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- 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.
- Evaluation of Paracentrotus lividus (Lamarck, 1816) exotrophic larvae as live feed for marine decapod crustacean larvaePublication . Repolho, Tiago; Luís, Orlando de Jesus, 1954-; Yúfera Ginés, ManuelIn the present study, we have evaluated 4‐arm exotrophic larvae of sea urchin Paracentrotus lividus (Echinodermata: Echinoidea) as live feed in marine decapod crustacean larviculture, in comparison to Artemia spp. naupliar stages, a commonly used live prey in marine hatcheries. We therefore investigated several key parameters to assess the potential of P. lividus plutei as live feed for crustacean larvae, namely: 1) broodstock diet manipulation in order to obtain both quantitative and qualitative year round production of 4‐arm echinoplutei, free from environmental and reproductive seasonal constraints; 2) best possible biotic conditions to perform sea urchin in vitro fertilization, namely sperm:egg ratios and egg concentrations, and its relation to early stage segmentation and larvae development; 3) mass production possibility in terms of larvae media culture conditions, plutei stocking densities and larvae feed and enrichment; and acceptability as live feed by predator larvae (Lysmata seticaudata, Palaemon elegans, Maja brachydactyla, Pachygrapsus marmoratus and Xantho incisus). Additionally, we studied the possibility to differentiate P. lividus broodstock sex by means of a spine external morphological characteristic. Under controlled laboratory conditions, percent egg fertilization above 99% and high values for percent normal development (≥85%) were obtained when captive breed P. lividus broodstock was fed an inert diet based upon maize and wheat flour mixture. Whole egg total amino acid composition was similar between P. lividus fed this inert diet and wild caught organisms. Enrichment potential in terms 4‐arm plutei fatty acid profile and lipid content was possible through manipulation of the lipid source chosen for captive P. lividus broodstock diet. Sperm:egg ratios were found to influence percent egg fertilization and segmentation development after 90 minutes post‐fertilization, but not plutei total length, post‐oral arm length and normal percent larvae development. Water renewal (every 2 days) during P. lividus larviculture was found to be an essential abiotic culture condition to sustain plutei development and survival until 18 days post‐fertilization. All plutei larval feeds (live microalgae, inert microdiets, single or mixed provided), supported P. lividus larvae growth and survival until 18 days post‐fertilization (DPF), with D. tertiolecta being found to be the most appropriate diet in terms of larvae development and survival outcome. When cultured at a initial stocking density of 40 plutei.ml‐1, inert microdiets were unable to sustain P. lividus plutei survival to 10 DPF. Plutei survival was found to be inversely correlated with increasing culture densities. Paracentrotus lividus plutei enrichment with Algamac 3050 flake, was found to cause mass mortality at 5 and 10 DPF. Paracentrotus lividus exotrophic 4‐arm plutei was ingested and preyed by 4 (Lysmata seticaudata, Maja brachydactyla, Pachygrapsus marmoratus and Xantho incisus) out of 5 crustacean larvae tested, but were unable to sustain complete larvae development and survival to settlement of L. seticaudata, M. brachydactyla and P. marmoratus species. No apparent advantage of P. lividus 4‐arm plutei as live feed for marine crustacean decapod larvae was found in comparison to Artemia spp.. Finally, the analysed spine morphological characteristic, as a tool for sex differentiation between P. lividus adults, does not allow accurate and feasible results.
- Deficit in digestive capabilities of bamboo shark early stages under climate changePublication . Rosa, Rui; Pimentel, Marta; Galan, Juan; Baptista, Miguel; Lopes, Vanessa M.; Couto, Ana; Guerreiro, Miguel; Sampaio, Eduardo; Castro, Joana; Santos, Catarina; Calado, Ricardo; Repolho, TiagoLittle empirical information is currently available on the potential effects of acidification and/or warming in sharks, but none exist about digestive capabilities under such future conditions. Here, we investigated the impact of both acidification (ΔpH = 0.5) and warming (+4; 30 °C) on the digestive enzyme levels of recently hatched tropical bamboo shark (Chiloscyllium punctatum). Thirty days post-hatching, juvenile sharks revealed a significant increase in pancreatic trypsin levels under warming, but also a significant decrease under acidification, namely a 42 % drop under present-day temperature and 44 % drop under the warming condition. A similar trend was recorded for the alkaline phosphatase activity in shark’s intestine, i.e. the impact of environmental hypercapnia was also quite notorious—a 50 % drop under present-day temperature and 49 % drop under the warming condition. Thus, our present findings suggest that acidification and warming acted antagonistically, leading to similar enzyme activities under present and future conditions. Future directions on this topic of research should point towards the study of other types of sharks, namely pelagic ones with quite higher energetic demands.
- 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.
- Negative synergistic impacts of ocean warming and acidification on the survival and proteome of the commercial sea bream, Sparus aurataPublication . Araújo, José E.; Madeira, Diana; Vitorino, Rui; Repolho, Tiago; Rosa, Rui; Diniz, M.Global change is impacting aquatic ecosystems, with high risks for food production. However, the molecular underpinnings of organismal tolerance to both ocean warming and acidification are largely unknown. Here we tested the effect of warming and acidification in a 42-day experiment on a commercial temperate fish, the gilt-head seabream Sparus aurata. Juvenile fish were exposed to control (C 18 °C pH 8), ocean warming (OW 22 °C pH 8), ocean acidification (OA 18 °C pH 7.5) and ocean warming and acidification (OWA 22 °C pH 7.5). Proxies of fitness (mortality; condition index) and muscle proteome changes were assessed; bioinformatics tools (Cytoscape, STRAP, STRING) were used for functional analyses. While there was no mortality in fish under OW, fish exposed to OA and both OWA showed 17% and 50% mortality, respectively. Condition index remained constant in all treatments. OW alone induced small proteome adjustments (up-regulation of 2 proteins) related to epigenetic gene regulation and cytoskeletal remodeling. OA and both OWA induced greater proteome changes (12 and 8 regulated proteins, respectively) when compared to OW alone, suggesting that pH is central to proteome modulation. OA exposure led to increased glycogen degradation, glycolysis, lipid metabolism, anion homeostasis, cytoskeletal remodeling, immune processes and redox based signaling while decreasing ADP metabolic process. OWA led to increased lipid metabolism, glycogen degradation, glycolysis, cytoskeleton remodeling and decreased muscle filament sliding and intermediate filament organization. Moreover, as rates of change in temperature and acidification depend on region we tested as proof of concept an (i) acidification effect in a hot ocean (22 °C pH 8 vs 22 °C pH 7.5) which led to the regulation of 7 proteins, the novelty being in a boost of anaerobic metabolism and impairment of proteasomal degradation; and (ii) warming effect in an acidified ocean (18 °C pH 7.5 vs 22 °C pH 7.5) which led to the regulation of 5 proteins, with an emphasis on anaerobic metabolism and transcriptional regulation. The negative synergistic effects of ocean warming and acidification on fish survival coupled to the mobilization of storage compounds, enhancement in anaerobic pathways and impaired proteasomal degradation could pose a serious threat to the viability of sea bream populations.
- Protein analysis and gene expression indicate differential vulnerability of Iberian fish species under a climate change scenarioPublication . Jesus, Tiago F.; Moreno, João M.; Repolho, Tiago; Athanasiadis, Alekos; Rosa, Rui; Almeida-Val, Vera M. F.; Coelho, Maria M.Current knowledge on the biological responses of freshwater fish under projected scenarios of climate change remains limited. Here, we examine differences in the protein configuration of two endemic Iberian freshwater fish species, Squalius carolitertii and the critically endangered S. torgalensis that inhabit in the Atlantic-type northern and in the Mediterranean-type southwestern regions, respectively. We performed protein structure modeling of fourteen genes linked to protein folding, energy metabolism, circadian rhythms and immune responses. Structural differences in proteins between the two species were found for HSC70, FKBP52, HIF1α and GPB1. For S. torgalensis, besides structural differences, we found higher thermostability for two proteins (HSP90 and GBP1), which can be advantageous in a warmer environment. Additionally, we investigated how these species might respond to projected scenarios of 3° climate change warming, acidification (ΔpH = -0.4), and their combined effects. Significant changes in gene expression were observed in response to all treatments, particularly under the combined warming and acidification. While S. carolitertii presented changes in gene expression for multiple proteins related to folding (hsp90aa1, hsc70, fkbp4 and stip1), only one such gene was altered in S. torgalensis (stip1). However, S. torgalensis showed a greater capacity for energy production under both the acidification and combined scenarios by increasing cs gene expression and maintaining ldha gene expression in muscle. Overall, these findings suggest that S. torgalensis is better prepared to cope with projected climate change. Worryingly, under the simulated scenarios, disturbances to circadian rhythm and immune system genes (cry1aa, per1a and gbp1) raise concerns for the persistence of both species, highlighting the need to consider multi-stressor effects when evaluating climate change impacts upon fish. This work also highlights that assessments of the potential of endangered freshwater species to cope with environmental change are crucial to help decision-makers adopt future conservation strategies.
- Bioaccumulation and elimination of mercury in juvenile seabass (Dicentrarchus labrax) in a warmer environmentPublication . Maulvault, Ana Luísa; Custódio, Ana; Anacleto, Patrícia; Repolho, Tiago; Pousão, Pedro; Nunes, Maria Leonor; Diniz, Mário; Rosa, Rui; Marques, AntónioWarming is an expected impact of climate change that will affect coastal areas in the future. These areas are also subjected to strong anthropogenic pressures leading to chemical contamination. Yet, the consequences of both factors for marine ecosystems, biota and consumers are still unknown. The present work aims to investigate, for the first time, the effect of temperature increase on bioaccumulation and elimination of mercury [(total mercury (THg) and methylmercury (MeHg)] in three tissues (muscle, liver, and brain) of a commercially important seafood species - European seabass (Dicentrarchus labrax). Fish were exposed to the ambient temperature currently used in seabass rearing (18°C) and to the expected ocean warming (+4°C, i.e. 22°C), as well as dietary MeHg during 28 days, followed by a depuration period of 28 days fed with a control diet. In both temperature exposures, higher MeHg contents were observed in the brain, followed by the muscle and liver. Liver registered the highest elimination percentages (EF; up to 64% in the liver, 20% in the brain, and 3% in the muscle). Overall, the results clearly indicate that a warming environment promotes MeHg bioaccumulation in all tissues (e.g. highest levels in brain: 8.1mg kg-1 ww at 22°C against 6.2mg kg-1 ww at 18°C after 28 days of MeHg exposure) and hampers MeHg elimination (e.g. liver EF decreases after 28 days of depuration: from 64.2% at 18°C to 50.3% at 22°C). These findings suggest that seafood safety may be compromised in a warming context, particularly for seafood species with contaminant concentrations close to the current regulatory levels. Hence, results point out the need to strengthen research in this area and to revise and/or adapt the current recommendations regarding human exposure to chemical contaminants through seafood consumption, in order to integrate the expected effects of climate change.