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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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Metabolic physiology of squid (Loligo vulgaris) late embryos and hatchlings: A) oxygen consumption rates (µmolO2h−1g−1), B) octopine concentration (µmol g−1), and C) individual energetic cost of the planktonic transition (cal day−1 ind−1), at the different temperature scenarios (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 asterisks represent significant differences between temperatures and developmental stages, respectively (more statistical details in Supporting Tables). In panel A, the “expected” trend is represented by the dash line assuming a Q10 of 2.5. In panel C, the energy-related values do not have any associated variance because they represent the metabolic augment (in calories, based on 4.7 kcal L−1 O2) from late embryos to planktonic paralarvae (i.e. using mean values from panel A).
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pone-0038282-g004: Metabolic physiology of squid (Loligo vulgaris) late embryos and hatchlings: A) oxygen consumption rates (µmolO2h−1g−1), B) octopine concentration (µmol g−1), and C) individual energetic cost of the planktonic transition (cal day−1 ind−1), at the different temperature scenarios (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 asterisks represent significant differences between temperatures and developmental stages, respectively (more statistical details in Supporting Tables). In panel A, the “expected” trend is represented by the dash line assuming a Q10 of 2.5. In panel C, the energy-related values do not have any associated variance because they represent the metabolic augment (in calories, based on 4.7 kcal L−1 O2) from late embryos to planktonic paralarvae (i.e. using mean values from panel A).

Mentions: Oxygen consumption rates (OCR) were significantly affected by temperature and developmental stage (Fig. 4A, two-way ANOVA, p<0.001). Late embryos displayed OCR ranging from 13.0 µmol O2 h−1g−1 at winter temperature (13°C) and 24.1 µmol O2 h−1g−1 at the summer warming condition (red symbol). Embryo’s Q10 values ranged around 1.5 (indicative of active metabolic suppression) above 15°C (Fig. 5). At normal operating temperatures, metabolic demand for oxygen increases with temperature with Q10 around 2–3 (this “expected” trend is represented by the dash line in Figure 4A).


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)

Metabolic physiology of squid (Loligo vulgaris) late embryos and hatchlings: A) oxygen consumption rates (µmolO2h−1g−1), B) octopine concentration (µmol g−1), and C) individual energetic cost of the planktonic transition (cal day−1 ind−1), at the different temperature scenarios (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 asterisks represent significant differences between temperatures and developmental stages, respectively (more statistical details in Supporting Tables). In panel A, the “expected” trend is represented by the dash line assuming a Q10 of 2.5. In panel C, the energy-related values do not have any associated variance because they represent the metabolic augment (in calories, based on 4.7 kcal L−1 O2) from late embryos to planktonic paralarvae (i.e. using mean values from panel A).
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3368925&req=5

pone-0038282-g004: Metabolic physiology of squid (Loligo vulgaris) late embryos and hatchlings: A) oxygen consumption rates (µmolO2h−1g−1), B) octopine concentration (µmol g−1), and C) individual energetic cost of the planktonic transition (cal day−1 ind−1), at the different temperature scenarios (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 asterisks represent significant differences between temperatures and developmental stages, respectively (more statistical details in Supporting Tables). In panel A, the “expected” trend is represented by the dash line assuming a Q10 of 2.5. In panel C, the energy-related values do not have any associated variance because they represent the metabolic augment (in calories, based on 4.7 kcal L−1 O2) from late embryos to planktonic paralarvae (i.e. using mean values from panel A).
Mentions: Oxygen consumption rates (OCR) were significantly affected by temperature and developmental stage (Fig. 4A, two-way ANOVA, p<0.001). Late embryos displayed OCR ranging from 13.0 µmol O2 h−1g−1 at winter temperature (13°C) and 24.1 µmol O2 h−1g−1 at the summer warming condition (red symbol). Embryo’s Q10 values ranged around 1.5 (indicative of active metabolic suppression) above 15°C (Fig. 5). At normal operating temperatures, metabolic demand for oxygen increases with temperature with Q10 around 2–3 (this “expected” trend is represented by the dash line in Figure 4A).

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