potentially compatible with its use as organic amendment. Regarding the N/P ratio, we found a significant increase (P < 0.001) in the dried samples from the beach compared to the wet samples and those collected in the sea (Figure 3B). Such increase in the N/P ratio indicates a decrease of P, which could be explained by a phosphorous lixiviation from Sargassum. In oligotrophic environments, such input would have to be quantified to determine how this flux can contribute to eutrophication, but bearing in mind the massive scale of Sargassum beaching.
Sargassum contamination by organic micropollutants has already be reported by Yasmeen et al. (2018) for 48 different molecules in/on S. wightii, Stout et al. (2017) and Torralba et al. (2017) for petroleum hydrocarbons due the Deepwater Horizon oil spill, but the contamination by organic micropollutant has not been reported with the same intensity that inorganic ones, particularly As, reported by Devault et al. (2020a). For the present study, results for the chlordecone concentration are presented in Figures 4A and 4B and highlight that organic micropollutants can contaminate Sargassum to concerning concentrations.
Chlordecone content is due to terrestrial pollution, leading to a coastal contamination. In this way, concentration level of chlordecone could be directly related to chlordecone-contaminated watersheds. In Guadeloupe, chlordecone has been used in the Southern part of Basse-Terre, i.e. the place where Sargassum are the most highly contaminated (Figures 4A and 4B, Figure 5). Pérou river, already studied intensively (Coat et al., 2011; Crabit et al., 2016; Mendez-Fernandez et al., 2018), is known to be a major source of chlordecone to the surrounding shell.
Chlordecone is only observed for sites of Basse-Terre of Guadeloupe, where average concentration is 127.0±169.7 µg/kg dw (minimum: 0.8 µg/kg dw, maximum 616.4 µg/kg dw) for the first sampling campaign and 495±828.5 µg/kg dw for the five sites concerned for the second campaign (minimum 15.9 µg/kg dw, maximum 2697 µg/kg dw). Concerning all the 7 sampling sites of Grande-Terre of Guadeloupe, chlordecone was never observed. Concerning Guadeloupe, chlordecone was only observed in Basse-Terre of Guadeloupe at places where contaminated watershed are known to discharge at sea (Dromard et al., 2019). In the concerned area fishing and collecting seafood is restricted due to the chlordecone threat. However, chlordecone was observed in Saintes archipelagos (first campaign), at 58.8±13.2 µg/kg dw and in Marie-Galante Island, at 7.7 µg/kg dw. These concentration highlight the risk of chlordecone marginal spread due to mats first landed on contaminated shores then drifted to chlrodecone-free coastal areas, where Devault et al. (2021) suggested than chlordecone and other micropollutants can transudate because Marie-Galante Island and Saintes archipelagos are chlordecone-free.
5b-hydrochlordecone was detected and quantified only twice, i.e. where chlordecone concentrations were maximal. Average concentration was 7.3±4.7 µg/kg dw, ranging from 2.4 to 15.26 µg/kg dw.
As for Guadeloupe, campaigns performed in Martinique sites discriminated by chlordecone are included into restricted area due to chlordecone contamination. Sargassum samples contaminated by chlordecone have an average chlordecone concentration of 137.9±90.9 µg/kg dw for the first campaign and 246.6±271.1 µg/kg dw (minimum 4.4 µg/kg dw, maximum 798.9 µg/kg dw) for the second campaign. In opposition to Guadeloupe results, where all the samples from the same sites where contaminated, samples from Martinique show a heterogeneity in the samples, with undetectable concentration and notable contamination on the same place among the replicates. 5b-hydrochlordecone was only observed in high-CLD concentration samples, i.e. a ratio about 0.06±0.01 with chlordecone concentration in agreement with Devault et al. (2016).
In the Sargassum piled sampled in Martinique, no chlordecone was observed but algae collected were sampled on chlordecone-free shores despite few chlordecone vestigial concentrations. Notwithstanding, other pollutions are reported in the Caribbean, due to crop as house contamination (Devault et al., 2020b) and have to be considered as well.
3.3. Consequences for Sargassum issue management
As contamination of Sargassum mat is inevitable because As is deep-sea accumulated by algae. Concerning As, the threat imposes to limit beaching and shallows. Boom cover could be a preliminary action : (1) they are efficient to avoid that sand be picked up with beached algae, sand limiting industrial valorization, (2) Sargassum decay induces leaks and anaerobiosis, worsening the Sargassum effect on biota by oxygen-deprivation, (3) As leaks will be more easily diluted into deeper water column than ashore, (4) chlordecone concentration will be limited due to seawater concentration dilution for estuaries to booms, (5) ease the transport from gathering places to stock even valorization plants.
The As content involves that Sargassum have to be picked up as soon as possible, ideally before a day, in order to limit the leak –and before sank, which occurs in about 3 days, as authors observed. Sargassum collected have to be gathered in dedicated landfill limiting the groundwater pollution and leaching of Sargassum piles have to be treated. As content limits the use of picked up algae: contamination level exceed animal even nutrition, neither crude Sargassum deposition on ground, as it occurs illegally. Shore piles on sand ground, the actual way of stock, have to be avoided. Large amounts of Sargassum, as observed in Pointe rouge (Martinique) and Porte d’Enfer (Guadeloupe) have to be monitored because population could have to walk the “pseudo-vase” in order to reach fishing device, as observed in the field. Abrasive for the human skin, this “pseudo-vase” can increase the risk of As contamination due to the interstitial water concentration.
Chlordecone is adsorbed on Sargassum in polluted bays: polluted and chlordecone-free Sargassum have to be piled separately in order to allow distinct valorization. Drift along the shoreline have to be obstructed in order to limit contaminated mat transfer to chlordecone-free areas, particularly in Guadeloupe where the coastline is less cup-shaped. Even more than for chlordecone-free Sargassum, chlordecone content induces that non-authorized Sargassum valorization has to be tracked.
Leaching from Sargassum occurs in dissolved phase, i.e. under labile and/or colloidal phase, even if the present study does not allow to conclude the prevalence of each. But dissolved phase is the phase in which micropollutants are bioavailable, as for inorganic the authoritative free-ion activity model (Morel, 1983) as for organic ones (Bosma et al., 1997; Leppänen et al., 2000, 2003, 2006; Kraaij et al., 2002, 2003; Kukkonen et al., 2004; Landrum et al., 2007; De Weert et al., 2008; Cui et al., 2013). Progressive contamination by As of the biota is a concern for the whole food web, firstly filtering species, and especially bivalves, which are eaten by local populations.
3.4. Recommendations for sampling strategy
During the present study, two sampling strategies were performed: sampling along the shoreline or sampling perpendicularly to shoreline in order to propose to environmental managers a way to collect beached Sargassum properly. Basing on Table A3 and focusing on As (total) value (i.e.: not the sum of the As species) because of the better quantification frequencies, metrological repeatability and lower standard deviation, blind sampling (i.e. whatever the position) leads to 81.6±30.8 µg/kg dw (standard deviation/mean: 37.8%), (1) grounded and at least partly dried and browned, being drifted to shore but not yet grounded (53±30.3 µg/kg dw ; standard deviation/mean 57.2%), (2) recently grounded, i.e. still wet (91.7±29.3 µg/kg dw ; standard deviation/mean/mean 32%), (3) close to be grounded, in the beating of the waves (92.2±21.9 µg/kg dw standard deviation/mean 23.7%), and (4) still in seawater (92.1±17.7 µg/kg dw ; standard deviation/mean 19.2%).
Considering such results, and regarding that sampling in condition (4) is the less ambiguous (floating, fresh and old gold colored algae), has the most homogenous As results and tends to reach the higher values, authors propose to environmental managers to sample them during their campaign. Considering chlordecone, 4-condition sampled Sargassum reach also the higher values.