Ocean cleaning stations under a changing climate: biological responses of tropical and temperate fish-cleaner shrimp to global warming.

Cleaning symbioses play an important role in the health of certain coastal marine communities. These interspecific associations often occur at specific sites (cleaning stations) where a cleaner organism (commonly a fish or shrimp) removes ectoparasites/damaged tissue from a 'client' (a larger cooperating fish). At present, the potential impact of climate change on the fitness of cleaner organisms remains unknown. This study investigated the physiological and biochemical responses of tropical (Lysmata amboinensis) and temperate (L. seticaudata) cleaner shrimp to global warming. Specifically, thermal limits (CTMax), metabolic rates, thermal sensitivity, heat shock response (HSR), lipid peroxidation [malondialdehyde (MDA) concentration], lactate levels, antioxidant (GST, SOD and catalase) and digestive enzyme activities (trypsin and alkaline phosphatase) at current and warming (+3 °C) temperature conditions. In contrast to the temperate species, CTMax values decreased significantly from current (24-27 °C) to warming temperature conditions (30 °C) for the tropical shrimp, where metabolic thermal sensitivity was affected and the HSR was significantly reduced. MDA levels in tropical shrimp increased dramatically, indicating extreme cellular lipid peroxidation, which was not observed in the temperate shrimp. Lactate levels, GST and SOD activities were significantly enhanced within the muscle tissue of the tropical species. Digestive enzyme activities in the hepatopancreas of both species were significantly decreased by warmer temperatures. Our data suggest that the tropical cleaner shrimp will be more vulnerable to global warming than the temperate Lysmata seticaudata; the latter evolved in a relatively unstable environment with seasonal thermal variations that may have conferred greater adaptive plasticity. Thus, tropical cleaning symbioses may be challenged at a greater degree by warming-related anthropogenic forcing, with potential cascading effects on the health and structuring of tropical coastal communities (e.g. coral reefs).

Defective skeletogenesis and oversized otoliths in fish early stages in a changing ocean.

Early life stages of many marine organisms are being challenged by rising seawater temperature and CO2 concentrations, but their physiological responses to these environmental changes still remain unclear. In the present study, we show that future predictions of ocean warming (+4°C) and acidification (ΔpH=0.5 units) may compromise the development of early life stages of a highly commercial teleost fish, Solea senegalensis. Exposure to future conditions caused a decline in hatching success and larval survival. Growth, metabolic rates and thermal tolerance increased with temperature but decreased under acidified conditions. Hypercapnia and warming amplified the incidence of deformities by 31.5% (including severe deformities such as lordosis, scoliosis and kyphosis), while promoting the occurrence of oversized otoliths (109.3% increase). Smaller larvae with greater skeletal deformities and larger otoliths may face major ecophysiological challenges, which might potentiate substantial declines in adult fish populations, putting in jeopardy the species' fitness under a changing ocean.

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 embryo's 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.

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-hatchling's 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.

Physiological resilience of a temperate soft coral to ocean warming and acidification.

Atmospheric 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.

Distinct Bleaching Resilience of Photosynthetic Plastid-Bearing Mollusks Under Thermal Stress and High CO2 Conditions.

The 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).

Size does matter: An assessment of reproductive potential in seahorses.

In most animals, the mother plays the key role in reproduction, but male pregnancy in seahorses raises the question of whether the female still is the only determinant of offspring size or if she shares some responsibility with the male. This study evaluates the effects of both male and female size on the reproductive output of the long-snouted seahorse, Hippocampus guttulatus. Results demonstrated that, with regard to reproductive potential, the bigger the better. Seahorses preferred similar-sized or larger mates. Larger females produced bigger eggs with larger yolk reserves. Larger males had larger brood pouches, but did not produced larger broods. Male size was negatively correlated with embryo density and positively correlated with juvenile size. Both parents proved to play a decisive role in the reproductive output of this species. Newborn juveniles from the same parents were 15% bigger and 30% heavier when incubated in smaller and lower-density broods. This trade-off between the number and size of embryos inside the brood pouch clearly indicates a limited carrying capacity of the male, and demonstrates that the size of newborn seahorses can be, in part, paternally determined.

Small pelagics in a changing ocean: biological responses of sardine early stages to warming.

Small pelagic fishes are known to respond rapidly to changes in ocean climate. In this study, we evaluate the effects of future environmental warming (+2°C) during the early ontogeny of the European sardine, Sardina pilchardus. Warming reduced the survival of 30-day-old larvae by half. Length at hatching increased with temperature as expected, but no significant effect was observed on the length and growth at 30 days post-hatching. Warming did not significantly affect the thermal tolerance of sardine larvae, even though the mean lethal temperature increased by 1°C. In the warm conditions, sardine larvae showed signs of thermal stress, indicated by a pronounced increase in larval metabolism (Q 10 = 7.9) and a 45% increase in the heat shock response. Lipid peroxidation was not significantly affected by the higher temperature, even though the mean value doubled. Warming did not affect the time larvae spent swimming, but decreased by 36% the frequency of prey attacks. Given the key role of these small pelagics in the trophic dynamics off the Western Iberian upwelling ecosystem, the negative effects of warming on the early stages may have important implications for fish recruitment and ecosystem structure.

Seahorses under a changing ocean: the impact of warming and acidification on the behaviour and physiology of a poor-swimming bony-armoured fish.

Seahorses are currently facing great challenges in the wild, including habitat degradation and overexploitation, and how they will endure additional stress from rapid climate change has yet to be determined. Unlike most fishes, the poor swimming skills of seahorses, along with the ecological and biological constraints of their unique lifestyle, place great weight on their physiological ability to cope with climate changes. In the present study, we evaluate the effects of ocean warming (+4°C) and acidification (ΔpH = -0.5 units) on the physiological and behavioural ecology of adult temperate seahorses, Hippocampus guttulatus. Adult seahorses were found to be relatively well prepared to face future changes in ocean temperature, but not the combined effect of warming and acidification. Seahorse metabolism increased normally with warming, and behavioural and feeding responses were not significantly affected. However, during hypercapnia the seahorses exhibited signs of lethargy (i.e. reduced activity levels) combined with a reduction of feeding and ventilation rates. Nonetheless, metabolic rates were not significantly affected. Future ocean changes, particularly ocean acidification, may further threaten seahorse conservation, turning these charismatic fishes into important flagship species for global climate change issues.

Oxidative Stress and Digestive Enzyme Activity of Flatfish Larvae in a Changing Ocean.

Until now, it is not known how the antioxidant and digestive enzymatic machinery of fish early life stages will change with the combined effects of future ocean acidification and warming. Here we show that high pCO2 (~1600 µatm) significantly decreased metabolic rates (up to 27.4 %) of flatfish larvae, Solea senegalensis, at both present (18 °C) and warmer temperatures (+4 °C). Moreover, both warming and hypercapnia increased the heat shock response and the activity of antioxidant enzymes, namely catalase (CAT) and glutathione S-transferase (GST), mainly in post-metamorphic larvae (30 dph). The lack of changes in the activity of CAT and GST of pre-metamorphic larvae (10 dph) seems to indicate that earlier stages lack a fully-developed antioxidant defense system. Nevertheless, the heat shock and antioxidant responses of post-metamorphic larvae were not enough to avoid the peroxidative damage, which was greatly increased under future environmental conditions. Digestive enzymatic activity of S. senegalensis larvae was also affected by future predictions. Hypercapnic conditions led to a decrease in the activity of digestive enzymes, both pancreatic (up to 26.1 % for trypsin and 74.5 % for amylase) and intestinal enzymes (up to 36.1 % for alkaline phosphatase) in post-metamorphic larvae. Moreover, the impact of ocean acidification and warming on some of these physiological and biochemical variables (namely, lower OCR and higher HSP and MDA levels) were translated into larvae performance, being significantly correlated with decreased larval growth and survival or increased incidence of skeletal deformities. The increased vulnerability of flatfish early life stages under future ocean conditions is expected to potentially determine recruitment and population dynamics in marine ecosystems.