Behavioral Impairment in Aquatic Organisms Exposed to Neurotoxic Pollutants

A special issue of Toxics (ISSN 2305-6304). This special issue belongs to the section "Ecotoxicology".

Deadline for manuscript submissions: closed (31 December 2021) | Viewed by 27008

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Guest Editor
Department Environmental Chemistry, IDAEA-CSIC, Jordi Girona 18, 08034 Barcelona, Spain
Interests: fish neurotoxicology; zebrafish model; fish developmental neurotoxicology
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Guest Editor
Institute of Environmental Assessment and Water Research (IDAEA-CSIC), Jordi Girona 18, 08034 Barcelona, Spain
Interests: analytical chemistry; aquatic toxicology; environmental risk assessment; toxicogenomics

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Guest Editor
Institute for Environmental Assessment and Water Research (IDAEA-CSIC), Jordi Girona 18, 08034 Barcelona, Spain
Interests: toxicology; biomarkers; environmental science; biological science; behaviour and neurotoxicity

Special Issue Information

Dear Colleagues,

It has been estimated that up to 30,000 of commercially used chemicals may have neurotoxic potential. Neuroactive chemicals, including neurotoxic pesticides, pharmaceuticals, and illicit drugs, are the largest group of micropollutants present in European rivers, where nearly 30% of all detected chemicals were linked to neurotoxicity. Furthermore, neurotoxic actions of environmental contaminants on non-target species have been determined. It is suspected that such actions include changes in the behavior of organisms. For example, environmental pollutants such as trace metals and organic toxicants have been reported to increase fish susceptibility to predation, antidepressant drug altered sex mating behavior in fish, phototaxis and feeding in amphipods, cladocerans and worms, altered mobility of snails, memory, cognitive function, and the ability to camouflage in cuttlefish at environmental relevant concentrations.

This Special Issue on “Behavioral Impairment in Aquatic Organisms Exposed to Neurotoxic Pollutants” aims to highlight research on behavioral analysis in aquatic organisms using automated image analysis systems. Studies that anchor behavioral impairment with molecular markers, and also with population level effects will be preferred. Research addressing exposure to environmental relevant concentrations of pollutants will receive priority. Methodological studies developing new tools for the automated behavioral analysis in aquatic organisms are also encouraged.

Authors are invited and welcome to submit original research papers, reviews, and short communications.

Dr. Demetrio Raldúa
Dr. Carlos Barata
Dr. Melissa Faria
Guest Editors

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Keywords

  • Behavioral analysis
  • Neuroactive chemicals
  • Neurotoxicity
  • Neuroendocrine disruption
  • Environmental relevant concentrations
  • Aquatic organisms

Published Papers (9 papers)

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Editorial

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4 pages, 222 KiB  
Editorial
Behavioral Impairment in Aquatic Organisms Exposed to Neurotoxic Pollutants
by Melissa Faria, Carlos Barata and Demetrio Raldúa
Toxics 2022, 10(5), 243; https://doi.org/10.3390/toxics10050243 - 10 May 2022
Cited by 1 | Viewed by 1375
Abstract
Neuroactive chemicals are compounds that can modulate, at very low concentrations, the normal function of the central nervous systems of an organism through various primary modes of action (MoA) [...] Full article

Research

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19 pages, 2058 KiB  
Article
Environmental Occurrence and Predicted Pharmacological Risk to Freshwater Fish of over 200 Neuroactive Pharmaceuticals in Widespread Use
by John P. Sumpter and Luigi Margiotta-Casaluci
Toxics 2022, 10(5), 233; https://doi.org/10.3390/toxics10050233 - 03 May 2022
Cited by 19 | Viewed by 3373
Abstract
There is a growing concern that neuroactive chemicals released into the environment can perturb wildlife behaviour. Among these chemicals, pharmaceuticals such as antidepressants and anxiolytics have been receiving increasing attention, as they are specifically prescribed to modify behavioural responses. Many laboratory studies have [...] Read more.
There is a growing concern that neuroactive chemicals released into the environment can perturb wildlife behaviour. Among these chemicals, pharmaceuticals such as antidepressants and anxiolytics have been receiving increasing attention, as they are specifically prescribed to modify behavioural responses. Many laboratory studies have demonstrated that some of these compounds can affect various aspects of the behaviour of a range of aquatic organisms; however, these investigations are focused on a very small set of neuroactive pharmaceuticals, and they often consider one compound at a time. In this study, to better understand the environmental and toxicological dimension of the problem, we considered all pharmaceuticals explicitly intended to modulate the central nervous system (CNS), and we hypothesised that these compounds have higher probability of perturbing animal behaviour. Based on this hypothesis, we used the classification of pharmaceuticals provided by the British National Formulary (based on their clinical applications) and identified 210 different CNS-acting pharmaceuticals prescribed in the UK to treat a variety of CNS-related conditions, including mental health and sleep disorders, dementia, epilepsy, nausea, and pain. The analysis of existing databases revealed that 84 of these compounds were already detected in surface waters worldwide. Using a biological read-across approach based on the extrapolation of clinical data, we predicted that the concentration of 32 of these neuroactive pharmaceuticals in surface waters in England may be high enough to elicit pharmacological effects in wild fish. The ecotoxicological effects of the vast majority of these compounds are currently uncharacterised. Overall, these results highlight the importance of addressing this environmental challenge from a mixture toxicology and systems perspective. The knowledge platform developed in the present study can guide future region-specific prioritisation efforts, inform the design of mixture studies, and foster interdisciplinary efforts aimed at identifying novel approaches to predict and interpret the ecological implications of chemical-induced behaviour disruption. Full article
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10 pages, 841 KiB  
Article
Pharmacological Modulation of Behaviour, Serotonin and Dopamine Levels in Daphnia magna Exposed to the Monoamine Oxidase Inhibitor Deprenyl
by Marina Bellot, Melissa Faria, Cristian Gómez-Canela, Demetrio Raldúa and Carlos Barata
Toxics 2021, 9(8), 187; https://doi.org/10.3390/toxics9080187 - 09 Aug 2021
Cited by 7 | Viewed by 2259
Abstract
This study assessed the effects of the monoamine oxidase (MAO) inhibitor deprenyl in Daphnia magna locomotor activity. The mechanisms of action of deprenyl were also determined by studying the relationship between behaviour, MAO activity and neurotransmitter levels. Modulation of the D. magna monoamine [...] Read more.
This study assessed the effects of the monoamine oxidase (MAO) inhibitor deprenyl in Daphnia magna locomotor activity. The mechanisms of action of deprenyl were also determined by studying the relationship between behaviour, MAO activity and neurotransmitter levels. Modulation of the D. magna monoamine system was accomplished by 24 h exposure to two model psychotropic pharmaceuticals with antagonistic and agonistic serotonin signalling properties: 10 mg/L of 4-chloro-DL-phenylalanine (PCPA) and 1 mg/L of deprenyl, respectively. Contrasting behavioural outcomes were observed for deprenyl and PCPA reflected in decreased basal locomotor activity and enhanced habituation for the former compound and delayed habituation for the latter one. Deprenyl exposure inhibited monoamine oxidase (MAO) activity and increased the concentrations of serotonin, dopamine and the dopamine metabolite 3-methoxytyramine in whole D. magna extracts. Our findings indicate that D. magna is a sensitive and useful nonvertebrate model for assessing the effects of short-term exposure to chemicals that alter monoamine signalling changes. Full article
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17 pages, 714 KiB  
Article
Environmentally Relevant Mixture of Pesticides Affect Mobility and DNA Integrity of Early Life Stages of Rainbow Trout (Oncorhynchus mykiss)
by Shannon Weeks Santos, Jérôme Cachot, Bettie Cormier, Nicolas Mazzella, Pierre-Yves Gourves, Christelle Clérandeau, Bénédicte Morin and Patrice Gonzalez
Toxics 2021, 9(8), 174; https://doi.org/10.3390/toxics9080174 - 22 Jul 2021
Cited by 5 | Viewed by 2504
Abstract
The aim of this study was to analyze the impact of three concentrations of a pesticide mixture on the first development stages of rainbow trout (Oncorhynchus mykiss). The mixture was made up of three commonly used pesticides in viticulture: glyphosate (GLY), [...] Read more.
The aim of this study was to analyze the impact of three concentrations of a pesticide mixture on the first development stages of rainbow trout (Oncorhynchus mykiss). The mixture was made up of three commonly used pesticides in viticulture: glyphosate (GLY), chlorpyrifos (CPF) and copper sulfate (Cu). Eyed stage embryos were exposed for 3 weeks to three concentrations of the pesticide mixture. Lethal and sub-lethal effects were assessed through a number of phenotypic and molecular endpoints including survival, hatching delay, hatching success, biometry, swimming activity, DNA damage (Comet assay), lipid peroxidation (TBARS), protein carbonyl content and gene expression. Ten target genes involved in antioxidant defenses, DNA repair, mitochondrial metabolism and apoptosis were analyzed using real-time RT-qPCR. No significant increase of mortality, half-hatch, growth defects, TBARS and protein carbonyl contents were observed whatever the pesticide mixture concentration. In contrast, DNA damage and swimming activity were significantly more elevated at the highest pesticide mixture concentration. Gene transcription was up-regulated for genes involved in detoxification (gst and mt1), DNA repair (ogg1), mitochondrial metabolism (cox1 and 12S), and cholinergic system (ache). This study highlighted the induction of adaptive molecular and behavioral responses of rainbow trout larvae when exposed to environmentally realistic concentrations of a mixture of pesticides. Full article
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14 pages, 3267 KiB  
Article
Pharmacological Modulation of Serotonin Levels in Zebrafish Larvae: Lessons for Identifying Environmental Neurotoxicants Targeting the Serotonergic System
by Melissa Faria, Eva Prats, Marina Bellot, Cristian Gomez-Canela and Demetrio Raldúa
Toxics 2021, 9(6), 118; https://doi.org/10.3390/toxics9060118 - 25 May 2021
Cited by 12 | Viewed by 2829
Abstract
This study examines the effects of acute pharmacological modulation of the serotonergic system over zebrafish larvae’s cognitive, basic, and defense locomotor behaviors, using a medium to high throughput screening assay. Furthermore, the relationship between behavior, enzyme activity related to neurotransmitter metabolism, neurotransmitter levels, [...] Read more.
This study examines the effects of acute pharmacological modulation of the serotonergic system over zebrafish larvae’s cognitive, basic, and defense locomotor behaviors, using a medium to high throughput screening assay. Furthermore, the relationship between behavior, enzyme activity related to neurotransmitter metabolism, neurotransmitter levels, and gene expression was also determined. Modulation of larvae serotonergic system was accomplished by 24 h exposure to single and opposite pharmacodynamics co-exposure to three model psychopharmaceuticals with antagonistic and agonistic serotonin signaling properties: 2.5 mM 4-Chloro-DL-phenylalanine (PCPA) and 5 µM deprenyl and 0.5 µM fluoxetine, respectively. Similar behavioral outcome was observed for deprenyl and fluoxetine, which was reflected as hypolocomotion, decrease in larvae defensive responses, and cognitive impairment. Contrarily, PCPA induced hyperlocomotion and increase in larvae escape response. Deprenyl exposure effects were more pronounced at a lower level of organization than fluoxetine, with complete inhibition of monoamine oxidase (MAO) activity, dramatic increase of 5-HT and dopamine (DA) levels, and downregulation of serotonin synthesis and transporter genes. PCPA showed mainly effects over serotonin and dopamine’s main degradation metabolites. Finally, co-exposure between agonistic and antagonist serotonin signaling drugs reviled full recovery of zebrafish impaired locomotor and defense responses, 5-HT synthesis gene expression, and partial recovery of 5-HT levels. The findings of this study suggest that zebrafish larvae can be highly sensitive and a useful vertebrate model for short-term exposure to serotonin signaling changes. Full article
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17 pages, 3995 KiB  
Article
Assessing Combined Effects for Mixtures of Similar and Dissimilar Acting Neuroactive Substances on Zebrafish Embryo Movement
by Afolarin O. Ogungbemi, Riccardo Massei, Rolf Altenburger, Stefan Scholz and Eberhard Küster
Toxics 2021, 9(5), 104; https://doi.org/10.3390/toxics9050104 - 06 May 2021
Cited by 7 | Viewed by 2672
Abstract
Risk assessment of chemicals is usually conducted for individual chemicals whereas mixtures of chemicals occur in the environment. Considering that neuroactive chemicals are a group of contaminants that dominate the environment, it is then imperative to understand the combined effects of mixtures. The [...] Read more.
Risk assessment of chemicals is usually conducted for individual chemicals whereas mixtures of chemicals occur in the environment. Considering that neuroactive chemicals are a group of contaminants that dominate the environment, it is then imperative to understand the combined effects of mixtures. The commonly used models to predict mixture effects, namely concentration addition (CA) and independent action (IA), are thought to be suitable for mixtures of similarly or dissimilarly acting components, respectively. For mixture toxicity prediction, one important challenge is to clarify whether to group neuroactive substances based on similar mechanisms of action, e.g., same molecular target or rather similar toxicological response, e.g., hyper- or hypoactivity (effect direction). We addressed this by using the spontaneous tail coiling (STC) of zebrafish embryos, which represents the earliest observable motor activity in the developing neural network, as a model to elucidate the link between the mechanism of action and toxicological response. Our objective was to answer the following two questions: (1) Can the mixture models CA or IA be used to predict combined effects for neuroactive chemical mixtures when the components share a similar mode of action (i.e., hyper- or hypoactivity) but show different mechanism of action? (2) Will a mixture of chemicals where the components show opposing effect directions result in an antagonistic combined effect? Results indicate that mixture toxicity of chemicals such as propafenone and abamectin as well as chlorpyrifos and hexaconazole that are known to show different mechanisms of action but similar effect directions were predictable using CA and IA models. This could be interpreted with the convergence of effects on the neural level leading to either a collective activation or inhibition of synapses. We also found antagonistic effects for mixtures containing substances with opposing effect direction. Finally, we discuss how the STC may be used to amend risk assessment. Full article
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20 pages, 4444 KiB  
Article
High-Throughput Screening of Psychotropic Compounds: Impacts on Swimming Behaviours in Artemia franciscana
by Shanelle A. Kohler, Matthew O. Parker and Alex T. Ford
Toxics 2021, 9(3), 64; https://doi.org/10.3390/toxics9030064 - 17 Mar 2021
Cited by 8 | Viewed by 4162
Abstract
Animal behaviour is becoming increasingly popular as an endpoint in ecotoxicology due to its increased sensitivity and speed compared to traditional endpoints. However, the widespread use of animal behaviours in environmental risk assessment is currently hindered by a lack of optimisation and standardisation [...] Read more.
Animal behaviour is becoming increasingly popular as an endpoint in ecotoxicology due to its increased sensitivity and speed compared to traditional endpoints. However, the widespread use of animal behaviours in environmental risk assessment is currently hindered by a lack of optimisation and standardisation of behavioural assays for model species. In this study, assays to assess swimming speed were developed for a model crustacean species, the brine shrimp Artemia franciscana. Preliminary works were performed to determine optimal arena size for this species, and weather lux used in the experiments had an impact on the animals phototactic response. Swimming speed was significantly lower in the smallest arena, whilst no difference was observed between the two larger arenas, suggesting that the small arena was limiting swimming ability. No significant difference was observed in attraction to light between high and low light intensities. Arena size had a significant impact on phototaxis behaviours. Large arenas resulted in animals spending more time in the light side of the arena compared to medium and small, irrespective of light intensity. The swimming speed assay was then used to expose specimens to a range of psychotropic compounds with varying modes of action. Results indicate that swimming speed provides a valid measure of the impacts of behaviour modulating compounds on A. franciscana. The psychotropic compounds tested varied in their impacts on animal behaviour. Fluoxetine resulted in increased swimming speed as has been found in other crustacean species, whilst oxazepam, venlafaxine and amitriptyline had no significant impacts on the behaviours measured. The results from this study suggest a simple, fast, high throughput assay for A. franciscana and gains insight on the impacts of a range of psychotropic compounds on the swimming behaviours of a model crustacean species used in ecotoxicology studies. Full article
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15 pages, 1497 KiB  
Article
Teratogenic, Oxidative Stress and Behavioural Outcomes of Three Fungicides of Natural Origin (Equisetum arvense, Mimosa tenuiflora, Thymol) on Zebrafish (Danio rerio)
by Raquel Vieira, Carlos Venâncio and Luís Félix
Toxics 2021, 9(1), 8; https://doi.org/10.3390/toxics9010008 - 09 Jan 2021
Cited by 7 | Viewed by 2970
Abstract
The improper use of synthetic fungicides has raised public concerns related to environmental pollution and animal health. Over the years, plant-derived antifungals have been investigated as safer alternatives, although little scientific evidence of its neurodevelopmental effects exist. The main objective of this study [...] Read more.
The improper use of synthetic fungicides has raised public concerns related to environmental pollution and animal health. Over the years, plant-derived antifungals have been investigated as safer alternatives, although little scientific evidence of its neurodevelopmental effects exist. The main objective of this study was to explore the effects of three alternative natural extracts (Equisetum arvense, Mimosa tenuiflora, Thymol) with antifungal properties during the early development of zebrafish by evaluating different teratogenic, oxidative stress and behavioural outcomes. Following the determination of the 96 h-LC50, exposure to sublethal concentrations showed the safety profile of both E. arvense and M. tenuiflora. However, following 96-h exposure to Thymol, increased lethality, pericardial oedema, yolk and eye deformations, and decreased body length were observed. The reduced and oxidized glutathione (GSH:GSSG) ratio was increased, and the glutathione-s-transferase activity in the group exposed to the highest Thymol concentration. Overall, these results support a more reducing environment associated with possible effects at the cellular proliferation level. In addition, the disruption of behavioural states (fear- and anxiety-like disorders) were noted, pointing to alterations in the c-Jun N-terminal kinase developmental signalling pathway, although further studies are required to explore this rationale. Notwithstanding, the results provide direct evidence of the teratogenic effects of Thymol, which might have consequences for non-target species. Full article
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Review

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22 pages, 1136 KiB  
Review
Not Only Toxic but Repellent: What Can Organisms’ Responses Tell Us about Contamination and What Are the Ecological Consequences When They Flee from an Environment?
by Cristiano V. M. Araújo, Abdelmourhit Laissaoui, Daniel C. V. R. Silva, Eloisa Ramos-Rodríguez, Enrique González-Ortegón, Evaldo L. G. Espíndola, Francisco Baldó, Freylan Mena, Gema Parra, Julián Blasco, Julio López-Doval, Marta Sendra, Mohamed Banni, Mohammed Ariful Islam and Ignacio Moreno-Garrido
Toxics 2020, 8(4), 118; https://doi.org/10.3390/toxics8040118 - 12 Dec 2020
Cited by 19 | Viewed by 3611
Abstract
The ability of aquatic organisms to sense the surrounding environment chemically and interpret such signals correctly is crucial for their ecological niche and survival. Although it is an oversimplification of the ecological interactions, we could consider that a significant part of the decisions [...] Read more.
The ability of aquatic organisms to sense the surrounding environment chemically and interpret such signals correctly is crucial for their ecological niche and survival. Although it is an oversimplification of the ecological interactions, we could consider that a significant part of the decisions taken by organisms are, to some extent, chemically driven. Accordingly, chemical contamination might interfere in the way organisms behave and interact with the environment. Just as any environmental factor, contamination can make a habitat less attractive or even unsuitable to accommodate life, conditioning to some degree the decision of organisms to stay in, or move from, an ecosystem. If we consider that contamination is not always spatially homogeneous and that many organisms can avoid it, the ability of contaminants to repel organisms should also be of concern. Thus, in this critical review, we have discussed the dual role of contamination: toxicity (disruption of the physiological and behavioral homeostasis) vs. repellency (contamination-driven changes in spatial distribution/habitat selection). The discussion is centered on methodologies (forced exposure against non-forced multi-compartmented exposure systems) and conceptual improvements (individual stress due to the toxic effects caused by a continuous exposure against contamination-driven spatial distribution). Finally, we propose an approach in which Stress and Landscape Ecology could be integrated with each other to improve our understanding of the threat contaminants represent to aquatic ecosystems. Full article
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