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Ocean warming enhances malformations, premature hatching, metabolic suppression and oxidative stress in the early life stages of a keystone squid.

Rosa R, Pimentel MS, Boavida-Portugal J, Teixeira T, Trübenbach K, Diniz M - PLoS ONE (2012)

Bottom Line: However, the greater exposure to environmental stress by the hatchlings seemed to be compensated by physiological mechanisms that reduce the negative effects on fitness.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.

View Article: PubMed Central - PubMed

Affiliation: Laboratório Marítimo da Guia, Centro de Oceanografia, Faculdade de Ciências da Universidade de Lisboa, Cascais, Portugal. rrosa@fc.ul.pt

ABSTRACT

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.

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Antioxidant response of Loligo vulgaris’ late embryos and hatchlings at the different temperature scenarios: A) GST (nmol min−1mg−1), B) CAT (pmol mg−1), C) SOD (U g−1) and d) malondialdehyde (MDA; pmol mg−1).Red symbols highlight the future summer scenario. Values are mean ± SD. Colored lines represent trendlines and different letters (capital letters for hatchlings; small letters for embryos) and asterisk represent significant differences between temperatures and developmental stages, respectively (more statistical details in Supporting Tables).
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pone-0038282-g007: Antioxidant response of Loligo vulgaris’ late embryos and hatchlings at the different temperature scenarios: A) GST (nmol min−1mg−1), B) CAT (pmol mg−1), C) SOD (U g−1) and d) malondialdehyde (MDA; pmol mg−1).Red symbols highlight the future summer scenario. Values are mean ± SD. Colored lines represent trendlines and different letters (capital letters for hatchlings; small letters for embryos) and asterisk represent significant differences between temperatures and developmental stages, respectively (more statistical details in Supporting Tables).

Mentions: Glutathione S-Transferase GST activity varied significantly between developmental stages, being significantly lower in the embryos (Fig. 7A, two-way ANOVA, p<0.001). Only the hatchlings revealed a significant positive temperature effect (p<0.05), but with a reversal pattern at 19°C (red symbol, Fig. 7A). Regarding catalase (CAT) activity, an opposite temperature effect between stages was observed (Fig. 7B, two-way ANOVA, p>0.05), with the hatchlings showing a non-significant positive trend. It is worth noting that CAT was the only variable analyzed that did not show a significant interaction between temperature and developmental stage (see also Table S2).


Ocean warming enhances malformations, premature hatching, metabolic suppression and oxidative stress in the early life stages of a keystone squid.

Rosa R, Pimentel MS, Boavida-Portugal J, Teixeira T, Trübenbach K, Diniz M - PLoS ONE (2012)

Antioxidant response of Loligo vulgaris’ late embryos and hatchlings at the different temperature scenarios: A) GST (nmol min−1mg−1), B) CAT (pmol mg−1), C) SOD (U g−1) and d) malondialdehyde (MDA; pmol mg−1).Red symbols highlight the future summer scenario. Values are mean ± SD. Colored lines represent trendlines and different letters (capital letters for hatchlings; small letters for embryos) and asterisk represent significant differences between temperatures and developmental stages, respectively (more statistical details in Supporting Tables).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3368925&req=5

pone-0038282-g007: Antioxidant response of Loligo vulgaris’ late embryos and hatchlings at the different temperature scenarios: A) GST (nmol min−1mg−1), B) CAT (pmol mg−1), C) SOD (U g−1) and d) malondialdehyde (MDA; pmol mg−1).Red symbols highlight the future summer scenario. Values are mean ± SD. Colored lines represent trendlines and different letters (capital letters for hatchlings; small letters for embryos) and asterisk represent significant differences between temperatures and developmental stages, respectively (more statistical details in Supporting Tables).
Mentions: Glutathione S-Transferase GST activity varied significantly between developmental stages, being significantly lower in the embryos (Fig. 7A, two-way ANOVA, p<0.001). Only the hatchlings revealed a significant positive temperature effect (p<0.05), but with a reversal pattern at 19°C (red symbol, Fig. 7A). Regarding catalase (CAT) activity, an opposite temperature effect between stages was observed (Fig. 7B, two-way ANOVA, p>0.05), with the hatchlings showing a non-significant positive trend. It is worth noting that CAT was the only variable analyzed that did not show a significant interaction between temperature and developmental stage (see also Table S2).

Bottom Line: However, the greater exposure to environmental stress by the hatchlings seemed to be compensated by physiological mechanisms that reduce the negative effects on fitness.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.

View Article: PubMed Central - PubMed

Affiliation: Laboratório Marítimo da Guia, Centro de Oceanografia, Faculdade de Ciências da Universidade de Lisboa, Cascais, Portugal. rrosa@fc.ul.pt

ABSTRACT

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.

Show MeSH
Related in: MedlinePlus