Ciguatera in the Seaflower Biosphere Reserve: Projecting the Approach on HABs to Assess and Mitigate Their Impacts on Public Health, Fisheries and Tourism

Humanity’s expectations of development based on oceanic sources have been increasing because of the decrease in terrestrial sources, and although the exploration and use of the ocean for well-being and prosperity is nothing new, the scope, intensity, and diversity of current aspirations are unprecedented (Jouffray et al. 2019). In this way, societies rely more and more on marine ecosystems for food, materials, novel bioactive compounds, space, and recreational resources (GlobalHAB 2021).

The drivers of climate change, along with the intensive use of marine resources, have already altered the dynamics among biotic and abiotic components, rapidly transforming the structure and functions of some marine ecosystems in diverse regions worldwide. In particular, the dynamics of some photosynthetic organisms seem to be particularly affected by climate change (GlobalHAB 2021).

Microalgae, together with seaweeds and phanerogams constitute the basis of marine food webs and are essential for both marine and terrestrial ecosystems, since they produce around 50% of all the planet’s oxygen. However, they can also become a serious threat to fishery resources, aquaculture, tourism, and human health in certain circumstances. Of the approximately 5,000 known species of algae globally, more than 135 can produce harmful events. Harmful algal blooms (HABs) may be harmful in two ways: some species produce toxins that affect the food chain, including human health, while other species are non-toxic, but may produce high biomass (GlobalHAB 2021). These latter microalgae produce great amounts of organic matter that, when algae die, sink to the ocean floor. Decomposition of this matter by bacteria can result in oxygen depletion, with dead-zone formation and mass death of marine organisms. Although considered natural events that have been historically documented in marine ecosystems, several studies in recent decades have linked HAB events to local mesoscale oceanographic and atmospheric phenomena (Sunesen et al. 2021), generating concern that global climate-driven changes will exacerbate HABs (GlobalHAB 2021). Likewise, other global problems such as nutrient discharge and the introduction of alien species have been associated with HABs’ increase in frequency, intensity, and geographic distribution (Cuellar-Martinez et al. 2018; Heisler et al. 2008). Trends analyzed in Latin America and the Caribbean up to 2019 are related to the increasing awareness of the presence of toxic species, the geographical expansion of already known species, the detection of new toxins for the region, and HAB events’ duration and/or impacts (Sunesen et al. 2021).

The GlobalHAB Program of the Intergovernmental Oceanographic Commission (IOC-UNESCO) and the Scientific Committee on Oceanic Research (SCOR) has been strengthening a conceptual framework for the understanding and management of HABs’ impacts based on multidisciplinary international coordination and ongoing training (www.​globalhab.​info). However, this very program recognizes that one of the unknown and main challenges to face is how we can prevent or mitigate future HAB impacts (GlobalHAB 2021).

As has been stated in Chap. 1 of this book, Biosphere Reserves (BR) are “living, dynamic laboratories”, and therefore represent ideal places to study and replicate interdisciplinary adaptation strategies. The Archipelago of San Andrés, Providencia, and Santa Catalina (hereafter, the archipelago), located in the southwest Caribbean, typifies the definition of small oceanic islands. It has an important wealth of marine and terrestrial natural capital, the ecological characteristics of its islands favor biodiversity but are limited by freshwater supply and are showing signs of great vulnerability to extreme weather events. In 2000, Seaflower, an area of 180,000 km² located in the archipelago, was declared an International Biosphere Reserve by UNESCO, and in 2005, part of the BR (65,000 km²) was declared a Marine Protected Area by the Colombian government.

Considering that effective climate change adaptation and mitigation decisions are based on the relationship between science and society, involving a wide variety of analytical methods to evaluate the associated risks and benefits, the purpose of this chapter is to evaluate HABs in the Seaflower Biosphere Reserve (SBR), based on the economic cost of its impacts on fishing, tourism, and the cost of monitoring and training programs. We hope that this analysis can serve as input for both the design of the early warning system and for an ambitious social training program.

In the Colombian Caribbean, 25 reported species appear in the IOC-UNESCO Taxonomic Reference List of Harmful Micro Algae (https://​www.​marinespecies.​org/​hab/​) (Table 1). Most of them are benthic dinoflagellates, like those of the genus Gambierdiscus, known to cause toxic problems such as ciguatera in tropical and subtropical regions (Arencibia-Carballo et al. 2009; Chinain et al. 2021). Ciguatera is an intoxication caused by the ingestion of marine organisms with lipid-soluble ciguatoxins in their tissues; these toxins are originally produced by Gambierdiscus and Fukuyoa, two genera of dinoflagellates, and are accumulated along the chain web. Ciguatera affects between 10,000 and 50,000 people in the world annually (Friedman et al. 2008; Chinain et al. 2021). However, it is considered underdiagnosed, estimating that less than 10% of cases are reported (Friedman et al. 2008).

The dinoflagellate Gambierdiscus toxicus (Adachi and Fukuyo 1979), which lives as an epiphyte of seagrasses and macroalgae colonizing coral reefs (Lehane and Lewis 2000), has been considered for years the main cause of ciguatera. However, a detailed taxonomic and toxin characterization of the species in the genus confirms the involvement of other Gambierdiscus as well as Fukuyoa species as toxin producers to a greater or lesser degree (Litaker et al. 2009). It cannot be discarded that other benthic dinoflagellate genera such as Amphidinium, Coolia, Ostreopsis, and Prorocentrum (Besada et al. 1982), and some cyanobacterial taxa (Laurent et al. 2008), which are often found in association with G. toxicus, may also be involved in ciguatera poisonings. Among them, the genus Prorocentrum has great relevance, due to the number of species identified as toxic or potentially toxic, and due to its abundance in natural environments (Delgado et al. 2002; Arbeláez et al. 2020).

The oldest known historical record of ciguatera in the world dates back to 1525 in the Eastern Atlantic, when the captains of seven Spanish ships that anchored in the Gulf of Guinea consumed barracuda. All those who ate the barracuda became ill with diarrhea and fell unconscious (Urdaneta 1580, in Fraga et al. 2011) and died months later due to unknown causes (de Miguel 2009, in Fraga et al. 2011). Since then, ciguatera has caused serious problems, such as the death in 1748 of 1,500 people in the Indo-Pacific islands (Halstead and Cox 1973). It has even been suggested that ancient Polynesian migrations were driven by ciguatera events (Rongo et al. 2009). Cases of ciguatera have been reported in the Caribbean since 1862 when, in the Gulf of Mexico, the crew of a French ship became poisoned by eating parrotfish (Halstead 1967). Patterns of resource use by the Arawak and Caribe groups inhabiting the Eastern Caribbean may indicate that they too faced problems with the intoxication (Price 1966). Like other types of marine poisonings, ciguatera is underestimated in much of the Caribbean, making its study highly pertinent in the region, even more if one considers that less than 0.1% of those intoxicated receive medical attention (Tosteson 1995). Reported symptomatology for ciguatera is variable, including gastrointestinal, neurological, cardiovascular, and neuropsychological disorders, ranging from mild and short-term to severe and long-term, in the worst cases leading to death (Arencibia et al. 2009; Faust 2009).

A significant increase in the incidence of ciguatera has been reported in different regions of the world. Skinner et al. (2011) found that during the past three decades, the incidence of ciguatera in the South Pacific increased by 60%, while Tester et al. (2020) and Celis and Mancera-Pineda (2015) detected an increase of 32% among member countries of the Caribbean Epidemiology Center (CAREC). These increases could be even greater in the future due to changes in global weather patterns, overfishing, and the degradation of marine ecosystems (Tester et al. 2020).

Numerous species of dinoflagellates associated with Thalassia testudinum beds, macroalgae, and debris from coral reefs and mangrove forests have been found in the Caribbean Sea (Faust 1993a, b, 2000, 2009; Faust et al. 1999; Valerio González and Díaz 2008; Rodríguez et al. 2010). Taking into account the increase in ciguatera in the Caribbean (Mancera-Pineda et al. 2014; Celis and Mancera-Pineda 2015), the presence of potentially toxic dinoflagellates associated with seagrasses and macroalgae (Rodríguez et al. 2010) and the wide diversity of macroalgae and other substrates that make up the drift on the island of San Andrés (Ortiz and Gavio 2012), it is necessary to expand the evaluation of potentially toxic microalgae with a view to generate a comprehensive risk management plan.

Marine biotoxins threaten both human health and food and nutritional security (FAO 2005). In addition to ciguatera, other forms of seafood-borne poisonings caused by microalgae have been identified, whose toxins can enter food webs and affect human health through the ingestion of fishery products. The best-known toxins are paralytic (PST), diarrheal (DST), amnesic (AST), and neurotoxin (NST) (Lagos 2002). The current concern about the impact generated by potentially toxic microalgae in society is great, given that in recent years poisoning events seem to have increased in frequency, intensity, and geographic distribution (Hallegraeff et al. 2021).

In a recent scoping review aimed at mapping the evidence for associations between marine HABs and observed acute and chronic human health effects, it was found that 58% of the 220 publications made between 1985 and 2019 were related to ciguatera poisoning (Young et al. 2020). But while the public health implications of ciguatera have been established, its true regional and global incidence has been difficult to determine due to underreporting of cases. This underreporting is due both to the difficulty in differentiating its symptoms from other syndromes, and to deficiencies in the epidemiological data recording systems of the affected countries (Friedman et al. 2008, 2017; Skinner et al. 2011). Despite the difficulties of diagnosis and notification, ciguatera is now recognized as a major health problem around the world, in addition to its strong socioeconomic consequences (Chinain et al. 2021).

In a study on the historical incidence of ciguatera in San Andrés and the Caribbean island states (Celis and Mancera-Pineda 2015), the results show that, in the period 1980–2010, there were 10,710 registered cases from 18 CAREC countries, with an average annual incidence of 42/100,000 inhabitants. Likewise, there was an increase between the periods 1980–1990 and 2000–2010, with an annual average calculated from the reported cases of 34.2 and 45.2/100,000, respectively. The island of Montserrat had the highest incidence in the region, 350/100,000, while San Andrés had an incidence of 25/100,000 inhabitants, ranking eighth among the islands in the study. The rate ratio for CAREC countries (average annual incidence from 2000 to 2010/average annual incidence from 1980 to 1990) was 1.36, so there was a 32% increase in average annual incidence across countries, and an increase of nearly 300% between the two time periods. The level of reported incidence of ciguatera in the Caribbean has increased in the last 31 years, mainly in the Eastern Caribbean, since island states such as the Bahamas, Antigua, and Barbuda contribute greatly to the total reported increase. Considering that the development model of much of the region is based on the tourism industry and that fish is an important source of protein for Caribbean communities, we may affirm that ciguatera is a problem expected to increase in parallel with environmental changes.

To generate a baseline to quantify the relationship between climate, its variation, and HAB-related diseases, an interdisciplinary approach is required to determine the true burden of  the intoxication, after acute and chronic exposures, including impacts on the environment and human well-being (Young et al. 2020).

Bearing in mind that the problems associated with marine toxins are on the rise and that these not only cause problems in ecosystems, but also to public health and productive activities, it is essential to design a management plan that allows the reduction of vulnerability to, and therefore the risk of, this threat. In the SBR and Cartagena, 166 cases of ciguatera have been confirmed in the period 2010–2020 (INS 2021; Celis and Mancera-Pineda 2015).

Although there is no clear trend in the distribution of cases over time (Fig. 1), this incidence of ciguatera—14.4 cases per year—could have negative implications for tourism, even more so considering the possible high levels of underreporting. Tourism is the basis of the development model of the archipelago, as well as that of a good part of the insular Caribbean, and given that ciguatera is a growing phenomenon worldwide, this syndrome constitutes a risk and therefore must be taken into account in development plans. The design and implementation of a monitoring program that becomes an early warning system should be a priority, as well as the training of health and tourism personnel. In this sense, the island of San Andrés could become a model of risk management in the Caribbean.

A bar graph presents the number of Ciguatera cases registered in years between 2077 and 2019. The highest number of 37 cases are registered in 2031, and 2015. Only one case is registered in 2020, the the lowest in all.

The effects of climate change will continue to grow for many years, but we cannot ameliorate or manage negative impacts on humans or ecosystems without a better knowledge of those impacts. Understanding the processes thriving HABs has been a very challenging task and one that scientists have not yet fully accomplished. The main reason is that HABs are very complex events: they include a huge variety of species, belonging to evolutionary distinct groups; their life histories are diverse, and may include resistance stages, and sexual as well as vegetative reproduction; the ecosystems involved span from freshwater to brackish and marine, both nearshore and offshore, from tropical to cold temperate and polar latitudes; and their impacts may vary in space and time (Anderson et al. 2015). Furthermore, there are many abiotic and biotic factors triggering HABs (Table 1), including, but not limited to, temperature, salinity, nutrients, biogeochemical cycles, grazing, and anthropic activities such as ballast water discharge and climate change (Anderson et al. 2015; Wells et al. 2015).

Global climate change affects different abiotic factors in marine systems, which, in turn, influence the growth and distribution of bloom-forming algae. With climate change, variations in temperature, salinity, pH, oxygen content, and stratification are expected (Tester et al. 2020; Wells et al. 2015).

The severity of ciguatera impacts in the SBR is poorly understood. However, considering that this syndrome could increase with climate change, it may become a serious development threat. Fishing represents an important source of protein for visitors and local communities, and is therefore essential for food security (Jaramillo-Campuzano et al. 2009; Santos-Martínez et al. 2013), while the economy of the BR is based on tourism, as occurs in other Caribbean locations (Kingsbury 2005; Pantojas 2006; Prato and Newball 2016). The tourism industry in the Caribbean reports more than USD $25,000 billion per year (Burke and Maidens 2005), which represents 20% of GDP. In the SBR, tourism represents around USD $266 million per year (reported in USD 2014) (Prato and Newball 2016). Tourism’s associated economic revenues and incomes could be expanded to the trading, fisheries, restaurants, bars, and labor sectors, which makes tourism a very important component of the SBR’s market economy. These economic benefits could be threatened by HABs, while their economic impacts could be reduced, avoided, or mitigated through investments in effective monitoring and management programs.

Marine environmental management faces great challenges in maintaining the social benefits provided by ecosystem services (ES) (de Jonge et al. 2003; Elliott 2011; Turner and Schaasfsma 2015). This management must consider the high complexity of the ecological interactions of these systems, which are modulated by the interaction of the atmosphere, the land, and the ocean (von Glasow et al. 2013). HABs could also impacts ecosystems and their ES, modifying food webs and affecting other organisms and ES (Anderson et al. 2000; van Tussenbroek et al. 2017). Non-market values and ES provided by the SBR’s marine ecosystems such as seagrasses, mangroves, and coral reefs, represent considerably higher benefits for wellbeing than tourism. An economic valuation of SBR ES estimated that they represent around USD 267 billion per year (Prato and Newball 2016). These benefits could be at risk due to HABs in the SBR and the Caribbean.

The estimation of the economic impacts caused by HAB events has included a wide range of factors such as the loss of gross income in fishery products, public health costs, tourism and recreation impacts, environmental monitoring, and management expenses, or other costs that would not exist in the absence of HABs (Anderson et al. 2000). According to Bernard et al. (2014) significant expenses are sustained annually due to HAB events, which vary by region. Japan may lose more than USD 1 billion dollars, while Europe USD 850 million, and the USA around USD 95 million. Impacts on aquaculture industries could also be very high. For example, in Norway, just one HAB incident impacted tons of Atlantic salmon, generating losses of around USD 300 million (Trainer 2020). In Florida, recurrent Karenia brevis blooms (commonly known as “Florida red tides”) have been estimated to cause over USD 20 million in tourism-related losses every year (Anderson et al. 2000).

The cost of ciguatera and other HABs varies depending on the conditions of each country, city, or particular territory. Additionally, those costs may have a higher magnitude depending on factors such as the size of the population at risk, the size of each economic activity (aquaculture, tourism, fisheries), and the dependence of people and the economy on each activity.

Economic impacts on public health due to ciguatera cases in US territories vary depending on where those cases occur and the average healthcare cost in each place. For example, the estimated costs for ciguatera related illness treatment and healthcare per reported case in the USA could be around USD 1,000 per reported case and USD 700 per unreported case, while in the specific case of Puerto Rico, the average cost per case might be lower (around USD 530) (Hoagland et al. 2002). Anderson et al. (2000), estimated the economic impacts of ciguatera on public health, and found costs between USD 18 million to USD 24 million per year, averaging USD 21 million per year. Hoagland et al. (2002), also estimated similar economic impacts of ciguatera for public health averaging USD 19 million dollars per year for US tropical territories. Morin et al. (2016) estimated the public health costs of ciguatera cases in the Moorea Island society of approximately USD 50,000 per year.

On the other hand, ciguatera could also affect fisheries due to a reduction in fish sales and consumption as well as other factors that affect artisanal fisheries, sellers, and several actors in the fish market chain. It has been estimated that the economic impacts of ciguatera in Hawaii increased by USD 3 million per year based on the dollars per pound of fish that are unmarketable due to ciguatera (Hoagland et al. 2002). Since fish and shellfish are the main local protein source in the archipelago, ciguatera could be a threat not only to fisheries and the economy, but also to food security in these insular territories.

Ciguatera’s economic impacts on public health are likely to be underestimated on different levels for many reasons. For example, (1) unreported cases of sick people that do not go to healthcare providers, (2) misdiagnosed cases considered “standard” poisonings, and (3) unregistered cases due to the insufficient statistical and reporting systems of local healthcare providers. The underreporting of cases may vary from one place to another. Hoagland et al. (2002), presented different “reported” to “unreported” illness ratios, for example, they found rations of 1:4 for Florida, 1:10 for the Northern Mariana Islands and American Samoa, and 1:100 for Hawaii, Guam, Puerto Rico, and the U.S. Virgin Islands. This can have effects on calculations of the economic impacts of HABs. These underreported cases could influence the results of an economic approach, so improved registration, diagnosis, and statistics mechanisms are encouraged for better management.

Economic impacts (economic losses and costs) of HABs such as ciguatera, must be considered from a multi-perspective approach, to better consider their economic impacts and risks, as well as to visualize the benefits of investing in effective management in terms of avoided costs. A cost–benefit analysis could be performed to present to decision-makers, presenting the gains and advantages that effective management and monitoring programs could have. Since there are data limitations and underreporting of ciguatera cases and their impacts, periodically updating calculations of their economic impacts is an appropriate strategy to improve accuracy and to provide more awareness about the importance of avoiding related costs by investing in management plans. These updates must be done as the available data on ciguatera improve in the archipelago and surrounding Caribbean insular territories. This recalls the need for Caribbean territories to invest in better registration and statistics mechanisms for HAB management.

Based on experiences of the assessment and reports of ciguatera and other HABs’ economic impacts (Anderson et al. 2000; Sanseverino et al. 2016; Trick et al. 2020), here we provide tools to estimate the economic impacts on the SBR. It is important to consider that the accuracy of economic impact estimates depends on the quality and amount of available data and statistics related to ciguatera cases and related costs. Despite all the limitations due to lack of data, these tools may prove useful to better understand and inform decision-makers about the economic relevance of: (1) the economic impacts of ciguatera; (2) the importance of investing in effective management and monitoring strategies; (3) the importance of investing in improving ciguatera diagnosis, registration, cost, effects, and other related data availability and HABs statistics in the SBR. Here we present some equations as tools to estimate the economic impacts (E_impacts) of ciguatera and other HABs in the SBR and other Caribbean insular territories:

in which: Ti: Impacts on Tourism (Eq. 2), LFi: Impacts on Labor Force (Eq. 3), Phi: Impacts on Public Health (Eq. 4), Fi: Impacts on Fisheries (Eq. 5) and Si: Societal impacts (Eq. 6). All the costs and data are suggested to be calculated by year (total or averages per year) to facilitate calculations.

in which, Tr: Tourism reduction percentage (given in decimal units –0 to 1), Tanu: Average annual number of tourists visiting the island or destination. Tainc: Total average revenues generated by a tourist (including local and national taxes such as the “Tourism card” (tarjeta de turismo), VAT and airport taxes, flight tickets, hotel, restaurants, food expenses, drinks, and leisure expenses).

in which, Naw: Number of affected workers (average per year), Da: Average of days of affectation (disease) per worker (days off work), Awag: Average daily wage per worker. ARw: Average revenue per worker (production or revenues for the firm or employer), Naw: Average number of affected workers.

in which, Cpd: Cost per day of medical care (including hospitalization if needed and care and medical attention cost, medical exams, and others), Da: Days of affectation per worker, Cm: Costs of medicine. This must be included per person, and for all the registered people affected by ciguatera.

For Eqs. 3 and 4, it is important to consider that the underreporting, under-registration, and underdiagnosis of ciguatera cases may affect the amounts calculated for LFi and PHi, and that the number of workers or patients affected by ciguatera must be higher. It is also important to remember that the under-diagnosed factor has been estimated to be around just 10% of ciguatera cases reported (Friedman et al. 2008) and that less than 0.1% of those intoxicated go to health services (Tosteson 1995).

To consider and include the under-registration and underdiagnosis of ciguatera in the equation to calculate its economic impacts, we can modify Eq. 1, to include and correct the expected real number of cases and their consequent economic impacts in Eq. 1a. These corrections could be performed if well-based “reported-not reported rates” (R) are available:

in which R: Reported/not reported rate. For example, if the reported ciguatera cases are 10% (1:10), then R = 0.1. Also, if the reported-not reported rate is 3:10 (30%), then R = 0.3.

Since detailed data about healthcare costs could be limited, Eq. 4 could be simplified to Eq. 4a based on averages from the available information:

in which, Cpda: Average cost per day of medical care per patient, Daa: Average days of affectation, Cma: Average cost of medicine, Npa: Number of people affected.

in which Fi is the sum of impacts for all the affected producers (fisherman or fisheries firms). Ras: Reduction of average monthly sales, Mas: Average monthly sales per firm or artisanal fisherman, Nma: Number of affected months, Caa: Cost of additional analyses and controls on fish or shellfish products per firm (tissue toxin detection, special laboratory analyses, monitoring, insurances, and other related costs).

in which, Sim_i: Available data about each indirect economic impact on society, such as indirect wages or job losses related to tourism or fisheries impacts, lawsuits, and extra costs of food substitutes, among others. Indirect economic impacts such as impacts on fuel sales, boat maintenance, jobs, and other related indirect impacts in the fisheries market chain, for example, on wages or revenues, could be difficult to include or consider in these analyses (Anderson et al. 2000). Nevertheless, we included this Si factor in the equation to allow the inclusion and consideration of these inputs in the economic impact estimations.

Other important costs of HABs, usually included in economic assessments of its impacts, are the “monitoring and management” costs (Anderson et al. 2000; Sanseverino et al. 2016). Those must be also considered in the total accounting for HABs’ economic impacts. Despite this, we didn’t include these costs in Eq. 1, due to our perspective that “monitoring and management” costs should be considered an investment that could mitigate the negative economic impacts of ciguatera and other HAB events. Monitoring and management costs could include water quality testing, the operation of shellfish and fish tissue toxin monitoring programs, plankton monitoring, and other activities.

Regional implementation of management strategies is needed to contribute to reducing the risk of HABs in the Caribbean Sea, especially within the framework of climate change adaptation. Effective actions to improve water quality, reduce nutrients supplied anthropogenically by agriculture, domestic and industrial sewage, as well as those generated by fires that destroy forests and that are later washed into the sea by the rains, which has been identified as one of the mechanisms of the blooms of Sargassum (not included in this chapter), which are also affecting tourism, fishing and coastal ecosystems in the Caribbean (Méndez-Tejada and Rosaldo-Jiménez 2019), but to a lesser extent in the SBR. Likewise, the investment in ecosystem-based adaptation of the whole Caribbean Basin will be vital for a better present and future for island territories.

During the third UN World Conference on Disaster Risk Reduction held in 2015 in Sendai, Japan, the Sendai Framework for Disaster Risk Reduction 2015–2030 was adopted. This framework proposes that to effectively protect livelihoods, health, cultural heritage, socioeconomic assets, and ecosystems, and to build resilience, it is essential to anticipate and plan for risk. It also emphasizes the need to improve the understanding of risk in its different dimensions, characteristics of exposure, vulnerability, and hazard. The framework also raises the importance of strengthening governance, the resilience of health infrastructure, international cooperation, and accountability processes (UNISDR 2015).

Risk conditions are determined by a relationship between threats and vulnerabilities. Threats are external factors represented by the potential occurrence of a dangerous natural or anthropogenic phenomenon. The analysis of the threat entails knowing its dynamics, characteristics, historical behavior, potential, and area of influence. Vulnerability, on the other hand, is an internal, intrinsic factor, determined by its own characteristics, represented by the limitation or inability to withstand, avoid, mitigate, adapt, and/or resist adverse events and recover from them. Risk management requires a broad approach, focused on people, with multi-risk and multi-sector practices that are inclusive and accessible. It also requires effective collaboration between the public and private sectors, civil society organizations, academia, and research institutions (UNISDR 2015).

The set of material or information resources existing in each place constitutes its Natural Capital (Constanza et al. 1997). The flows of this capital or its interaction with human beings constitute ES, that is, they are the elements of an ecosystem that are used actively or passively to produce the well-being of human populations (Fisher et al. 2009). ES are exposed to damage or deterioration, which can be evaluated through risk theory (Schäfer 2012). In addition to the threats caused by climatic phenomena, inappropriate use can compromise the sustainability of marine resources whenever they deteriorate ecosystem functions (Lozoya et al. 2011).

Due to the high environmental and economic dependence on coastal areas, small islands such as San Andrés, Providencia, and Santa Catalina correspond to the regions with the highest risk from the impacts of climate change and extreme weather events. Marine-coastal ecosystems such as coral reefs, seagrass and macroalgal meadows, beaches, and mangrove forests, provide coastal protection as an ES and, due to their high biodiversity, represent natural farms and great tourist attractions, which allows development and the sustainability of economic activities. Therefore, success in marine-coastal environmental management is a permanent challenge that makes it essential to improve scientific knowledge of the relationships between natural and social systems to reduce vulnerability and increase resilience, that is, the ability to face disturbances such as those produced by HABs and continue generating ES. Considering the effects of climate change, greater adaptive responses will be required to deal with the impacts of natural phenomena in coastal areas.

As a result of the efforts of the ANCA-IOCARIBE network, part of the HAB Program of IOC-UNESCO, several Colombian institutions have begun a collaborative initiative aimed at managing the risk of HABs on the country’s Pacific and Caribbean coasts. Since it is essential to collect information on the appearance of toxic microalgae and to describe their temporal variability, a monitoring program is being carried out, the main results of which were included as part of the Global HAB Status Report (Sunesen et al. 2021).

Considering the vulnerability of the archipelago to HABs, it is urgent to design and apply an early warning system (EWS) for risk reduction. This EWS must include an effective monitoring plan with strategic actions to face and mitigate the challenges of intoxications transmitted by organisms. Considering that early warnings are critical and fundamental elements in risk reduction and/or mitigation, an important factor for EWS effectiveness lies in the level of citizen participation. The communities at risk must be an active part of the system, receiving timely information, training, and exchanging knowledge with other stakeholders.

EWSs must integrate monitoring data, which, in the case of HAB events, correspond to the presence of species, oceanographic and atmospheric variables, and toxicity levels (Table 2). Comprehensive analysis of these data should lead to the generation of information on risk forecasting and prediction. The specific risk assessment is the basic input for the authorities to make decisions and to communicate them to the community and other potentially affected organizations in a timely manner. EWSs, then, must prevent, prepare for, and address the negative impacts generated by HABs (Fig. 2).

A chart illustrates the feedback for system improvement. It includes monitoring, analyzing, and forecasting the hazards and possible consequences.