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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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Effect of warming in the early ontogeny squid, Loligo vulgaris, namely: Development time (A), survival rates (B) and growth rates (% - C; mm day−1 - D) of embryos at the different temperature scenarios (red symbols highlight the future summer scenario).Values are mean ± SD. Blue lines represent trendlines and different letters represent significant differences (more statistical details in Supporting Tables).
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pone-0038282-g001: Effect of warming in the early ontogeny squid, Loligo vulgaris, namely: Development time (A), survival rates (B) and growth rates (% - C; mm day−1 - D) of embryos at the different temperature scenarios (red symbols highlight the future summer scenario).Values are mean ± SD. Blue lines represent trendlines and different letters represent significant differences (more statistical details in Supporting Tables).

Mentions: As expected, the duration of the embryonic period in L. vulgaris was significantly shortened with increasing temperature (Fig. 1A, F = 459.0, p<0.001). During the winter season, embryogenesis lasted 27±1 days; yet, the summer embryos incubated in the future warming scenario (19°C) hatched after 14±2 days. The survival rates ranged between 96% and 92% under the present-day scenarios (between 13°C and 17°C, respectively). However, the projected near-future ocean warming elicited a significant negative effect, with survival rates decreasing up to 71% (red symbol, Fig. 1B, F = 4.22, p = 0.046, see also Table S1).


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)

Effect of warming in the early ontogeny squid, Loligo vulgaris, namely: Development time (A), survival rates (B) and growth rates (% - C; mm day−1 - D) of embryos at the different temperature scenarios (red symbols highlight the future summer scenario).Values are mean ± SD. Blue lines represent trendlines and different letters represent significant differences (more statistical details in Supporting Tables).
© Copyright Policy
Related In: Results  -  Collection

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

pone-0038282-g001: Effect of warming in the early ontogeny squid, Loligo vulgaris, namely: Development time (A), survival rates (B) and growth rates (% - C; mm day−1 - D) of embryos at the different temperature scenarios (red symbols highlight the future summer scenario).Values are mean ± SD. Blue lines represent trendlines and different letters represent significant differences (more statistical details in Supporting Tables).
Mentions: As expected, the duration of the embryonic period in L. vulgaris was significantly shortened with increasing temperature (Fig. 1A, F = 459.0, p<0.001). During the winter season, embryogenesis lasted 27±1 days; yet, the summer embryos incubated in the future warming scenario (19°C) hatched after 14±2 days. The survival rates ranged between 96% and 92% under the present-day scenarios (between 13°C and 17°C, respectively). However, the projected near-future ocean warming elicited a significant negative effect, with survival rates decreasing up to 71% (red symbol, Fig. 1B, F = 4.22, p = 0.046, see also Table S1).

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