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Assessment of fipronil toxicity to the freshwater midge Chironomus riparius: Molecular, biochemical, and organismal responses

Publication . Monteiro, Hugo R.; Pestana, João L. T.; Novais, Sara C.; Leston, Sara; Ramos, Fernando; Soares, Amadeu M. V. M.; Devreese, Bart; Lemos, Marco F. L.

Fipronil is a phenylpyrazole insecticide that entered the market to replace organochlorides and organophosphates. Fipronil impairs the regular inhibition of nerve impulses that ultimately result in paralysis and death of insects. Because of its use as a pest control, and due to runoff events, fipronil has been detected in freshwater systems near agricultural areas, and therefore might represent a threat to non-target aquatic organisms. In this study, the toxicity of fipronil to the freshwater midge Chironomus riparius was investigated at biochemical, molecular, and whole organism (e.g. growth, emergence, and behavior) levels. At the individual level, chronic (28 days) exposure to fipronil resulted in reduced larval growth and emergence with a lowest observed effect concentration (LOEC) of 0.081 μg L−1. Adult weight, which is directly linked to the flying performance and fecundity of midges, was also affected (LOEC = 0.040 μg L−1). Additionally, behavioral changes such as irregular burrowing behavior of C. riparius larvae (EC50 = 0.084 μg L−1) and impairment of adult flying performance were observed. At a biochemical level, acute (48 h) exposure to fipronil increased cellular oxygen consumption (as indicated by the increase of electron transport system (ETS) activity) and decreased antioxidant and detoxification defenses (as suggested by the decrease in catalase (CAT) and glutathione S-transferase (GST) activities). Exposure to fipronil also caused alterations in the fatty acid profile of C. riparius, since high levels of stearidonic acid (SDA) were observed. A comparison between exposed and nonexposed larvae also revealed alterations in the expression of globins, cytoskeleton and motor proteins, and proteins involved in protein biosynthesis. These alterations may aid in the interpretation of potential mechanisms of action that lead to the effects observed at the organism level. Present results show that environmentally relevant concentrations of fipronil are toxic to chironomid populations which call for monitoring of phenylpyrazole insecticides and of their ecological effects in freshwaters. Present results also emphasize the importance of complementing ecotoxicological data with molecular approaches such as proteomics, for a better interpretation of the mode of action of insecticides in aquatic invertebrates.

2019-11Journal article

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Using biomarkers to address the impacts of pollution on limpets ( Patella depressa ) and their mechanisms to cope with stress

Publication . Silva, Cátia S. E.; Novais, Sara C.; Simões, Tiago; Caramalho, Márcia; Gravato, Carlos; Rodrigues, Maria J.; Maranhão, Paulo; Lemos, Marco F. L.

Contaminant discharges, derived from human activities, are major concerns as they exert a continuous ecological pressure on aquatic systems, causing in fact cascading community effects. Although with associated ecological and fitness costs, physiological and biochemical defense mechanisms may restore the organism’s internal balance. Several studies have pointed biomarkers as tools to assess contamination levels, and also to understand potential mechanisms to cope with stress. In the present study, the fitness costs of limpets Patella depressa located in two different contaminated sites and when transplanted into a different common environment – with no known historical contamination – were assessed through the measurement of oxidative stress, energy metabolism responses, and fatty acid profile changes. Integrated biomarker response index (IBR) revealed differences in responses between organisms of the different origin sites, with greater antioxidant and detoxification activities in the site with the higher contamination life-history (higher IBR index). Moreover, different abilities of this species to deal with the new environmental condition were also observed. After the transplant, and despite the differences in the initial profiles, response patterns became similar between both populations (similar IBR index), with organisms from the less contaminated site suffering a higher impact with a demarked increase in their detoxification and antioxidant defenses, as well as higher changes on fatty acid abundance/composition. Through an integrated biomarker profile analysis in a transplant context, this work provides a distinct insight on the mechanisms of response and tolerance to environmental stress, and fitness costs of this potential sentinel marine species in the context of environmental contamination changes.

2018Journal article

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Reproductive trade-offs in a temperate reef fish under high pCO2 levels

Publication . Faria, A. M.; Lopes, A. F.; Silva, C. S. E.; Novais, S. C.; Lemos, M. F. L.; Gonçalves, E. J.

Fishes are currently facing novel types of anthropogenic stressors that have never experienced in their evolutionary history, such as ocean acidification. Under these stressful conditions, energetically costly processes, such as reproduction, may be sacrificed for increased chances of survival. This trade-off does not only affect the organism itself but may result in reduced offspring fitness. In the present study, the effects of exposure to high pCO2 levels were tested on the reproductive performance of a temperate species, the two-spotted goby, Gobiusculus flavescens. Breeding pairs were kept under control (∼600 μatm, pH∼ 8.05) and high pCO2 levels (∼2300 μatm, pH∼ 7.60) conditions for a 4-month period. Additionally, oxidative stress and energy metabolism-related biomarkers were measured. Results suggest that reproductive activity is stimulated under high pCO2 levels. Parental pairs in the simulated ocean acidification conditions exhibited increased reproductive output, with 50% more clutches and 44% more eggs per clutch than pairs under control conditions. However, there was an apparent trade-off between offspring number and size, as larvae of parental pairs under high pCO2 levels hatched significantly smaller, suggesting differences in parental provisioning, which could be related to the fact that these females produce more eggs. Moreover, results support the hypothesis of different energy allocation strategies used by females under high pCO2 conditions. These changes might, ultimately, affect individual fitness and population replenishment.

2018-06Journal article

Open access

Effects of ocean acidification on the swimming ability, development and biochemical responses of sand smelt larvae

Publication . Silva, Cátia S. E.; Novais, Sara C.; Lemos, Marco F. L.; Mendes, Susana; Oliveira, Ana P.; Gonçalves, Emanuel J.; Faria, Ana M.

Ocean acidification, recognized as a major threat to marine ecosystems, has developed into one of the fastest growing fields of research in marine sciences. Several studies on fish larval stages point to abnormal behaviours, malformations and increased mortality rates as a result of exposure to increased levels of CO2. However, other studies fail to recognize any consequence, suggesting species-specific sensitivity to increased levels of CO2, highlighting the need of further research. In this study we investigated the effects of exposure to elevated pCO2 on behaviour, development, oxidative stress and energy metabolism of sand smelt larvae, Atherina presbyter. Larvae were caught at Arrábida Marine Park (Portugal) and exposed to different pCO2 levels (control: ~ 600 μatm, pH = 8.03; medium: ~ 1000 μatm, pH = 7.85; high: ~ 1800 μatm, pH = 7.64) up to 15 days, after which critical swimming speed (Ucrit), morphometric traits and biochemical biomarkers were determined. Measured biomarkers were related with: 1) oxidative stress — superoxide dismutase and catalase enzyme activities, levels of lipid peroxidation and DNA damage, and levels of superoxide anion production; 2) energy metabolism — total carbohydrate levels, electron transport system activity, lactate dehydrogenase and isocitrate dehydrogenase enzyme activities. Swimming speed was not affected by treatment, but exposure to increasing levels of pCO2 leads to higher energetic costs and morphometric changes, with larger larvae in high pCO2 treatment and smaller larvae in medium pCO2 treatment. The efficient antioxidant response capacity and increase in energetic metabolism only registered at the medium pCO2 treatment may indicate that at higher pCO2 levels the capacity of larvae to restore their internal balance can be impaired. Our findings illustrate the need of using multiple approaches to explore the consequences of future pCO2 levels on organisms.

2016-09-01Journal article

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Stress responses of the sea cucumber Holothuria forskali during aquaculture handling and transportation

Publication . Tonn, Nina; Novais, Sara C.; Silva, Cátia S. E.; Morais, Hugo A.; Correia, João P. S.; Lemos, Marco F. L.

Animal welfare during handling and transportation to aquaculture facilities or public aquaria is commonly estimated by addressing injury and mortality levels. Although these procedures have been optimized for different species, data on individual species’ cellular capabilities to tolerate stress are still scarce. In the present study, several biomarkers related with oxidative stress and energy metabolism were assessed in Holothuria forskali during animal acclimation, pre-transport, transport and quarantine. Combined analyses confirmed that sea cucumbers experienced high oxidative stress during transport, but had the capability to deal with it using a complex of cellular defence mechanisms, which enabled recovery from oxidative stress without permanent damage. Through a better understanding of individual species and the development of optimal parameters, this approach has the potential to improve animal wellbeing during and after acclimation, transportation and recovery processes.

2016-10-12Journal article

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