Thermal sensitivity links to cellular cardiac decline in three spiny lobsters

Michael Oellermann,Anthony J R Hickey,Greg Smith,Quinn P Fitzgibbon

doi:10.1038/s41598-019-56794-0

Michael Oellermann, Anthony J R Hickey + Show 2 more

Open Access

https://doi.org/10.1038/s41598-019-56794-0

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Journal: Scientific Reports	Publication Date: Jan 14, 2020
Citations: 17	License type: open-access

Affiliation: University of Tasmania, University of Auckland

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.

Highlights

Understanding mechanisms of thermal sensitivity is key to predict responses of marine organisms to changing temperatures
While oxygen consumption increased in all three species with increasing temperature (Fig. 2a, 14–24 °C for J. edwardsii, 20–28 °C for S. verreauxi, 27–35 °C for P. ornatus), heart rate did not increase significantly in J. edwardsii and P. ornatus, except for S. verreauxi (Fig. 2b)
Heart rate and pseudo cardiac output changed at much lower rates than oxygen consumption relative to their initial starting temperature (Fig. 2a–c, refer to percentage values), with a maximal gap between relative change of oxygen consumption (82% ± CI 54%) and pseudo cardiac output (−29% ± CI 10%) in P. ornatus (Fig. 2a,c)

Summary

Introduction

Understanding mechanisms of thermal sensitivity is key to predict responses of marine organisms to changing temperatures. While oxygen demands increased with rising temperatures, heart function became limited or declined in all three species of lobsters. The cardiac ganglion is the prime candidate for control of the crustacean neurogenic heart[45], alternative intrinsic mechanisms that define thermal sensitivity have not been well considered Mitochondria present one such target within cardiac tissues and are well known to respond to rising temperatures through a decline in oxidative phosphorylation efficiency through impaired inner mitochondrial membrane integrity[46,47,48,49]. To date the relation between the thermal sensitivity of mitochondrial function and cardiac performance has been poorly assessed in crustaceans It has only been tested by comparison of two species of portunid crab, but not for other crustaceans of diverse climatic origins[49]. It is unclear whether patterns of thermal sensitivity remain consistent across closely related species of lobsters that have differing thermal histories (i.e. thermal adaptation) or un-linear change occurs, as the case for distinct populations of European green crabs[50]

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