Daniel Robledo1*†
Erika Vázquez-Delfín1†
Yolanda Freile-Pelegrín1
Román Manuel Vásquez-Elizondo1
Zujaila Nohemy Qui-Minet1
Adán Salazar-Garibay2,3- 1Applied Phycology Laboratory, Marine Resource Department, CINVESTAV Merida Unit, Mérida, Mexico
- 2CentroGeo Mérida, Parque Científico Tecnológico Yucatán Sierra Papacal, Mérida, Mexico
- 3Mexican Space Agency (AEM), Ciudad de México, Mexico
Mass blooms and stranding of pelagic Sargassum spp. in the Atlantic, termed Sargassum events are becoming more frequent in response to several factors: nutrient enrichment, increased temperature, changes in climatological patterns, but some causes remain unknown. The magnitude of Sargassum events in the Caribbean Sea since 2011 make us aware of the necessity to tackle these events, and macroalgal blooms generally, not only locally but on a regional scale. At least three pelagic species of Sargassum have been dominant in the blooms that have occurred along Caribbean coastlines in great quantities. Due to the regional scale of these events and its complexity, its management should be based on basic and applied information generated by different collaborative actors (national and international) through interdisciplinary and transdisciplinary work. To address this, we propose different phases (exploratory, valorization, and management) and the approach for their study should include detection, collection, stabilization and experimentation. This information will help identify the potential applications and/or ecological services to develop for the exploitation and mitigation strategies in the region. Relevant challenges and opportunities are discussed, remarking on the necessity to evaluate the spatiotemporal variation in the abundance and chemical composition of floating and stranded biomass. The above-mentioned will provide management strategies and economic opportunities as possible solutions to their extensive impact in the Caribbean.
Beyond the Sargasso Sea
The Sargasso Sea, always shrouded in mystery and an object of interest during antiquity, continues today to arouse interest in various fields of knowledge. Commonly known as the subtropical gyre of the North Atlantic, the Sargasso Sea is a region where an immense body of water is bounded by a vast system of circular currents flowing from east to west (North Equatorial Current) and west to east (Gulf Stream). Winds and oceanographic conditions combine to give these waters a very particular identity; from a physical point of view, they are waters of temperature >17°C and particular biogeochemical properties (Bates and Johnson, 2020), and from a biological point of view they are the habitat of several species of the pelagic algae in the genus Sargassum, which supports and incredible amount of marine life (Coston-Clements et al., 1991; Huffard et al., 2014).
The name of the Sargasso Sea was supposedly given by Christopher Columbus or by one of the Portuguese sailors who accompanied him. The term “sargaço,” probably derives, according to the Dictionary of the Spanish Language, from “argaço” (via “algaço,” used in ancient documents to designate algae) and from the Latin Salix (willow trees known colloquially as “sarga” morphologically similar to sargaso). The term could be also related the Portuguese “sal” or “salgado,” meaning salted (Cabral, 2005). Currently, “sargasso” is the colloquial name given to pelagic marine macroalgae found within the Atlantic region.
Since 2011 climatological and environmental conditions promote the transport of floating biomass out of the Sargasso Sea, proliferating in tropical Atlantic between West Africa and South America (Putman et al., 2018; Johns et al., 2020). Tons of these seaweeds have been deposited on beaches, generating beach-cast events that severely impact the Atlantic and Caribbean coasts (Table 1). Although some of these macroalgal arrivals are part of a natural seasonal phenomenon due to biological (life cycles, reproduction and senescence, growth, elongation or biomass increase) and climatological factors (storms, currents, tidal waves, and/or winds) (Orr et al., 2005; Barreiro et al., 2011); additional factors such as increases in seawater nutrients and/or sea surface temperature, changes in ocean currents and wind patterns, hurricanes and maritime traffic have been reported as the causes of the excessive proliferation of Sargassum biomass and its transport to the coasts (Lapointe et al., 2014; Sanchez-Rubio et al., 2018; Wang et al., 2019; Johns et al., 2020; Trinanes et al., 2021). Scientific communities have raised a series of questions about the origin, prevalence and impacts of this phenomenon many of which remain unknown. In the present work we review some of the impacts reported for the Atlantic and Caribbean coasts and the strategies that should be followed to develop an adequate management of this phenomenon, while identifying some of the challenges and opportunities for the Caribbean region.
Table 1. Sargassum events reported for the Caribbean region. Location, scope of the study and term used to describe the phenomenon.
Different terminology has been applied for describing the unprecedent quantities of holopelagic Sargassum impacting the coasts, including “Sargassum blooms” (Lapointe, 2019; Wang et al., 2019), “Massive Golden Tides” (Smetacek and Zingone, 2013), “Sargassum Brown Tides” (van Tussenbroek et al., 2017), “Sargassum events” (Fidai et al., 2020) and “Sargassum influx” (Franks et al., 2012); or colloquially “massive arrivals” and “Sargassum massive accumulations”. However, there is no consensus about the term to define the phenomenon observed. More recently, “Sargassum event” has been defined by Fidai et al. (2020) as a “continuous bloom of any Sargassum in open oceans or, an aggregation of landed Sargassum with the potential to disrupt local social, economic or ecosystem functioning, or to impact human health; an event can affect one country or several contiguous countries.” In the present manuscript, we use “Sargassum event” as an appropriate term for the observed phenomenon in the Caribbean region, which includes a large quantity of stranded biomass that generates ecological and socioeconomic impacts in the coastal areas.
Sargassum Species in the Caribbean Events
The genus Sargassum C. Agardh has the highest morphological complexity in the class Phaeophyceae, with species distributed in almost all ocean basins (Phillips and Fredericq, 2000). The great variability of morphological characteristics between individuals of the same species or even in the same individual in response to climatic and environmental conditions (Kilar et al., 1992) complicates the delineation and identification of Sargassum species in the Atlantic (Parr, 1939; Mattio and Payri, 2011; Schell et al., 2015). Therefore, studies in recent years have included molecular and biochemical characters (Amaral-Zettler et al., 2017; González-Nieto et al., 2020; Rosado-Espinosa et al., 2020; Hernández-Bolio et al., 2021). Nevertheless, molecular markers (ITS, psaA, RuBisCO spacer, rbcl, COI, cox3, 23S-tRNA val spacer and partial mt23S) are not conclusive and the taxonomy of the group needs further analysis (Stiger et al., 2003; Mattio and Payri, 2011; Amaral-Zettler et al., 2017; González-Nieto et al., 2020). Recent studies in the Caribbean and Gulf of México have confirmed the presence of the holopelagic species Sargassum natans (morphotypes I and VIII) and S. fluitans (morphotype III) in the recent Sargassum events (García-Sánchez et al., 2020) (Figure 1). Ongoing research in our laboratory to characterize the stranded biomass in the Mexican Caribbean has allowed to identify the presence of the 3 holopelagic taxa mentioned above, representing 99.5% of the fresh biomass. Moreover, six Sargassum benthic species (S. acinarium, S. buxifolium, S. platycarpum, S. polyceratium var. ovatum, S. pteuropleuron, and S. ramifolium) and three seagrass species (Thalassia testudinum, Syringodium filiforme, and Halodule wrightii) have been also identified as a minor component of the events, but can reach up to 22% of the fresh biomass depending on the season. These efforts have expanded to include the development of digital tools to identify and characterize the pelagic and benthic species of Sargassum of the Mexican Caribbean (Vázquez-Delfín et al., 2020).
Figure 1. Pelagic taxa involved in the Sargassum events at the Caribbean. (A): Sargassum natans I; (B): S. fluitans III; (C): S. natans VIII (Parr, 1939). Scale: 1 cm. Leaf shape, axes and shape of vesicles are shown. For detailed morphological descriptions see Vázquez-Delfín et al., 2020. (D): Sentinel-2 satellite image for the north coast of the Mexican Caribbean coast showing Sargassum floating biomass (red); (E): Management of Sargassum stranded biomass in the Mexican Caribbean coast.
Environmental and Socioeconomic Concerns
Sargassum events have resulted in excessive seaweed-stranding biomass causing considerable damage to the environment, human health and local economy of the Caribbean, the Gulf of Mexico and West Africa (Table 2). In the Caribbean Sea, from the coasts of Trinidad and Tobago, Guadeloupe and Martinique, Dominican Republic, Cuba, Colombia and the Mexican Caribbean coasts, between 2011 and 2020, Sargassum events have been recorded and have increased in volume and damage over time (Table 1). Current reports estimate that around 20 million metric tons of floating Sargassum biomass can accumulate off the coast of northeastern South America and potentially distributed throughout the Caribbean (Wang et al., 2019).
Table 2. Ecological and socioeconomic impacts of Sargassum events for the Atlantic coasts, with special attention to the Caribbean region/Western Atlantic.
Sargassum events have adverse impacts on the coastal ecosystems and human communities (Table 2). The contamination of beaches, due to the in situ decomposition of excessive algal material, and groundwater, due to leachates from onshore algal disposal sites, impacts the environment and the economic activities developed in coastal areas (Franks et al., 2012; Chávez et al., 2020). It should be noted that the degradation of species of Sargassum depends on the dissolution and degradation of alginate, the main structural component of its cell walls, while other reactive compounds in the algae also affect degradation (Forro, 1987; Conover et al., 2016; Thomas et al., 2017). In most cases, the degradation of the algae after an event can cause adverse effects on the health of the surrounding ecosystems. In near-shore environments, and even in deeper areas, the rate of organic matter degradation is determined by factors such as microbial accessibility, temperature, and pH. As a product of the biological degradation of brown algae, gases (H2S, NH3, CO2, CH4), organic matter, and a high biological oxygen demand (BOD) area is formed, giving rise to anaerobic zones (Song et al., 2020). In addition, different dissolved compounds, such as mannitol, volatile fatty acids, alcohols and polyphenols, can be released from their tissues. Bacteria involved in these processes generally use the products to maintain their own metabolism (Thomas et al., 2017), while some other nutrients or ions released may cause eutrophication (van Tussenbroek et al., 2017). Nevertheless, there is a lack of knowledge regarding the factors that trigger Sargassum proliferation and degradation, which constrains predictions of their impact on the environment.
Beyond the negative effects of Sargassum events, it should be noted that floating and stranded biomass provides some important elements to coastal and marine ecosystems (Table 2) and some emergent opportunities have been identified for local communities (see section “Valorization and management of Sargassum biomass: opportunities”). Sargassum holopelagic species may also play a unique role in the North Atlantic sub-gyre as they are home to an iconic drifting pelagic ecosystem, including some endemic species (Lopez et al., 2008; Louime et al., 2017; Brooks et al., 2018). Large quantities of holopelagic Sargassum suggests that carbon sequestration can be a positive outlook of this phenomena, particularly counterbalancing habitat loss and sequestration capacity of seagrasses and mangroves, both highly impacted and degraded by anthropogenic activities (Duarte, 2017). The relevance of macroalgae communities to sequester and transfer carbon and consequently their potential use as mitigation strategy to climate change seems clear, albeit arguable (Duarte, 2017; Krause-Jensen et al., 2018; Smale et al., 2018). Macroalgal communities can take up to 1.5 Pg C yr–1 globally via net production from which 0.173 Pg C yr–1 (88%) is sequestered in deep ocean (Krause-Jensen and Duarte, 2016; Krause-Jensen et al., 2018). The Sargassum biomass in Atlantic, spread over 227 × 104 km2, produces an estimated mean annual carbon stock of 7.5 PgC (Gouvêa et al., 2020) similar to seagrass or mangroves (5–8 Pg C) (Howard et al., 2017). If those numbers are correct, holopelagic Sargassum must be considered as an important pathway for CO2 removal from the atmosphere. Moreover, its interconnectivity with deep ocean and coastal zones makes pelagic Sargassum a key element for Blue Carbon strategies, but the fate of this carbon should be further investigated. Alternatively, artificial burial in isolated areas or deposition in the deep ocean deserves attention since it will take carbon out of its cycle. Nevertheless, Sargassum biomass does not constitute a static resource and the estimates of sequestration potential should be taken with caution. Additionally, possible uses of the harvested seaweed biomass, either to be used as biofuel (López-Sosa et al., 2020), methanisation and/or for extracting valuable compounds could be an efficient solution for the management of the Sargassum biomass. The adequate management of this resource to counteract negative impacts of Sargassum events is desirable but requires further investigation.
Strategies to Approach the Study of the Phenomenon: From the Exploration to Management
Sargassum events are complex phenomena that involves different participatory actors and decision makers, affects human health, the economy and ecological marine and coastal systems. It also has a large spatiotemporal variation that affects different countries at a regional scale, either simultaneously or at different time points. Therefore, to address this phenomenon, we should include different perspectives, interdisciplinary and transdisciplinary approaches and participative management, which are current topics in sustainability and international collaboration (Kasemir et al., 2003; Lang et al., 2012). Some of the priority issues identified are: gathering information to forecast the distribution and arrival of floating biomass, explore the causes and effects of the phenomenon, identify the challenges of their offshore collection and the implementation of stabilization strategies to avoid degradation of the feedstock. Finally, it is crucial to obtain information to valorize the biomass of pelagic Sargassum, and for the development of its exploitation and mitigation strategies to achieve effective management. To reach this ambitious objective we summarize the different phases and some of the factors that should be considered, focusing on the exploratory phase, which is a current ongoing phase in several Caribbean countries (Figure 2). Although in some countries different exploitation proposals (Rodríguez and Orellana, 2008; Carrillo et al., 2012; Velasco-González et al., 2013; Cuxim and Balam, 2015; Rodríguez-Martínez et al., 2016; Mohammed et al., 2019) and some mitigation strategies have been developed (SEMARNAT, 2015; CONACYT, 2020), they have been unsuccessful due to the lack of exploratory and basic information, and the lack of international cooperation that is required to address a phenomenon of this magnitude. It is worth mentioning that Sargassum events impacts the coastal human communities, thus, anthropological and socio-economic studies are required in the exploratory phase to develop normativity and regulations. In relation to the participatory actors (government, academic institutions, local communities, private enterprises), we remark on the necessity of their involvement in all the proposed phases in a collaborative way. It is noteworthy that the relevance of local communities to natural resource management has been demonstrated as both effective and relevant on sustainability and conservation topics (Shackleton et al., 2002; Fabricius, 2004; Fabricius and Collins, 2007). However, there is no published information on the role of local communities to address the Sargassum events in the region for the proposed phases, so its role is undefined and the opportunity for participation is missing.
Figure 2. Strategies to address the management of Sargassum events in the region. The actions needed, relevant factors and actors involved are included, from exploratory to management phase. ?: indicates that official information is not available to identify the specific role of local communities.
The exploratory phase of Sargassum events has allowed the development of valuable information about the phenomenon. The detection and monitoring of floating biomass has been successful for over a decade (Franks et al., 2012; Gower et al., 2013; Congedo, 2016; Arellano-Verdejo et al., 2018; Cuevas et al., 2018; Wang et al., 2018; Arellano-Verdejo and Lazcano-Hernández, 2021). Thus, low, moderate and high spatial resolution satellite images have been employed to implement algorithms for the monitoring of pelagic Sargassum. The most used remote sensing inputs for mapping Sargassum coverage are the optical images which use solar radiation (Landsat, Sentinel-2, MODIS, and SPOT). The Maximum Chlorophyll Index (MCI) (Gower et al., 2006), the MODIS Red Edge (MRE) (Gower et al., 2013), Normalized Difference Vegetation Index (NDVI) (Lasquites et al., 2019) and the Floating Algae Index (FAI) are some of the straightforward image-processing algorithms that are also commonly used. However, more complex algorithms need to be implemented such as Alternate Floating Algae Index (AFAI) (Wang and Hu, 2016), Random Forest algorithm (Cuevas et al., 2018) and Deep Learning and Recursive Neural Networks approaches (Arellano-Verdejo et al., 2018). Hence, low resolution data allows for covering more extensive areas in one image and daily monitoring of Sargassum, whereas high resolution data gives more specific details, but lacks the daily supply of images. The spatial configuration of pelagic Sargassum masses tends to generate elongated lines of few metres wide, termed windows, or its accumulation in small patches. If these configurations do not exceed the minimum detection size and density limit (20% of the area of the pixel), then the ability to detect Sargassum through satellite images is severely restricted (Hu et al., 2015). In this sense, low resolution sensors may underestimate the presence of floating algae. Therefore, the use of high-resolution data (<10 m resolution) is highly recommended to detect and map the distribution and cover of Sargassum on open sea surface. According to Hu et al. (2015), the area of Sargassum inside of a 10 m resolution pixel should be bigger than 20 m2 in order to be accurately detected by any of the aforementioned algorithms.
Other actions needed in the exploratory phase are scarce or restricted to some countries and focus on specific aspects such as the determination of the chemical composition of pelagic Sargassum (Lapointe et al., 2014; Sissini et al., 2017; Lapointe, 2019; Chávez et al., 2020; García-Sánchez et al., 2020; Rodríguez-Martínez et al., 2020; Amador-Castro et al., 2021; Davis et al., 2021).
In the management phase, national and local authorities, civil society and private sector have made some efforts, which include implementation of forecasting systems, trials on different strategies of containment to avoid the arrival of floating biomass to the coasts, and removal actions of the stranded biomass either by hand or using machinery (Rodríguez-Martínez et al., 2016; Chávez et al., 2020). However, some of these efforts have been unsuccessful. For example, in 2018 a barrier system project was implemented in some areas of the Mexican Caribbean coast, but the amount of Sargassum biomass exceeded the capacity of the barriers and failed, causing severe accumulations not only on the beaches but on the seabed due to the sinking of the biomass accumulated in the barriers (personal observation EVD, DR). Some private initiatives have developed not only containment barriers, but diversion barriers to deflect the biomass to particular areas where it is removed (DESMI project, 2021). Nevertheless, the collection of pelagic Sargassum at sea should include the development of methods to avoid incidental capture of the macrofauna associated with pelagic masses, such as juvenile fishes and turtles (Maurer et al., 2015).
Valorization and Management of Sargassum Biomass: Opportunities
The valorization of algal biomasses, i.e., improving or attempting to improve the value, price or use of Sargassum, can be an opportunity to ameliorate the economic damage generated in the region (Table 2). This may be particularly effective if authorities are able to harvest biomass at a proper time and exhaustively avoiding its accumulation in order to prevent some of the damage caused after stranding. However, this task has proven to be difficult, especially during massive events, as mentioned above. Also, Sargassum spp. capacity to absorb heavy metals and its discontinuous and unreliable supply due to seasonal variations are the main constraints to harvest this alga for commercial exploitation, as has been shown for the invasive S. muticum in Europe (Lodeiro et al., 2004; Carro et al., 2015). Therefore, understanding the spatiotemporal changes in its abundance, biochemical composition and the impact of Sargassum proliferation, persistence and degradation is critical.
During the inundations of the Gulf of Mexico and the Caribbean in 2015, approximately 10,000 tons of fresh seaweed were stranded on beaches daily (Milledge and Harvey, 2016). Tourism in the Caribbean is worth $29.2 billion dollars, and it has been estimated that it will cost at least $120 million dollars to clean-up the Sargassum inundations in this region (Milledge and Harvey, 2016). Due to the economic cost of removing the stranded seaweed, there is an imperative need to define technical and ecological measures to forecast an event and reduce its proliferation and valorize its biomass. Large volumes of algae reaching the beaches have a great potential to be used for different purposes, as proposed in recent publications (Milledge et al., 2015; Milledge and Harvey, 2016; Amador-Castro et al., 2021; Davis et al., 2021). However, in order to propose its further use and harvesting strategies, it is essential to know basic aspects of the incoming resource. Several elementary questions need to be answered: Which are the species found and what is its relative abundance? What are the regional and local factors that promote proliferation and accumulation of biomass in the beaches? What is the chemical composition of the species, and how this composition varies spatiotemporally? These are fundamental areas of research to understand the potential use of the resource.
Interestingly, each year Sargassum events in the Caribbean have been characterized by the predominance of a particular taxon depending on the geographical location. For example, S. natans VIII was described as the predominant species in 2015 events (Amaral-Zettler et al., 2017), but recent studies have shown that predominant taxa could vary according to location and time (Schell et al., 2015; García-Sánchez et al., 2020). In other coastal areas such as the Mexican Caribbean the predominance of S. fluitans has been more evident throughout the years, although different proportions of the other holopelagic and benthic species of Sargassum are also present (Vázquez-Delfín et al., 2020). Differences in the occurrence and relative abundance of Sargassum species/taxa may translate into significant differences in the biochemical composition of the biomass, including toxic metals content such as Arsenic (Rodríguez-Martínez et al., 2020). Furthermore, the high ash and water content are important constraints in the use of Sargassum biomass as a biofuel source (Milledge et al., 2014). Nevertheless, previous studies on Sargassum species have shown that through a biorefinery approach other high value compounds such as antioxidants are viable to obtain (Namvar et al., 2013; Milledge et al., 2015).
Sargassum species have the potential to produce a wide range of high value biochemicals, nutraceuticals and pharmaceuticals (Davis et al., 2021). However, considerable research is still required in order to characterize and understand Sargassum events, including seasonal variation in biochemical composition, as well as processes with high added value and the development of commercial products. Biomolecules of interest may vary with physical-chemical parameters such as light intensity, nutrient availability, and temperature (Tanniou et al., 2013). Therefore, work should focus on the quantity and quality of potential compounds, for example those with antioxidant properties such as carbohydrates, lipids, carotenoids, phenols and proteins, which may vary spatiotemporally. Important insights on when and how to collect and preserve the algae or how heavy metals uptake and accumulation behaves in relation to species are research areas of interest. Holopelagic Sargassum is always moving and exposed to very contrasting environments, from marine to coastal areas, with significant differences in temperature, nutrient loading, exposure to heavy metals, etc., and thus changing and adjusting its metabolic performance. This, in turn affects the chemical composition of pelagic seaweeds. The main challenge of the affected countries is to manage and valorize Sargassum biomass under a sustainable and economically efficient approach. Nevertheless, we must first understand what are the main environmental factors that induce their proliferation, regulate physiology and growth, and how these affect yield and quality of commercial interest compounds (Figure 2).
The basic chemical composition of stranded Sargassum biomass from the Mexican Caribbean is shown in Figure 3; however, these values may vary depending on several factors including species, seasonality and extraction methods (Rosado-Espinosa et al., 2020; Terme et al., 2020). Care must be taken to consider the level of degradation of Sargassum spp. while stranded in the beach, where microbial composition and decomposition rates vary with physical-chemical parameters. Moreover, high light intensities will also promote photodegradation of both floating and stranded Sargassum (Powers et al., 2019). The decay of macroalgal also depends on their biochemical composition and morphological complexity (Braeckman et al., 2019).
Figure 3. Chemical composition of stranded biomass of Sargassum spp. from Mexican Caribbean. Elemental and proximal composition and commercial interest polysaccharides. Analysis from samples collected at Puerto Morelos, Quintana Roo, Mexico during 2018 Sargassum event. Values are reported with respect to the dry weight (dw).
Amongst the brown seaweeds commonly used commercially, Sargassum spp. is the least exploited genus, despite its enormous quantities found all over the world and in recent events. Valuable hydrocolloids, such as alginate and fucoidan, are also found in Sargassum, as in other Phaeophycean algae. Alginates are cellular wall polysaccharides found in the matrix of brown seaweeds, composed of linear binary copolymers of (1 → 4)-linked β -D-mannuronic acid (M) and ∝ -L-guluronic acid (G) monomers, whereas fucoidans designate a group of fucose-containing sulfated polysaccharides, which are highly heterogeneous in structure, made up of fucose, galactose, mannose, xylose, glucose, uronic acids, sulfate substituents, and sometimes acetyl groups (Draget et al., 2005). A broad number of applications have been described for brown algae polysaccharides, most notably antioxidant, anticoagulant and antithrombotic, antiviral, anticancer, antidiabetic, immunomodulating, anti-inflammatory, antilipidemic and anti-fertilization effects (Ale et al., 2011). However, Sargassum species typically give low yields (< 19%) of poor-quality alginate (Torres et al., 2007), but they may be potential sources of fucose-containing sulfated polysaccharides.
As part of an ongoing research program in the Mexican Caribbean, estimates of alginate or fucoidan content in stranded Sargassum biomass were determined (Figure 3). Mean content of alginates and fucoidans are higher in S. fluitans than S. natans I, and both cell wall polysaccharides account for ∼40% in dry weight (dw), with alginate content almost four-fold higher than fucoidan. Manuronic (M) and guluronic (G) blocks forming the alginate structure are also important to define the quality of alginates, a higher proportion of G blocks results in higher gel strength (Mohammed et al., 2019). These authors found optimum extraction conditions for S. natans with a yield between 17 and 28% after a two stage extraction processes resulting in an alginate with an M/G ratio of 0.45, indicating high guluronic acid content, aligned to high gelling capabilities (Mohammed et al., 2019).
On the other hand, fucoidans found in various Sargassum species are prominently sulfated galactofurans, which may differ considerably in chemical composition, molecular mass and structure, depending on the algal species studied, spatial and temporal variation, or on the type of tissue sampled (Duarte et al., 2001). Extraction and purification methods may greatly affect the structure and the composition of the isolated fucoidan and may significantly affect the results obtained when the fucoidan products are being evaluated for bioactivity (Hifney et al., 2016). These authors developed an efficient and effective extraction process for the sulfated polysaccharides from Sargassum sp. with a fucoidan yield and sulfate content of 19 and 47.6% (dw) respectively, preserving their structure and biological activity.
Currently, alginates and fucoidans are the only compounds of Sargassum spp. with a current developed value chain. However, further studies should be performed to find other potential uses and other extractable compounds. Thus, the variation in the relative abundance of species and its chemical composition during each Sargassum event will determine their valorization and management strategy.
Challenges and Concluding Remarks
The management of Sargassum events represent a challenge to the participatory actors, stakeholders and decision makers, which includes governments, research institutions, local communities, tourist industry and other private sectors. Some priority actions are needed:
a) Continuous monitoring of physicochemical parameters in strategic areas. Relevant seawater physicochemical parameters, i.e., dissolved oxygen (DO), pH, turbidity and nutrient concentrations. Measurement of toxic gases (H2S and NH3) when significant amounts of Sargassum remain stranded in the beach for more than 72 h is required (Resiere et al., 2020). This monitoring is fundamental for understanding how Sargassum events impact ecosystems/locations and to define management policies. Safe protocols for Sargassum collection and biomass removal will help prevent negative impacts during extreme events.
b) To address the Sargassum events in the Caribbean Sea under a sustainable development approach, we must combine ecological, physiological, biotechnological and socioeconomic approaches. Interdisciplinary research must focus, not exclusively, but consistently in: (i) improving our knowledge on the physiology of Sargassum species and how they respond to environmental changes in order to estimate the triggering factors and abundance of their biomass. (ii) understanding how environmental conditions affect the quality and quantity of compounds of interest in Sargassum species and therefore determine the optimal collection opportunities, in order to develop a sustainable bioprocess to valorize Sargassum biomass.
c) Develop standardization protocols for Sargassum studies through international cooperation and transdisciplinary work, i.e., threshold values for heavy metal content, H2S and NH3 air concentrations (ANSES, 2017; Lähteenmäki-Uutela et al., 2021). International consensus on regulations for Sargassum detention, collection and treatment methods to avoid/reduce environmental damage are required. Caribbean Regional Fisheries Mechanisms (CRFM) has a model protocol for the management of extreme accumulations of Sargassum for member States (CRFM, 2016); whereas countries like France and Mexico have also prepared recommendations to manage and regulate Sargassum events (ANSES, 2017; CONACYT, 2020).
The above-mentioned actions will definitely aid in finding the right balance between the valorization of natural resources, technological development and responding to the need for coastal management in the affected areas. Interaction between the different actors is fundamental to the development of strategic management, processes and technologies.
Author Contributions
DR, EV-D, R-VE, ZQ-M, AS-G, and YF-P revised and agreed on the content of the work. All authors contributed to the article and approved the submitted version.
Funding
CONACyT PN2015-01-575 “Valorización de la biomasa de arribazón del género Sargassum para su uso y aprovechamiento” funded this research.
Conflict of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Acknowledgments
This manuscript was presented at the Mini symposium “Macroalgal blooms on the rise around the world” convened by Peimin He (China), Jang K. Kim (South Korea) at the International Seaweed Symposium 23rd in Jeju, South Korea, in 2019. RM-VE acknowledges the CONACYT Program “Estancias Posdoctorales Nacionales, 2019–2020” for a postdoctoral fellowship (CVU 206050).
References
Ale, M. T., Mikkelsen, J. D., and Meyer, A. S. (2011). Important determinants for fucoidan bioactivity: a critical review of structure-function relations and extraction methods for fucose-containing sulfated polysaccharides from brown seaweeds. Mar. Drugs 9, 2106–2130. doi: 10.3390/md9102106
Amador-Castro, F., García-Cayuela, T., Alper, H. S., Rodriguez-Martinez, V., and Carrillo-Nieves, D. (2021). Valorization of pelagic sargassum biomass into sustainable applications: current trends and challenges. J. Environ. Manage. 283:112013. doi: 10.1016/j.jenvman.2021.112013
Amaral-Zettler, L. A., Dragone, N. B., Schell, J., Slikas, B., Murphy, L. G., Morrall, C. E., et al. (2017). Comparative mitochondrial and chloroplast genomics of a genetically distinct form of Sargassum contributing to recent “Golden Tides” in the Western Atlantic. Ecol. Evol. 7, 516–525. doi: 10.1002/ece3.2630
ANSES (2017). Expositions Aux Émanations D’algues Sargasses en Décomposition Aux ANTILLES et en Guyane. (in French). Créteil: ANSES.
Arellano-Verdejo, J., and Lazcano-Hernández, H. E. (2021). Collective view: mapping Sargassum distribution along beaches. PeerJ Comput. Sci. 7:e528. doi: 10.7717/peerj-cs.528
Arellano-Verdejo, J., Lazcano-Hernandez, H.-E., and Cabanillas-Terán, N. (2018). ERISNet: deep learning network for sargassum detection along the coastline of the Mexican Caribbean. PeerJ 7:1. doi: 10.7287/peerj.preprints.27445
Azanza, J., and Pérez, R. (2016). Impact of Sargassum influx during 2015 summer on marine turtles of Playa la Barca, Peninsula de Guanahacabibes. Rev. Investig. Mar. 36, 54–62.
Barreiro, F., Gómez, M., Lastra, M., López, J., and De La Huz, R. (2011). Annual cycle of wrack supply to sandy beaches: effect of the physical environment. Mar. Ecol. Prog. Ser. 433, 65–74. doi: 10.3354/meps09130
Bates, N. R., and Johnson, R. J. (2020). Acceleration of ocean warming, salinification, deoxygenation and acidification in the surface subtropical North Atlantic Ocean. Nat. Commun. Earth Environ. 1:33. doi: 10.1038/s43247-020-00030-5
Braeckman, U., Pasotti, F., Vázquez, S., Zacher, K., Hoffmann, R., Elvert, M., et al. (2019). Degradation of macroalgal detritus in shallow coastal Antarctic sediments. Limnol. Oceanogr. 64, 1423–1441. doi: 10.1002/lno.11125
Brooks, M., Coles, V. J., Hood, R. R., and Gower, J. F. R. (2018). Factors controlling the seasonal distribution of pelagic Sargassum. Mar. Ecol. Prog. Ser. 599, 1–18. doi: 10.3354/meps12646
Cabral, J. P. (2005). A apanha de algas na Ilha da Ínsua (Caminha) nos séculos XVII-XIX. Singularities and conflitos. Finisterra XL 80, 5–22.
Carrillo, S., Bahena, A., Casas, M., Carranco, M. E., Calvo, C. C., Ávila, E., et al. (2012). El alga Sargassum spp. como alternativa para reducir el contenido de colesterol en el huevo. Rev. Cuba. Cienc. Agríc. 46, 181–186.
Carro, L., Barriada, J. L., Herrero, R., and de Vicente, M. E. S. (2015). Interaction of heavy metals with Ca-pretreated Sargassum muticum algal biomass: characterization as a cation exchange process. Chem. Eng. J. 264, 181–187. doi: 10.1016/j.cej.2014.11.079
Chávez, V., Uribe-Martínez, A., Cuevas, E., Rodríguez-Martínez, R. E., van Tussenbroek, B. I., Francisco, V., et al. (2020). Massive influx of pelagic Sargassum spp. on the coasts of the Mexican Caribbean 2014–2020: challenges and opportunities. Water 12, 1–24. doi: 10.3390/w12102908
CONACYT (2020). Agenda de Ciencia, Tecnología e Innovación Para la Atención, Adaptación y Mitigación Del Arribo De Sargazo Pelágico a México. Mexico: CONACYT.
Conover, J., Green, L. A., and Thornber, C. S. (2016). Biomass decay rates and tissue nutrient loss in bloom and non-bloom-forming macroalgal species. Estuar. Coast. Shelf Sci. 178, 58–64. doi: 10.1016/j.ecss.2016.05.018
Coston-Clements, L., Settle, L. R., Hoss, D. E., and Cross, F. A. (1991). Utilization of the Sargassum Habitat by Marine Invertebrates and Vertebrates: A Review. NOAA Technical Memorandum NMFS-SEFSC-296. Washington, DC: NOAA.
CRFM (2016). Model Protocol for the Management of Extreme Accumulations of Sargassum on the Coasts of CRFM Member States. Technical & Advisory Document, No. 2016/5. New Delhi: CRFM.
Cuevas, E., Uribe-Martínez, A., and Liceaga-Correa, M. Á (2018). A satellite remote-sensing multi-index approach to discriminate pelagic Sargassum in the waters of the Yucatan Peninsula, Mexico. Int. J. Remote Sens. 39, 3608–3627. doi: 10.1080/01431161.2018.1447162
Cuxim, M. E., and Balam, R. V. (2015). Proceso para la elaboración de un biofertilizante a base de Sargassum. Rev. Ingeniantes 1, 56–59.
Davis, D., Simister, R., Campbell, S., Marston, M., Bose, S., McQueen-Mason, S. J., et al. (2021). Biomass composition of the golden tide pelagic seaweeds Sargassum fluitans and S. natans (morphotypes I and VIII) to inform valorisation pathways. Sci. Total Environ. 762:143134. doi: 10.1016/j.scitotenv.2020.143134
DESMI project (2021). Available online at: https://www.desmi.com/customer-stories/the-desmi-sea-turtle-sargazo-project/ (accessed June 10, 2021).
Draget, K. I., Smidsrød, O., and Skjåk-Bræk, G. (2005). “Alginates from algae,” in Polysaccharides and Polyamides in the Food Industry, eds A. Steinbüchel and S. K. Rhee (Hoboken, NJ: Wiley).
Duarte, C. M. (2017). Reviews and syntheses: hidden forests, the role of vegetated coastal habitats in the ocean carbon budget. Biogeosciences 14, 301–310. doi: 10.5194/bg-14-301-2017
Duarte, M. E. R., Cardoso, M. A., Noseda, M. D., and Cerezo, A. S. (2001). Structural studies on fucoidans from the brown seaweed Sargassum stenophyllum. Carbohydr. Res. 333, 281–293. doi: 10.1016/s0008-6215(01)00149-5
Fabricius, C. (2004). “The fundamentals of community-based natural resource management,” in Rights Resources and Rural Development Community-based Natural Resource Management in Southern Africa, eds C. Fabricius, E. Koch, S. Turner, and H. Magome (London: Earthscan), 18–58.
Fabricius, C., and Collins, S. (2007). Community-based natural resource management: governing the commons. Water Policy 9, 83–97. doi: 10.2166/wp.2007.132
Fidai, Y. A., Dash, J., Tompkins, E. L., and Tonon, T. (2020). A systematic review of floating and beach landing records of Sargassum beyond the Sargasso Sea. Environ. Res. Commun. 2:122001. doi: 10.1088/2515-7620/abd109
Forro, J. (1987). “Microbial degradation of marine biomass,” in Seaweed Cultivation for Renewable Resources, eds K. T. Bird and P. H. Benson (Amsterdam: Elsevier), 305–325.
Franks, J., Jhonson, D., Ko, D., Sanchez-Rubio, G., Hendon, J., and Lay, M. (2012). “Unprecedented influx of pelagic Sargassum along Caribbean island coastlines during summer 2011,” in Proceedings of the 64th Gulf and Caribbean Fisheries Institute, Mexico.
García-Sánchez, M., Graham, C., Vera, E., Escalante-Mancera, E., Álvarez-Filip, L., and van Tussenbroek, B. I. (2020). Temporal changes in the composition and biomass of beached pelagic Sargassum species in the Mexican Caribbean. Aquat. Bot. 167:103275. doi: 10.1016/j.aquabot.2020.103275
Gavio, B., Rincón-Díaz, M. N., and Santos-Martínez, A. (2015). Massive quantities of pelagic Sargassum on the shores of San Andres Island, Southwestern Caribbean. Acta Biol. Colomb. 20, 239–241. doi: 10.15446/abc.v20n1.46109
González-Nieto, D., Oliveira, M. C., Resendiz, M. L. N., Dreckmann, K. M., Mateo-Cid, L. E., and Sentíes, A. (2020). Molecular assessment of the genus Sargassum (Fucales, Phaeophyceae) from the Mexican coasts of the Gulf of Mexico and Caribbean, with the description of S. xochitlae sp. nov. Phytotaxa 461, 254–274. doi: 10.11646/phytotaxa.461.4.3
Gouvêa, L. P., Assis, J., Gurgel, C. F. D., Serrão, E. A., Silveira, T. C. L., Santos, R., et al. (2020). Golden carbon of Sargassum forests revealed as an opportunity for climate change mitigation. Sci. Total Environ. 729:138745. doi: 10.1016/j.scitotenv.2020.138745
Gower, J., Hu, C., Borstad, G., and King, S. (2006). Ocean color satellites show extensive lines of floating Sargassum in the Gulf of Mexico. IEEE Trans. Geosci. Remote Sens. 44, 3619–3625. doi: 10.1109/TGRS.2006.882258
Gower, J., Young, E., and King, S. (2013). Satellite images suggest a new Sargassum source region in 2011. Remote Sens. Lett. 4, 764–773. doi: 10.1080/2150704X.2013.796433
Hernández-Bolio, G. I., Fagundo-Mollineda, A., Caamal-Fuentes, E. E., Robledo, D., Freile-Pelegrín, Y., and Hernández-Núñez, E. (2021). NMR Metabolic profiling of Sargassum species under different stabilization/extraction processes. J. Phycol. 57, 655–663. doi: 10.1111/jpy.13117
Hifney, A. F., Fawzy, M. A., Abdel-Gawad, K. M., and Gomaa, M. (2016). Industrial optimization of fucoidan extraction from Sargassum sp. and its potential antioxidant and emulsifying activities. Food Hydrocolloids 54, 77–88. doi: 10.1016/j.foodhyd.2015.09.022
Howard, J., Sutton-Grier, A., Herr, D., Kleypas, J., Landis, E., Mcleod, E., et al. (2017). Clarifying the role of coastal and marine systems in climate mitigation. Front. Ecol. Environ. 15, 42–50. doi: 10.1002/fee.1451
Hu, C., Feng, L., Hardy, R. F., and Hochberg, E. J. (2015). Spectral and spatial requirements of remote measurements of pelagic Sargassum macroalgae. Remote Sens. Environ. 167, 229–246. doi: 10.1016/j.rse.2015.05.022
Huffard, C. L., von Thun, S., Sherman, A. D., Sealey, K., and Smith, K. L. (2014). Pelagic Sargassum community change over a 40-year period: temporal and spatial variability. Mar. Biol. 161, 2735–2751. doi: 10.1007/s00227-014-2539-y
Johns, E. M., Lumpkin, R., Putman, N. F., Smith, R. H., Muller-Karger, F. E., Rueda-Roa, T., et al. (2020). The establishment of a pelagic Sargassum population in the tropical Atlantic: biological consequences of a basin-scale long distance dispersal event. Prog. Oceanogr. 182:102269. doi: 10.1016/j.pocean.2020.102269
Kasemir, B., Jager, J., Gardner, M., Clark, W., and Wokaun, A. (2003). Public Participation in Sustainability Science: A Handbook. Cambridge, MA: Cambridge University Press.
Kilar, J. A., Hanisak, M. D., and Yoshida, T. (1992). “On the expression of phenotypic variability: why is Sargassum so taxonomically difficult?,” in Taxonomy of Economic Seaweeds: With Reference to Some Pacific and Western Atlantic Species Vol III, ed. I. A. Abbott (La Jolla, CA: Sea Grant College), 95–117.
Krause-Jensen, D., and Duarte, C. M. (2016). Substantial role of macroalgae in marine carbon sequestration. Nat. Geosci. 9, 737–742. doi: 10.1038/ngeo2790
Krause-Jensen, D., Lavery, P., Serrano, O., Marba, N., Masque, P., and Duarte, C. M. (2018). Sequestration of macroalgal carbon: the elephant in the Blue Carbon room. Biol. Lett. 14:e0236. doi: 10.1098/rsbl.2018.0236
Lähteenmäki-Uutela, A., Rahikainen, M., Camarena-Gómez, M. T., Piiparinen, J., Spilling, K., and Yang, B. (2021). European Union legislation on macroalgae products. Aquac. Int. 29, 487–509. doi: 10.1007/s10499-020-00633-x
Lang, D. J., Wiek, A., Bergmann, M., Stauffacher, M., Martens, P., Moll, P., et al. (2012). Transdisciplinary research in sustainability science: practice, principles, and challenges. Sustain. Sci. 7, 25–43. doi: 10.1007/s11625-011-0149-x
Lapointe, B. E. (2019). Chasing nutrients and algal blooms in Gulf and Caribbean waters: a personal story. Gulf Caribb. Res. 30, 16–30. doi: 10.18785/GCR.3001.10
Lapointe, B. E., West, L. E., Sutton, T. T., and Hu, C. (2014). Ryther revisited: nutrient excretions by fishes enhance productivity of pelagic Sargassum in the western North Atlantic Ocean. J. Exp. Mar. Bio. Ecol. 458, 46–56. doi: 10.1016/j.jembe.2014.05.002
Lasquites, J. J., Blanco, A. C., and Tamondong, A. (2019). Mapping of Sargassum distribution in the eastern coast of southern leyte using sentinel 2 satellite imagery. Int. Arch. Photogramm. Remote Sens. Spat. Inf. Sci. ISPRS Arch. 42, 289–295. doi: 10.5194/isprs-archives-XLII-4-W19-289-2019
Lodeiro, P., Cordero, B., Grille, Z., Herrero, R., and de Vicente, M. E. S. (2004). Physicochemical studies of cadmium (II) biosorption by the invasive alga in Europe, Sargassum muticum. Biotechnol. Bioeng. 88, 237–247. doi: 10.1002/bit.20229
Lopez, C. B., Dortch, Q., Jewett, E. B., and Garrison, D. (eds) (2008). “Scientific assessment of marine harmful algal blooms,” in Interagency Working Group on Harmful Algal Blooms, Hypoxia and Human Health of the Joint Subcommittee on Ocean Science and Technology, (Washington, DC: NOAA), 9–19.
López-Sosa, L. B., Alvarado-Flores, J. J., Corral-Huacuz, J. C., Aguilera-Mandujano, A., Rodríguez-Martínez, R. E., Guevara-Martínez, S. J., et al. (2020). A prospective study of the exploitation of pelagic Sargassum spp. As a solid biofuel energy source. Appl. Sci. 10, 1–17. doi: 10.3390/app10238706
Louime, C., Fortune, J., and Gervais, G. (2017). Sargassum invasion of coastal environments: a growing concern. Am. J. Environ. 13, 58–64. doi: 10.3844/ajessp.2017.58.64
Mattio, L., and Payri, C. E. (2011). 190 years of Sargassum taxonomy, facing the advent of DNA phylogenies. Bot. Rev. 77, 31–70. doi: 10.1007/s12229-010-9060-x
Maurer, A. S., De Neef, E., and Stapleton, S. (2015). Sargassum accumulation may spell trouble for nesting sea turtles. Front. Ecol. Environ. 13:394. doi: 10.1890/1540-9295-13.7.394
Milledge, J. J., and Harvey, P. J. (2016). Golden tides: problem or golden opportunity? The valorisation of Sargassum from beach inundations. J. Mar. Sci. Eng. 4, 1–19. doi: 10.3390/jmse4030060
Milledge, J. J., Nielsen, B. V., and Bailey, D. (2015). High-value products from macroalgae: the potential uses of the invasive brown seaweed, Sargassum muticum. Rev. Environ. Sci. Biotechnol. 15, 67–88. doi: 10.1007/s11157-015-9381-7
Milledge, J. J., Smith, B., Dyer, P. W., and Harvey, P. (2014). Macroalgae-derived biofuel: a review of methods of energy extraction from seaweed biomass. Energies 7, 7194–7222. doi: 10.3390/en7117194
Mohammed, C., Mahabir, S., Mohammed, K., John, N., Lee, K. Y., and Ward, K. (2019). Calcium alginate thin films derived from Sargassum natans for the selective adsorption of Cd2+, Cu2+, and Pb2+ ions. Ind. Eng. Chem. Res. 58, 1417–1425. doi: 10.1021/acs.iecr.8b03691
Moreira, Á, and Alfonso, G. (2013). Inusual arribazón de Sargassum fluitans (Børgesen) Børgesen en la costa centro-sur de Cuba. Rev. Invest. Mar. 33, 17–20.
Namvar, F., Mohamad, R., Baharara, J., Zafar-Balanejad, S., Fargahi, F., and Rahman, H. S. (2013). Antioxidant, antiproliferative, and antiangiogenesis effects of polyphenol-rich seaweed (Sargassum muticum). BioMed Res. Int. 9:604787. doi: 10.1155/2013/604787
Orr, M., Zimmer, M., Jelinnski, D., and Mews, M. (2005). Wrack deposition on different beach types: spatial and temporal variation in the pattern of subsidy. Ecology 86, 1496–1507. doi: 10.1890/04-1486
Paraguay-Delgado, F., Carreño-Gallardo, C., Estrada-Guel, I., Zabala-Arceo, A., Martinez-Rodriguez, H. A., and Lardizábal-Gutierrez, D. (2020). Pelagic Sargassum spp. capture CO2 and produce calcite. Environ. Sci. Pollut. Res. 27, 25794–25800. doi: 10.1007/s11356-020-08969-w
Parr A. E. (ed) (1939). “Quantitative observations on the pelagic Sargassum vegetation of the western North Atlantic with preliminary discussion of morphology and relationships,” in Bulletin of the Bingham Oceanographic Collection, (New Haven: Bingham Oceanographic Laboratory, Yale University).
Phillips, N., and Fredericq, S. (2000). Biogeographic and phylogenetic investigations of the pantropical genus Sargassum (Fucales, Phaeophyceae) with respect to the Gulf of México species. Gulf México Sci. 2, 77–87. doi: 10.4490/algae.2005.20.2.077
Powers, L. C., Hertkorn, N., McDonald, N., Schmitt-Kopplin, P., Del Vecchio, R., Blough, N. V., et al. (2019). Sargassum sp. act as a large regional source of marine dissolved organic carbon and polyphenols. Glob. Biogeochem. Cycles 33, 1423–1439. doi: 10.1029/2019GB006225
Putman, N. F., Goni, G. J., Gramer, L. J., Hu, C., Johns, E. M., Trinanes, J., et al. (2018). Simulating transport pathways of pelagic Sargassum from the Equatorial Atlantic into the Caribbean Sea. Prog. Oceanogr. 165, 205–214. doi: 10.1016/j.pocean.2018.06.009
Resiere, D., Mehdaoui, H., Florentin, J., Gueye, P., Lebrun, T., Blateau, A., et al. (2020). Sargassum seaweed health menace in the Caribbean: clinical characteristics of a population exposed to hydrogen sulfide during the 2018 massive stranding. Clin. Toxicol. 2, 1–9. doi: 10.1080/15563650.2020.1789162
Rodríguez, W., and Orellana, R. (2008). Utilización de las algas marinas como componente de sustratos para la producción de plántulas de acelga y lechuga. Agric. Orgán. 3, 30–40.
Rodríguez-Martínez, R., Van Tussenbroek, B. I., and Jordán-Dahlgren, E. (2016). “Afluencia masiva de sargazo pelágico a la costa,” in Florecimientos Algales Nocivos en México, eds E. García-Mendoza, S. I. Quijano-Scheggia, A. Olivos-Ortiz, and E. N. úñez-Vázquez (Ensenada: CICESE), 352–365.
Rodríguez-Martínez, R. E., Roy, P. D., Torrescano-Valle, N., Cabanillas-Terán, N., Carrillo-Domínguez, S., Collado-Vides, L., et al. (2020). Element concentrations in pelagic Sargassum along the Mexican Caribbean coast in 2018-2019. PeerJ 8:e8667. doi: 10.7717/peerj.8667
Rosado-Espinosa, L. A., Freile-Pelegrín, Y., Hernández-Nuñez, E., and Robledo, D. (2020). A comparative study of Sargassum species from the Yucatan Peninsula coast: morphological and chemical characterisation. Phycologia 59, 261–271. doi: 10.1080/00318884.2020.1738194
Sanchez-Rubio, G., Perry, H., Franks, J. S., and Johnson, D. R. (2018). Occurrence of pelagic Sargassum in waters of the U.S. Gulf of Mexico in response to weather-related hydrographic regimes associated with decadal and interannual variability in global climate. Fish. Bull. 116, 93–106. doi: 10.7755/FB.116.1.10
Schell, J. M., Goodwin, D. S., and Siuda, A. N. S. (2015). Recent Sargassum inundation events in the Caribbean: shipboard observations reveal dominance of a previously rare form. Oceanography 28, 8–10. doi: 10.5670/oceanog.2015.70
SEMARNAT (2015). Lineamientos Generales Para la Remoción de Sargazo de las Playas del Caribe Mexicano. Mexico: SEMARNAT.
Shackleton, S., Campbell, B., Wollenberg, E., and Edmunds, D. (2002). Devolution and community-based natural resource management: creating space for local people to participate and benefit? Nat. Resour. Perspect. 76, 1–6. doi: 10.1002/9781118786352.wbieg0630
Sissini, M. N., De Barros Barreto, M. B. B., Szeæhy, M. T. M., De Lucena, M. B., Oliveira, M. C., Gower, J., et al. (2017). The floating Sargassum (Phaeophyceae) of the South Atlantic Ocean - likely scenarios. Phycologia 56, 321–328. doi: 10.2216/16-92.1
Smale, D. A., Moore, P. J., Queirós, A. M., Higgs, N. D., and Burrows, M. T. (2018). Appreciating interconnectivity between habitats is key to blue carbon management. Front. Ecol. Environ. 16, 71–73. doi: 10.1002/fee.1765
Smetacek, V., and Zingone, A. (2013). Green and golden seaweed tides on the rise. Nature 504, 84–88. doi: 10.1038/nature12860
Song, N., Bai, L., Xu, H., and Jiang, H.-L. (2020). The composition difference of macrophyte litter-derived dissolved organic matter by photodegradation and biodegradation: role of reactive oxygen species on refractory component. Chemosphere 242:125155. doi: 10.1016/j.chemosphere.2019.125155
Stiger, V., Horiguchi, T., Yoshida, T., Coleman, A. W., and Masuda, M. (2003). Phylogenetic relationship within the genus Sargassum (Fucales, Phaeophyceae), inferred from ITS-2 nr DNA, with an emphasis on the taxonomic subdivision of the genus. Phycol. Res. 51, 1–10. doi: 10.1111/j.1440-1835.2003.tb00164.x
Tanniou, A., Serrano-Leon, E., Laurent, V., Ibañez, E., Mendiola, J. A., Cerantola, S., et al. (2013). Green improved processes to extract bioactive phenolic compounds from brown macroalgae using Sargassum muticum as model. Talanta 104, 44–52. doi: 10.1016/j.talanta.2012.10.088
Terme, N., Hardouin, K., Pliego Cortès, H., Peñuela, A., Freile-Pelegrín, Y., Robledo, D., et al. (2020). “Emerging extraction techniques: enzyme-assisted extraction a key step of seaweed biorefinery? Sustainable seaweed technologies cultivation, biorefinery, and applications advances,” in Green Chemistry, eds M. D. Torres, S. Kraan, and H. Dominguez (Netherlands: Elsevier), 225–256. doi: 10.1016/b978-0-12-817943-7.00009-3
Thomas, F., Bordron, P., Eveillard, D., and Michel, G. (2017). Gene expression analysis of zobellia galactanivorans during the degradation of algal polysaccharides reveals both substrate-specific and shared transcriptome-wide responses. Front. Microbiol. 8:1808. doi: 10.3389/fmicb.2017.01808
Torres, M. R., Sousa, A. P., Silva Filho, E. A., Melo, D. F., Feitosa, J. P., de Paula, R. C., et al. (2007). Extraction and physicochemical characterization of Sargassum vulgare alginate from Brazil. Carbohydr. Res. 342, 2067–2074. doi: 10.1016/j.carres.2007.05.022
Trinanes, J., Putman, N. F., Goni, G., Hu, C., and Wang, M. (2021). Monitoring pelagic Sargassum inundation potential for coastal communities. J. Oper. Oceanogr. [Epub ahead of print]. doi: 10.1080/1755876X.2021.1902682
UNEP (2018). Sargassum White Paper - Sargassum outbreak in the Caribbean: Challenges, Opportunities and Regional Situation. Panama: UNEP.
van Tussenbroek, B. I., Hernández Arana, H. A., Rodríguez-Martínez, R. E., Espinoza-Avalos, J., Canizales-Flores, H. M., González-Godoy, C. E., et al. (2017). Severe impacts of brown tides caused by Sargassum spp. on near-shore Caribbean seagrass communities. Mar. Pollut. Bull. 122, 272–281. doi: 10.1016/j.marpolbul.2017.06.057
Vázquez-Delfín, E., Ávila-Velázquez, V., and Robledo, D. (2020). SargaZoom, Cinvestav Mérida (Version 1.1.2.214).
Velasco-González, O., Echavarría-Almeida, S., de León, A. S. D., and Casas-Valdez, M. (2013). Uso del alga marina Sargassum spp. adicionada a la harina de trigo para preparar galletas alimenticias para consumo humano. Bioagro 25, 189–194.
Wang, M., and Hu, C. (2016). Mapping and quantifying Sargassum distribution and coverage in the Central West Atlantic using MODIS observations. Remote Sens. Environ. 183, 350–367. doi: 10.1016/j.rse.2016.04.019
Wang, M., Hu, C., Barnes, B. B., Mitchum, G., Lapointe, B., and Montoya, J. P. (2019). The great Atlantic Sargassum belt. Science 365, 83–87. doi: 10.1126/science.aaw7912
Wang, M., Hu, C., Cannizzaro, J., English, D., Han, X., Naar, D., et al. (2018). Remote sensing of Sargassum biomass, nutrients, and pigments. Geophys. Res. Lett. 45, 359–412. doi: 10.1029/2018GL078858
Keywords: Caribbean, Golden tides, environmental concerns, Sargassum, valorization, management strategies
Citation: Robledo D, Vázquez-Delfín E, Freile-Pelegrín Y, Vásquez-Elizondo RM, Qui-Minet ZN and Salazar-Garibay A (2021) Challenges and Opportunities in Relation to Sargassum Events Along the Caribbean Sea. Front. Mar. Sci. 8:699664. doi: 10.3389/fmars.2021.699664
Received: 23 April 2021; Accepted: 02 July 2021;
Published: 22 July 2021.
Edited by:
Ricardo A. Melo, University of Lisbon, PortugalReviewed by:
Struan R. Smith, Bermuda Aquarium, Museum and Zoo, BermudaJuan J. Vergara, University of Cádiz, Spain
Copyright © 2021 Robledo, Vázquez-Delfín, Freile-Pelegrín, Vásquez-Elizondo, Qui-Minet and Salazar-Garibay. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Daniel Robledo, daniel.robledo@cinvestav.mx
†These authors have contributed equally to this work and share first authorship