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- Sex differences in oxidative stress responses of tropical topshells (Trochus histrio) to increased temperature and high pCO2Publication . F. Grilo, Tiago; Lopes, Ana Rita; Sampaio, Eduardo; Rosa, Rui; Cardoso, Patrícia G.Given scarcity of knowledge on gender ecophysiological responses of tropical marine organisms to global climate change, the major aim of this research was to investigate potential sex differences in oxidative status of topshell Trochus histrio, after a combined exposure to increased temperature and pCO2. Lipid peroxidation, heat-shock response and antioxidant enzymatic activities were evaluated. Lipid peroxidation varied differently between sexes, with males undergoing cellular damage under high pCO2, which was elevated temperature-counteracted. Heat shock response was thermo- and sex-regulated, with males exhibiting significantly higher heat shock proteins production than females. Catalase activity increased with temperature and was exacerbated in combination with hypercapnia, being highest in females, while glutathione S-transferases activity peaked in males. These results clearly support the existence of distinct physiological strategies to cope oxidative stress between sexes, apparently more efficient in females, and also reinforce for the need of encompassing sex as meaningful variable in future biomarker studies.
- Short-term effects of increased temperature and lowered pH on a temperate grazer-seaweed interaction (Littorina obtusata/Ascophyllum nodosum)Publication . Cardoso, Patricia G.; F. Grilo, Tiago; Dionísio, Gisela; Aurelio, Maria; Lopes, Ana Rita; Pereira, Ricardo; Pacheco, Mário; Rosa, RuiThere has been a significant increase in the literature regarding the effects of warming and acidification on the marine ecosystem. To our knowledge, there is very little information on the potential effects of both combined stressors on marine grazer-seaweed interactions. Here, we evaluated, for the first time several phenotypic responses (e.g periwinkle survival, condition index, consumption rates, seaweed photosynthetic activity and oxidative stress) of the temperate periwinkle Littorina obtusata (grazer) and the brown seaweed Ascophyllum nodosum (prey) to such climate change-related variables, for 15 days. Increased temperature (22 °C, pH 8.0) elicited a significant lethal effect on the periwinkle within a short-term period (mortality rate > 90%). Acidification condition (18 °C, pH 7.6) was the one that showed lower mortality rates (≈20%), reflected by lower impact on periwinkle fitness and consumption rates. Under a scenario of increased temperature and lowered pH the antioxidant defences of L. obtusata seemed to be supressed increasing the risk of peroxidative damage. The seaweed evidenced signs of cellular damage under such conditions. These results suggest that: i) lower pH per se seems to benefit the interaction between grazer and seaweed while, ii) a combined scenario of increased temperature and lowered pH may be negative for the interaction, due to the unbalance between periwinkle mortality rates and consumption rates. But most importantly, since grazing often plays an important role on structuring natural communities, such predator-prey disturbances can elicit cascading effects on the remaining community structure and functioning of the temperate rocky-shore ecosystems.
- Neuro-oxidative damage and aerobic potential loss of sharks under elevated CO2 and warmingPublication . Rosa, Rui; Paula, José Ricardo; Sampaio, Eduardo; Pimentel, Marta; Lopes, Ana Rita; Baptista, Miguel; Guerreiro, Miguel; Santos, Catarina; Campos, Derek; Almeida-Val, Vera M.F.; Calado, Ricardo; Diniz, Mário; Repolho, TiagoSharks occupy high trophic levels in marine habitats and play a key role in the structure and function of marine communities. Their populations have been declining worldwide by ≥90 %, and their adaptive potential to future ocean conditions is believed to be limiting. Here we experimentally exposed recently hatched bamboo shark (Chiloscyllium punctatum) to the combined effects of tropical ocean warming (+4; 30 °C) and acidification (ΔpH 0.5) and investigated the respiratory, neuronal and antioxidant enzymatic machinery responses. Thirty days post-hatching, juvenile sharks revealed a significant decrease in brain aerobic potential (citrate synthase activity), in opposition to the anaerobic capacity (lactate dehydrogenase). Also, an array of antioxidant enzymes (glutathione S-transferase, superoxide dismutase activity and catalase) acted in concert to detoxify ROS, but this significant upregulation was not enough to minimize the increase in brain’s peroxidative damage and cholinergic neurotransmission. We argue that the future conditions may elicit deleterious deficiencies in sharks’ critical biological processes which, at the long-term, may have detrimental cascading effects at population and ecosystem levels.
- Different ecophysiological responses of freshwater fish to warming and acidificationPublication . Jesus, Tiago F.; Rosa, Inês C.; Repolho, Tiago; Lopes, Ana Rita; Pimentel, Marta; Almeida-Val, Vera M.F.; Coelho, Maria M.; Rosa, RuiFuture climate change scenarios predict threatening outcomes to biodiversity. Available empirical data concerning biological response of freshwater fish to climate change remains scarce. In this study, we investigated the physiological and biochemical responses of two Iberian freshwater fish species (Squalius carolitertii and the endangered S. torgalensis), inhabiting different climatic conditions, to projected future scenarios of warming (+3°C) and acidification (ΔpH=-0.4). Herein, metabolic enzyme activities of glycolytic (citrate synthase - CS, lactate dehydrogenase - LDH) and antioxidant (glutathione S-transferase, catalase and superoxide dismutase) pathways, as well as the heat shock response (HSR) and lipid peroxidation were determined. Our results show that, under current water pH, warming causes differential interspecific changes on LDH activity, increasing and decreasing its activity in S. carolitertii and in S. torgalensis, respectively. Furthermore, the synergistic effect of warming and acidification caused an increase in LDH activity of S. torgalensis, comparing with the warming condition. As for CS activity, acidification significantly decreased its activity in S. carolitertii whereas in S. torgalensis no significant effect was observed. These results suggest that S. carolitertii is more vulnerable to climate change, possibly as the result of its evolutionary acclimatization to milder climatic condition, while S. torgalensis evolved in the warmer Mediterranean climate. However, significant changes in HSR were observed under the combined warming and acidification (S. carolitertii) or under acidification (S. torgalensis). Our results underlie the importance of conducting experimental studies and address species endpoint responses under projected climate change scenarios to improve conservation strategies, and to safeguard endangered freshwater fish.
- 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).
- Seagrass ecophysiological performance under ocean warming and acidificationPublication . Repolho, Tiago; Duarte, Bernardo; Dionísio, Gisela; Paula, José Ricardo; Lopes, Ana Rita; Rosa, Inês; F. Grilo, Tiago; Caçador, Isabel; Calado, Ricardo; Rosa, RuiSeagrasses play an essential ecological role within coastal habitats and their worldwide population decline has been linked to different types of anthropogenic forces. We investigated, for the first time, the combined effects of future ocean warming and acidification on fundamental biological processes of Zostera noltii, including shoot density, leaf coloration, photophysiology (electron transport rate, ETR; maximum PSII quantum yield, Fv/Fm) and photosynthetic pigments. Shoot density was severely affected under warming conditions, with a concomitant increase in the frequency of brownish colored leaves (seagrass die-off). Warming was responsible for a significant decrease in ETR and Fv/Fm (particularly under control pH conditions), while promoting the highest ETR variability (among experimental treatments). Warming also elicited a significant increase in pheophytin and carotenoid levels, alongside an increase in carotenoid/chlorophyll ratio and De-Epoxidation State (DES). Acidification significantly affected photosynthetic pigments content (antheraxanthin, β-carotene, violaxanthin and zeaxanthin), with a significant decrease being recorded under the warming scenario. No significant interaction between ocean acidification and warming was observed. Our findings suggest that future ocean warming will be a foremost determinant stressor influencing Z. noltii survival and physiological performance. Additionally, acidification conditions to occur in the future will be unable to counteract deleterious effects posed by ocean warming.
- Physiological resilience of a temperate soft coral to ocean warming and acidificationPublication . Lopes, Ana Rita; Faleiro, Filipa; Rosa, Inês C.; Pimentel, Marta; Trubenbach, Katja; Repolho, Tiago; Diniz, Mário S.; Rosa, RuiAtmospheric concentration of carbon dioxide (CO2) is increasing at an unprecedented rate and subsequently leading to ocean acidification. Concomitantly, ocean warming is intensifying, leading to serious and predictable biological impairments over marine biota. Reef-building corals have proven to be very vulnerable to climate change, but little is known about the resilience of non-reef-building species. In this study, we investigated the effects of ocean warming and acidification on the antioxidant enzyme activity (CAT-catalase, and GST-glutathione S-transferase), lipid peroxidation (using malondialdehyde, MDA-levels as a biomarker) and heat shock response (HSP70/HSC70 content) of the octocoral Veretillum cynomorium. After 60 days of acclimation, no mortalities were registered in all treatments. Moreover, CAT and GST activities, as well as MDA levels, did not change significantly under warming and/or acidification. Heat shock response was significantly enhanced under warming, but high CO2 did not have a significant effect. Contrasting to many of their tropical coral-reef relatives, our findings suggest that temperate shallow-living octocorals may be able to physiologically withstand future conditions of increased temperature and acidification.
- Absence of cellular damage in tropical newly hatched sharks (Chiloscyllium plagiosum) under ocean acidification conditionsPublication . Lopes, Ana Rita; Sampaio, Eduardo; Santos, Catarina; Couto, Ana; Pegado, Maria Rita; Diniz, Mário S.; Munday, Philip L.; Rummer, Jodie L.; Rosa, RuiSharks have maintained a key role in marine food webs for 400 million years and across varying physicochemical contexts, suggesting plasticity to environmental change. In this study, we investigated the biochemical effects of ocean acidification (OA) levels predicted for 2100 (pCO2 ~ 900 μatm) on newly hatched tropical whitespotted bamboo sharks (Chiloscyllium plagiosum). Specifically, we measured lipid, protein, and DNA damage levels, as well as changes in the activity of antioxidant enzymes and non-enzymatic ROS scavengers in juvenile sharks exposed to elevated CO2 for 50 days following hatching. Moreover, we also assessed the secondary oxidative stress response, i.e., heat shock response and ubiquitin levels. Newly hatched sharks appear to cope with OA-related stress through a range of tissue-specific biochemical strategies, specifically through the action of antioxidant enzymatic compounds. Our findings suggest that ROS-scavenging molecules, rather than complex enzymatic proteins, provide an effective defense mechanism in dealing with OA-elicited ROS formation. We argue that sharks' ancient antioxidant system, strongly based on non-enzymatic antioxidants (e.g., urea), may provide them with resilience towards OA, potentially beyond the tolerance of more recently evolved species, i.e., teleosts. Nevertheless, previous research has provided evidence of detrimental effects of OA (interacting with other climate-related stressors) on some aspects of shark biology. Moreover, given that long-term acclimation and adaptive potential to rapid environmental changes are yet experimentally unaccounted for, future research is warranted to accurately predict shark physiological performance under future ocean conditions.
- 3D chemoecology and chemotaxonomy of corals using fatty acid biomarkers: Latitude, longitude and depthPublication . Figueiredo, Cátia; Baptista, Miguel; Rosa, Inês; Lopes, Ana Rita; Dionísio, Gisela; Rocha, Rui J.M.; Cruz, Igor C.S.; Kikuchi, Ruy K.P.; Simões, Nuno; Leal, Miguel Costa; Tojeira, Inês; Bandarra, Narcisa; Calado, Ricardo; Rosa, RuiWith the objective of uncovering differences in the fatty acid (FA) composition of hexa- and octocorals from different climatic zones (equatorial, subtropical and tropical) and distinct habitats (e.g. rock and coral reefs; intertidal to deep-sea environments), the FA composition of 36 hexa- and octocoral species (132 specimens) was analysed (including the first characterization of organisms from the order Zoantharia and deep-sea gorgonians). PCA was applied in a FA matrix of the ten major PUFAs to detect differences among coral groups. Fatty acid profile analysis confirmed that C24 polyunsaturated FAs are suitable chemotaxonomic biomarkers to separate hexa- and octocorals. The polyunsaturated FA 22:6n-3 was identified as a useful biomarker to distinguish between zoantharians and scleractinians. Also, we discuss the role of food availability (type of phytoplankton assemblage) in relation to autotrophic carbon significance and in the establishment of FA profiles of octocorals from the West and East coasts of the Atlantic Ocean. Furthermore, we show that the occurrence of high levels of primary productivity hinder the use of FA profiles to distinguish between zooxanthellate and azooxanthellate octocorals. Finally, we present and discuss the particular traits of the FA profile of deep-sea gorgonians while comparing it with that of shallow species.
- Effect of tidal environment on the trophic balance of mixotrophic hexacorals using biochemical profile and photochemical performance as indicatorsPublication . Rosa, Inês C.; Rocha, Rui J.M.; Cruz, Igor; Lopes, Ana Rita; Menezes, Natália; Bandarra, Narcisa; Kikuchi, Ruy; Serôdio, João; Soares, Amadeu M.V.M.; Rosa, RuiFluctuations of environmental factors in intertidal habitats can disrupt the trophic balance of mixotrophic cnidarians. We investigated the effect of tidal environments (subtidal, tidal pools and emerged areas) on fatty acid (FA) content of Zoanthus sociatus and Siderastrea stellata. Effect on photophysiology was also accessed as an autotrophy proxy. There was a general tendency of a lower percentage of zooplankton-associated FAs in colonies from emerged areas or tidal pools when compared with colonies from the subtidal environment. Moreover, tidal environment significantly affected the photophysiology of both species. Colonies from the subtidal generally showed lower values of α, ETRmax and Ek when compared with their conspecifics from tidal pools or emerged areas. However, the absence of consistent patterns in Fv/Fm and in dinoflagellate-associated FAs, suggest that these corals are well adapted to intertidal conditions. This suggests that intertidal pressures may disturb the trophic balance, mainly by affecting heterotrophy of these species.