Rui Rosa

Synergistic effects of climate-related variables suggest future physiological impairment in a top oceanic predator

By the end of this century, anthropogenic carbon dioxide (CO2) emissions are expected to decrease the surface ocean pH by as much as 0.3 unit. At the same time, the ocean is expected to warm with an associated expansion of the oxygen minimum layer (OML). Thus, there is a growing demand to understand the response of the marine biota to these global changes. We show that ocean acidification will substantially depress metabolic rates (31%) and activity levels (45%) in the jumbo squid, Dosidicus gigas, a top predator in the Eastern Pacific. This effect is exacerbated by high temperature. Reduced aerobic and locomotory scope in warm, high-CO2 surface waters will presumably impair predator–prey interactions with cascading consequences for growth, reproduction, and survival. Moreover, as the OML shoals, squids will have to retreat to these shallower, less hospitable, waters at night to feed and repay any oxygen debt that accumulates during their diel vertical migration into the OML. Thus, we demonstrate that, in the absence of adaptation or horizontal migration, the synergism between ocean acidification, global warming, and expanding hypoxia will compress the habitable depth range of the species. These interactions may ultimately define the long-term fate of this commercially and ecologically important predator.

Ocean Warming Enhances Malformations, Premature Hatching, Metabolic Suppression and Oxidative Stress in the Early Life Stages of a Keystone Squid

Background The knowledge about the capacity of organisms’ early life stages to adapt to elevated temperatures is very limited but crucial to understand how marine biota will respond to global warming. Here we provide a comprehensive and integrated view of biological responses to future warming during the early ontogeny of a keystone invertebrate, the squid Loligo vulgaris. Methodology/Principal Findings Recently-spawned egg masses were collected and reared until hatching at present day and projected near future (+2°C) temperatures, to investigate the ability of early stages to undergo thermal acclimation, namely phenotypic altering of morphological, behavioural, biochemical and physiological features. Our findings showed that under the projected near-future warming, the abiotic conditions inside the eggs promoted metabolic suppression, which was followed by premature hatching. Concomitantly, the less developed newborns showed greater incidence of malformations. After hatching, the metabolic burst associated with the transition from an encapsulated embryo to a planktonic stage increased linearly with temperature. However, the greater exposure to environmental stress by the hatchlings seemed to be compensated by physiological mechanisms that reduce the negative effects on fitness. Heat shock proteins (HSP70/HSC70) and antioxidant enzymes activities constituted an integrated stress response to ocean warming in hatchlings (but not in embryos). Conclusions/Significance The stressful abiotic conditions inside eggs are expected to be aggravated under the projected near-future ocean warming, with deleterious effects on embryo survival and growth. Greater feeding challenges and the lower thermal tolerance limits of the hatchlings are strictly connected to high metabolic demands associated with the planktonic life strategy. Yet, we found some evidence that, in the future, the early stages might support higher energy demands by adjusting some cellular functional properties to increase their thermal tolerance windows.

Biochemical composition of deep-sea decapod crustaceans with two different benthic life strategies off the Portuguese south coast

The objectives of the present study were to characterize the benthic life strategies of Aristeus antennatus (Crustacea: Penaeidea), Parapenaeus longirostris (Crustacea: Penaeidea) and Nephrops norvegicus (Crustacea: Astacidea) on the basis of biochemical composition (proximate chemical composition, total lipids, glycogen and cholesterol contents), and its response to biological and environmental factors (sex, maturation, reproduction, food availability and depth) into account. The specimens were collected at depths between 200 and 600 m off the Portuguese south coast (Algarve). The nektobenthic species (A. antennatus and P. longirostris) showed higher protein, lipid, cholesterol and glycogen contents, and lower moisture content in the muscle than the benthic–endobenthic species (N. norvegicus). Consequently, the energy content of the nektobenthic species was also higher. Principal component analyses were used to assess the relationship between the different biochemical contents and to relate them to the biotic and abiotic factors. Depth seems to have the most important role in the observed trends of the biochemical composition. The increase of the ovarian lipid levels occurs as a result of the maturation process. The highest values were obtained in mature N. norvegicus females. The differences can be due to maternal investment (lipid metabolism of the female is geared to the provision of egg lipid), since N. norvegicus produce large lecithotrophic eggs. The biochemical differences observed in the three species did not seem to be due to distinct trophic strategies, but instead were a consequence of depth, which may have a significant interspecific effect on food intake. It was also evident that reproductive cycle has profound effects upon the biochemistry of the three species. Gonadal maturation has large associated energy costs due to the increase in biosynthetic work. Moreover, the biochemical composition would be influenced by or synchronized with seasonal feeding activity or food availability. r 2003 Elsevier Science Ltd. All rights reserved.

Biochemical changes during the embryonic development of Norway lobster, Nephrops norvegicus

The objectives of the present study were to investigate the total and free amino acid profiles and lipid dynamics (lipid classes and fatty acids) during embryogenesis of Nephrops norvegicus, in order to understand the early larval protein and lipid requirements. There was a significant increase in total essential (EAA) and nonessential amino acid (NEAA) contents during embryonic development (P<0.05). The major EAA were arginine, histidine and leucine, while the most important NEAA were glutamic acid, aspartic acid, glycine and proline. The higher percent increase occurred in respect to NEAA (19.9%), mainly due to the significant increase of glycine (51.8%) and alanine (35.1%). The free amino acid (FAA) content, especially the free nonessential amino acids (FNEAA), also increased significantly, being the quantitatively most important glycine, proline, taurine and glutamic acid. The free essential amino acids (FEAA) also revealed significant variations and the most important were arginine, lysine and leucine. A higher percent increase was attained with FNEAA (66.8%) in comparison to FEAA (49.6%), mainly due to the significant increase of homocystine (87.7%), valine (83.5%), glutamine (82.5%) and glutamic acid (76.1%). The absorption of dissolved organic compounds from seawater can explain the increase in free and total amino acid (FAA and TAA) contents, because a significant increase in the water content during development was observed (P<0.05). A substantial decrease in all neutral lipid classes (P<0.05) was observed during embryonic development, namely diacylglycerols (DAG) (97.9% of utilization), triacylglycerols (TAG) (93.2%), sterol esters (StE) (91.3%) and monoacylglycerols (MAG) (90.4%). The quantitatively most important fatty acids were the saturates (SFA) 14:0, 16:0 and 18:0, the monounsaturates (MUFA) 16:1n-7, 18:1n-9 and 18:1n-7, and the polyunsaturates (PUFA) 18:2n-6, 18:3n-3, 20:4n-6, 20:5n-3 and 22:6n-3. The unsaturated fatty acids (UFA) are used up at a higher rate (54.5% of utilization) than SFA (42.8%); within the UFA, MUFA are more consumed than PUFA (59.3% and 52.7%, respectively). In terms of the utilization of individual fatty acids, there was a preferential consumption of 20:4n-3, 22:6n-3, 18:1n-9, 22:5n-3 and 16:1n-7. It is evident that N. norvegicus depends primarily on lipid reserves of the egg during early ontogeny. On the contrary, this species tends to conserve EAA and increase NEAA and FNEAA contents during embryonic development.

Differential impacts of ocean acidification and warming on winter and summer progeny of a coastal squid (Loligo vulgaris)

Little is known about the capacity of early life stages to undergo hypercapnic and thermal acclimation under the future scenarios of ocean acidification and warming. Here, we investigated a comprehensive set of biological responses to these climate change-related variables (2°C above winter and summer average spawning temperatures and ΔpH=0.5 units) during the early ontogeny of the squid Loligo vulgaris. Embryo survival rates ranged from 92% to 96% under present-day temperature (13–17°C) and pH (8.0) scenarios. Yet, ocean acidification (pH 7.5) and summer warming (19°C) led to a significant drop in the survival rates of summer embryos (47%, P<0.05). The embryonic period was shortened by increasing temperature in both pH treatments (P<0.05). Embryo growth rates increased significantly with temperature under present-day scenarios, but there was a significant trend reversal under future summer warming conditions (P<0.05). Besides pronounced premature hatching, a higher percentage of abnormalities was found in summer embryos exposed to future warming and lower pH (P<0.05). Under the hypercapnic scenario, oxygen consumption rates decreased significantly in late embryos and newly hatched paralarvae, especially in the summer period (P<0.05). Concomitantly, there was a significant enhancement of the heat shock response (HSP70/HSC70) with warming in both pH treatments and developmental stages. Upper thermal tolerance limits were positively influenced by acclimation temperature, and such thresholds were significantly higher in late embryos than in hatchlings under present-day conditions (P<0.05). In contrast, the upper thermal tolerance limits under hypercapnia were higher in hatchlings than in embryos. Thus, we show that the stressful abiotic conditions inside the embryos capsules will be exacerbated under near-future ocean acidification and summer warming scenarios. The occurrence of prolonged embryogenesis along with lowered thermal tolerance limits under such conditions is expected to negatively affect the survival success of squid early life stages during the summer spawning period, but not winter spawning.

LARGE-SCALE DIVERSITY PATTERNS OF CEPHALOPODS IN THE ATLANTIC OPEN OCEAN AND DEEP SEA

Although the oceans cover 70% of the Earths surface and the open ocean is by far the largest ecosystem on the planet, our knowledge regarding diversity patterns of pelagic fauna is very scarce. Here, we examine large-scale latitudinal and depth-related patterns of pelagic cephalopod richness in the Atlantic Ocean in relation to ambient thermal and productive energy availability. Diversity, across 17 biogeochemical regions in the open ocean, does not decline monotonically with latitude, but is positively correlated to the availability of oceanic resources. Mean net primary productivity (NPP), determined from ocean color satellite imagery, explains 37% of the variance in species richness. Outside the poles, the range in NPP explains over 40% of the variability. This suggests that cephalopods are well adapted to the spatial patchiness and seasonality of open-ocean resources. Pelagic richness is also correlated to sea surface temperature, with maximum richness occurring around 15 degrees C and decreasing with both colder and warmer temperatures. Both pelagic and benthos-associated diversities decline sharply from sublittoral and epipelagic regions to the slope and bathypelagic habitats and then steadily to abyssal depths. Thus, higher energy availability at shallow depths seems to promote diversification rates. This strong depth-related trend in diversity also emphasizes the greater influence of the sharp vertical thermal gradient than the smoother and more seasonal horizontal (latitudinal) one on marine diversity.

Seafood traceability: current needs, available tools, and biotechnological challenges for origin certification

Market globalization and recurring food safety alerts have resulted in a growing consumer awareness of the need for food traceability. This is particularly relevant for seafood due to its perishable nature and importance as a key protein source for the population of the world. Here, we provide an overview of the current needs for seafood origin traceability, along with the limitations and challenges for its implementation. We focus on geochemical, biochemical, and molecular tools and how they should be optimized to be implemented globally and to address our societal needs. We suggest that seafood traceability is key to enforcing food safety regulations and fisheries control, combat fraud, and fulfill present and future expectations of conscientious producers, consumers, and authorities.

Future challenges in cephalopod research

We thank Anto´nio M. de Frias Martins, past President of the Unitas Malacologica and Peter Marko, President of the American Malacological Society for organizing the 2013 World Congress of Malacology, and the Cephalopod International Advisory Committee for endorsing a symposium held in honour of Malcolm R. Clarke. In particular, we would like to thank the many professional staff from the University of the Azores for their hospitality, organization, troubleshooting and warm welcome to the Azores. We also thank Malcolm Clarke’s widow, Dorothy, his daughter Zoe¨, Jose´ N. Gomes-Pereira and numerous colleagues and friends of Malcolm’s from around the world for joining us at Ponta Delgada. We are grateful to Lyndsey Claro (Princeton University Press) for granting copyright permissions.

Early-life exposure to climate change impairs tropical shark survival

Sharks are one of the most threatened groups of marine animals worldwide, mostly owing to overfishing and habitat degradation/loss. Although these cartilaginous fish have evolved to fill many ecological niches across a wide range of habitats, they have limited capability to rapidly adapt to human-induced changes in their environments. Contrary to global warming, ocean acidification was not considered as a direct climate-related threat to sharks. Here we show, for the first time, that an early ontogenetic acclimation process of a tropical shark (Chiloscyllium punctatum) to the projected scenarios of ocean acidification (ΔpH = 0.5) and warming (+4°C; 30°C) for 2100 elicited significant impairments on juvenile shark condition and survival. The mortality of shark embryos at the present-day thermal scenarios was 0% both at normocapnic and hypercapnic conditions. Yet routine metabolic rates (RMRs) were significantly affected by temperature, pH and embryonic stage. Immediately after hatching, the Fulton condition of juvenile bamboo sharks was significantly different in individuals that experienced future warming and hypercapnia; 30 days after hatching, survival rapidly declined in individuals experiencing both ocean warming and acidification (up to 44%). The RMR of juvenile sharks was also significantly affected by temperature and pH. The impact of low pH on ventilation rates was significant only under the higher thermal scenario. This study highlights the need of experimental-based risk assessments of sharks to climate change. In other words, it is critical to directly assess risk and vulnerability of sharks to ocean acidification and warming, and such effort can ultimately help managers and policy-makers to take proactive measures targeting most endangered species.

Lower hypoxia thresholds of cuttlefish early life stages living in a warm acidified ocean

The combined effects of future ocean acidification and global warming on the hypoxia thresholds of marine biota are, to date, poorly known. Here, we show that the future warming and acidification scenario led to shorter embryonic periods, lower survival rates and the enhancement of premature hatching in the cuttlefish Sepia officinalis. Routine metabolic rates increased during the embryonic period, but environmental hypercapnia significantly depressed pre-hatchlings energy expenditures rates (independently of temperature). During embryogenesis, there was also a significant rise in the carbon dioxide partial pressure in the perivitelline fluid (PVF), bicarbonate levels, as well as a drop in pH and oxygen partial pressure (pO2). The critical partial pressure (i.e. hypoxic threshold) of the pre-hatchlings was significantly higher than the PVF oxygen partial pressure at the warmer and hypercapnic condition. Thus, the record of oxygen tensions below critical pO2 in such climate scenario indicates that the already harsh conditions inside the egg capsules are expected to be magnified in the years to come, especially in populations at the border of their thermal envelope. Such a scenario promotes untimely hatching and smaller post-hatching body sizes, thus challenging the survival and fitness of early life stages.