Contaminant screening and tissue distribution in the critically endangered Brazilian guitarfish Pseudobatos horkelii☆
Graphical abstract
Introduction
For the past decades, several compounds were considered as major contaminants in coastal regions due to their persistency and potential deleterious effects on organisms (Fleeger et al., 2003). On the other hand, a variety of newly synthesized compounds, considered as of emerging concern (CE), such as pharmaceuticals and personal care products (PPCPs), has been recently determined in marine ecosystems (Arpin-Pont et al., 2014). These compounds lack of monitoring and are potentially harmful to aquatic environments and wildlife (Sauvé and Desrosiers, 2014; Zenker et al., 2014). Whereas trace metals and legacy contaminants are persistent in the environment and prone to accumulate in marine wildlife, CEs are generally considered pseudo-persistent due to their indiscriminate use and chronic release in aquatic systems (Boxall et al., 2012; Overturf et al., 2015), despite their relatively rapid degradation. Yet, little is known on their occurrence and potential to accumulate in marine species. Impacts of CEs have already been hypothesized to be associated with population declines in birds (Oaks et al., 2004), and femininization of freshwater fishes with consequences at a population-level (Kidd et al., 2007), but studies conducted on marine species are mostly limited by experimental designs on traditional model species (Dann and Hontela, 2010; Fabbri and Franzellitti, 2016).
Elasmobranchs tend to accumulate high levels of contaminants due to their higher trophic positions, acting as meso and apex predators, and life history parameters, such as longevity. Accumulation of legacy contaminants and trace metals has been extensively studied among this group (Gelsleichter and Walker, 2010), whereas studies evaluating CEs are incipient, with only a few compounds being analyzed (Gelsleichter and Szabo, 2013; Lyons et al., 2018; Nakata, 2005; Nakata et al., 2009; Xue and Kannan, 2016; Xue et al., 2017). However, due to their trophic proximity, as well as k-strategy life-history patterns, with other taxa in which PPCPs have been detected (Gago-Ferrero et al., 2013; Fair et al., 2009; Nakata, 2005), it is highly expected to also detect these compounds and its metabolites in elasmobranch tissues. Regarding tissue distribution, a few studies have evaluated the distribution of contaminants (De Boeck et al., 2010; Corsolini et al., 2014), but are still scarce, especially considering CEs. For this reason, studies analyzing organotropism of contaminants are determinant for understanding the kinetics and associated physiological impacts of environmental contamination in elasmobranchs.
The Brazilian guitarfish Pseudobatos horkelii is a bottom-dweller endemic species from the Southwestern Atlantic occurring from southeastern Brazil to Argentina (Menni and Stehmann, 2000). This species shows a synchronous reproductive cycle, with pregnant females approaching shallow waters during the summer for embryonic development and parturition (Lessa et al., 1986; Martins et al., 2018). Southern Brazil represents a nursery area for southern populations, which are considered resident (Vooren et al., 2005). This species was categorized as “Critically Endangered” by the IUCN Red List of Threatened Species (Lessa and Vooren, 2016) and landing and commercialization are, therefore, prohibited by the Brazilian legislation (IBAMA, 2004). Despite this, P. horkelii is still illegally traded (De-Franco et al., 2012; Bunholi et al., 2018) and consumed, especially in southern Brazil.
Urban, industrial, agricultural and harbor activities have been impacting the southern Brazilian estuaries, mostly from inland sources (Mirlean et al., 2003; Wallner-Kersanach et al., 2016). The Patos Lagoon is the largest water body from South America and receives most of freshwater systems input, which are possible sources of contamination (Amado et al., 2006). This input of contaminants ends up in the marine environment, especially through the Rio Grande Channel. Caldas et al. (2019) detected several emerging compounds in surface and even drinking water from this area, suggesting that aquatic organisms might be exposed to emerging pesticides and PPCPs. Moreover, livestock and agricultural activities might also impact organisms in southern wetlands (Quintela et al., 2019), which run off to the coast. Considering this, it is likely that agricultural runoff, added to the already mentioned activities might also impact marine ecosystems and organisms, especially those inhabiting shallow waters.
In the light of the above, we hypothesize that P. horkelii might be exposed to environmental contamination of anthropogenic sources in southern Brazil. Furthermore, considering that its meat is illegally consumed, contaminant levels for this species are of great interest regarding human health. Taking this into account, we aimed to characterize, for the first time, the levels and tissue distribution of organic and inorganic compounds in five tissues of the Brazilian guitarfish P. horkelii, sampled in southern Brazil.
Section snippets
Study site
The Patos Lagoon is located in Rio Grande do Sul State, southern Brazil and has been receiving an input of contaminants from anthropogenic sources for about 15 years (Wallner-Kersanach et al., 2016). The southernmost estuarine region has been particularly affected due to an increase in port and naval activities, mostly in Rio Grande city (209,378 inhabitants, IBGE, 2017), where one of the largest harbors in southern Brazil is located. In addition, urban, industrial (fertilizer-producing plants,
Results and discussion
Descriptive statistics of concentrations of all organic contaminants in each tissue analyzed are provided in Table 1 and detection frequencies are provided in Table S4.
Conclusions
Our results indicate that P. horkelii is exposed to several contaminants in southern Brazil. Acute exposure was hypothesized to be related to liver levels whereas high concentrations in less metabolic tissues (e.g. muscle), especially of PAHs and emerging pesticides might reflect chronic exposure. However, high liver levels can also indicate chronic exposure and should not be only associated with acute exposure, since elasmobranchs are less efficient in xenobiotics metabolism in comparison with
Main findings
Pseudobatos horkelii is exposed to trace metals, polycyclic aromatic hydrocarbons and emerging contaminants and the highest levels were found in liver samples.
Notes
The authors declare no competing financial interest.
CRediT authorship contribution statement
Mariana F. Martins: Conceptualization, Formal analysis, Investigation, Writing - original draft, Writing - review & editing, Visualization, Funding acquisition. Patrícia G. Costa: Conceptualization, Methodology, Validation, Investigation, Writing - review & editing. Adalto Bianchini: Conceptualization, Resources, Writing - review & editing, Supervision.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001 and partially funded by the Save Our Seas Foundation (SOSF 422). A. Bianchini is a research fellow from the Brazilian Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq # 307647/20161). The authors thank the artisanal and recreational fisherman from Rio Grande, southern Brazil for donating the samples.
References (87)
- et al.
Metal accumulation and expression of genes encoding for metallothionein and copper transporters in a chronically exposed wild population of the fish Hyphessobrycon luetkenii
Comp. Biochem. Physiol. C
(2018) - et al.
Detection of PPCPs in marine organisms from contaminated coastal waters of the Saudi Red Sea
Sci. Total Environ.
(2018) - et al.
Biomarkers in croakers Micropogonias furnieri (Teleostei: sciaenidae) from polluted and non-polluted areas from the Patos Lagoon estuary (Southern Brazil): evidences of genotoxic and immunological effects
Mar. Pollut. Bull.
(2006) - et al.
Trace metals and persistente organic pollutants contamination in batoids (Chrondrichthyes:Batoidea): a systematic review
Environ. Pollut.
(2019) - et al.
The fishing and illegal trade of the angelshark: DNA barcoding against misleading identifications
Fish. Res.
(2018) - et al.
Monitoring organic and inorganic pollutants in juvenile live sea turtles: results from a study of Chelonia mydas and Eretmochelys imbricate in Cape Verde
Sci. Total Environ.
(2014) - et al.
Organotropism of persistent organic pollutants and heavy metals in the Greenland shark Somniosus microcephalus in NE Greenland
Mar. Pollut. Bull.
(2014) - et al.
Integration of multi-tissue PAH and PCB burdens with biomarker activity in three coastal shark species from the northwestern Gulf of Mexico
Sci. Total Environ.
(2019) - et al.
Concentrations and distributions of metals in tissues of stranded green sea turtles (Chelonia mydas) from the Southern Atlantic coast of Brazil
Sci. Total Environ.
(2014) - et al.
Metal accumulation and metallotionein induction in the spotted dogfish Scyliorhinus canicula
Comp. Biochem. Physiol. A
(2010)
Occurrence of triclosan in plasma of wild Atlantic bottlenose dolphins (Tursiops truncates) and in their environment
Environ. Pollut.
Indirect effects of contaminants in aquatic ecosystems
Sci. Total Environ.
Uptake of human pharmaceuticals in bull sharks (Carcharhinus leucas), inhabiting a wastewater-impacted river
Sci. Total Environ.
Mercury contamination in the recently described Brazilian White-tail dogfish Squalus albicaudus (Squalidae, Chondrichthyes)
Chemosphere
Eco-pharmacovigilance of non-steroidal anti-inflammatory drugs: necessity and opportunities
Chemosphere
Trace-elements, methylmercury and metallothionein levels in Magellanic penguin (Spheniscus magellanicus) found stranded on the Southern Brazilian coast
Mar. Pollut. Bull.
Worldwide occurrence and effects of antifouling paint booster biocides in the aquatic environment: a review
Environ. Int.
Occurrence, bioaccumulation and risk assessment of lipophilic pharmaceutically active compounds in the downstream rivers of sewage treatment plants
Sci. Total Environ.
Toxic and essential metals in Narcine brasiliensis (Elasmobranchii: narcinidae): a baseline ecotoxicological study in Southeast Atlantic and preliminary maternal transfer implications
Mar. Pollut. Bull.
Sex may influence environmental diphenhydramine accumulation in Round Stingrays
Mar. Pollut. Bull.
Distribution and composition pattern of polycyclic aromatic hydrocarbons in different tissues of sturgeons collected from Iranian coastline of the Caspian Sea
Chemosphere
Natural and anthropogenic hydrocarbon inputs to sediments of Patos Laggon Estuary, Brazil
Environ. Int.
A review of the pharmaceutical exposome in aquatic fauna
Environ. Pollut.
Mercury pollution sources in sediments of Patos Lagoon estuary, southern Brazil
Mar. Pollut. Bull.
Occurrence of organic UV filters and metabolites in lebranche mullet (Mugil liza) from Brazil
Sci. Total Environ.
Concentrations of trace elements in a rare and threatened coastal shark from the Arabian Gulf (smoothtooth blacktip Carcharhinus leiodon)
Mar. Pollut. Bull.
Occurrences, levels and risk assessment studies of emerging pollutants (pharmaceuticals, perfluoroalkyl and endocrine disrupting compounds) in fish samples from Kalk Bay harbor, South America
Environ. Pollut.
Occurrence and level of emerging organic contaminant in fish and mollusk from Klang River estuary, Malaysia and assessment on human health risk
Environ. Pollut.
Occurrence of pharmaceuticals and cocaine in a Brazilian coastal zone
Sci. Total Environ.
High arsenic and low lead concentrations in fish and reptiles from Taim wetlands, a Ramsar site in southern Brazil
Sci. Total Environ.
Occurrence, interactive effects and ecological risk of diclofenac in environmental compartments and biota- a review
Sci. Total Environ.
Toxic effects of the non-steroidal anti-inflammatory drug diclofenac
Aquat. Toxicol.
Lipid dynamics in fish: aspects of absorption, transportation, deposition and mobilization
Comp. Biochem. Physiol. B
Cadmium concentration in liver and muscle of silky shark (Carcharhinus falciformis) in the tip of Baja California south, México
Mar. Pollut. Bull.
Fish bioaccumulation and biomarkers in environmental risk assessment: a review
Environ. Toxicol. Pharmacol.
Bioaccumulation and biomagnification potential of pharmaceuticals with a focus to the aquatic environment
J. Environ. Manag.
Tissue distribution of organic contaminants in stranded pregnant sperm whale (Physeter microcephalus) from the Huizhou coast of the South China Sea
Mar. Pollut. Bull.
Bioaccumulation of polycyclic aromatic hydrocarbons in fish and invertebrates of lagos Lagoon, Nigeria
J. Emerg. Trends Eng. Appl. Sci.
Occurrence of PPCPs in the marine environment: a review
Environ. Sci. Pollut. Res.
Trace metal content trend of mussel Perna perna (linnaeus, 1758) from the Atlantic coast of southern Brazil
Water Air Soil Pollut.
Bioaccumulation and bioconcentration in aquatic organisms
Comparative organochlorine accumulation in two ecologically similar shark species (Carcharodon carcharias and Carcharhinus obscurus) with divergent uptake based on different life history
Environ. Toxicol.
Occurrence of pharmaceutical and personal care products (PPCPs) in marine sediments in the Todos of Santos Bay and the north coast of Salvador, Bahia, Brazil
J. Soils Sediments
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