Integrated multi-biomarker responses of juvenile seabass to diclofenac, warming and acidification co-exposure

Ana Luísa Maulvault, Vera Barbosa, Ricardo Alves, Patrícia Anacleto, Carolina Camacho, Sara Cunha, José O. Fernandes, Pedro Pousão Ferreira, Rui Rosa, António Marques, Mário Diniz

Research output: Contribution to journalArticle

11 Citations (Scopus)

Abstract

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.

Original languageEnglish
Pages (from-to)65-79
Number of pages15
JournalAquatic Toxicology
Volume202
DOIs
Publication statusPublished - 1 Sep 2018

Fingerprint

Diclofenac
acidification
biomarker
biomarkers
warming
Biomarkers
Climate Change
drug
drugs
climate change
Fishes
Pharmaceutical Preparations
marine fish
Toxicology
synthesis
erythrocytes
Erythrocytes
brain
viability
muscle

Keywords

  • Acidification
  • Diclofenac
  • Fish
  • IBR
  • Multi-biomarkers
  • Warming

Cite this

Maulvault, Ana Luísa ; Barbosa, Vera ; Alves, Ricardo ; Anacleto, Patrícia ; Camacho, Carolina ; Cunha, Sara ; Fernandes, José O. ; Ferreira, Pedro Pousão ; Rosa, Rui ; Marques, António ; Diniz, Mário. / Integrated multi-biomarker responses of juvenile seabass to diclofenac, warming and acidification co-exposure. In: Aquatic Toxicology. 2018 ; Vol. 202. pp. 65-79.
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abstract = "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.",
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Integrated multi-biomarker responses of juvenile seabass to diclofenac, warming and acidification co-exposure. / Maulvault, Ana Luísa; Barbosa, Vera; Alves, Ricardo; Anacleto, Patrícia; Camacho, Carolina; Cunha, Sara; Fernandes, José O.; Ferreira, Pedro Pousão; Rosa, Rui; Marques, António; Diniz, Mário.

In: Aquatic Toxicology, Vol. 202, 01.09.2018, p. 65-79.

Research output: Contribution to journalArticle

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AU - Maulvault, Ana Luísa

AU - Barbosa, Vera

AU - Alves, Ricardo

AU - Anacleto, Patrícia

AU - Camacho, Carolina

AU - Cunha, Sara

AU - Fernandes, José O.

AU - Ferreira, Pedro Pousão

AU - Rosa, Rui

AU - Marques, António

AU - Diniz, Mário

N1 - Sem PDF conforme despacho. info:eu-repo/grantAgreement/EC/FP7/311820/EU# info:eu-repo/grantAgreement/FCT/5876/147321/PT# info:eu-repo/grantAgreement/FCT/5876/147258/PT# The research leading to these results has received funding from the European Union Seventh Framework Programme (FP7/2007-2013) under the ECsafeSEAFOOD project (grant agreement n 311820), the strategic projects granted to MARE (FCT project UID/MAR/04292/ 2013) and to the Applied Molecular Biosciences Unit-UCIBIO (FCT/MCTES project UID/Multi/04378/2013 co-financed by the ERDF under the PT2020 Partnership Agreement POCI-01-0145-FEDER-007728). The Portuguese Foundation for Science and Technology supported the contract of SCC (IF/01616/2015), AM (IF/00157/2014) and RR (IF/ 01373/2013) in the framework of the IF program, as well as the PhD Grant of ALM (SFRH/BD/103569/2014) and Post -PhD Grant of PA (SFRH/BPD/100728/2014). We thank Sparos Lda company for providing the experimental feeds, Drs Carolina Madeira and Diana Madeira from Nova University of Lisbon, for the consultancy on the IBRs computation, and the teams from IPMA aquaculture pilot station and LMG for the technical support.

PY - 2018/9/1

Y1 - 2018/9/1

N2 - 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.

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