← Back to Search
Integrated Multi-biomarker Responses Of Juvenile Seabass To Diclofenac, Warming And Acidification Co-exposure.
A. Maulvault, Vera Barbosa, R. Alves, Patrícia Anacleto, C. Camacho, S. Cunha, J. Fernandes, P. P. Ferreira, R. Rosa, A. Marques, M. Diniz
Published 2018 · Biology, Medicine
Save to my Library
Download via 🐼 PaperPanda Download via oaDOI Download via OAB Download via LibKey Download via Google Google ScholarAnalyze on Scholarcy Visualize in Litmaps
Reduce the time it takes to create your bibliography by a factor of 10 by using the world’s favourite reference manager
Time to take this seriously.
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.
This paper references
A new and rapid colorimetric determination of acetylcholinesterase activity.
G. Ellman (1961)
Glutathione S-transferases. The first enzymatic step in mercapturic acid formation.
W. Habig (1974)
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
M. M. Bradford (1976)
Computation and interpretation of biological statistics of fish populations
W. Ricker (1977)
Determination of malonaldehyde precursor in tissues by thiobarbituric acid test.
M. Mihara (1978)
A simple method for clinical assay of superoxide dismutase.
Y. Sun (1988)
A spectrophotometric method for determination of catalase activity in small tissue samples.
L. Johansson (1988)
Assessment of the Piscine Micronucleus Test as an in situ Biological indicator of Chemical Contaminant Effects
Kenneth R. Carrasco (1990)
Heat shock, stress proteins, chaperones, and proteotoxicity
L. Hightower (1991)
Vitellogenin as a Biomarker of Exposure for Estrogen or Estrogen Mimics
N. Denslow (1999)
A rapid and accurate spectroscopic method for alkalinity measurements in sea water samples
G. Sarazin (1999)
Integrated biomarker response: a useful tool for ecological risk assessment.
B. Beliaeff (2002)
Toxic effects of the non-steroidal anti-inflammatory drug diclofenac. Part II: cytological effects in liver, kidney, gills and intestine of rainbow trout (Oncorhynchus mykiss).
R. Triebskorn (2004)
Comparison of two ELISAs for the determination of Hsp70 in serum.
R. Njemini (2005)
Innate immunity of fish (overview).
B. Magnadóttir (2006)
Hormonal control of salt and water balance in vertebrates.
S. McCormick (2006)
Endocrine disruptors in marine organisms: approaches and perspectives.
C. Porte (2006)
Non-steroidal anti-inflammatory drugs disrupt the heat shock response in rainbow trout.
A. Gravel (2007)
Immunological alterations in juvenile Pacific herring, Clupea pallasi, exposed to aqueous hydrocarbons derived from crude oil.
C. Kennedy (2008)
Vitellogenin as a biomarker of exposure to estrogenic compounds in aquatic invertebrates: a review.
V. Matozzo (2008)
Effects of ECF-Kraft pulp mill effluent treated with fungi (Rhizopus oryzae) on reproductive steroids and liver CYP1A of exposed goldfish (Carassius auratus)
M. Diniz (2009)
Immune effects of HFO on European sea bass, Dicentrarchus labrax, and Pacific oyster, Crassostrea gigas.
A. Bado-Nilles (2009)
Climate change and seafood safety: Human health implications
António Marques (2010)
Spatial and temporal variations of biological responses to environmental pollution in the freshwater zebra mussel.
Edwige Guerlet (2010)
Assessing the estrogenic potency in a Portuguese wastewater treatment plant using an integrated approach.
M. Diniz (2010)
Climate change effects on fishes and fisheries: towards a cause-and-effect understanding.
H. Pörtner (2010)
Non-steroidal anti-inflammatory drug (NSAID) ibuprofen distresses antioxidant defense system in mussel Mytilus galloprovincialis gills.
M. González-Rey (2011)
Effects of carbofuran on the sea bass (Dicentrarchus labrax L.): study of biomarkers and behaviour alterations.
D. Hernández-Moreno (2011)
Cytotoxicity assessment of four pharmaceutical compounds on the zebra mussel (Dreissena polymorpha) haemocytes, gill and digestive gland primary cell cultures.
M. Parolini (2011)
Ecotoxicological impacts of clofibric acid and diclofenac in common carp (Cyprinus carpio) fingerlings: hematological, biochemical, ionoregulatory and enzymological responses.
M. Saravanan (2011)
Application of an integrated biomarker response index (IBR) to assess temporal variation of environmental quality in two Portuguese aquatic systems
A. Serafim (2012)
Fast and comprehensive multi-residue analysis of a broad range of human and veterinary pharmaceuticals and some of their metabolites in surface and treated waters by ultra-high-performance liquid chromatography coupled to quadrupole-linear ion trap tandem mass spectrometry.
M. Gros (2012)
Sustained high temperature increases the vitellogenin response to 17α-ethynylestradiol in mummichog (Fundulus heteroclitus).
K. Chandra (2012)
Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function
G. Nilsson (2012)
Diclofenac-induced oxidative stress in brain, liver, gill and blood of common carp (Cyprinus carpio).
H. Islas-Flores (2013)
The effects of diclofenac on early life stages of common carp (Cyprinus carpio).
S. Štěpánová (2013)
Analysis of multi-class pharmaceuticals in fish tissues by ultra-high-performance liquid chromatography tandem mass spectrometry.
B. Huerta (2013)
Bioaccumulation and biomagnification potential of pharmaceuticals with a focus to the aquatic environment.
A. Zenker (2014)
Synergistic Effects of Toxic Elements on Heat Shock Proteins
K. Mahmood (2014)
The physiology of fish at low pH: the zebrafish as a model system
R. W. M. Kwong (2014)
Sources, impacts and trends of pharmaceuticals in the marine and coastal environment
S. Gaw (2014)
Subchronic atrazine exposure changes defensive behaviour profile and disrupts brain acetylcholinesterase activity of zebrafish.
Ademir J Schmidel (2014)
Effects of increasing temperatures on biomarker responses and accumulation of hazardous substances in rope mussels (Mytilus galloprovincialis) from Bizerte lagoon
Naouel Kamel (2014)
Histopathological alterations, physiological limits, and molecular changes of juvenile Sparus aurata in response to thermal stress
D. Madeira (2014)
Effects of non-steroidal anti-inflammatory drug (NSAID) diclofenac exposure in mussel Mytilus galloprovincialis.
M. González-Rey (2014)
Long-term exposure of the isopod Porcellionides pruinosus to nickel: Costs in the energy budget and detoxification enzymes.
N. Ferreira (2015)
Environmental contaminants of emerging concern in seafood--European database on contaminant levels.
G. Vandermeersch (2015)
Evaluation of ecotoxicological effects of drugs on Daphnia magna using different enzymatic biomarkers.
L. L. D. Oliveira (2015)
Effects of trophic exposure to dexamethasone and diclofenac in freshwater fish.
I. C. Guiloski (2015)
Predictive Ecotoxicology and Environmental Assessment
C. Amiard-Triquet (2015)
Ocean acidification and global warming impair shark hunting behaviour and growth
Jennifer C. A. Pistevos (2015)
Trypan Blue Exclusion Test of Cell Viability
W. Strober (2015)
Behavioural lateralization and shoaling cohesion of fish larvae altered under ocean acidification
A. Lopes (2016)
Ecotoxicological potential of non-steroidal anti-inflammatory drugs (NSAIDs) in marine organisms: Bioavailability, biomarkers and natural occurrence in Mytilus galloprovincialis.
M. Mezzelani (2016)
Diclofenac and its transformation products: Environmental occurrence and toxicity - A review.
Linson Lonappan (2016)
Physiological constraints to climate warming in fish follow principles of plastic floors and concrete ceilings
E. Sandblom (2016)
Future ocean hypercapnia driven by anthropogenic amplification of the natural CO2 cycle
B. McNeil (2016)
Coping with seawater acidification and the emerging contaminant diclofenac at the larval stage: A tale from the clam Ruditapes philippinarum.
M. Munari (2016)
Effects of trophic exposure to diclofenac and dexamethasone on hematological parameters and immune response in freshwater fish.
J. Ribas (2016)
Foraging behaviour, swimming performance and malformations of early stages of commercially important fishes under ocean acidification and warming
M. Pimentel (2016)
Ocean warming alters cellular metabolism and induces mortality in fish early life stages: A proteomic approach.
D. Madeira (2016)
Climate Change and Considerations for Fish Health and Fish Health Professionals
L. Chiaramonte (2016)
Altered brain ion gradients following compensation for elevated CO2 are linked to behavioural alterations in a coral reef fish
Rachael M. Heuer (2016)
Thermal acclimation in clownfish: An integrated biomarker response and multi-tissue experimental approach
Carolina Madeira (2016)
Immunological and health-state parameters in the Patagonian rockfish Sebastes oculatus. Their relation to chemical stressors and seasonal changes.
M. Sueiro (2016)
Seasonal and size-related variation of subcellular biomarkers in quagga mussels (Dreissena bugensis) inhabiting sites affected by moderate contamination with complex mixtures of pollutants
A. Ács (2016)
The effects of the painkiller diclofenac and hypoxia on gene transcription and antioxidant system in the gills of three-spined stickleback.
Pedro Lubiana (2016)
Neuro-oxidative damage and aerobic potential loss of sharks under elevated CO2 and warming
R. Rosa (2016)
Mussels as bioindicators of diclofenac contamination in coastal environments.
S. Cunha (2017)
Chronic diclofenac exposure affects gill integrity and pituitary gene expression and displays estrogenic activity in nile tilapia (Oreochromis niloticus).
Frederike Gröner (2017)
Evaluation of DNA damage and physiological responses in Nile tilapia, Oreochromis niloticus (Linnaeus, 1758) exposed to sub-lethal diclofenac (DCF).
P. Pandey (2017)
Immune responses in the aquatic gastropod Lymnaea stagnalis under short-term exposure to pharmaceuticals of concern for immune systems: Diclofenac, cyclophosphamide and cyclosporine A.
P. Boisseaux (2017)
Neurotoxic responses in brain tissues of rainbow trout exposed to imidacloprid pesticide: Assessment of 8-hydroxy-2-deoxyguanosine activity, oxidative stress and acetylcholinesterase activity.
A. Topal (2017)
Effects of environmentally relevant concentrations of the anti-inflammatory drug diclofenac in freshwater fish Rhamdia quelen.
I. C. Guiloski (2017)
Ecophysiological responses of juvenile seabass (Dicentrarchus labrax) exposed to increased temperature and dietary methylmercury.
A. Maulvault (2017)
Do environmental factors affect male fathead minnow (Pimephales promelas) response to estrone? Part 2. Temperature and food availability.
N. Shappell (2018)
Differential behavioural responses to venlafaxine exposure route, warming and acidification in juvenile fish (Argyrosomus regius).
A. Maulvault (2018)
Different ecophysiological responses of freshwater fish to warming and acidification.
T. F. Jesus (2018)
Fish energy budget under ocean warming and flame retardant exposure
Patrícia Anacleto (2018)
Effects of low concentrations of ibuprofen on freshwater fish Rhamdia quelen.
Francielle Tatiana Mathias (2018)
Single and combined effects of microplastics and mercury on juveniles of the European seabass (Dicentrarchus labrax): Changes in behavioural responses and reduction of swimming velocity and resistance time.
L. G. A. Barboza (2018)
This paper is referenced by
Abundance and spatial patterns over time of Vibrionaceae and Vibrio harveyi in water and biofilm from a seabass aquaculture facility
Julia Mougin (2021)
The Influence of Temperature Increase on the Toxicity of Mercury Remediated Seawater Using the Nanomaterial Graphene Oxide on the Mussel Mytilus galloprovincialis
Francesca Coppola (2021)
How efficient is graphene-based nanocomposite to adsorb Hg from seawater. A laboratory assay to assess the toxicological impacts induced by remediated water towards marine bivalves.
Francesca Coppola (2021)
Single and combined acute and subchronic toxic effects of microplastics and copper in zebrafish (Danio rerio) early life stages.
D. Santos (2021)
Sublethal diclofenac induced oxidative stress, neurotoxicity, molecular responses and alters energy metabolism proteins in Nile tilapia, Oreochromis niloticus
M. N. Ajima (2021)
Primary, secondary, and tertiary stress responses of juvenile seahorse Hippocampus reidi exposed to acute acid stress in brackish and seawater.
M. D. Carneiro (2021)
Effects of anti-inflammatory diclofenac assessed by toxicity tests and biomarkers in adults and larvae of Danio rerio.
Larissa Cristine de Carvalho Penha (2020)
Adverse Effects of Ultraviolet Radiation on Growth, Behavior, Skin Condition, Physiology, and Immune Function in Gilthead Seabream (Sparus aurata)
R. Alves (2020)
Potential environmental toxicity of sewage effluent with pharmaceuticals
R. Bisognin (2020)
Depressed, hypertense and sore: Long-term effects of fluoxetine, propranolol and diclofenac exposure in a top predator fish.
Irina A Duarte (2020)
Lack of oxidative damage on temperate juvenile catsharks after a long-term ocean acidification exposure
M. R. Pegado (2020)
Mercury in Juvenile Solea senegalensis: Linking Bioaccumulation, Seafood Safety, and Neuro-Oxidative Responses under Climate Change-Related Stressors
C. Camacho (2020)
Influence of aquatic colloids on the bioaccumulation and biological effects of diclofenac in zebrafish (Danio rerio).
Yu Sun (2020)
Effects of pH on salicylic acid toxicity in terms of biomarkers determined in the marine gastropod Gibbula umbilicalis.
R. Dionísio (2020)
Impacts of nanoplastics on bivalve: Fluorescence tracing of organ accumulation, oxidative stress and damage.
Zhenling Li (2020)
Integrative indices for health assessment in reef corals under thermal stress
Marta Dias (2020)
Can ocean warming alter sub-lethal effects of antiepileptic and antihistaminic pharmaceuticals in marine bivalves?
Â. Almeida (2020)
Acquiring an evolutionary perspective in marine ecotoxicology to tackle emerging concerns in a rapidly changing ocean.
A. Rodríguez-Romero (2020)
Paralytic Shellfish Toxins and Ocean Warming: Bioaccumulation and Ecotoxicological Responses in Juvenile Gilthead Seabream (Sparus aurata)
V. Barbosa (2019)
The influence of climate change related factors on the response of two clam species to diclofenac.
Silvana Costa (2019)
Bioaccumulation and ecotoxicological responses of juvenile white seabream (Diplodus sargus) exposed to triclosan, warming and acidification.
A. Maulvault (2019)
Ecotoxicological responses of a reef calcifier exposed to copper, acidification and warming: A multiple biomarker approach.
J. A. Marques (2019)
Behavioral toxicity of tannery effluent in zebrafish (Danio rerio) used as model system.
Thales Quintão Chagas (2019)
The non‐steroidal anti‐inflammatory drug diclofenac sodium induces abnormal embryogenesis and delayed lethal effects in early life stage zebrafish (Danio rerio)
Y. Horie (2019)
Bioconcentration, metabolism and the effects of tetracycline on multiple biomarkers in Chironomus riparius larvae.
Zhengxin Xie (2019)
Living in a multi‐stressors environment: An integrated biomarker approach to assess the ecotoxicological response of meagre (Argyrosomus regius) to venlafaxine, warming and acidification
A. Maulvault (2019)
Ecological effects of elevated CO₂ on marine and freshwater fishes: from individual to community effects
P. Munday (2019)
Climate change and emerging chemical contaminants in marine organisms: Bioaccumulation, ecotoxicology and public health impacts
Ana Luísa Maulvault (2018)