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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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Related in: MedlinePlus

Abnormalities found during the early development squid, Loligo vulgaris.Panel A shows a “normal” hatchling and panel B a typical premature-hatchling. The most common abnormality types found in embryos: C) Eye dimorphism; D) Complete body deformity, E) Elongated body, F) Mantle deformity; and in hatchlings: G) Mantle detached; H) Mantle deformity; I) Complete body deformity.
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pone-0038282-g002: Abnormalities found during the early development squid, Loligo vulgaris.Panel A shows a “normal” hatchling and panel B a typical premature-hatchling. The most common abnormality types found in embryos: C) Eye dimorphism; D) Complete body deformity, E) Elongated body, F) Mantle deformity; and in hatchlings: G) Mantle detached; H) Mantle deformity; I) Complete body deformity.

Mentions: Future warming (19°C) significantly affected the early ontogenetic growth (Fig. 1C,D, Table S1). Embryo growth rates (expressed as % increase from beginning to the end of embryogenesis, and mm day−1) increased significantly under the present-day scenarios, but there was a significant trend reversal at future summer conditions (red symbols, 19°C, Fig. 1C,D, F = 92.3, p<0.001). Figure 2 shows the most common types of abnormalities observed. Early embryos showed mostly underdeveloped mantles, complete body deformities and eye dimorphism. Late embryos also showed elongated bodies and mantle deformities. Lastly, hatchlings revealed greater incidence of mantle detachment, mantle deformity and also complete body deformities. The incidence of abnormalities increased significantly with temperature and varied between stages; the higher percentage of abnormalities was found in late embryos exposed to the summer warming scenario (Fig. 3A, two-way ANOVA, p<0.001). Hatchlings presented the lower percentage of abnormalities in all thermal scenarios.


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)

Abnormalities found during the early development squid, Loligo vulgaris.Panel A shows a “normal” hatchling and panel B a typical premature-hatchling. The most common abnormality types found in embryos: C) Eye dimorphism; D) Complete body deformity, E) Elongated body, F) Mantle deformity; and in hatchlings: G) Mantle detached; H) Mantle deformity; I) Complete body deformity.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0038282-g002: Abnormalities found during the early development squid, Loligo vulgaris.Panel A shows a “normal” hatchling and panel B a typical premature-hatchling. The most common abnormality types found in embryos: C) Eye dimorphism; D) Complete body deformity, E) Elongated body, F) Mantle deformity; and in hatchlings: G) Mantle detached; H) Mantle deformity; I) Complete body deformity.
Mentions: Future warming (19°C) significantly affected the early ontogenetic growth (Fig. 1C,D, Table S1). Embryo growth rates (expressed as % increase from beginning to the end of embryogenesis, and mm day−1) increased significantly under the present-day scenarios, but there was a significant trend reversal at future summer conditions (red symbols, 19°C, Fig. 1C,D, F = 92.3, p<0.001). Figure 2 shows the most common types of abnormalities observed. Early embryos showed mostly underdeveloped mantles, complete body deformities and eye dimorphism. Late embryos also showed elongated bodies and mantle deformities. Lastly, hatchlings revealed greater incidence of mantle detachment, mantle deformity and also complete body deformities. The incidence of abnormalities increased significantly with temperature and varied between stages; the higher percentage of abnormalities was found in late embryos exposed to the summer warming scenario (Fig. 3A, two-way ANOVA, p<0.001). Hatchlings presented the lower percentage of abnormalities in all thermal scenarios.

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