Ocean Warming Enhances Malformations, Premature Hatching, Metabolic Suppression and Oxidative Stress in the Early Life Stages of a Keystone Squid (original) (raw)
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Journal of Experimental Biology, 2014
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.
Physiological and Biochemical Zoology, 2015
An organism's physiological processes form the link between its life-history traits and the prevailing environmental conditions, especially in species with complex life cycles. Understanding how these processes respond to changing environmental conditions, thereby affecting organismal development, is critical if we are to predict the biological implications of current and future global climate change. However, much of our knowledge is derived from adults or single developmental stages. Consequently, we investigated the metabolic rate, organic content, carapace mineralization, growth, and survival across each larval stage of the European lobster Homarus gammarus, reared under current and predicted future ocean warming and acidification scenarios. Larvae exhibited stage-specific changes in the temperature sensitivity of their metabolic rate. Elevated PCO 2 increased C∶N ratios and interacted with elevated temperature to affect carapace mineralization. These changes were linked to concomitant changes in survivorship and growth, from which it was concluded that bottlenecks were evident during H. gammarus larval development in stages I and IV, the transition phases between the embryonic and pelagic larval stages and between the larval and megalopa stages, respectively. We therefore suggest that natural changes in optimum temperature during ontogeny will be key to larvae survival in a future warmer ocean. The interactions of these natural changes with elevated temperature and PCO 2 significantly alter physiological condition and body size of the last larval stage before the transition from a planktonic to a benthic life style. Thus, living and growing in warm, hypercapnic waters could compromise larval lobster growth, development, and recruitment.
Climate change has pervasive effects on marine ecosystems, altering biodiversity patterns, abundance and distribution of species, biological interactions, phenology, and organisms' physiology, performance and fitness. Fish early life stages have narrow thermal windows and are thus more vulnerable to further changes in water temperature. The aim of this study was to address the sensitivity and underlying molecular changes of larvae of a key fisheries species, the sea bream Sparus aurata, towards ocean warming. Larvae were exposed to three temperatures: 18 °C (control), 24 °C (warm) and 30 °C (heat wave) for seven days. At the end of the assay, i) survival curves were plotted for each temperature treatment and ii) entire larvae were collected for proteomic analysis via 2D gel electrophoresis, image analysis and mass spectrometry. Survival decreased with increasing temperature, with no larvae surviving at 30 °C. Therefore, proteomic analysis was only carried out for 18 °C and 24 °C. Larvae up-regulated protein folding and degradation, cytoskeletal reorganization , transcriptional regulation and the growth hormone while mostly down-regulating cargo transporting and porphyrin metabolism upon exposure to heat stress. No changes were detected in proteins related to energetic metabolism suggesting that larval fish may not have the energetic plasticity needed to sustain cellular protection in the long-term. These results indicate that despite proteome modulation, S. aurata larvae do not seem able to fully acclimate to higher temperatures as shown by the low survival rates. Consequently, elevated temperatures seem to have bottleneck effects during fish early life stages, and future ocean warming can potentially compromise recruitment's success of key fisheries species.
Marine Biology, 2015
temperatures, in ranges expected to occur over the next century. The negative effects of decreasing food availability on the development of P. lividus larvae will be significantly modulated, however, by increasing seawater temperature. These results show that surviving sea urchin larvae are capable of shifting their energy budget to successfully grow and develop under the stressful conditions presented by the combined effects of environmental factors.
Journal of Thermal Biology, 2013
Thermal tolerance limits of marine intertidal zone organisms are elevated compared to subtidal species, but are typically just slightly higher than maximal habitat temperatures. The small thermal safety margins maintained by intertidal zone organisms suggest that high thermal tolerance is associated with a physiological cost. If true, we hypothesize that species that transition between intertidal zone and planktonic habitats during ontogeny, will adjust their thermal tolerance accordingly to capitalize upon potential energy savings while in a thermally benign habitat. We tested this hypothesis in porcelain crabs that transition between the thermally stressful, intertidal zone as embryos, to the thermally benign pelagic zone as larvae, and back at settlement. We found the more thermally tolerant, midintertidal zone species, Petrolisthes cinctipes, and the less thermally tolerant, subtidal zone species, Petrolisthes manimacilis, exhibited reduced thermal tolerance (LT 50 ) in the transition from embryos to larvae. This was associated with an increased oxygen consumption rate in both species, though P. cinctipes exhibited a significantly greater increase in oxygen consumption. P. cinctipes also showed an increase in thermal tolerance in settled juveniles compared to pelagic zoea I larvae, resulting in an overall V-shaped thermal tolerance relationship during ontogeny, while in P. manimaculis thermal tolerance was significantly lower in juveniles compared to zoea I. In neither species were these changes (zoea I to juvenile) associated with a significant change in metabolism. While embryos and juveniles of P. cinctipes have thermal tolerance limits near intertidal habitat thermal maxima ( $ 32.5 1C), all three life-history stages in P. manimaculis (especially embryos and larvae) exhibit considerable thermal safety margins. The mechanisms underlying this ''excess'' thermal tolerance in P. manimacilis embryos are unknown, but suggest that patterns of thermal tolerance in early life history stages are species-specific.
Relative mortality increased upon warming, reaching 80 % at 30 °C. Oxidative damage was higher at moderate temperatures and decreased at 24 °C probably due to a significant increase in superoxide dismutase's (SODs) activity. Hsp70 chaperone levels also increased at 26 °C, but unfolding persisted at higher temperatures as shown by the increase in total ubiquitin at 26 and 28 °C, indicating protein damage. Skeletal muscle showed disor-ganization of muscle fibers from 24 °C onwards. Overall , protein denaturation seems to be the major cause of larval mortality, potentially compromising recruitment's success from 22 °C onwards, since larvae migrate into nursery grounds by spring and summer (i.e., high temperatures), thus hindering the viability of local fish stocks. These data demonstrate that the biochemical homeostasis of fish can be disturbed within an ecologically realistic thermal range and emphasize the risks of rising global temperatures for larval fishes. Abstract Understanding physiological and molecular compensation mechanisms that shape thermotolerance is crucial for estimating the effects of ocean warming on fish stocks, especially during early life stages, whose tolerance determines recruitment success and population viability. The aims of this study were to assess the sensitivity of fish larvae toward ocean warming and heat wave events in the commercial species, Sparus aurata, whose habitat is likely to be affected by rising water temperatures. We (1) estimated its critical thermal maximum (CT max) and relative mortality upon warming, (2) quantified stress biomarkers: heat shock protein 70 kDa, total ubiquitin, antioxidant enzymes (superoxide dismutase, catalase, glutathione-S-transferase), lipid peroxidation and protein carbonylation, and (3) analyzed histopatho-logical changes as a result of thermal stress. Larvae showed increasing levels of lethargy with increasing temperature , attaining a cumulative CT max value of 30 °C.
Journal of Comparative Physiology B, 2014
The ability to understand and predict the effects of ocean warming (under realistic scenarios) on marine biota is of paramount importance, especially at the most vulnerable early life stages. Here we investigated the impact of predicted environmental warming (?3°C) on the development, metabolism, heat shock response and antioxidant defense mechanisms of the early stages of the common octopus, Octopus vulgaris. As expected, warming shortened embryonic developmental time by 13 days, from 38 days at 18°C to 25 days at 21°C. Concomitantly, survival decreased significantly (*29.9 %). Size at hatching varied inversely with temperature, and the percentage of smaller premature paralarvae increased drastically, from 0 % at 18°C to 17.8 % at 21°C. The metabolic costs of the transition from an encapsulated embryo to a free planktonic form increased significantly with warming, and HSP70 concentrations and glutathione S-transferase activity levels were significantly magnified from late embryonic to paralarval stages. Yet, despite the presence of effective antioxidant defense mechanisms, ocean warming led to an augmentation of malondialdehyde levels (an indicative of enhanced ROS action), a process considered to be one of the most frequent cellular injury mechanisms. Thus, the present study provides clues about how the magnitude and rate of ocean warming will challenge the buffering capacities of octopus embryos and hatchlings' physiology. The prediction and understanding of the biochemical and physiological responses to warmer temperatures (under realistic scenarios) is crucial for the management of highly commercial and ecologically important species, such as O. vulgaris.
A review and meta-analysis of the effects of multiple abiotic stressors on marine embryos and larvae
Global Change Biology, 2014
Marine organisms are simultaneously exposed to anthropogenic stressors with likely interactive 36 effects, including synergisms in which the combined effects of multiple stressors are greater than 37 the sum of individual effects. Early life stages of marine organisms are potentially vulnerable to the 38 stressors associated with global change, but identifying general patterns across studies, species and 39 response variables is challenging. This review represents the first meta-analysis of multi-stressor 40 studies to target early marine life stages (embryo to larvae), particularly between temperature, 41 salinity and pH as these are the best studied. Knowledge gaps in research on multiple abiotic 42 stressors and early life stages are also identified. The meta-analysis yielded several key results: 1) 43
Small pelagics in a changing ocean: biological responses of sardine early stages to warming
Conservation physiology, 2016
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...
Molecular Ecology, 2018
Global warming will have far-reaching consequences for marine species over coming decades, yet the magnitude of these effects may depend on the rate of warming across generations. Recent experiments show coral reef fishes can compensate the metabolic challenges of elevated temperature when warm conditions are maintained across generations. However, the effects of a gradual temperature increase across generations remain unknown. In the present study, we analyzed metabolic and molecular traits in the damselfish Acanthochromis polyacanthus that were exposed to +1.5˚C in the first generation and +3.0˚C in the second (Step +3.0˚C). This treatment of step-wise warming was compared to fish reared at current-day temperatures (Control), secondgeneration fish of control parents reared at +3.0˚C (Developmental +3.0˚C), and fish exposed to elevated temperatures for two generations (Transgenerational +1.5˚C and Transgenerational +3.0˚C). Hepatosomatic index, oxygen consumption and liver gene expression were compared in second-generation fish of the multiple treatments. Hepatosomatic index increased in fish that developed at +3.0˚C, regardless of the parental temperature. Routine oxygen consumption of Step +3.0˚C fish was significantly higher than Control, however their aerobic scope recovered to the same level as Control fish. Step +3.0˚C fish exhibited significant upregulation of genes related to mitochondrial activity and energy production, which could be associated to their increased metabolic rates. These results indicate that restoration of aerobic scope is possible when fish experience gradual thermal increase across multiple generations, but the metabolic and molecular responses are different from fish reared at the same elevated thermal conditions in successive generations.