Mercury dynamics in macroinvertebrates in relation to environmental factors in a highly impacted tropical estuary: Buenaventura Bay, Colombian Pacific

Environmental Science and Pollution Research (2020) 27:4044–4057 https://doi.org/10.1007/s11356-019-06970-6 RESEARCH ARTICLE Mercury dynamics in macroinvertebrates in relation to environmental factors in a highly impacted tropical estuary: Buenaventura Bay, Colombian Pacific Diego Esteban Gamboa-García 1 & Guillermo Duque 2 & Pilar Cogua 3 & José Luis Marrugo-Negrete 4 Received: 5 July 2019 / Accepted: 5 November 2019 / Published online: 10 December 2019 # The Author(s) 2019 Abstract The environmental health of Buenaventura Bay, a highly impacted tropical estuary, is influenced by numerous human activities, including mining upstream. Large- and small-scale fishing plays an important role in the local economy, so we investigated the dynamic processes of bioaccumulation of mercury at basal trophic levels. Four samples were taken at each of the four locations in Buenaventura Bay during each of the four seasons of 2015. We measured the total mercury content (T-Hg, dry weight) in sediments and in muscle tissue across 17 macroinvertebrate species. The most abundant were the blue crab (C. arcuatus) and the mantis shrimp (S. aculeata aculeata). Blue crab showed an average muscle T-Hg value exceeding the limit of 0.2 g·g-1, which is the maximum T-Hg level suggested for food consumption by vulnerable humans and populations: pregnant women, children, and the community that feeds from this source of protein on a daily basis. It was found that, 6.22% of individuals exceeded the 0.5 g·g-1 level, which is the maximum T-Hg level suggested for food consumption by the general population: the population that consumes it sporadically. Significantly high values of T-Hg in blue crab and mantis shrimp occurred during low salinity conditions in the estuary, suggesting that Hg mainly originates from river runoff during the rainy season. Nevertheless, the biota-sediment accumulation factor (BSAF) was favored in high salinity, which could mean greater availability of Hg for higher levels of the estuarine food web in the dry season and in marine waters. In general, the T-Hg levels in some samples exceeded 0.2 g·g−1. Therefore this pollutant must be monitored due to its biomagnification potential and as a threat to human health, especially that for the local population of fishermen and their families. Keywords Epibenthic invertebrates . Tropical estuary . Human health . Artisanal fisheries . Macroinvertebrates Introduction Responsible editor: Severine Le Faucheur * Diego Esteban Gamboa-García * Guillermo Duque * Pilar Cogua 1 Facultad de Ciencias Agropecuarias, Universidad Nacional de Colombia, Palmira, Colombia 2 Facultad de Ingeniería y Administración, Universidad Nacional de Colombia, Palmira, Colombia 3 Facultad de Ciencias Básicas, Universidad Santiago de Cali, Cali, Colombia 4 Facultad de Ciencias Básicas, Universidad de Córdoba, Montería, Colombia Coastal ecosystems are recognized for their wide variety of habitats that permit a broad diversity of species and generate high biological productivity. At the global level, marine resources provide at least 15% of the animal protein for 2.9 billion people and livelihoods for 520 million people (FAO 2009). Of this global productivity, 5.2% comes from estuaries, which sustain commercially important artisanal and coastal fisheries (Blaber 2013; Houde and Rutherford 1993). Nevertheless, these areas are susceptible to the incursion of pollutants affecting natural dynamics. Particularly intense in these environments is the retention of heavy metals (Bayen 2012), which may have both socioeconomic and ecological implications. Mercury (Hg) contamination of marine organisms has socioeconomic implications, as high concentrations of the metal in these organisms’ muscle tissue would potentially violate 4045 Environ Sci Pollut Res (2020) 27:4044–4057 regulations for human consumption (Costa et al. 2016; Padula et al. 2016), thereby affecting fish trade. In the highly impacted coastal estuary of Buenaventura Bay, Colombia, artisanal fisheries account for 50% of total fish production, and about 3000 inhabitants depend heavily on this activity for their income and food supply (Escobar Cárdenas 2009). On the Pacific coast of Colombia, the annual per capita fish consumption is 250 kg, compared to the national average of 4.5 kg (Villanueva and Flores-Nava 2019), highlighting the relevance of the human health concern. Although Hg can occur naturally in estuaries through atmospheric transport and deposition or through river discharge, the main sources globally are chlor-alkali plant discharge, fossil fuel burning, dental waste, and gold mining (Amos et al. 2014; Costa et al. 2012; Horowitz et al. 2014). On the Pacific coast of Colombia, Hg mainly originates from the mining of alluvial gold, whose polluting waste is transported by the rivers that flow into the coastal zones (CVC 2010), reaching even estuaries that are protected areas (Duque et al. 2018) In addition, the presence of Hg in sediments has been assigned a moderate ecological risk level (Cardoso et al. 2009; Guo et al. 2010; Li et al. 2019). Hg hosted in sediments can be accumulated in the long term by organisms, harming their reproductive and developmental processes (Hong et al. 2012). This issue, along with other stressors, can lead to a decline in populations and even present a threat to the dynamics of estuarine communities throughout the trophic web (Boening 2000; Lopes et al. 2014). The socioeconomic and ecological implications are important to address, as in some estuarine ecosystems, Hg concentrations have increased in both organisms and environmental compartments (Bayen 2012; Lamborg et al. 2014), raising the risk to human health. In particular, in Buenaventura Bay, the presence and accumulation of Hg have been reported in sediments and organisms (Duque and Cogua 2016; Gamboa-García 2017; (GamboaGarcía et al. 2018; Panesso Guevara 2017; Velásquez and Cortés 1997) and even in human blood and hair (Ardila Benavides 2000). This bioaccumulation occurs because Hg is not biodegradable and accumulates in biotic and abiotic compartments. Organic Hg (e.g., methyl mercury, MeHg) is stored not only in fatty tissue but also in the muscle. In the blue crab (Callinectes sapidus), 98%–100% of the total mercury (T-Hg) occurs as methyl mercury (Adams and Engel 2014), so in the present study, only T-Hg was measured in the muscle of macroinvertebrates. According to Adams and Engel (2014), the principal route of entry of T-Hg is by feeding; thus, T-Hg levels in the muscle serve as evidence of bioaccumulation. Moreover, due to the biomagnification processes, Hg can be transferred via the food web to human consumers (Olivero-Verbel et al. 2002; Taylor et al. 2014). Vulnerable groups, such as pregnant women and fishermen who live along coastal areas, can be at particular risk from direct or indirect exposure to Hg (Ausili et al. 2008; Costa et al. 2012; Zhang and Wong 2007). On the Pacific coast of (...truncated)