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Thermal sensitivity links to cellular cardiac decline in three spiny lobsters.

ABSTRACT: Understanding mechanisms of thermal sensitivity is key to predict responses of marine organisms to changing temperatures. Sustaining heart function is critical for complex organisms to oxygenate tissues, particularly under temperature stress. Yet, specific mechanisms that define thermal sensitivity of cardiac function remain unclear. Here we investigated whole animal metabolism, cardiac performance and mitochondrial function in response to elevated temperatures for temperate, subtropical and tropical spiny lobster species. While oxygen demands increased with rising temperatures, heart function became limited or declined in all three species of lobsters. The decline in cardiac performance coincided with decreases in mitochondrial efficiency through increasing mitochondrial proton leakage, which predicts impaired compensation of ATP production. Species differences were marked by shifts in mitochondrial function, with the least thermal scope apparent for tropical lobsters. We conclude that acute temperature stress of spiny lobsters, irrespective of their climatic origin, is marked by declining cellular energetic function of the heart, contributing to an increasing loss of whole animal performance. Better understanding of physiological thermal stress cascades will help to improve forecasts of how changing environmental temperatures affect the fitness of these ecologically and commercially important species.

SUBMITTER: Oellermann M

PROVIDER: S-EPMC6959275 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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Thermal sensitivity links to cellular cardiac decline in three spiny lobsters.

Oellermann Michael M Hickey Anthony J R AJR Fitzgibbon Quinn P QP Smith Greg G

Scientific reports 20200114 1

Understanding mechanisms of thermal sensitivity is key to predict responses of marine organisms to changing temperatures. Sustaining heart function is critical for complex organisms to oxygenate tissues, particularly under temperature stress. Yet, specific mechanisms that define thermal sensitivity of cardiac function remain unclear. Here we investigated whole animal metabolism, cardiac performance and mitochondrial function in response to elevated temperatures for temperate, subtropical and tro ...[more]

PMID: 31937868

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Project description:Predation risk can strongly shape prey ecological traits, with specific anti-predator responses displayed to reduce encounters with predators. Key environmental drivers, such as temperature, can profoundly modulate prey energetic costs in ectotherms, although we currently lack knowledge of how both temperature and predation risk can challenge prey physiology and ecology. Such uncertainties in predator-prey interactions are particularly relevant for marine regions experiencing rapid environmental changes due to climate change. Using the octopus (Octopus maorum)-spiny lobster (Jasus edwardsii) interaction as a predator-prey model, we examined different metabolic traits of sub adult spiny lobsters under predation risk in combination with two thermal scenarios: 'current' (20°C) and 'warming' (23°C), based on projections of sea-surface temperature under climate change. We examined lobster standard metabolic rates to define the energetic requirements at specific temperatures. Routine metabolic rates (RMRs) within a respirometer were used as a proxy of lobster activity during night and day time, and active metabolic rates, aerobic scope and excess post-exercise oxygen consumption were used to assess the energetic costs associated with escape responses (i.e. tail-flipping) in both thermal scenarios. Lobster standard metabolic rate increased at 23°C, suggesting an elevated energetic requirement (39%) compared to 20°C. Unthreatened lobsters displayed a strong circadian pattern in RMR with higher rates during the night compared with the day, which were strongly magnified at 23°C. Once exposed to predation risk, lobsters at 20°C quickly reduced their RMR by ~29%, suggesting an immobility or 'freezing' response to avoid predators. Conversely, lobsters acclimated to 23°C did not display such an anti-predator response. These findings suggest that warmer temperatures may induce a change to the typical immobility predation risk response of lobsters. It is hypothesized that heightened energetic maintenance requirements at higher temperatures may act to override the normal predator-risk responses under climate-change scenarios.

Project description:BACKGROUND: Molecular tools may help to uncover closely related and still diverging species from a wide variety of taxa and provide insight into the mechanisms, pace and geography of marine speciation. There is a certain controversy on the phylogeography and speciation modes of species-groups with an Eastern Atlantic-Western Indian Ocean distribution, with previous studies suggesting that older events (Miocene) and/or more recent (Pleistocene) oceanographic processes could have influenced the phylogeny of marine taxa. The spiny lobster genus Palinurus allows for testing among speciation hypotheses, since it has a particular distribution with two groups of three species each in the Northeastern Atlantic (P. elephas, P. mauritanicus and P. charlestoni) and Southeastern Atlantic and Southwestern Indian Oceans (P. gilchristi, P. delagoae and P. barbarae). In the present study, we obtain a more complete understanding of the phylogenetic relationships among these species through a combined dataset with both nuclear and mitochondrial markers, by testing alternative hypotheses on both the mutation rate and tree topology under the recently developed approximate Bayesian computation (ABC) methods. RESULTS: Our analyses support a North-to-South speciation pattern in Palinurus with all the South-African species forming a monophyletic clade nested within the Northern Hemisphere species. Coalescent-based ABC methods allowed us to reject the previously proposed hypothesis of a Middle Miocene speciation event related with the closure of the Tethyan Seaway. Instead, divergence times obtained for Palinurus species using the combined mtDNA-microsatellite dataset and standard mutation rates for mtDNA agree with known glaciation-related processes occurring during the last 2 my. CONCLUSION: The Palinurus speciation pattern is a typical example of a series of rapid speciation events occurring within a group, with very short branches separating different species. Our results support the hypothesis that recent climate change-related oceanographic processes have influenced the phylogeny of marine taxa, with most Palinurus species originating during the last two million years. The present study highlights the value of new coalescent-based statistical methods such as ABC for testing different speciation hypotheses using molecular data.

Dataset Information

Thermal sensitivity links to cellular cardiac decline in three spiny lobsters.

Publications

Thermal sensitivity links to cellular cardiac decline in three spiny lobsters.

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