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- Antidepressants in a changing ocean: Venlafaxine uptake and elimination in juvenile fish (Argyrosomus regius) exposed to warming and acidification conditionsPublication . Luísa Maulvault, Ana; Santos, Lúcia H.M.L.M.; Camacho, Carolina; Anacleto, Patrícia; Barbosa, Vera; Alves, Ricardo; Pousão Ferreira, Pedro; Serra-Compte, Albert; Barceló, Damià; Rodriguez-Mozaz, Sara; Rosa, Rui; Diniz, Mário S.; Marques, AntónioThe presence of antidepressants, such as venlafaxine (VFX), in marine ecosystems is increasing, thus, potentially posing ecological and human health risks. The inherent mechanisms of VFX uptake and elimination still require further understanding, particularly accounting for the impact of climate change-related stressors, such as warming and acidification. Hence, the present work aimed to investigate, for the first time, the effects of increased seawater temperature (ΔT°C = +5 °C) and pCO2 levels (ΔpCO2 ∼1000 μatm, equivalent to ΔpH = -0.4 units) on the uptake and elimination of VFX in biological tissues (muscle, liver, brain) and plasma of juvenile meagre (Argyrosomus regius) exposed to VFX through two different exposure pathways (via water, i.e. [VFX ] ∼20 μg L-1, and via feed, i.e. [VFX] ∼160 μg kg-1 dry weight, dw). Overall, results showed that VFX can be uptaken by fish through both water and diet. Fish liver exhibited the highest VFX concentration (126.7 ± 86.5 μg kg-1 and 6786.4 ± 1176.7 μg kg-1 via feed and water exposures, respectively), as well as the highest tissue:plasma concentration ratio, followed in this order by brain and muscle, regardless of exposure route. Both warming and acidification decreased VFX uptake in liver, although VFX uptake in brain was favoured under warming conditions. Conversely, VFX elimination in liver was impaired by both stressors, particularly when acting simultaneously. The distinct patterns of VFX uptake and elimination observed in the different scenarios calls for a better understanding of the effects of exposure route and abiotic conditions on emerging contaminants' toxicokinetics.
- Will seabass (Dicentrarchus labrax) quality change in a warmer ocean?Publication . Barbosa, Vera; Luísa Maulvault, Ana; Alves, Ricardo N.; Anacleto, Patrícia; Pousão-Ferreira, Pedro; Carvalho, Maria Luísa; Nunes, Maria Leonor; Rosa, Rui; Marques, AntónioThe impacts of climate change on seafood quality, safety and human health are still unknown. The present study investigated the effect of warming on fatty acids and elements content in two tissues (muscle and liver) of the relevant commercial seabass species (Dicentrarchus labrax). After exposing fish to increased seawater temperature for a period of 60days, higher saturated fatty acid (SFA) levels were observed in fish muscle (2.16% increase); whereas lower SFA levels were observed in fish liver (5.42% decrease). On the other hand, monounsaturated fatty acids (MUFA) and polyunsaturated fatty acids (PUFA) contents decreased in both muscle (1.77% and 0.39%, respectively) and liver (10.54% and 8.11%, respectively) of fish subjected to warmer conditions. Additionally, warming promoted changes in fish elemental profiles, leading to significantly higher levels of Cl in the muscle and lower levels of Rb in the liver. Overall, data showed that fatty acids and elemental contents were affected by temperature, though representing small implications to human health. Moreover, this preliminary study highlights the importance of conducting further seafood risk-benefit assessments under climate change contexts.
- Differential behavioural responses to venlafaxine exposure route, warming and acidification in juvenile fish (Argyrosomus regius)Publication . Luísa Maulvault, Ana; Santos, Lúcia H.M.L.M.; Paula, José Ricardo; Camacho, Carolina; Pissarra, Vasco; Fogaça, Fabiola; Barbosa, Vera; Alves, Ricardo; Ferreira, Pedro Pousão; Barceló, Damià; Rodriguez-Mozaz, Sara; Marques, António; Diniz, Mário S.; Rosa, RuiAntidepressants, such as venlafaxine (VFX), which are considered emerging environmental pollutants, are increasingly more present in the marine environment, and recent evidence suggest that they might have adverse effects on fish behaviour. Furthermore, altered environmental conditions associated to climate change (e.g. warming and acidification) can also have a determinant role on fish behaviour, fitness and survival. Yet, the underlying interactions between these environmental stressors (pharmaceuticals exposure and climate change) are still far from being fully understood. The aim of this study was to assess behavioural responses (in juvenile meagre (Argyrosomus regius) exposed to VFX via water ([VFX] ~20μgL-1) and via dietary sources ([VFX] ~160μgkg-1 dry weight), as well as to increased temperature (ΔT°C=+5°C) and high CO2 levels (ΔpCO2 ~1000μatm; equivalent to ΔpH=-0.4units). Overall, VFX bioaccumulation in fish plasma was enhanced under the combination of warming and acidification. VFX triggered fish exploration, whereas fish activity and shoal cohesion were reduced. Acidification alone decreased fish exploration and shoal cohesion, and reversed fish preference to turn leftwards compared to control conditions. Such alterations were further enhanced by VFX exposure. The combination of warming and acidification also reduced shoal cohesion and loss of lateralization, regardless of VFX exposure. The distinct behaviour observed when VFX contamination, acidification and warming acted alone or in combination highlighted the need to consider the likely interactive effects of seawater warming and acidification in future research regarding the toxicological aspects of chemical contaminants.
- Ocean acidification dampens physiological stress response to warming and contamination in a commercially-important fish (Argyrosomus regius)Publication . Sampaio, Eduardo; Lopes, Ana Rita; Francisco, Sofia; Paula, José Ricardo; Pimentel, Marta; Luísa Maulvault, Ana; Repolho, Tiago; F. Grilo, Tiago; Pousão-Ferreira, Pedro; Marques, António; Rosa, RuiIncreases in carbon dioxide (CO2) and other greenhouse gases emissions are changing ocean temperature and carbonate chemistry (warming and acidification, respectively). Moreover, the simultaneous occurrence of highly toxic and persistent contaminants, such as methylmercury, will play a key role in further shaping the ecophysiology of marine organisms. Despite recent studies reporting mostly additive interactions between contaminant and climate change effects, the consequences of multi-stressor exposure are still largely unknown. Here we disentangled how Argyrosomus regius physiology will be affected by future stressors, by analysing organ-dependent mercury (Hg) accumulation (gills, liver and muscle) within isolated/combined warming (ΔT=4°C) and acidification (ΔpCO2=1100μatm) scenarios, as well as direct deleterious effects and phenotypic stress response over multi-stressor contexts. After 30 days of exposure, although no mortalities were observed in any treatments, Hg concentration was enhanced under warming conditions, especially in the liver. On the other hand, elevated CO2 decreased Hg accumulation and consistently elicited a dampening effect on warming and contamination-elicited oxidative stress (catalase, superoxide dismutase and glutathione-S-transferase activities) and heat shock responses. Thus, potentially unpinned on CO2-promoted protein removal and ionic equilibrium between hydrogen and reactive oxygen species, we found that co-occurring acidification decreased heavy metal accumulation and contributed to physiological homeostasis. Although this indicates that fish can be physiologically capable of withstanding future ocean conditions, additional experiments are needed to fully understand the biochemical repercussions of interactive stressors (additive, synergistic or antagonistic).
- Effects of depuration on metal levels and health status of bivalve molluscsPublication . Anacleto, Patrícia; Luísa Maulvault, Ana; Nunes, Maria Leonor; Carvalho, Maria Luísa; Rosa, Rui; Marques, AntónioDepuration has been mandatory to eliminate microorganisms in bivalve molluscs, but not to eliminate toxic chemicals, since there is still shortage of scientific evidence about the efficacy of depuration to decrease the levels of toxic chemicals in bivalves. This study aims to assess the effects of depuration on the levels of toxic, macro and trace elements in three bivalve species (Ruditapes philippinarum-RP, Mytilus galloprovincialis-MG and Scrobicularia plana-SP), taking into account their condition. During depuration, a significant reduction of elements occurred in RP (Fe, Pb, Cu, Rb, Br, Hg, Cd and As), MG (Cl, Sr, Fe, Pb and Br) and SP (Fe, Pb, Cu and Rb), while an increase was registered for other elements in RP (Cl and Sr), MG (S and Zn) and SP (Cl, Zn, Br and Sr). After two days of depuration, Pb in SP had decreased to levels below the permissible limits, thus allowing this species to be acceptable for human consumption as far as toxic elements are concerned. SP revealed the highest glycogen levels compared to the other species indicating different physiological requirements. However, in this species glycogen levels significantly decreased after two days of depuration and mortality increased. In contrast, in MG and RP glycogen and mortality did not vary significantly during depuration. Therefore, SP should be only depurated for a maximum period of two days. Overall, the results of this study are particularly useful to retailers to ensure high quality bivalve products for consumers. Additionally, glycogen can be used as a suitable biomarker of healthy status of bivalve species during depuration.
- Integrated multi-biomarker responses of juvenile seabass to diclofenac, warming and acidification co-exposurePublication . Luísa Maulvault, Ana; Barbosa, Vera; Alves, Ricardo; Anacleto, Patrícia; Camacho, Carolina; Cunha, Sara; Fernandes, José O.; Ferreira, Pedro Pousão; Rosa, Rui; Marques, António; Diniz, Mário S.Pharmaceutical drugs, such as diclofenac (DCF), are frequently detected in the marine environment, and recent evidence has pointed out their toxicity to non-target marine biota. Concomitantly, altered environmental conditions associated with climate change (e.g. warming and acidification) can also affect the physiology of marine organisms. Yet, the underlying interactions between these environmental stressors (pharmaceutical exposure and climate change-related stressors) still require a deeper understanding. Comprehending the influence of abiotic variables on chemical contaminants' toxicological attributes provides a broader view of the ecological consequences of climate change. Hence, the aim of this study was to assess the ecotoxicological responses of juvenile seabass Dicenthrachus labrax under the co-exposure to DCF (from dietary sources, 500 ± 36 ng kg-1 dw), warming (ΔTºC = +5 °C) and acidification (ΔpCO2 ∼1000 μatm, equivalent to ΔpH = -0.4 units), using an "Integrated Biomarker Response" (IBR) approach. Fish were exposed to these three stressors, acting alone or combined, for 28 days in a full cross-factorial design, and blood, brain, liver and muscle tissues were subsequently collected in order to evaluate: i) animal/organ fitness; ii) hematological parameters and iii) molecular biomarkers. Results not only confirmed the toxicological attributes of dietary exposure to DCF in marine fish species at the tissue (e.g. lower HSI), cellular (e.g. increased ENAs and lower erythrocytes viability) and molecular levels (e.g. increased oxidative stress, protein degradation, AChE activity and VTG synthesis), but also showed that such attributes are altered by warming and acidification. Hence, while acidification and/or warming enhanced some effects of DCF exposure (e.g. by further lowering erythrocyte viability, and increasing brain GST activity and Ub synthesis in muscle), the co-exposure to these abiotic stressors also resulted in a reversion/inhibition of some molecular responses (e.g. lower CAT and SOD inhibition and VTG synthesis). IBRs evidenced that an overall higher degree of stress (i.e. high IBR index) was associated with DCF and warming co-exposure, while the effects of acidification were less evident. The distinct responses observed when DCF acted alone or the animals were co-exposed to the drug together with warming and acidification not only highlighted the relevance of considering the interactions between multiple environmental stressors in ecotoxicological studies, but also suggested that the toxicity of pharmaceuticals can be aggravated by climate change-related stressors (particularly warming), thus, posing additional biological challenges to marine fish populations.
- Bioaccumulation and elimination of mercury in juvenile seabass (Dicentrarchus labrax) in a warmer environmentPublication . Maulvault, Ana Luísa; Custódio, Ana; Anacleto, Patrícia; Repolho, Tiago; Pousão, Pedro; Nunes, Maria Leonor; Diniz, Mário; Rosa, Rui; Marques, AntónioWarming is an expected impact of climate change that will affect coastal areas in the future. These areas are also subjected to strong anthropogenic pressures leading to chemical contamination. Yet, the consequences of both factors for marine ecosystems, biota and consumers are still unknown. The present work aims to investigate, for the first time, the effect of temperature increase on bioaccumulation and elimination of mercury [(total mercury (THg) and methylmercury (MeHg)] in three tissues (muscle, liver, and brain) of a commercially important seafood species - European seabass (Dicentrarchus labrax). Fish were exposed to the ambient temperature currently used in seabass rearing (18°C) and to the expected ocean warming (+4°C, i.e. 22°C), as well as dietary MeHg during 28 days, followed by a depuration period of 28 days fed with a control diet. In both temperature exposures, higher MeHg contents were observed in the brain, followed by the muscle and liver. Liver registered the highest elimination percentages (EF; up to 64% in the liver, 20% in the brain, and 3% in the muscle). Overall, the results clearly indicate that a warming environment promotes MeHg bioaccumulation in all tissues (e.g. highest levels in brain: 8.1mg kg-1 ww at 22°C against 6.2mg kg-1 ww at 18°C after 28 days of MeHg exposure) and hampers MeHg elimination (e.g. liver EF decreases after 28 days of depuration: from 64.2% at 18°C to 50.3% at 22°C). These findings suggest that seafood safety may be compromised in a warming context, particularly for seafood species with contaminant concentrations close to the current regulatory levels. Hence, results point out the need to strengthen research in this area and to revise and/or adapt the current recommendations regarding human exposure to chemical contaminants through seafood consumption, in order to integrate the expected effects of climate change.
- Fish energy budget under ocean warming and flame retardant exposurePublication . Anacleto, Patrícia; Figueiredo, Cátia; Baptista, Miguel; Luísa Maulvault, Ana; Camacho, Carolina; Pousão-Ferreira, Pedro; Valente, Luísa M.P.; Marques, António; Rosa, RuiClimate change and chemical contamination are global environmental threats of growing concern for the scientific community and regulatory authorities. Yet, the impacts and interactions of both stressors (particularly ocean warming and emerging chemical contaminants) on physiological responses of marine organisms remain unclear and still require further understanding. Within this context, the main goal of this study was to assess, for the first time, the effects of warming (+ 5 °C) and accumulation of a polybrominated diphenyl ether congener (BDE-209, brominated flame retardant) through dietary exposure on energy budget of the juvenile white seabream (Diplodus sargus). Specifically, growth (G), routine metabolism (R), excretion (faecal, F and nitrogenous losses, U) and food consumption (C) were calculated to obtain the energy budget. The results demonstrated that the energy proportion spent for G dominated the mode of the energy allocation of juvenile white seabream (56.0-67.8%), especially under the combined effect of warming plus BDE-209 exposure. Under all treatments, the energy channelled for R varied around 26% and a much smaller percentage was channelled for excretion (F: 4.3-16.0% and U: 2.3-3.3%). An opposite trend to G was observed to F, where the highest percentage (16.0 ± 0.9%) was found under control temperature and BDE-209 exposure via diet. In general, the parameters were significantly affected by increased temperature and flame retardant exposure, where higher levels occurred for: i) wet weight, relative growth rate, protein and ash contents under warming conditions, ii) only for O:N ratio under BDE-209 exposure via diet, and iii) for feed efficiency, ammonia excretion rate, routine metabolic rate and assimilation efficiency under the combination of both stressors. On the other hand, decreased viscerosomatic index was observed under warming and lower fat content was observed under the combined effect of both stressors. Overall, under future warming and chemical contamination conditions, fish energy budget was greatly affected, which may dictate negative cascading impacts at population and community levels. Further research combining other climate change stressors (e.g. acidification and hypoxia) and emerging chemical contaminants are needed to better understand and forecast such biological effects in a changing ocean.
- Ecophysiological responses of juvenile seabass (Dicentrarchus labrax) exposed to increased temperature and dietary methylmercuryPublication . Luísa Maulvault, Ana; Barbosa, Vera; Alves, Ricardo; Custódio, Ana; Anacleto, Patrícia; Repolho, Tiago; Pousão Ferreira, Pedro; Rosa, Rui; Marques, António; Diniz, Mário S.The ecotoxicological effects of methylmercury (MeHg) exposure have been intensively described in literature. Yet, it is still unclear how marine biota will respond to the presence of MeHg under climate change, namely ocean warming. The present study aimed to investigate, for the first time, fish condition [Fulton's K index (K), hepatosomatic index (HIS) and brain-to-body mass ratio (BB-ratio)] and several stress-related responses in an ecologically and commercially important fish species (Dicentrachus labrax) exposed for 28 days to dietary MeHg (8.0 mg kg-1 dw) and temperature increase (+ 4 °C). Results showed significant impairments on fish condition, i.e. up to 34% decrease on K, > 100% increase on HIS and 44% decrease on BB-ratio, compared to control conditions. Significant changes on tissue biochemical responses were observed in fish exposed to both stressors, acting alone or combined, evidencing the relevance of assessing possible interactions between different environmental stressors in ecotoxicological studies. For instance, muscle showed to be the least affected tissue, only revealing significant alterations in GST activity of MeHg-enriched fish. On the other hand, liver exhibited a significant induction of GST (> 100%) and CAT (up to 74%) in MeHg-enriched fish, regardless of temperature exposure, as well as decreased SOD activity (19%) and increased HSP70/HSC70 content (87%) in fish exposed to warming alone. Brain showed to be affected by temperature (69% of GST inhibition and > 100% of increased CAT activity), MeHg (> 100% of increased CAT activity, 47% of SOD inhibition and 55% of AChE inhibition), as well as by the combination of both (GST, SOD and AChE inhibition, 17%, 48% and 53%, respectively). Hence, our data provides evidences that the toxicological aspects of MeHg ca be potentiated by warmer temperatures, thus, evidencing the need for further research combining contaminants exposure and climate change effects, to better forecast ecological impacts in the ocean of tomorrow.