Physiochemical responses of an asterinid starfish (Echinodermata: Asteroidea) to global ocean change

Abstract

The continuous increase in greenhouse gas (GHG) emissions, especially carbon dioxide (CO2), since the beginning of global industrialization has resulted in significant alterations in seawater physicochemical properties, particularly elevated seawater temperatures (ocean warming, OW) and ocean acidification (OA). These changes have wide-ranging consequences for marine organisms, affecting their biological functions and ecological roles. The combined effects of OW and OA may amplify adverse outcomes compared to individual stressors due to the complex reorganization of cellular mechanisms and molecular pathways, which subsequently appear in behavioral modifications. However, organismal reactions and thresholds to these stressors are variable, which might differ within organism ontogeny or among taxa, making predictions challenging. Therefore, increasing research has been performed to better understand the potential mechanisms underlying the ability of marine organisms to alleviate the effects of environmental change, mainly due to OW and OA. Thus, employing multiple bioindicators, specifically keystone species such as starfish, to evaluate the impacts of OW and OA offers a comprehensive approach to examining their effects not simply on the organism concerned but also on the broader ecosystem.

The presented studies in this thesis aim to contribute to the understanding the role of physiochemistry and trade-offs on marine ectotherms, particularly asterinid starfish, in coping with environmental stress. For this purpose, mineralogic, metabolic, behavioral, lipidomics, and enzymatic activity approaches are used. The research summarized in this thesis provides the first investigation of the effects of global ocean change on biomineralization and physiological traits through long-term experiments using asterinid starfish species, Aquilonastra yairi, distributed in tropical to subtropical regions (across the Mediterranean Sea, Red Sea, and Gulf of Suez). The starfish were exposed to two temperature levels (27 °C and 32 °C) crossed with three pCO2 regimes (455 µatm, 1052 µatm, and 2066 µatm), representing factorial combinations of ambient conditions and future levels of CO2 and temperature change according to the IPCC-Representative Concentration Pathways (RCPs) 8.5 greenhouse gas emission scenario for the year 2100.

The present work revealed that asterinid starfish demonstrate high stressor tolerance and resilience to increased temperature and pCO2 through adaptive adjustments in physiological functions or behavioral activities, suggesting high homeostatic capacities and the ability to regulate physiochemical response to maintain survival, fitness, and metabolic biosynthesis under chronic conditions. The temperature was the predominant factor, exerting a significant effect on the magnitude and frequency of the affected physiological-related processes; however, concurrent exposure to OA and OW stress produced synergistic effects on some of the starfish physiology-related responses tested. While decreased pH negatively affects starfish calcification performance, the increased temperature potentially mitigates these effects. However, increased temperature might also lead to more magnesium (Mg2+) incorporation into the calcite lattice, potentially compromising the starfish skeleton. Furthermore, it was revealed that starfish can preserve lipid-associated biochemistry (FAs) under elevated temperature and pCO2, which potentially provides molecular instruments to cope with future OA and OW scenarios. However, combined OA and OW significantly affected Ca-ATPase and Mg-ATPase enzyme activities, which are recognized to play an important role in the biomineralization pathway, raising concerns about potential susceptibilities in skeletal development and preservation.

Investigating the complex impacts of global ocean change on marine organisms requires a comprehensive research approach that encompasses diverse biological, chemical, and physical traits. Understanding the physiological and chemical responses of bioindicator species, e.g., asterinid starfish, to combined stressors OW and OA is important to comprehend the relationships and interactions between biological processes and abiotic environmental conditions, which in turn essential for accurately predicting their resilience, ecological implication, and broader ecosystem dynamics. At the ecosystem scale, this study significantly contributes to the ongoing knowledge for future studies of the impact of climate change on coral reef-associated invertebrates. Specifically, this finding is beneficial for the conservation of coral reef ecosystems under future ocean conditions.