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- 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.
- Foraging behaviour, swimming performance and malformations of early stages of commercially important fishes under ocean acidification and warmingPublication . Pimentel, Marta; Faleiro, Filipa; Marques, Tiago; Bispo, Regina; Dionísio, Gisela; Faria, Ana M.; Machado, Jorge; Peck, Myron A.; Pörtner, Hans; Pousão-Ferreira, Pedro; Gonçalves, Emanuel J.; Rosa, RuiEarly life stages of many marine organisms are being challenged by climate change, but little is known about their capacity to tolerate future ocean conditions. Here we investigated a comprehensive set of biological responses of larvae of two commercially important teleost fishes, Sparus aurata (gilthead seabream) and Argyrosomus regius (meagre), after exposure to future predictions of ocean warming (+4 °C) and acidification (ΔpH = 0.5). The combined effect of warming and hypercapnia elicited a decrease in the hatching success (by 26.4 and 14.3 % for S. aurata and A. regius, respectively) and larval survival (by half) in both species. The length for newly-hatched larvae was not significantly affected, but a significant effect of hypercapnia was found on larval growth. However, while S. aurata growth was reduced (24.8–36.4 % lower), A. regius growth slightly increased (3.2–12.9 % higher) under such condition. Under acidification, larvae of both species spent less time swimming, and displayed reduced attack and capture rates of prey. The impact of warming on these behavioural traits was opposite but less evident. While not studied in A. regius, the incidence of body malformations in S. aurata larvae increased significantly (more than tripled) under warmer and hypercapnic conditions. These morphological impairments and behavioural changes are expected to affect larval performance and recruitment success, and further influence the abundance of fish stocks and the population structure of these commercially important fish species. However, given the pace of ocean climate change, it is important not to forget that species may have the opportunity to acclimate and adapt.
- Revisiting in vivo staining with alizarin red S - a valuable approach to analyse zebrafish skeletal mineralization during development and regenerationPublication . Bensimon-Brito, A.; Cardeira, J.; Dionísio, Gisela; Huysseune, A.; Cancela, M. L.; Witten, P. E.Background: The correct evaluation of mineralization is fundamental for the study of skeletal development, maintenance, and regeneration. Current methods to visualize mineralized tissue in zebrafish rely on: 1) fixed specimens; 2) radiographic and μCT techniques, that are ultimately limited in resolution; or 3) vital stains with fluorochromes that are indistinguishable from the signal of green fluorescent protein (GFP)-labelled cells. Alizarin compounds, either in the form of alizarin red S (ARS) or alizarin complexone (ALC), have long been used to stain the mineralized skeleton in fixed specimens from all vertebrate groups. Recent works have used ARS vital staining in zebrafish and medaka, yet not based on consistent protocols. There is a fundamental concern on whether ARS vital staining, achieved by adding ARS to the water, can affect bone formation in juvenile and adult zebrafish, as ARS has been shown to inhibit skeletal growth and mineralization in mammals. Results: Here we present a protocol for vital staining of mineralized structures in zebrafish with a low ARS concentration that does not affect bone mineralization, even after repetitive ARS staining events, as confirmed by careful imaging under fluorescent light. Early and late stages of bone development are equally unaffected by this vital staining protocol. From all tested concentrations, 0.01 % ARS yielded correct detection of bone calcium deposits without inducing additional stress to fish. Conclusions: The proposed ARS vital staining protocol can be combined with GFP fluorescence associated with skeletal tissues and thus represents a powerful tool for in vivo monitoring of mineralized structures. We provide examples from wild type and transgenic GFP-expressing zebrafish, for endoskeletal development and dermal fin ray regeneration.
- 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.
- 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.
- “Gone with the wind”: Fatty acid biomarkers and chemotaxonomy of stranded pleustonic hydrozoans (Velella velella and Physalia physalis)Publication . Lopes, Ana Rita; Baptista, Miguel; Rosa, Inês; Dionísio, Gisela; Gomes-Pereira, José; Paula, José Ricardo; Figueiredo, Cátia; Bandarra, Narcisa; Calado, Ricardo; Rosa, RuiMarine pleustonic species such as the hydrozoans Velella velella and Physalia physalis, are known to drift in the world's oceans driven by winds, currents and tides. Here we present the first chemotaxonomic characterization, based on the fatty acid (FA) profile, of these two charismatic oceanic species that thrive in the interface layer between air and the water column in adult stages. Moreover, we compared their FA profiles with those from other representative cnidarian orders (Rhizostomeae, Anthomedusae, Siphonophorae, Alcyonacea, Scleractinia, Helioporacea and Pennatulacea). Velella velella and P. physalis mainly differed in the presence of symbiotic dinoflagellates markers (18:3n-6, 18:4n-3 and 20:5n-3 polyunsaturated FAs), present in higher percentage in the former, and bacterial markers (odd-numbered, branched and 18:1n-7 FAs), which were more representative in the latter. When comparing these species' FA profiles with the ones of other cnidarians orders, the presence/absence of endosymbionts and of specific FAs (tetracosapentaenoic and tetracosahexaenoic acids) as well as the latitudinal habitats were the main drivers for the distinction between groups.
- Ocean acidification promotes cellular burst on photosynthetic (kleptoplastic) sea slugsPublication . Dionísio, Gisela; Cruz, S.; Serôdio, J.; Calado, R.; Rosa, RuiOcean acidification is known to trigger deleterious effects on several marine photosynthetic invertebrates [1]. Photosymbiosis, whereby photosynthetic microorganisms or organelles live inside an animal (host) is widespread in the marine biota, underlying a wide range of ecologically and biogeochemically significant processes that remain largely unclear [1]. One of the most remarkable symbiosis is between sacoglossan molluscs and algal chloroplasts [2]. These organisms are able to “steal” functional chloroplasts (termed kleptoplasts) from their algal prey and keep them functional inside digestive diverticula [2]. The aim of this study was to investigate the impact of environmental hypercapnia on cellular structures of kleptoplastic animals. Elysia viridis (Sacoglossa) were exposed to different pH conditions (pH 8, 7.5, 6.8 and 6.1) for 24 h.
- Distinct Bleaching Resilience of Photosynthetic Plastid-Bearing Mollusks Under Thermal Stress and High CO2 ConditionsPublication . Dionísio, Gisela; Faleiro, Filipa; Bispo, Regina; Lopes, Ana Rita; Cruz, Sónia; Paula, José Ricardo; Repolho, Tiago; Calado, Ricardo; Rosa, RuiThe impact of temperature on photo-symbiotic relationships has been highly studied in the tropical reef-forming corals but overlooked in less charismatic groups such as solar-powered sacoglossan sea slugs. These organisms display one of the most puzzling symbiotic features observed in the animal kingdom, i.e., their mollusk-plastid association, which enables them to retain photosynthetic active chloroplasts (i.e., kleptoplasts) retrieved from their algae feed sources. Here we analyze the impact of thermal stress (+4°C) and high pCO2 conditions (ΔpH = 0.4) in survival, photophysiology (i.e., bleaching, photosynthetic efficiency, and metabolism) and stress defense mechanisms (i.e., heat shock and antioxidant response) of solar-powered sacoglossan sea slugs, from tropical (Elysia crispata) and temperate (E. viridis) environments. High temperature was the main factor affecting the survival of both species, while pH only affected the survival of the temperate model. The photobiology of E. viridis remained stable under the combined scenario, while photoinhibition was observed for E. crispata under high temperature and high pCO2. In fact, bleaching was observed within all tropical specimens exposed to warming (but not in the temperate ones), which constitutes the first report where the incidence of bleaching in tropical animals hosting photosynthetic symbionts, other than corals, occurs. Yet, the expulsion of kleptoplasts by the tropical sea slug, allied with metabolic depression, constituted a physiological response that did not imply signs of vulnerability (i.e., mortality) in the host itself. Although the temperate species revealed greater heat shock and antioxidant enzyme response to environmental stress, we argue that the tropical (stenotherm) sea slug species may display a greater scope for acclimatization than the temperate (eurytherm) sea slug. E. crispata may exhibit increased capacity for phenotypic plasticity by increasing fitness in a much narrower thermal niche (minimizing maintenance costs), which ultimately may allow to face severe environmental conditions more effectively than its temperate generalist counterpart (E. viridis).
- Nudibranchs out of water: long-term temporal variations in the abundance of two Dendrodoris species under emersionPublication . Cyrne, Ricardo; Rosa, Inês; Faleiro, Filipa; Dionísio, Gisela; Baptista, Miguel; Couto, Ana; Pola, Marta; Rosa, RuiThe sudden appearance and disappearance of nudibranchs in intertidal areas have puzzled researchers all over the world, giving rise to a great diversity of theories to explain it. Here we conducted a five-year survey to evaluate seasonal changes in the abundance of Dendrodoris herytra and D. grandiflora in the Sado estuary (Portugal) and to explore a possible relationship with environmental factors such as temperature, salinity, turbidity and dissolved oxygen. Moreover, we report, for the first time, the capacity of Dendrodoris nudibranchs to tolerate emersion (unhidden and completely exposed to sun exposure) during low tides. Our results showed that both species consistently started to appear emerged in March, reaching a peak abundance between April and May, and completely disappearing in July. In both species, this temporal trend was significantly associated with water temperature, turbidity, and dissolved oxygen, but not with salinity. We argue that the sudden appearance and disappearance of these nudibranchs in intertidal areas may result from a seasonal horizontal movement of adult nudibranchs from subtidal areas to mate in intertidal areas during spring, when phytoplankton production is enhanced and planktotrophic larvae may benefit from greater food availability.