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- Occurrence and distribution of persistent organic pollutants in the liver and muscle of Atlantic blue sharks: Relevance and health risksPublication . Muñoz-Arnanz, Juan; Bartalini, Alice; Alves, Luís; Lemos, Marco F.L.; Novais, Sara C.; Jiménez, BegoñaBlue shark score among the most abundant, widely distributed and worldwide consumed elasmobranchs. In this work contents of PCBs, PCDD/Fs and PBDEs were studied by means of GC-HRMS in muscle and liver of sixty blue sharks from the North East Atlantic sampled in 2019. Concentrations relatively similar were found for PCBs and PCDD/Fs in comparison with those in Atlantic specimens from the same area sampled in 2015. In contrast, PBDE loads doubled, likely mirroring the increased environmental presence of these pollutants. This, together with the different congener profiles reported for the same species in other geographical areas, highlighted the blue shark’s potential as bioindicator of the degree and fingerprints of regional pollution by POPs. Interesting dissimilarities between muscle and liver concentrations were detected, most likely ascribed to distinct toxicokinetics involved for the different pollutants. Whereas most POPs preferentially accumulated in liver, some did the opposite in muscle. BDE-209 was the most prominent example, being almost negligible its presence in liver (0.3%) while accounting for ca. 14% of the total PBDE content in muscle. Different findings in this regard described for other shark species call for focused research to ascertain the role of the species in this apparent favored metabolization of BDE-209 in the liver. From a consumption perspective, the concentrations found in muscle -the most relevant part in the human diet-for PCBs and dioxin-like POPs were below the EU maximum allowed levels in foodstuff. Conversely, in liver about 58% and 78% of samples overpassed the European levels for tolerable intake of i-PCBs and dioxin POPs, respectively. Concentrations of PBDEs exceeded EQS (0.0085 ng/g w.w.) established by the European Water Framework Directive in 100% and 92% of liver and muscle samples, respectively, which adds to the open debate of such as a reduce value for this current EQS.
- Accumulation of chemical elements and occurrence of microplastics in small pelagic fish from a neritic environmentPublication . Silva, Joana M. da; Alves, Luís M.F.; Laranjeiro, Maria I.; Bessa, Filipa; Silva, Andreia V.; Norte, Ana C.; Lemos, Marco F.L.; Ramos, Jaime A.; Novais, Sara C.; Ceia, Filipe R.The assessment of contaminant exposure in marine organisms often focuses on the most toxic chemical elements from upper trophic level species. Information on mid-trophic level species and particularly on potentially less harmful elements is lacking. Additionally, microplastics have been considered emergent contaminants in aquatic environments which have not been extensively studied in species from mid-trophic levels in food chains. This study aims to contribute to an overall assessment of environmental impacts of such chemicals in a community of small pelagic fish in the North Atlantic. The concentrations of 16 chemical elements, rarely simultaneously quantified (including minerals, trace elements and heavy metals), and the presence of microplastics were analysed in sardines (Sardina pilchardus) and mackerels (Scomber spp. and Trachurus trachurus) sampled along the Portuguese coast. Biochemical stress assessments and stable isotope analyses were also performed. The chemical element concentrations in S. pilchardus, T. trachurus, and Scomber spp. were relatively low and lower than the levels reported for the same species in the North Atlantic and adjacent areas. No clear relationships were found between chemical elements and oxidative damage in fish. However, the concentration of several chemical elements showed differences among species, being related with the species’ habitat use, trophic niches, and specific feeding strategies. The presence of plastic pieces in the stomachs of 29% of the sampled fishes is particularly concerning, as these small pelagic fish from mid-trophic levels compose a significant part of the diet of humans and other top predators. This study highlights the importance of multidisciplinary approaches focusing on the individual, including position data, stable isotopes, and oxidative stress biomarkers as complementary tools in contamination assessment of the marine mid-trophic levels in food chains.
- Assessment of contaminants in blue sharks from the Northeast Atlantic: Profiles, accumulation dynamics, and risks for human consumersPublication . Alves, Luís M.F.; Lemos, Marco F.L.; Moutinho, Ariana; Ceia, Filipe R.; Jiménez, Begoña; Cabral, Henrique; Muñoz-Arnanz, Juan; Novais, Sara C.Chemical pollution is a major threat to marine ecosystems, and top predators such as most shark species are extremely vulnerable to being exposed and accumulating contaminants such as metals and persistent organic pollutants (POPs). This work aimed to study the degree, composition, and the sources of contamination in the blue shark (Prionace glauca) inhabiting the Northeast Atlantic, as well as the potential risk faced by human consumers. A total of 60 sharks were sampled in situ aboard fishing vessels, and the concentrations of a set of metals and POPs were analysed in various tissues and complemented with stable isotope analyses. High levels of contaminants were found in most sharks sampled. The concentrations of most metals were higher in the muscle when compared with the liver. Regarding the dangers to consumers posed by the concentrations of arsenic (As), mercury (Hg), and lead (Pb), over 75% of the sharks presented muscle concentrations of at least one contaminant above the legal limits for human consumption, and a risk assessment determined that consumption of meat of these sharks exceeding 0.07 Kg per week could potentially expose human consumers to dangerous amounts of methylmercury (MeHg). Additionally, the assessment of single contaminants may lead to an underestimation of the risk for the human health. Finally, the overall accumulation of contaminants seems to be mostly influenced by the sharks’ geographical distribution, rather than sex, size, or trophic level of their prey.
- Year-round element quantification of a wide-ranging seabird and their relationships with oxidative stress, trophic ecology, and foraging patternsPublication . Laranjeiro, Maria I.; Alves, Luís M.; Silva, Joana M. da; Pereira, Jorge M.; Norte, Ana C.; Paiva, Vitor H.; Lemos, Marco F.L.; Ramos, Jaime A.; Novais, Sara C.; Ceia, Filipe R.Multidisciplinary approaches are essential to diligently assess environmental health status of ecosystems. In this study, year-round chemical elements’ exposure and impacts were assessed on the wide-ranging Cory’s shearwater Calonectris borealis breeding in Berlenga Island, offshore Portugal, North Atlantic Ocean. The aim was to identify potential contamination and oxidative stress sources associated with trophic ecology, habitat and spatial use, and foraging patterns. A set of 20 chemical elements were quantified, along with oxidative stress biomarkers, stable isotope analyses, and GPS tracking data. Birds presented higher accumulation to some nonessential elements along the year (i.e. arsenic, As; cadmium, Cd; mercury, Hg; lead, Pb; and strontium, Sr), in which concentrations were similar or surpassed other procellariform seabird populations all over the world. No significant differences were found for any of the elements between different periods within the breeding season, with exception of Hg. However, a Principal Component Analysis taking into consideration a group of elements showed differences between pre-laying and chick-rearing periods, with overall higher concentrations in the former. Individuals spending more time engaging in an intensive search for food, and in more coastal environments, presented overall higher element concentrations, and particularly Hg. Contrary to expectations, no relationships were found between chemical elements and oxidative stress. On the other hand, spatial use and foraging patterns of Cory’s shearwaters influenced their oxidative stress responses. Our results highlight the need for multidisciplinary approaches to deepen understanding of the large-scale vulnerability of bioindicators such as seabirds and, by extension, the overall environmental health of ecosystems in which they rely.
- Evidence of contamination-associated damage in blue sharks (Prionace glauca) from the Northeast AtlanticPublication . Alves, Luís M.F.; Moutinho, Ariana B.; Gómez, Luis J.; Oropesa, Ana L.; Muñoz-Arnanz, Juan; Jiménez, Begoña; Lemos, Marco F.L.; Fonseca, Vanessa F.; Cabral, Henrique; Novais, Sara C.Top predators such as most shark species are extremely vulnerable to amassing high concentrations of contaminants, but not much is known about the effects that the contaminant body burden imparts on these animals. Species like the blue shark (Prionace glauca) are very relevant in this regard, as they have high ecological and socioeconomic value, and have the potential to act as bioindicators of pollution. This work aimed to assess if differences in contaminant body burden found in blue sharks fromthe Northeast Atlantic would translate into differences in stress responses. Biochemical responses related to detoxification and oxidative stress, and histological alterations were assessed in the liver and gills of 60 blue sharks previously found to have zone-related contamination differences. Similar zone-related differences were found in biomarker responses, with the sharks from the most contaminated zone exhibiting more pronounced responses. Additionally, strong positive correlations were found between contaminants (i.e., As, PCBs, and PBDEs) and relevant biomarkers (e.g., damaged DNA and protective histological alterations). The present results are indicative of the potential that this species and these tools have to be used to monitor pollution in different areas of the Atlantic.
- Biomonitoring atlantic deep waters through the assessment of shark biomarkersPublication . Alves, Luís Miguel Fonseca; Lemos, Marco Filipe Loureiro; Correia, João Pedro Santos; Novais, Sara CalçadaOs ecossistemas marinhos estão continuamente a ser sobrecarregados com contaminantes derivados de atividades humanas resultando numa dimunuição dos recursos marinhos. A exposição crónica a contaminantes, como metais pesados e poluentes orgânicos persistentes (POPs), pode afetar negativamente o ambiente marinho e, eventualmente, também os seres humanos. Grandes predadores pelágicos, como tubarões, são particularmente afetados pela poluição, principalmente através de processos de bioacumulação e biomagnificação. A fim de resolver o problema acima mencionado, são necessários estudos de avaliação de risco ambiental para prever os padrões de contaminação e evitar efeitos adversos que muitas vezes só são visíveis quando é tarde demais para tomar ações preventivas. Análises de concentração de químicos fornecem-nos informações sobre o nível de contaminação no ambiente; no entanto, podem não ser suficientes para entender como os organismos estão a ser afetados e há uma necessidade de relacionar essas quantificações com parâmetros biológicos. A avaliação de parâmetros bioquímicos, como a atividade enzimática, pode fornecer uma visão mais sensível e precisa sobre os níveis de contaminação. Tubarões como Prionace glauca são predadores de topo e portanto extremamente importantes nos ecossistemas marinhos. A sua grande distribuição, juntamente com o fácil acesso a amostras, fornecidas por barcos de pesca comercial, tornou-as um alvo favorável para utilização em ensaios toxicológicos. Este estudo teve como objetivo avaliar o potencial de P. glauca como uma espécie sentinela para pesquisas de monitorização de poluição, através do desenvolvimento e da aplicação de biomarcadores apropriados. As amostras de tecidos foram recolhidas de vinte tintureiras na costa de Portugal, a bordo de um barco comercial de pesca de espadarte. Níveis de POPs, assim como parâmetros bioquímicos relacionados com destoxificação, stress oxidativo e funções neuronais, foram medidos. A caracterização prévia da atividade das colinesterases no músculo e cérebro de P. glauca foi feita, já que não havia dados disponíveis sobre esta matéria. Esta caracterização foi essencial devido à existência de três classes de ChE conhecidas em peixes, acetilcolinesterase (AChE), butirilcolinesterase (BChE) e propionilcolinesterase (PChE), todas bastante suscetíveis a agentes anticolinérgicos, e outros contaminantes, tornando-as biomarcadores relevantes em estudos de monitorização de poluição. Os resultados obtidos indicaram que o cérebro de P. glauca aparenta possuir ChEs atípicas, revelando propriedades mistas de AChE e BChE e, que o músculo aparentemente possui maioritariamente AChE. A exposição in vitro a chloropyrifos-oxon provocou inibição de ChE das tintureiras em ambos os tecidos, com o cérebro sendo o tecido mais sensível e, por isso, o mais adequado para a detecção de compostos anticolinérgicos no ambiente. Este estudo indica que a actividade de ChE em tintureiras tem potencial para ser usada como um biomarcador sensível e fiável em programas de biomonitorização marinha. O fígado apresentou níveis mais elevados de POP, quando comparado com músculo. Foram encontradas correlações positivas e negativas entre os parâmetros de contaminação e de stresse oxidativo. Este estudo destaca a importância da caracterização de Che antes de a usar como um biomarcador em estudos ecotoxicológicos, e demonstra o grande potencial de P. glauca como espécie modelo e como sentinela de poluição marinha, através do uso de biomarcadores adequados.
- Oxidative stress responses and cellular energy allocation changes in microalgae following exposure to widely used human antibioticsPublication . Aderemi, Adeolu O.; Novais, Sara C.; Lemos, Marco F.L.; Alves, Luís M.; Hunter, Colin; Pahl, OleThe individual effect of four human antibiotics on the microalgae Raphidocelis subcapitata was investigated following a 120-h exposure. The effects were assessed by analyzing growth, and biochemical parameters related with: 1) antioxidant capacity and oxidative damage by measuring superoxide dismutase (SOD) activity and lipid peroxidation (LPO) levels; and 2) cellular energy allocation (CEA) by quantifying the content in energy reserves, which represents the energy available (Ea), and the electron transport system activity that represents a measure of oxygen and cellular energy consumption (Ec). Growth yield inhibitory concentrations of sulfamethoxazole (18–30%), clarithromycin (28.7%), ciprofloxacin (28%) and erythromycin (17–39%) were found to elicit a considerable increase in Ec, thereby causing a significant decrease in the CEA. The elevated Ec can be a result of the need to respond to oxidative stress occurring under those conditions given the significant increase in SOD activity at these levels. For sulfamethoxazole, erythromycin and ciprofloxacin, the antioxidant responses do not seem to be enough to cope with the reactive oxygen species and prevent oxidative damage, given the elevated LPO levels observed. A stimulatory effect on growth yield was observed (up to 16%) at ciprofloxacin lowest concentration, which highly correlated with the increase in CEA. Based on the no observed effect concentration (NOECs) and/or effective concentration (EC10) results, Ec, SOD and CEA were more sensitive than the classical endpoint of growth rate for all the tested antibiotics. By revealing the antibiotic stress effects in R. subcapitata at the cellular level, this study suggests CEA as a more reliable indicator of the organisms’ physiological status.
- Boat noise impacts early life stages in the Lusitanian toadfish: a field experimentPublication . Faria, A.; Fonseca, P. J.; Vieira, M.; Alves, L. M. F.; Lemos, Marco F.L.; Novais, Sara C.; Matos, A. B.; Vieira, D.; Amorim, M. C. P.Marine traffic is themost common and chronic source of ocean noise pollution. Despite the evidence of detrimental effects of noise exposure on fish, knowledge about the effects on the critical early life stages - embryos and larvae - is still scarce. Here, we take a natural habitat-based approach to examine potential impacts of boat noise exposure in early life stages in a wild fish population of the Lusitanian toadfish (Halobatrachus didactylus). In-situ experiments were carried out in the Tagus estuary, an estuary with significant commercial and recreational boat traffic. Nestswith eggswere exposed to either ambient (control) or boat noise (treatment), for 1 fortnight. Eggs were photographed before being assigned to each treatment, and after exposure, to count number of eggs and/or larvae to assess survival, and sampled to study development and oxidative stress and energy metabolism-related biomarkers. Data concerns 4 sampling periods (fortnights) from 2 years. Results indicate that offspring survival did not differ between treatments, but boat noise induced a detrimental effect on embryos and larvae stress response, and on larvae development. Embryos showed reduced levels of electron transport system (ETS), an energy metabolism-related biomarker, while larvae showed higher overall stress responses, with increased levels of superoxide dismutase (SOD) and DNA damage (oxidative stress related responses), ETS, and reduced growth. With this study,we provided the first evidence of detrimental effects of boat noise exposure on fish development in the field and on stress biomarker responses. If these critical early stages are not able to compensate and/or acclimate to the noise stress later in the ontogeny, then anthropogenic noise has the potential to severely affect this and likely other marine fishes, with further consequences for populations resilience and dynamics.
- Scyliorhinus canicula (Linnaeus, 1758) metal accumulation: A public health concern for Atlantic fish consumers?Publication . Marques, Alexandre F.S.; Alves, Luís M.F.; Moutinho, Ariana; Lemos, Marco F.L.; Novais, Sara C.One of the most landed sharks in Portuguese fisheries is the lesser-spotted dogfish (Scyliorhinus canicula), which is ever-present in Portuguese fish markets and consumed as cheap fish protein source. The focus of this study was to evaluate element contamination in consumed tissues of Atlantic S. canicula, with the intent of safeguarding possible public health issues. A total of 74 specimens were analysed for metals and metalloids in the deeper white muscle and skin. Arsenic, zinc, iron and aluminium were the elements with higher mean values. There was a tendency for higher levels in the skin, with differences between life-stage and gender. Many individuals surpassed stipulated guideline limits for mercury and arsenic, posing a risk for human consumption (according to the health risk assessment performed for the average Portuguese fish consumption) or even for use in feed production. Besides the public health concern, this study also evidences troubling signs on marine contamination status.
- The potential of cholinesterases as tools for biomonitoring studies with sharks: Biochemical characterization in brain and muscle tissues of Prionace glaucaPublication . Alves, Luís M.; Lemos, Marco F.L.; Correia, João P. S.; Costa, Nuno A.R. da; Novais, Sara C.Cholinesterases (ChE) are a family of enzymes that play an essential role in neuronal and motor functions. Because of the susceptibility of these enzymes to anticholinergic agents and to other contaminants, their activity is frequently used as biomarker in pollution monitoring studies. The three known types of ChE in fish are acetilcholinesterase (AChE), butyrylcholinesterase (BChE) and propionylcholinesterase (PChE). The presence of these enzymes in each tissue differs between species, and thus their usage as biomarkers requires previous enzyme characterization. Sharks, mostly acting as apex predators, help maintain the balance of fish populations performing a key role in the ecosystem. Blue sharks (Prionace glauca) are one of the most abundant and heavily fished sharks in the world, thus being good candidate organisms for ecotoxicology and biomonitoring studies. The present study aimed to characterize the ChE present in the brain and muscle of the blue shark using different substrates and selective inhibitors, and to assess the in vitro sensitivity of these sharks' ChE to chlorpyrifos-oxon, a metabolite of a commonly used organophosphorous pesticide, recognized as amodel anticholinesterase contaminant. The results suggest that the brain of P. glauca seems to contain atypical ChEs, displayingmixed properties of AChE and BChE, and that the muscle tissue seems to contain mainly AChE. In vitro exposures to chloropyrifosoxon inhibited blue shark's ChE in both tissues, the brain being the most sensitive tissue and therefore the most suitable for detection of exposure to low concentrations of anticholinergic compounds in the environment. This study indicates that ChE activity in blue sharks has the potential to be used as a sensitive and reliable biomarker in marine biomonitoring programs.